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European Urology
Volume 54, issue 6, pages 1209-1454, December 2008Reviews
Cystic Nephroma and Mixed Epithelial and Stromal Tumour of the Kidney: Opposite Ends of the Spectrum of the Same Entity?
Rodolfo Montironi a 
, Roberta Mazzucchelli a, Antonio Lopez-Beltran b, Guido Martignoni c, Liang Cheng d, Francesco Montorsi e, Marina Scarpelli a.
Accepted 22 October 2007, Published online 1 November 2007, pages 1237 - 1246
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Abstract
Objectives
The term “renal epithelial and stromal tumour” (REST) was proposed recently to encompass the spectrum of findings observed in cystic nephroma (CN) and mixed epithelial and stromal tumour (MEST) of the kidney. Our aim was to review the broad spectrum of usual and unusual clinical and morphologic findings observed in CN and MEST.
Methods
Based on Medline database searches, all aspects of CN and MEST were assessed.
Results
CN and MEST have a remarkable similarity in sex predilection, age distribution, and morphologic attributes of both the epithelial and stromal components and immunohistochemical profile, albeit with variation in individual categories, with higher prevalence of stromal-to-epithelial ratio, prominent ovarian-like stroma, smaller cysts, and stromal luteinisation in MEST, and large cysts, thin septa, and low stromal-to-epithelial ratio in CN. The stromal component in both lesions expresses estrogen and progesterone receptors. Rare and unusual morphologic features, such as endometrioid, cervical, and intestinal differentiation, and luteinised ovarian-like stroma, have been described in MEST. The epithelial element occasionally shows estrogen and progesterone receptors. Rare aggressive behaviour has been reported for both neoplasms.
Conclusions
Considerable overlap is apparent between the two lesions, which suggests that they may represent opposite ends of the spectrum of the same process. Even though an aggressive behaviour has been reported in very few cases, in general both neoplasms are considered benign and surgical excision is curative.
Keywords: Cystic nephroma, Mixed epithelial and stromal tumour of the kidney, Renal epithelial and stromal tumour, REST.
Article Outline
1. Introduction
The term “renal epithelial and stromal tumour” has been recently proposed to encompass cystic nephroma (CN) and mixed epithelial and stromal tumour (MEST) of the kidney [1].
CN is a rare benign mixed epithelial and stromal neoplasm whose diagnostic criteria were originally established by Joshi and Beckwith [2] for paediatric cases of cystic partially differentiated nephroblastoma and subsequently defined by Eble and Bonsib for adult cases [3]. It is a unilateral, solitary, multilocular lesion with epithelial-lined cysts, but no communication between cysts or between the cysts and the renal pelvis. Bilateral cases have been reported [4]. Presenting symptoms have been nonspecific: flank mass or haematuria; many neoplasms have been asymptomatic and found radiographically in the course of work-up for other conditions. CN presents after age 30 and shows an 8:1 female-to-male ratio. It has occurred with other neoplasms, such as angiomyolipoma [5], [6], and [7].
MEST is a rare complex renal neoplasm composed of a mixture of cystic and solid areas. It was originally described in 1993 by Pawade et al [8] as cystic hamartoma of the renal pelvis. The term “mixed epithelial and stromal tumour” of the kidney was proposed by Michal and Syrucek [9]. Other names such as adult mesoblastic nephroma, leiomyomatous renal hamartoma, solid and cystic biphasic tumour, and cystic hamartoma of the renal pelvis have been used. Presenting sings and symptoms include flank mass, flank pain, haematuria, or symptoms of urinary tract infection; 25% of tumours are found incidentally. The mean age of the patients with MEST is 46 yr, with a 6:1 predominance of women over men. Histories of estrogen therapy are common. In at least one male patient the diagnosis was made after he underwent hormonal treatment for prostate cancer [10].
The histogenesis of CN and MEST is unknown, and it has been proposed that both components of the tumour, stromal and epithelial, are neoplastic. It has also been suggested that MEST might be the renal counterpart of similar mixed epithelial and stromal neoplasms that occur in the biliary tract and pancreas [9]. The latter are also characterised by cystic structures lined by epithelium admixed with ovarian-like stroma.
CNs and MESTs do not show distinctive clinical features so they cannot be diagnosed before operation. There are no reports showing that such neoplasms can be distinguished with imaging techniques from other renal cystic and partially cystic lesions, including renal cell carcinoma. A greater awareness among urologists and radiologists of the morphologic features of CNs and MESTs could help them identify such lesions preoperatively, even with the aid of a needle biopsy, and plan the most appropriate type of renal surgery.
This paper reviews the broad spectrum of usual and unusual clinical and morphologic findings observed in CNs and MESTs.
2. Morphologic features
2.1. Macroscopy
CNs are encapsulated, well-demarcated tumours composed entirely of cysts and cyst septa [3]. No solid areas are present. The cysts contain serosanguinous fluid that can occasionally appear haemorrhagic. The lesions may be focal or replace the entire kidney. CNs commonly herniate into the renal sinus or may bulge from the convexity of the renal cortex. The tumours vary widely in size (mean = 9 cm).
MESTs often arise centrally in the kidney and grow as expansile masses, frequently herniating into the renal pelvic cavity. The tumours are typically composed of multiple cysts and solid areas [11], and [12]. The solid component is typically an off-white firm tissue, sometimes with a whorled texture, reminiscent of leiomyoma (Fig. 1). The tumours vary in size (mean = 6 cm).
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Fig. 1
Macroscopic appearance of a mixed epithelial and stromal tumour. It is composed of multiple cysts and solid areas. The solid component is an off-white firm tissue, reminiscent of leiomyoma.
Fig. 2 – Whole-mount section of a cystic nephroma. It is an encapsulated, well-demarcated tumour composed entirely of cysts and thin septa.
Fig. 3 – Microscopic appearance of a cystic nephroma. The cyst is lined by flattened hobnail epithelium. The septal stroma consists of fibrous tissue.
Fig. 4 – Whole-mount section of a mixed epithelial and stromal tumour. It is a well-demarcated tumour composed of large cysts, microcysts, and tubules and of cellular stroma (see Fig. 5).
Fig. 5 – Microscopic appearance of a mixed epithelial and stromal tumour. It includes microcysts and tubules and ovarian-like stroma.
Fig. 6 – The epithelial component of the cystic nephroma, similarly to mixed epithelial and stromal tumour, is intensely stained with antibodies against cytokeratins AE1/AE3.
Fig. 7 – The stromal cells in both cystic nephroma and mixed epithelial and stromal tumour are intensely positive for vimentin.
Fig. 8 – The stromal cells in both cystic nephroma and mixed epithelial and stromal tumour are positive for smooth muscle actin.
Fig. 9 – The epithelial cells are focally positive for calretinin. Scattered positive cells are seen in the stroma.
2.2. Microscopy
CNs are well demarcated from the surrounding kidney by a thick fibrous pseudocapsule (Fig. 2). The cysts contain clear or haemorrhagic fluid and range in size from microscopic to ≥5 cm. The cysts are lined by flattened, cuboidal, or hobnail epithelium (Fig. 3). Occasionally, the lining cells have clear cytoplasm. Mitotic figures are not found or are very rare. Many tumours have areas of cystic surface that lack epithelium. The septa are thin (typically <5 mm), translucent, and uniform and correspond to the outlines of the cysts. The septal stroma consists of fibrous tissue, which varies from myxoid to collagenous; occasionally it is cellular and has a wavy appearance resembling ovarian-like stroma. Skeletal muscle, fat, and smooth muscle have not been found in CNs. The septa of CNs often contain small cysts lined by bland cuboidal epithelial cells resembling renal tubules cut in cross-section. The septa may become calcified. Necrosis and haemorrhage are rare except when the tumour has herniated into the renal pelvis [1], [13], [14], [15], and [16].
MESTs are complex tumours composed of large cysts, microcysts, and tubules (Fig. 4). The largest cysts are lined by columnar and cuboidal epithelium that sometimes forms small papillary tufts. Urothelium, which may be hyperplastic, may also line some portion of the cysts. The microcysts and tubules are lined by flattened, cuboidal, or columnar cells. Their cytoplasm ranges from clear, to pale, to eosinophilic, or vacuolated. The architecture of the microcysts is varied and ranges from simple microcysts with abundant stroma between them to densely packed clusters of microcysts, to complex branching channels that may be dilated. These varied elements often are present intermingled in the same area of the tumour. The stroma consists of a variably cellular population of spindle cells with plump nuclei and abundant cytoplasm, that is, ovarian-like stroma (Fig. 5). Areas of myxoid stroma and fascicles of smooth muscle cells may be prominent. Densely collagenous stroma is common and fat is occasionally present [1], [10], [14], [17], [18], and [19].
3. Immunoprofile
CNs and MESTs have similar immunoprofiles [10], [15], [20], [21], and [22] (Table 1). Both show reactivity of the epithelial component with antibodies to cytokeratins (Fig. 6). In particular, both frequently react with cytokeratin 7. Focal positivity for high-molecular- weight cytokeratin (34βE12) has been also noted. The stromal component in both lesions expresses vimentin (Fig. 7), smooth muscle actin (Fig. 8), caldesmon, and desmin.
Table 1 Immunoprofile in the stromal components of cystic nephroma and mixed epithelial and stromal tumour*
| % of positive cases | ||
|---|---|---|
| Cystic nephroma | Mixed epithelial and stromal tumour | |
| Inhibin | 36% | 42% |
| Calretinin | 41% | 69% |
| CD10 | 50% | 77% |
| Estrogen receptors | 19% | 62% |
| Progesterone receptors | 40% | 85% |
*
In general, CD10, calretinin, inhibin, estrogen receptor (ER), and progesterone receptor (PR) expression are seen in both CNs and MESTs [22], and [23]. All markers are expressed in more cases and in greater proportion in the stromal component of MESTs with the staining being mostly localised in the ovarian-type stroma. A direct relationship between the presence of ovarian-type stroma and expression of ER, PR, calretinin, CD10, and inhibin is present.
CD10 exhibits focal strong cytoplasmic positivity in the stromal component of 40% of CNs and 71% of MESTs, with positive stromal cells being predominantly localised immediately surrounding the cysts and glands. These cells do not appear to correspond to luteinised cells, highlighted by the inhibin and the calretinin stains. Strong focal brush border staining can be seen in the epithelial component of CNs and MESTs. Normal glomeruli and proximal convoluted tubules are strongly positive for CD10 in the brush border and cytoplasm.
Calretinin staining shows strong focal nuclear and cytoplasmic staining of the stromal component in isolated cells and clusters of luteinised stromal cells in 35% of CNs and 64% MESTs [1]. In addition, very few MEST and CN cases show diffuse positivity for calretinin in the cytoplasm of the epithelial component, which is considered nonspecific (Fig. 9). The adjacent kidney parenchyma does not react with this antibody.
Inhibin highlights small clusters and scattered single cells in the stromal component, corresponding to luteinised cells, in 25% of CNs and 36% of MESTs [1]. The epithelial component of both tumours and normal kidney fail to express inhibin.
ER and PR are detected in the nuclei of the stromal cells of both CNs and MESTs; the staining is strong and especially prominent in the areas of ovarian-type stroma. The expression of PR is more extensive and is present in more cells than is ER [22], [23], and [24] (Figs. 10 and 11). The uninvolved kidney does not express sex steroid receptors.
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Fig. 10
Estrogen receptors are seen in the nuclei of the stromal cells of both cystic nephromas and mixed epithelial and stromal tumours.
Fig. 11 – Progesterone receptors are seen in the nuclei of the stromal cells of both cystic nephromas and mixed epithelial and stromal tumours. The expression of progesterone receptor is more extensive and is present in more cells than estrogen receptor (see Fig. 10 for comparison).
Fig. 12 – Mixed epithelial and stromal tumour with stroma composed of smooth muscle cells indistinguishable from a leiomyoma.
Fig. 13 – Same case as in Fig. 12. The stromal cells are positive for desmin.
Fig. 14 – Same case as in Fig. 12. The stromal cells are positive for caldesmon.
Fig. 15 – Mixed epithelial and stromal tumour in which the epithelial component shows areas of solid growth with intracytoplasmic small lumina.
Fig. 16 – Higher magnification of the same cases as in Fig. 15. The nuclei are enlarged and slightly irregular, with recognisable nucleoli.
Fig. 17 – Progesterone receptors are seen in the nuclei of the epithelial cells of a mixed epithelial and stromal tumour. Very few positive nuclei are seen in the stroma (Insert shows epithelial cells with estrogen receptors; same case as in Figs. 15 and 16).
Fig. 18 – Whole-mount section of a mixed epithelial and stromal tumour. The stroma is composed of dense collagen and is calcified (Insert shows epithelial lining with vacuolated cytoplasm).
Both CNs and MESTs fail to express HMB-45, melan-A, WT1, S-100, CD99, and Ulex.
4. Unusual features
Unusual morphologic features in the epithelial and stromal components of CNs and MESTs have been described. These include endometrioid [12], cervical, and intestinal differentiation of the epithelial component [25], as well as luteinised ovarian-like stroma [26] and stromal scarring interpreted as hyalinised scars left by ovarian corpora albicantia. Calretinin and α-inhibin have been described as strongly positive in cases with luteinised ovarian-like stroma. Occasionally the stroma is composed almost exclusively of smooth muscle cells without dysmorphic blood vessels to the point that the solid part of a MEST might become indistinguishable from a leiomyoma (Figs. 12–14).
An unusual immunohistochemical feature is represented by the presence of ERs and PRs in the epithelial component [1], and [27]. Recently we have seen a case with typical macroscopic and microscopic features of a MEST in a perimenopausal woman. The epithelial component showed areas of compact growth with small intracytoplasmic lumina, slight nuclear atypia with prominent nucleoli, and diffuse ER and PR expression (Figs. 15–17). The cell features of our case are similar to those mentioned by Turbiner et al [1] in three of their patients, who had focal areas with increased nuclear-to-cytoplasmic ratio, nuclear atypia, and prominent nucleoli and interpreted as reactive.
MESTs and CNs can undergo regressive changes, probably as a consequence of changes in the hormonal stimulation or blood supply. Focal regressive changes are included in most microscopic descriptions of these two tumours. In particular, the septa may be calcified in CNs, whereas foci of densely collagenous stroma are common and fat is occasionally present in MESTs. Recently we have seen a case with the macroscopic appearance of a MEST in a women 72 yr old. The stroma is composed of dense collagen, focally calcified, with scattered myxoid areas and small foci of adipose tissue. Only very tiny foci of ovarian-like stroma are identifiable. Some of the cysts are devoid of an epithelial lining, whereas others show a monolayered epithelium with vacuolated cytoplasm (Fig. 18). Our interpretation is that of a MEST with diffuse regressive changes.
5. Malignant transformation
CNs and MESTs behave as benign lesions. Reports asserting malignant behaviour in a few cases have been not always diagnostically convincing [3], [28], [29], [30], [31], [32], [33], and [34].
5.1. Sarcomatous transformation
Aggressive CN has been described as a sarcoma arising from CN, including undifferentiated sarcoma, leiomyosarcoma, rhabdomyosarcoma (ie, rhabdoid differentiation), pleomorphic sarcoma, and malignant mesenchymoma [3], and [28]. Recently, three patients with a MEST with a local recurrence of tumour with dismal clinical course have been described [29], and [30]. In at least two of them, the recurrent tumour was composed exclusively of malignant stromal component [29], [30], and [31].
5.2. Carcinomatous transformation
Clear-cell malignant transformation in CN has been mentioned by Jevremovic et al [32]. Omar et al [33] published a case of cystic renal cell carcinoma arising from multilocular cystic nephroma. A patient with MEST displaying malignant transformation to a sarcomatoid carcinoma with heterologous components was recently encountered by Shen et al [34].
6. Differential diagnoses
The differential diagnosis mainly includes cystic partially differentiated nephroblastoma, multilocular cystic renal cell carcinoma, angiomyolipoma with epithelial cysts, and synovial sarcoma. A full list of differential diagnoses is given in Table 2.
Table 2 Differential diagnoses
| • Cystic partially differentiated nephroblastoma |
| • Multilocular cystic renal cell carcinoma |
| • Angiomyolipoma with epithelial cysts |
| • Synovial sarcoma of the kidney |
| • Metanephric adenofibroma |
| • Renal cell carcinoma surrounded by angiomyolipoma |
| • Renal cell carcinoma associated with prominent angioleiomyoma-like proliferation |
| • Sarcomatoid carcinoma with heterologous elements |
| • Teratoma |
6.1. Cystic partially differentiated nephroblastoma
Rarely, Wilms tumour may be composed entirely of cysts with delicate septa. Such tumours are called “cystic partially differentiated nephroblastoma” [35], and [36]. This tumour occurs almost exclusively in children younger than 2 yr.
Cystic partially differentiated nephroblastomas often are large, ranging up to 180 mm in diameter. Cystic partially differentiated nephroblastoma is well circumscribed from the remaining kidney by a fibrous pseudocapsule and consists entirely of cysts of variable size. The septa are thin and there are no expansile nodules to alter the rounded contour of the cysts.
The cysts in cystic partially differentiated nephroblastoma are lined with flattened, cuboidal, or hobnail epithelium, or lack lining epithelium [36]. The septa are variably cellular and contain undifferentiated and differentiated mesenchyma, blastema, and nephroblastomatous epithelial elements [36]. Skeletal muscle and myxoid mesenchyma are present in the septa of most tumours. Cartilage and fat are present occasionally [2], and [37]. Focally, the septal elements may protrude into the cysts in microscopic papillary folds, or gross polyps in the papillonodular variant of cystic partially differentiated nephroblastoma. The epithelial components consist mainly of mature and immature microscopic cysts resembling cross-sections of tubules and stubby papillae resembling immature glomeruli.
The relationship between cystic partially differentiated nephroblastoma and CN is controversial, but the demographic differences between the two groups of patients indicate that although their gross appearances are similar, they are probably two different disorders [3], and [38].
6.2. Multilocular cystic renal cell carcinoma
The great majority of CNs occur in men >30 yr old. In this population, the most important differential diagnostic consideration is multilocular cystic renal cell carcinoma [39], [40], [41], [42], and [43]. This variant of clear-cell renal cell carcinoma contains microscopic clusters of epithelial cells with clear cytoplasm in some of the septa. Often the population of cells with clear cytoplasm is small so thorough sampling is important. Individually, these cells are identical to Fuhrman grade 1 and, less frequently, grade 2 clear-cell renal cell carcinoma [41], and [44]. Because histiocytes in the septa may be difficult to distinguish from the clear cells, immunohistochemistry for epithelial membrane antigen, cytokeratins, vimentin, or CD68 can be useful to confirm the nature of the cells.
6.3. Angiomyolipoma with epithelial cysts
Angiomyolipoma with epithelial cysts (AMLEC) is a recently described distinct cystic variant of angiomyolipoma (AML) [45], and [46]. Histologically, the tumour includes three components: epithelial cysts lined by cuboidal to hobnail cells, compact subepithelial müllerian-like AML stroma with admixed chronic inflammation, and muscle-predominant AML with dysmorphic blood vessels exterior to the subepithelial stroma. Immunohistochemically, the subepithelial stroma stains most intensely with HMB-45 and melan-A, whilst the muscle-predominant AML areas stain most intensely with smooth muscle actin and desmin. ER, PR, and CD10 stain most intensely in the subepithelial stroma. The epithelial cells in the cyst lining are positive for pancytokeratin, but negative for HMB-45, melan-A, ER, PR, and CD10.
6.4. Synovial sarcoma of the kidney
This is mostly a tumour of young adults, the age distribution paralleling that of soft tissue synovial sarcomas [47], and [48]. Most cases are cystic and multiple areas of haemorrhage and necrosis can be observed on macroscopic examination. Microscopically, tumour areas are characterised by mitotically active, monomorphic plump spindle cells with indistinct cell borders growing in short, intersecting fascicles or in solid sheets. Grossly identified cysts are lined by mitotically inactive polygonal eosinophilic cells with apically located nuclei (“hobnailed epithelium”). Areas of solid aggregation or fascicles of the tumour cells alternating with hypocellular myxoid tissues, together with areas displaying a prominent hemangiopericytoma-like pattern, may be found.
The tumour cells are consistently immunoreactive with vimentin, but desmin and muscle-specific actin stains, cytokeratins (AE1/AE3, or CAM 5.2), were uniformly negative in the tumour cells. Epithelial lining cells of the cysts are highlighted by the cytokeratins. Epithelial membrane antigen (EMA) is focally positive in some cases. The spindled tumour cells are variably immunoreactive for BCL2, Ulex, S-100, and CD99.
In contrast to soft tissue synovial sarcoma where the SYT-SSX1 gene fusion is more common than the alternative SYT-SSX2 form of the gene fusion, the majority of renal synovial sarcomas have so far demonstrated the SYT-SSX2 gene fusion [47], [48], [49], and [50].
Synovial sarcoma has to be considered in the differential diagnosis of CN and MEST when it shows paucicellular septa lined by hobnail epithelium. It is possible that at least some of the cases reported as sarcomatous transformation of CN are, in fact, synovial sarcomas.
Table 3 summarises the main morphologic and immunohistochemical features distinguishing CN and MEST from the other diagnostic entities to be considered in the differential diagnosis.
Table 3 Features distinguishing CN and MEST from the other diagnostic entities
| Ovarian-like stroma | Hobnail epithelium | Clear cells in the septa | Dysmorphic vessels | Blastema | Skeletal muscle | Vimentin positive epithelial cells | ER and PR | HMB45 and melan-A | WT1 | SYT-SSX2 gene fusion | |
|---|---|---|---|---|---|---|---|---|---|---|---|
| CN | + | + | − | − | − | − | − | + | − | − | − |
| MEST | + | + | − | − | − | − | − | + | − | − | − |
| CPDNB | − | − | − | − | + | + | − | − | − | + | − |
| MCRCC | − | − | + | − | − | − | + | − | − | − | − |
| AMLEC | − | − | − | + | − | − | − | + | + | − | − |
| SS | − | + | − | − | − | − | − | − | − | − | + |
CN = cystic nephroma; MEST = mixed epithelial and stroma tumour; CPDNB = cystic partially differentiated nephroblastoma; MCRCC = multilocular cystic renal cell carcinoma; AMLEC = angiomyolipoma with epithelial cysts; SS = synovial sarcoma.
7. Conclusions
•CNs and MESTs have similarities but they also show some differences. The similarities consist in sex predilection, age distribution, and some morphologic and immunohistochemical features, whereas the differences are based primarily on the degree of solid growth and the cellularity of the stroma.
•Rare and unusual morphologic features have been described.
•As for prognosis and treatment, even though an aggressive behaviour has been reported in very few cases, both neoplasms are benign and surgical excision is curative.
Conflicts of interest
The authors have nothing to disclose.
Appendix A.
The 18 figures were taken from four cases (one CN and three MESTs) seen in routine practice by one of the authors (R.M.). All these cases were discovered incidentally in women with a history of estrogen therapy, three perimenopausal women, and the fourth 80 yr old. The follow-up of these women was uneventful. These cases were circulated among the other authors of this paper and all agree on the diagnosis made originally when reported.
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Footnotes
a Section of Pathological Anatomy, Polytechnic University of the Marche Region, School of Medicine, United Hospitals, Ancona, Italy
b Department of Pathology, Reina Sofia University Hospital and Faculty of Medicine, Cordoba, Spain
c Section of Pathological Anatomy, University of Verona, School of Medicine, Verona, Italy
d Department of Pathology and Laboratory Medicine, Indiana University School of Medicine, Indianapolis, IN, USA
e Department of Urology, University Vita-Salute, Scientific Institute H San Raffaele, Milan, Italy
Corresponding author. Polytechnic University of the Marche Region, School of Medicine, United Hospitals, Via Conca 71, I–60020 Torrette, Ancona, Italy.
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