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1
Mallinckrodt Institute of Radiology, Washington University School of Medicine,
St. Louis, MO 63110.
2
Department of Radiology/Nuclear Medicine, F. Edward
Hébert School of Medicine, Uniformed Services
University of the Health Sciences, Bethesda, MD 20814.
3
Present address: Department of Radiology, National Naval Medical Center,
Bethesda, MD 20889.
4
Department of Radiologic Pathology, Armed Forces Institute of Pathology,
Washington, DC 20306.
Received May 4, 2000;
accepted after revision July 3, 2000.
The opinions and assertions contained herein are the private views of the
authors and are not to be construed as official or as reflecting the views of
the Department of the Navy, Army, or Defense.
Abstract
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MATERIALS AND METHODS. Radiologic studies from 17 patients with pathologically proven collecting duct carcinoma were analyzed by two reviewers.
RESULTS. The tumors varied in size from 1.5 to 19 cm (mean, 7.7 cm). Medullary involvement was present on CT in 16 (94%) of 17 cases, but cortical involvement or an exophytic component was also present in 15 cases (88%) and 10 cases (59%), respectively. The reniform contour of the kidney was preserved in seven cases (41%) and correlated with a smaller tumor size (p<0.01). Tumors showed an infiltrative appearance on CT in 11 cases (65%), but an expansile component was also present in eight of these cases. A cystic component was present on CT in six (35%) of 17 cases. On sonography, the solid tumor component was hyperechoic to normal renal parenchyma in six of seven cases and isoechoic in the other. On MR imaging, all tumors (4/4) were hypointense on T2-weighted imaging. On urography, all lesions (5/5) distorted the intrarenal collecting system. On angiography, all tumors (3/3) were hypovascular.
CONCLUSION. Medullary involvement and an infiltrative appearance are common findings on cross-sectional imaging and may suggest the diagnosis of collecting duct carcinoma. In large tumors, however, these features are frequently overshadowed by an exophytic or expansile component that cannot be distinguished from the more common cortical renal cell carcinoma.
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The clinical data were reviewed to determine the age, sex, and clinical presentation of these patients. Final histopathologic diagnoses were confirmed by one pathologist at each institution. The radiologic studies available for review included CT in all 17 patients, sonography in seven patients, MR imaging in four patients, excretory urography in five patients, retrograde urography in three patients, and renal angiography in three patients.
The CT technique varied somewhat because of the retrospective nature of the study; however, iodinated IV contrast material was administered in all 17 patients. In general, the nephrographic phase of contrast enhancement was analyzed. Unenhanced images were available in 12 cases. MR imaging technique also varied, but T1- and T2-weighted imaging was available in all four cases.
Two reviewers analyzed the images together, a process that resulted in a consensus interpretation. On CT, the location of tumor involvement was described as medullary (central), cortical, or exophytic; the relative contribution from each location was assessed. Medullary involvement was supported by protrusion into the renal pelvis, replacement of the renal sinus fat, or distortion of the intrarenal collecting system. Cortical involvement was supported by a peripheral location of the tumor and contact with the outer renal capsule. An exophytic component was considered to be present when the tumor focally extended beyond the expected renal confines and disrupted the reniform shape of the kidney. An exophytic component or frank perinephric invasion implied cortical involvement as well.
The presence of an infiltrative or expansile pattern of growth was assessed, as well as which pattern predominated in each case. Infiltrative growth on CT is characterized by poorly marginated borders between the tumor and normal renal parenchyma, whereas expansile growth is characterized by well-defined bulging tumor margins that displace normal parenchyma. CT attenuation characteristics of the tumor were also assessed, including homogeneity, relative contribution of cystic and solid components, presence of calcification, high attenuation on unenhanced images, and degree of enhancement. The presence of intraabdominal metastatic disease was also evaluated.
Sonographic examinations were evaluated primarily for echotexture of the solid component of the tumor relative to the normal renal parenchyma and renal sinus fat (hyper-, iso-, or hyperechoic). Sonograms were also evaluated for a cystic component. On MR imaging, the signal intensity characteristics on T1- and T2-weighted images were noted. The sonograms and MR images were also evaluated for the presence of a hypoechoic or hypointense rim, respectively, surrounding the tumor, which would suggest a pseudocapsule [6, 7]. On urography, the tumor's effect on the collecting system was assessed. Finally, tumor vascularity was evaluated on angiography.
Statistical analysis for comparing tumor size versus preservation of the reinform contour and for predilection of right versus left kidney was performed using the Student's t test.
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CT Findings
Abdominal CT scans were available for all 17 patients. Maximal tumor
diameter ranged from 1.5 to 19 cm (mean diameter, 7.7 ± 4.6 cm); four
tumors measured greater than 10 cm. Collecting duct carcinoma involved the
right kidney in 14 (82%) of 17 cases and the left kidney in the other three
cases (p = 0.10).
Central or medullary involvement by tumor, with protrusion into the renal pelvis or replacement of the renal sinus fat, was present in 16 (94%) of 17 cases (Figs. 1A,1B and 2A,2B). Cortical involvement was noted in 15 (88%) of 17 cases; an exophytic component beyond the expected renal contour was seen in 10 (59%) of 17 cases (Fig. 3). Medullary involvement without cortical involvement was seen in two cases, medullary and cortical involvement without an exophytic component was seen in five cases, and all three components were present in nine cases. In one case, there was cortical involvement and an exophytic component without apparent medullary involvement. The predominate region of involvement or center of tumor bulk was judged to be medullary in seven cases, cortical in four, and extrarenal in six. The reniform contour of the involved kidney was preserved in seven (41%) of 17 cases; the remaining 10 tumors had an exophytic component. The mean tumor size (±SD) among cases with a preserved reniform shape was 4.5 ± 2.8 cm versus 10.2 ± 4.3 cm among tumors with an exophytic component (p < 0.01).
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A CT appearance suggesting an infiltrative pattern of tumor growth was present in 11 (65%) of 17 cases but was thought to be the sole pattern of growth in only three cases (Fig. 1A,1B). An expansile appearance was present in 14 (82%) of 17 tumors and was the sole pattern of growth in six cases. Both patterns coexisted in eight cases (47%).
The lesions appeared solid (11/17) or complex solid and cystic (6/17) on CT. Among the six complex solid and cystic tumors, two were predominately solid with a small cystic component that represented areas of necrosis at pathologic examination. Four tumors were predominately cystic because of the presence of true epithelial cysts with endophytic papillary projections; two of these appeared multilocular (Fig. 4A), and two appeared unilocular (Fig. 4B). Of the 12 cases with unenhanced images, three showed increased attenuation of the soft-tissue component relative to the normal renal parenchyma (Fig. 5A,5B,5C,5D,5E). Calcification was present in four cases; the pattern of calcification was punctate in three cases, and rim calcification of cysts was seen in the fourth case. Caliectasis was apparent in two cases.
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After IV contrast administration, nine tumors were of homogeneous low attenuation compared with that of normal parenchyma, whereas eight tumors were of low attenuation but heterogeneous in appearance. Enhancement of the solid tumor component in cases with both unenhanced and contrast-enhanced images was graded as moderate in three cases and minimal in nine cases. Attenuation values were not measured in most cases but, when available, an increase of 15-40 H was seen on contrast-enhanced images when compared with unenhanced images (Fig. 5A,5B,5C,5D,5E).
Evidence of intraabdominal metastatic disease was present on CT in seven (41%) of 17 cases. Regional lymphadenopathy was seen in five cases, with coalescent nodal masses measuring more than 3 cm in three cases (Fig. 3). Direct invasion of the liver from right-sided tumors was seen in two cases, and an adrenal metastasis was seen in one case. Direct tumor extension into the venous system was not seen in any of the cases.
Other Imaging Findings
Of the seven patients evaluated on sonography, the solid component of the
tumor was isoechoic compared with normal renal parenchyma in one case,
hyperechoic to renal parenchyma but less echogenic than renal sinus fat in
five cases (Fig.
5A,5B,5C,5D,5E),
and isoechoic to renal sinus fat in one case. The average tumor diameter of
these seven cases was 8.1 cm; two tumors were smaller than 3 cm. In no case
was a well-defined hypoechoic rim seen at the tumor—parenchyma
interface. Anechoic cystic areas were noted in three cases, representing
either intratumoral cysts or cystic necrosis. Overall, three tumors appeared
homogeneous and four appeared heterogeneous.
On T1-weighted spin-echo MR images, the solid tumor component was isointense to normal renal parenchyma in all four cases (Fig. 2A,2B). In one tumor that was predominately cystic and multilocular, the T1-weighted signal intensity of individual cysts ranged from that of water up to high signal intensity equal to that of fat, representing hemorrhagic products. On T2-weighted spin-echo MR images, the solid tumor component was hypointense to normal renal parenchyma in all four cases (Fig. 5A,5B,5C,5D,5E). No marginal hypointense rim was seen in any case to suggest the presence of a pseudocapsule.
Of the five patients with available excretory urograms, three also had retrograde studies. Distortion of the intrarenal collecting system was noted in all five cases, consisting of calyceal displacement and associated filling defects (Fig. 1A,1B). Medial displacement of the ureter was seen in one case. In another case, focally prolonged cortical retention of contrast material was seen on a 1-hr delayed film in the region that supplied the medullary portion involved by tumor.
Selective renal angiography showed the tumors to be hypovascular compared with normal renal parenchyma in all three cases. In one case of a large 19-cm tumor, small tumor vessels were identified but the mass was hypovascular and without a tumor blush.
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Approximately 100 cases of collecting duct carcinoma have been reported previously in the literature, including a large subset from East Asia [1]. A wide patient age range exists, with a mean age at diagnosis of 55 years and a 2:1 male predominance [3]. Although these data are similar to the series we report, this demographic profile also applies to renal cell carcinoma in general and is therefore not a useful discriminator [9]. Clinical presentation for collecting duct carcinoma is also nonspecific and could apply to any renal malignancy. Similar to our findings, studies have shown that abdominal pain, flank mass, and gross hematuria are most common. Constitutional symptoms such as fever may also be seen, but no particular paraneoplastic syndrome has been reported. The tumor typically inflicts an aggressive clinical course, and metastatic disease has been reported in up to 40% of patients at the time of presentation, which, again, is similar to our findings.
Grossly, collecting duct carcinoma tends to be large at presentation. Despite its medullary derivation, almost all tumors exhibit focal cortical extension, and perinephric extension is also common [4]. As seen with our series, a medullary origin can be difficult to appreciate with large tumors. Collecting duct carcinoma tends to involve the kidney by infiltrative growth [10]. However, as we have shown, this pattern of growth may become less apparent on imaging if a large exophytic tumor component extends beyond the renal capsule. The histologic criteria for the diagnosis of collecting duct carcinoma are controversial, but tubular or ductlike structures resembling collecting ducts are seen, usually associated with a papillary element [8]. Most tumors are classified as high grade at histologic examination.
Before we discuss the specific imaging findings of collecting duct carcinoma, it is useful to further review the concept of expansile versus infiltrative growth by renal tumors. Most renal tumors grow by radial expansion with displacement of the normal parenchyma, focal bulging of the renal contour, and pseudocapsule formation (Fig. 6A,6B). Pseudocapsule formation results from compression, ischemia, and subsequent fibrosis of the adjacent parenchyma at the tumor margin [2]. One study found that, regardless of tumor size, 94% of cortical renal cell carcinomas exhibit an expansile appearance with exophytic growth that disrupts the reniform contour [11]. Infiltrative growth is a much less common pattern whereby tumor cells spread using the normal renal architecture as scaffolding for interstitial growth. The margin between an infiltrative tumor and kidney is often poorly defined because of a broad zone of transition (Fig. 6A,6B). Infiltrative lesions may enlarge the kidney but usually maintain the reniform contour. These growth patterns can often be distinguished on cross-sectional imaging through analysis of tumor morphology, particularly the interface between the tumor and the normal kidney. As evident in our series, both infiltrative and expansile patterns may coexist to various degrees [5].
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In addition to collecting duct carcinoma, there are other uncommon renal tumors that are typically infiltrative in nature. Renal medullary carcinoma is an aggressive malignancy that is strongly associated with sickle cell trait [12, 13]. Also derived from the renal medulla, its histopathologic relationship with collecting duct carcinoma is uncertain and classification of these tumors continues to evolve [1]. It is interesting to note that 23 (82%) of 28 cases of renal medullary carcinoma involved the right kidney in the original series [11]. This predilection for the right kidney is similar to our series of collecting duct carcinoma and is statistically significant when the two groups are combined. The reasons for this predilection are unknown.
Urothelial tumors of the renal pelvis, namely invasive transitional cell carcinoma and squamous cell carcinoma, also tend to involve the kidney by infiltration [2]. A centrally located collecting duct carcinoma with invasion into the renal pelvis may be indistinguishable from an invasive transitional cell carcinoma of the renal pelvis. This distinction, however, has important implications for treatment because nephroureterectomy is indicated for urothelial carcinomas, whereas nephrectomy is performed for renal parenchymal malignancies.
Although only about 6% of cortical renal cell carcinomas are truly infiltrative, it nonetheless represents a significant proportion of infiltrative tumors given its overall abundance [2, 11]. Distinguishing between cortical renal cell carcinoma and collecting duct carcinoma on preoperative imaging studies has prognostic significance but will not likely alter initial treatment of the patient. This could change, however, as more specific treatment protocols evolve.
The imaging features of collecting duct carcinoma have not been well characterized, which provided motivation for our study. Previously, the largest radiologic series consisted of five cases from Japan [14]. In that study, Fukuya et al. described the CT findings of small tumors, all measuring between 3 and 4.5 cm. These lesions were all centered in the renal medulla, four of five protruded in the central sinus, and none showed exophytic growth but, rather, preserved the reniform contour in all cases. Although a determination of infiltrative versus expansile growth was not specifically addressed, several of the illustrations show a poorly defined tumor margin. On renal angiography, four of five tumors were hypovascular. From these results it would appear that the diagnosis of collecting duct carcinoma might be reliably surmised from the imaging findings. Indeed, our results were similar for tumors less than 5 cm in diameter. However, the majority of tumors in our series were larger than 5 cm, and although many of the aforementioned features were present, there was often an expansile or exophytic component that resembled the more conventional cortical renal cell carcinomas.
Several of the CT findings of collecting duct carcinoma in our study, such as a cystic component, calcification, and regional lymphadenopathy, are nonspecific among epithelial renal malignancies. However, regional lymphadenopathy (Robson stage IIIB) and a true cystic component were both more common among collecting duct carcinoma in our series when compared with cortical renal cell carcinoma.
Although all lesions were hypodense relative to the normal renal parenchyma after administration of contrast material, tumor vascularity cannot be implied on this basis alone because all reviewed images were obtained after the arterial phase. Besides, even with the more common hypervascular variants of renal cell carcinoma, 97% of these tumors will appear hypodense during the nephrographic phase [11]. However, tumor hypovascularity was seen on all renal angiograms in our series. The role of angiography in the workup of renal malignancy has significantly diminished, but angiography may still be used when preoperative knowledge of vascular anatomy is crucial, as with nephron-sparing surgery [5].
On sonography, cortical renal cell carcinoma may be hypoechoic to normal renal parenchyma, isoechoic to renal parenchyma, hyperechoic to renal parenchyma but hypoechoic to renal sinus fat, or isoechoic to renal sinus fat. One study found that 86% of renal cell carcinomas were isoechoic to renal parenchyma, 10% were hypoechoic, and only 4% were hyperechoic. However, subsequent studies have shown that small tumors (<3 cm) are hyperechoic in 61-77% of the cases [15,16,17]. Although considerable overlap in echogenicity has been shown between hyperechoic renal cell carcinomas and angiomyolipomas, a hypoechoic rim corresponding to a pseudocapsule has been reported in 84% of the former but in none of the latter [6]. The presence of intratumoral cysts also favors renal malignancy. The frequency of increased echogenicity among collecting duct carcinomas in our series is noteworthy because the tumors tended to be larger than 3 cm, with an average diameter of 8.1 cm. In addition, a hypoechoic rim was not identified in any case, perhaps corresponding to the absence of a pseudocapsule with this infiltrative neoplasm.
The role of MR imaging in the evaluation of renal malignancy has continued to expand with the advent of faster imaging sequences. In general, renal cell carcinoma appears slightly hypointense to normal renal parenchyma on T1-weighted images and slightly hyperintense on T2-weighted images [18]. A hypointense rim corresponding to a pseudocapsule analogous to the hypoechoic rim on sonography is reportedly present in most renal cell carcinomas [7]. The solid tumor component of collecting duct carcinoma in our series was hypointense on all T2-weighted images and did not have a hypointense rim. Along with hyperechogenicity on sonography, hypointensity on T2-weighted images appears to favor collecting duct carcinoma, especially with a centrally located tumor.
There are several limitations to our study. Our relatively small study population precludes any definitive conclusions regarding the imaging of this rare tumor. Nonetheless, we have shown that imaging features suggestive of collecting duct carcinoma are usually present but may be overshadowed by an expansile or exophytic component in large tumors. The actual specificity of findings such as medullary location of the tumor and an infiltrative appearance on CT cannot be ascertained because we did not evaluate renal tumors other than collecting duct carcinoma. Such findings would also be expected with some of the other infiltrative tumors mentioned earlier, as well as in a subset of aggressive renal cell carcinomas.
In conclusion, imaging findings that support the diagnosis of collecting duct carcinoma include a medullary location and an infiltrative appearance on CT, hyperechogenicity on sonography, hypointensity on T2-weighted MR images, distortion of the renal collecting system on urography, and hypovascularity on angiography. These tumors, however, are often large at presentation and also have an expansile appearance and exophytic component that cannot be reliably distinguished from the more common cortical renal cell carcinomas.
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