DOI: 10.1148/rg.266065010
RadioGraphics 2006;26:1795-1806
© RSNA, 2006
Common and Uncommon Histologic Subtypes of Renal Cell Carcinoma: Imaging Spectrum with Pathologic Correlation1
Srinivasa R. Prasad, MD,
Peter A. Humphrey, MD, PhD,
Jay R. Catena, MD,
Vamsi R. Narra, MD,
John R. Srigley, MD,
Arthur D. Cortez, MD,
Neal C. Dalrymple, MD and
Kedar N. Chintapalli, MD
1 From the Department of Radiology, University of Texas Health Science Center, 7703 Floyd Curl Dr, San Antonio, TX 78229 (S.R.P., J.R.C., A.D.C., N.C.D., K.N.C.); the Department of Pathology, Washington University, St Louis, Mo (P.A.H.); the Department of Radiology, Mallinckrodt Institute of Radiology, St Louis, Mo (V.R.N.); and the Department of Pathology and Molecular Medicine, McMaster University, Mississauga, Ontario, Canada (J.R.S.). Recipient of a Magna Cum Laude award for an education exhibit at the 2004 RSNA Annual Meeting. Received January 24, 2006; revision requested February 24 and received March 30; accepted March 31. All authors have no financial relationships to disclose.
Address correspondence to S.R.P. (e-mail: prasads{at}uthscsa.edu).
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Abstract
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Renal cell carcinoma (RCC) is a cause of significant morbidity and mortality, with an estimated 35,000 new cases and 12,480 deaths in the United States in 2003. Recent advances in imaging technology, pathology, urology, and oncology permit early diagnosis of RCC and facilitate optimal management. The 2004 World Health Organization classification for renal neoplasms recognizes several distinct histologic subtypes of RCC. These subtypes include clear cell RCC, papillary RCC, chromophobe RCC, hereditary cancer syndromes, multilocular cystic RCC, collecting duct carcinoma, medullary carcinoma, mucinous tubular and spindle cell carcinoma, neuroblastoma-associated RCC, Xp11.2 translocation–TFE3 carcinoma, and unclassified lesions. Different histologic subtypes of RCC have characteristic histomorphologic and biologic profiles. Clear cell RCC is the most common subtype and has a less favorable prognosis (stage for stage) than do papillary RCC and chromophobe RCC. Collecting duct carcinoma and renal medullary carcinoma are associated with aggressive clinical behavior and a poor prognosis.
© RSNA, 2006
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LEARNING OBJECTIVES FOR TEST 5
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After reading this article and taking the test, the reader will be able to:- Describe the histologic spectrum of common and uncommon renal cell carcinomas.
- Identify the imaging features of different histologic subtypes of renal cell carcinoma.
- Discuss correlation of the imaging findings of various histologic subtypes of renal cell carcinoma with the gross and microscopic findings.
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Introduction
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Renal cell carcinoma (RCC) is the most common adult renal epithelial cancer, accounting for more than 90% of all renal malignancies (1). RCC is the most lethal of all urologic cancers, accounting for more than 12,000 annual deaths in the United States (out of an estimated 35,000 new cases in 2003) (2). The 5-year cancer-specific survivals of patients with pT4 RCC and lymph node metastases are 20% and 5%–30%, respectively (3). There is continued global increase in the incidence of RCC, partly due to early diagnosis with cross-sectional imaging modalities (4). Up to 30%–40% of RCCs may be serendipitously discovered at imaging (5).
In this article, we review the 2004 World Health Organization (WHO) classification of RCC, describe the cytogenetics of RCC, present the imaging features of common and uncommon histologic subtypes of RCC, and discuss the effect of accurate histologic classification on prognosis and treatment of RCC.
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2004 WHO Classification of RCC
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RCC is now thought to be a clinicopathologically heterogeneous disease that can be classified into clear cell, papillary, chromophobe, collecting duct carcinoma, medullary carcinoma, and unclassified categories (1). Clear cell RCC is the most common adult RCC, representing 70% of all RCCs (6). Papillary RCC accounts for 10%–15%, chromophobe RCC for 4%–6%, collecting duct carcinoma for less than 1%, and unclassified lesions for 4%–5% of RCCs (1,6). Some RCCs undergo sarcomatoid dedifferentiation that is thought to represent the high-grade end of all subtypes (1). Histologic differentiation of most subtypes of RCC can be accomplished with hematoxylin-eosin staining techniques. The WHO classification of RCC is summarized in Table 1 (1).
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Cytogenetics of RCC
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Until recently, RCC was thought to represent a monomorphic disease arising from a probable common precursor cell but with protean histologic and clinicobiologic manifestations. Genetic characterization based on cytogenetics and molecular biology has established that different subtypes of RCCs are characterized by distinct genetic abnormalities and molecular signatures reflecting the differences in the cell type, biology, and underlying molecular mechanisms (7–9). Additional tumor metabolic pathways may explain the biologic diversity of RCC.
For example, up to 96% of clear cell RCCs are associated with 3p deletions including somatic inactivating mutations of the von Hippel–Lindau gene (7). Papillary RCC is frequently associated with trisomies of chromosomes 3, 7, 12, 16, 17, and 20 and loss of the Y chromosome (8). A subset of sporadic papillary RCC demonstrates c-MET mutations (10). Diagnosis of specific genotypes and their associated molecular events will assist in accurate characterization and management of RCC (8). Cytogenetic abnormalities associated with different histologic subtypes of RCC are summarized in Table 2. Accurate subtyping of RCC is critical for designing optimal treatment protocols for patients and predicting prognosis (6,8).
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Common and Uncommon Histologic Subtypes of RCC
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Clear Cell RCC
Previously referred to as conventional RCC, clear cell RCC is the most common histologic subtype, accounting for 70% of all RCCs (1). Clear cell RCC recapitulates the epithelium of the proximal convoluted tubules (11). The intracytoplasmic glycogen and lipids get dissolved during histologic processing, rendering the cells "clear" (1).
Lipid-rich cells in clear cell RCC impart the classic golden yellow color at gross pathologic analysis. Clear cell RCC appears heterogeneous with areas of necrosis and hemorrhage (1) (Fig 1). Clear cell RCC may exhibit a variety of histo-architectural patterns including solid, alveolar, and acinar forms (1) (Fig 2). A profuse network of small, thin-walled sinusoid-like blood vessels is a characteristic diagnostic feature (1).
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Figure 2. Photomicrograph (original magnification, x200; hematoxylin-eosin [H-E] stain) of a clear cell RCC shows clear cells (black arrow) with prominent cell borders and prominent vasculature (blue arrow).
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Imaging features reflect the variegated histologic findings of clear cell RCC. Clear cell RCC commonly appears heterogeneous at imaging due to the presence of hemorrhage, necrosis, and cysts. Clear cell RCC originates from the renal cortex and typically exhibits an expansile growth pattern. Multicentricity and bilaterality are rare (<5%) in sporadic cases (12).
Clear cell RCCs typically show hypervascularity on contrast-enhanced studies including computed tomography (CT), magnetic resonance (MR) imaging, and catheter angiography (Figs 3, 4) (13–17).
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Figure 3. Contrast-enhanced CT scan of a clear cell RCC shows an expansile, heterogeneously enhancing right renal mass (arrows) with associated hypervascular retroperitoneal lymphadenopathy (arrowheads).
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The tumor hypervascularity has been ascribed to inactivation of tumor suppressor genes (such as the von Hippel–Lindau gene) and subsequent elaboration of vascular and other growth factors (18). The degree of contrast enhancement may help distinguish clear cell RCC from non–clear cell variants (16,17). In a study that evaluated the helical CT findings of 76 clear cell RCCs, Kim et al (16) found that clear cell RCC showed enhancement of more than 84 HU in the corticomedullary phase and 44 HU in the excretory phase (with a specificity of 100% and 91%, respectively).
Clear cell RCC is hypo- to isointense on T1-weighted MR images and iso- to hyperintense on T2-weighted MR images (13,15). Lesions with microscopic lipid content show a conspicuous drop in signal intensity on images obtained at an opposed-phase echo time compared to in-phase gradient-echo images. Clear cell RCC may demonstrate considerable signal drop on opposed-phase MR images due to the presence of abundant microscopic fat (15,19). Cystic change is seen in up to 15% of cases (Fig 5). Calcification (sometimes ossification) is seen in 10%–15% of tumors (1).
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Figure 5. Contrast-enhanced CT scan obtained during the corticomedullary phase shows a predominantly cystic clear cell RCC (arrows) with peripheral solid, enhancing components (arrowheads).
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About half of all clear cell RCCs are stage 1 and 2 (1). Capsular or renal vein invasion is seen in up to 45% of tumors (20). The lungs (75%), liver (40%), bone (40%), soft tissues (34%), and pleura (31%) are common target sites of metastasis (1). Sarcomatoid change occurs in 5% of cases and portends a poor outcome.
Multilocular Cystic RCC
Multilocular cystic RCC, as the name suggests, is a multiseptated cystic RCC whose septa contain small clusters of clear cells (1). Multilocular cystic RCC is found in adults aged 20–76 years with a mean age of 51 years. Males predominate with a male-to-female ratio of 3:1.
Multilocular cystic RCC is characterized by septated, variable-sized cysts separated from the kidney by a fibrous capsule (1) (Fig 6). The cyst fluid may be serous or hemorrhagic. Histopathologic analysis demonstrates cysts lined by a monolayer of epithelial cells with clear cytoplasm (1) (Fig 7).
Multilocular cystic RCCs typically manifest as multilocular cystic tumors (Fig 8). Asymmetric septal thickening may be seen. Twenty percent of tumors show septal or wall calcification (1). Multilocular cystic RCC carries an excellent prognosis following nephrectomy. Recurrence and metastasis have not been reported (1), to our knowledge.
Papillary RCC
Papillary RCC (chromophil RCC) is the second most common histologic subtype, making up 10%–15% of RCCs (1). Tumor epithelium is reminiscent of the epithelium of the proximal convoluted tubules (11). Papillary RCC commonly affects end-stage kidneys (21).
Macroscopically, papillary RCCs often contain areas of hemorrhage, necrosis, and cystic degeneration (1) (Fig 9). Papillary RCC is histologically characterized by a predominantly papillary growth pattern (Fig 10). The tumor papilla consists of a fibrovascular core with stromal aggregates of foamy macrophages with cholesterol crystals (1). There are two histomorphologic subtypes of papillary RCC (1,22). While type 1 tumors are characterized by a monolayer of small cells with scanty cytoplasm, type 2 tumors contain high-nuclear-grade cells with abundant eosinophilic cytoplasm.
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Figure 10. Photomicrograph (original magnification, x100; H-E stain) of a type 1 papillary RCC shows a monolayer of small cytologically bland basophils growing along papillary fibrovascular cores (arrows).
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Papillary RCCs typically appear hypovascular and homogeneous on imaging studies (16,23,24) (Fig 11).
Papillary RCC typically shows lesser degrees of contrast enhancement than clear cell RCC at contrast-enhanced CT (16,23). Herts et al (23) have shown that the likelihood of papillary RCC is close to 50% when the tumor-to-aorta or tumor-to-kidney enhancement ratio is less than 0.25. Another important feature of papillary RCC is that bilateral and multifocal tumors are more common than in other subtypes of RCC (especially with hereditary syndromes) (11). Larger tumors show heterogeneity due to necrosis, hemorrhage, and calcification (Fig 12 ).
Although extremely rare, the presence of macroscopic fat (corresponding histologically to cholesterol-laden macrophages) is also a helpful feature (25). Cystic papillary RCCs demonstrate peripheral soft-tissue mural nodules that may enhance after intravenous contrast material administration. Papillary RCC commonly demonstrates low signal intensity on T2-weighted MR images possibly due to the presence of by-products of hemorrhage and necrosis (13) (Fig 13 ). Unlike clear cell RCC, papillary RCC demonstrates relative hypovascularity at catheter angiography. Sarcomatoid dedifferentiation may be seen in about 5% of cases (1).
Papillary RCC is typically low stage; approximately 70% of all papillary RCCs are intrarenal at presentation. Five-year survivals for type 1 and 2 tumors in all stages range from 49% to 84%. Type 1 papillary RCC is typically of lower stage and grade than type 2 tumors and is thus associated with a better prognosis (1,22).
Chromophobe RCC
Chromophobe RCC is the third most common histologic subtype, accounting for less than 5% of RCCs (1). Chromophobe RCC is postulated to differentiate toward type B intercalated cells of the cortical collecting duct (26). Chromophobe RCC shows a mean age of incidence in the 6th decade. Men and women are equally affected.
Macroscopically, chromophobe RCCs are well circumscribed, solid, tan-brown tumors with a mildly lobulated surface (Fig 14). Chromophobe RCC is histopathologically characterized by large polygonal cells with prominent cell membranes (Fig 15). In contradistinction to clear cell RCC, the tumor blood vessels are thick walled and eccentrically hyalinized (1). Diffuse cytoplasmic staining with Hale colloidal iron stain is a key diagnostic criterion.
Chromophobe RCC appears uniformly hyperechoic at ultrasonography (27). Despite their large size, chromophobe RCCs demonstrate relatively homogeneous enhancement at CT and MR imaging (27) (Fig 16). A spoke-wheel pattern of contrast enhancement classically associated with oncocytomas has recently been described in association with chromophobe RCC (28). It is interesting to note that oncocytomas and chromophobe RCCs share similar ontogenic features, histologic features (on hematoxylin-eosin–stained slides), and some imaging findings (11). Oncocytomas develop from type B intercalated cells of the cortical collecting duct and are indistinguishable from RCC on imaging studies. Chromophobe RCC may appear hypointense on T2-weighted MR images. At catheter angiography, chromophobe RCC is commonly hypovascular.
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Figure 16. Axial gadolinium-enhanced fat-saturated three-dimensional gradient-echo MR image of a chromophobe RCC shows a relatively hypovascular, expansile right renal mass with slightly heterogeneous enhancement (arrows).
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Eighty-six percent of chromophobe RCCs are stage 1 and 2 at presentation (1). Renal vein invasion is seen in less than 5% of cases. Despite the overall favorable prognosis, large tumors may develop hepatic metastases (29).
Collecting Duct Carcinoma
Collecting duct carcinoma of the kidney is a highly aggressive subtype of RCC that accounts for less than 1% of all malignant renal neoplasms. Origin from the medullary collecting duct is suggested by immunocytochemistry findings that are similar to principal cells of the collecting ducts of Bellini (1,11). Collecting duct carcinoma shows a male-to-female ratio of approximately 2:1. The age range is 13–83 years (mean age, 55 years).
Collecting duct carcinoma typically appears as a gray-white infiltrative neoplasm with its epicenter in the pelvicaliceal system (1). Collecting duct carcinoma is histologically characterized by a constellation of findings such as tubular or tubulopapillary growth pattern, presence of inflammatory or desmoplastic stroma, and mucin production (30) (Fig 17). Tubular epithelial dysplasia in the adjacent renal parenchyma is a characteristic histologic feature.
Collecting duct carcinoma is characterized by an infiltrative growth pattern at imaging. When small, the medullary epicenter of the tumor is evident (31). Larger neoplasms are indistinguishable from the more common RCC subtypes. Collecting duct carcinoma may be hyperechoic, isoechoic, or hypoechoic to renal parenchyma at sonography (31,32) (Fig 18). At CT and MR imaging, collecting duct carcinoma appears heterogeneous with areas of necrosis, hemorrhage, and calcification (Fig 19). Collecting duct carcinoma commonly shows low signal intensity on T2-weighted MR images and hypovascularity at catheter angiography (31,32).
Most collecting duct carcinomas are biologically aggressive neoplasms; one-third of patients have metastatic disease at presentation, and less than one-third of patients survive more than 2 years after diagnosis (1).
Renal Medullary Carcinoma
Renal medullary carcinoma, also referred to as the seventh sickle cell nephropathy, is an extremely rare malignant neoplasm occurring almost exclusively in patients with sickle cell trait (33). Renal medullary carcinoma is hypothesized to arise from medullary collecting ducts. Renal medullary carcinoma is almost always found in young patients; the typical age range is between 10 and 40 years (mean age, 22 years). The male-to-female ratio is 2:1.
Renal medullary carcinoma appears as an infiltrative, heterogeneous mass with a medullary epicenter (1,33). At histologic analysis, renal medullary carcinomas show sheets of poorly differentiated, mucin-producing eosinophilic cells associated with inflammatory, fibrous, or edematous stroma (Fig 20). Characteristic sickled erythrocytes are found in most tumors (33).
Renal medullary carcinoma manifests as an infiltrative, heterogeneous medullary neoplasm (31,34) (Fig 21). Hemorrhage and necrosis contribute to tumor heterogeneity. Renal medullary carcinoma is typically associated with caliectasis. Renal medullary carcinoma appears hypointense on T2-weighted MR images likely due to the presence of by-products of hemorrhage and necrosis. Tumors are typically hypovascular at catheter angiography (34).
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Figure 21. Contrast-enhanced CT scan of a renal medullary carcinoma shows a heterogeneously enhancing right renal mass (black arrow) with associated cystic retroperitoneal lymphadenopathy (white arrows).
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The prognosis is poor for renal medullary carcinomas, with a mean duration of survival of 15 weeks (1). Bimodal, lymphohematogenous metastases occur rapidly; the liver and lung are the most common target sites of metastasis.
Mucinous Tubular and Spindle Cell Carcinoma
Mucinous tubular and spindle cell carcinoma (MTSCC) is a low-grade polymorphic epithelial carcinoma associated with a favorable prognosis (1,35). As the name implies, the neoplasm exhibits mucinous tubular and spindle cell morphology. MTSCC is believed to arise from the loop of Henle (35).
MTSCC predominantly affects women; the male-to-female ratio is 1:4 (1). Most MTSCCs are found in asymptomatic patients. The mean age of patients is 53 years with an age range of 17–82 years. Macroscopically, MTSCCs are well-circumscribed, uniform tumors that appear gray or light tan. Histologically, MTSCC consists of tightly packed, elongated tubules separated by mucinous or myxomatous stroma. Chronic inflammation, foam cell deposits, and areas of necrosis are infrequently seen (1).
MTSCC was previously mistaken for sarcomatoid RCC and other renal sarcomas (1). Salient radiologic findings have not yet been described with this newly characterized histologic subtype of RCC. MTSCC is generally considered nonaggressive with a favorable prognosis (1).
Xp11.2 Translocation–TFE3 Gene Fusion Carcinoma
Xp11.2 translocation–TFE3 gene fusion carcinomas account for approximately 20% of RCCs in the pediatric and adolescent age group (36). Both translocations t(X;17)(p11.2;q25) and t(X;1)(p11.2;q21.2) result in overexpression of transcription factor E3 protein. Macroscopically, Xp translocation carcinomas are yellow-tan with areas of hemorrhage and necrosis (1). Xp11.2 translocation–TFE3 gene fusion carcinomas typically show prominent "voluminous" clear cytoplasm and partially papillary architecture (Fig 22). Hyaline nodules and psammoma bodies are commonly seen (1).
No specific imaging findings are yet described with Xp translocation carcinomas. Initial clinical data suggest an indolent clinical course despite advanced stage at presentation (1).
Neuroblastoma-associated RCC
Neuroblastoma-associated RCC is a unique histologic subtype of RCC that occurs in long-term survivors of pediatric neuroblastoma (1,37). It is believed that treatment for neuroblastoma may predispose to genetic changes responsible for RCC. Neuroblastoma-associated RCC accounts for 2.5% of RCC in young patients. It occurs several years after the diagnosis of neuroblastoma. Males and females are equally involved. The age range of patients with neuroblastoma-associated RCC is 2–35 years.
Neuroblastoma-associated RCCs appear histologically heterogeneous. Some tumors contain solid and papillary architecture with most cells containing abundant eosinophilic cytoplasm (1,37) (Fig 23). Imaging findings likely reflect histologic features. No specific radiologic findings have been described. The diagnosis may be suggested based on a history of treatment for neuroblastoma.
Hereditary RCC Syndromes
Hereditary RCC syndromes are characterized by early development of bilateral and multicentric renal neoplasms in both sexes with a family history of RCC (24). Specific syndromes are associated with development of a distinct histologic subtype of RCC. For example, clear cell RCC occurs in patients with von Hippel–Lindau syndrome, and Birt-Hogg-Dubé syndrome is predominantly associated with development of chromophobe RCC, hybrid (oncocytoma-chromophobe) neoplasms, and oncocytomas (24,38,39). A detailed discussion of hereditary RCC syndromes is beyond the scope of this article and is summarized in Table 3.
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Effect of Accurate Histologic Classification on Prognosis and Treatment
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Accurate histologic and imaging characterization of RCC is very important from prognostic and management perspectives (1,6,8). The differences in clinical behavior are likely related to differences in cytogenetic changes and molecular events associated with diverse histologic subtypes of RCC. It is well established that clear cell RCC is associated with a less favorable prognosis compared with papillary and chromophobe carcinoma (6,8). It is also well known that collecting duct carcinomas and renal medullary carcinomas are associated with aggressive clinical behavior and poor prognosis (1,30,31,34). Precise classification of RCC also allows institution of tailored treatment protocols. For example, diagnosis of meta-static non–clear-cell histology is critical from a management perspective, as it is associated with high resistance and poor response rates to interleukin-based therapy (40). Histologic and radiologic profiles of diverse subtypes of RCC can be used as biologic indicators of clinical behavior, response to treatment, and prognosis.
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Conclusion
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RCC consists of a heterogeneous group of malignant neoplasms that have characteristic histopathologic features, cytogenetic abnormalities, biologic behavior, and imaging findings.
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Footnotes
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Abbreviations: H-E = hematoxylin-eosin, MTSCC = mucinous tubular and spindle cell carcinoma, RCC = renal cell carcinoma, WHO = World Health Organization
See also the commentary by Choyke immediately following this article.
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Abstract
LEARNING OBJECTIVES FOR TEST...
