Abstract

We report a rare case of Bellini duct carcinoma, which is an unusual variant of renal cell carcinoma. The patient, a 56-year-old man, was admitted to our hospital for detailed examination of a renal mass on the left side. He had no clinical symptoms such as gross hematuria or flank pain. Abdominal ultrasonography, computed tomography and magnetic resonance imaging revealed a tumor 4 cm in diameter at the lower pole of the left kidney. Selective renal angiography showed an avascular mass lesion. We performed left transperitoneal radical nephrectomy with a preoperative diagnosis of left renal tumor, T2N0M0. The histopathological diagnosis was Bellini duct carcinoma of papillary tubular type. Lectin histochemistry demonstrated positive staining with soyabean agglutinin and peanut agglutinin. These findings supported our conclusion that the tumor might have originated from the Bellini duct epithelium. The patient currently remains disease-free. The pathogenesis and management of this rare condition are discussed.

Introduction

Renal cell carcinomas are usually recognized as epithelial cell tumors originating from the proximal tubules. However, recently developed techniques of lectin histochemistry have revealed an unusual variant of renal cell carcinoma, thought to originate from the collecting ducts of Bellini, as a new entity within the spectrum of renal cell carcinoma. As this Bellini duct carcinoma (BDC) sometimes has a progressive clinical course, analysis of its character and establishment of treatment modalities for this malignancy are essential. Here we present a rare case of BDC supported by the results of lectin histochemistry studies.

Case Report

A 56-year-old man was referred to our hospital in November 1994 for detailed examination of a left renal mass, which had been pointed out by a local physician who was treating the patient for acute myocardial infarction. The patient had no symptoms suggestive of urological diseases such as gross hematuria or flank pain. Laboratory examinations including urinary cytological examination revealed no abnormalities except for modest elevation of carcinoembryonic antigen and C-reactive protein levels. The results of intravenous pyelography were normal, but abdominal ultrasonography and dynamic CT demonstrated a solid mass 4 cm in diameter, which was not enhanced by contrast medium. Magnetic resonance imaging revealed a solid mass expanding from the renal medulla through the cortex at the lower pole of the left kidney. Selective renal angiography showed an avascular mass lesion. Systemic evaluation including chest CT and bone scintigraphy revealed no metastasis. The patient underwent transperitoneal radical nephrectomy on the left side with a preoperative diagnosis of renal tumor, T2N0M0. The resected kidney weighed 406 g and macroscopically showed a reddisbrown tumor 43 mm in diameter with partial necrosis surrounded by a thin fibrous capsule (Fig. 1). Microscopic examination revealed a prominent papillary structure, low-grade adenocarcinoma with cuboidal cells, eosinophilic cytoplasm and a hobnail appearance. The cells were similar to the collecting duct epithelium. The histopathological diagnosis was papillary-type BDC (Fig. 2). Lectin histochemistry using paraffin-embedded sections revealed positivity with soyabean agglutinin (SBA), peanut agglutinin (PNA) and wheatgerm agglutinin (WGA) (Fig. 3), suggesting that the tumor might have originated from the distal tubules or collecting ducts of Bellini. The postoperative clinical course was good, and the patient is currently alive and disease-free, 14 months after surgery.

Discussion

Bellini duct tumor is an unusual variant of renal cell carcinoma which has received some attention in the recent literature. The first report to indicate that the Bellini duct epithelium could give rise to tumors was that made by Mancilla-Jimenz (1), based on findings of atypical hyperplastic change in the collecting duct distant from a renal papillary tumor. Since Cromie (2) defined this rare disease, other investigators have subsequently considered its origin as being the collecting duct epithelium of Bellini. Fleming and Lewi (3) defined the diagnostic criteria and established collecting duct carcinoma of the kidney as a separate histological entity arising in the renal medulla. In the international classification of tumors by the World Health Organization (4), it has been grouped with renal cell carcinoma with the sub-designation ‘Bellini duct carcinoma’.

Figure 1

Macroscopic appearance of the resected kidney. A reddish-brown tumor 43 mm in diameter with partial necrosis is located at the lower pole of the kidney (arrow).

Figure 1

Macroscopic appearance of the resected kidney. A reddish-brown tumor 43 mm in diameter with partial necrosis is located at the lower pole of the kidney (arrow).

Previous reports have suggested that this tumor originates from the collecting duct epithelium, based on its location in the renal medulla, the histopathological features of the tumor cells and an architecture similar to that of the distal collecting tubules. Thoenes et al. (5) also reported a review of the cytomorphological typing of renal cell carcinomas in relation to the different parts and cell types of the nephron and collecting duct. BDC was divided into two histological types (6,7). The papillary type was grayish-white in color with a yellow tinge, and microscopically the tumor cells demonstrated an eosinophilic cytoplasm, nuclear polymorphism, distinct nucleoli with a papillary or tubulopapillary structure and a resemblance to the distal collecting duct epithelium (6–9). Therefore, if the tumor were small, it would be located in the renal medulla only as a nodular mass (8). On the other hand, the mixed type was grayish-white in color macroscopically, with microscopic features of tubulopapillary adenocarcinoma and areas of transitional cell differentiation (3,6,7,10). The tumor cells showed a ring-shaped arrangement mimicking the mesonephric duct.

Recently, histochemistry using lectins such as PNA, SBA and Dolichos biflorus agglutinin (DBA), and antibodies against cytokeratin (CK) and vimentin reactive with several portions of the normal renal tubule, several investigators have achieved differential diagnosis from common papillary renal cell carcinoma in a majority of cases. The binding sites for PNA and SBA which we employed in this study are located predominantly in the distal portion of the tubule, whereas those for WGA are located in all tubule segments (11). Our results with lectin histochemistry confirmed those of Fleming and Symes (12), Aizawa et al. (5), Kikuchi (13) and Kennedy et al. (14), who demonstrated positive staining with PNA, SBA, CK and/or DBA in tumors identified as BDC.

Figure 2

(a) Histological findings of BDC containing papillary fronds. (b) High-power view of BDC showing papillary fronds lined by cuboidal cells with large pleomorphic nuclei and eosinophilic cytoplasm. A hobnail appearance is evident.

Figure 2

(a) Histological findings of BDC containing papillary fronds. (b) High-power view of BDC showing papillary fronds lined by cuboidal cells with large pleomorphic nuclei and eosinophilic cytoplasm. A hobnail appearance is evident.

With regard to the incidence of BDC, Rumpelt et al. (15) found six BDCs (0.4%) among 1400 consecutive renal cell carcinomas. To our knowledge, there have been detailed clinical reports on 38 cases of BDC in Japan including the present case. While patients of all ages may be affected, most BDCs have occurred in young individuals, and there is a male predominance. Most cases reported previously (15,16) had a tendency for early dissemination and a fatal clinical course, as can be seen in Table 1. Of the 38 cases, the average age of the patients was 55 years (range 37–76), and the male:female ratio was 4.4:1. There was no predominant laterality of the affected side, 17 cases affecting the right kidney and 21 the left. The surgical method was nephrectomy in 28 cases, partial nephrectomy in two and nephroureterectomy in eight. Of the 29 cases for which the clinical outcome was reported, 14 (48%) of the patients died due directly to the tumor or its metastases. The site of metastasis was the lung in eight cases, lymph nodes in seven, bone in six, liver in five and skin in one. Nomura et al. (17) reported a patient with BDC who died from multiple metastatic lung lesions with rapid dissemination 4 months after resection of the tumor, which was classified histologically as mixed type. As can be seen in Table 1, although eight patients were treated with various combinations of chemotherapeutic agents, the outcome was fatal in five and progressive in two, with one exception presenting no further evidence of disease. Immunoactive agents such as interferon or interleukin, and combination chemotherapy for relapsed desease or metastatic lesions, usually seem to be ineffective (15,18).

Figure 3

Lectin histochemistry using (a) soyabean agglutinin, (b) peanut agglutinin, (c) wheatgerm agglutinin. All show a strongly positive reaction.

Figure 3

Lectin histochemistry using (a) soyabean agglutinin, (b) peanut agglutinin, (c) wheatgerm agglutinin. All show a strongly positive reaction.

In conclusion, BDC is a rare tumor with a clinically rapid and progressively malignant course. This makes it important to determine the origin of all renal tumors and to distinguish rare forms such as BDC from common types of renal cell carcinoma. Moreover, it is highly desirable that a modality of treatment be established for this malignancy. Detailed, long-term follow-up to detect local recurrence or distant metastasis is, of course, also necessary.

Acknowledgement

We thank Professor Eigoro Okajima, Department of Urology, Nara Medical University, for his critical review of the manuscript.

Abbreviations

  • BDC

    Bellini duct carcinoma

  • SBA

    soyabean agglutinin

  • PNA

    peanut agglutinin

  • WGA

    wheatgerm agglutinin

  • DBA

    Dolichos biflorus agglutinin

  • CK

    cytokeratin

References

1
Mancilla-Jimenez
R
Stanley
RJ
Blath
RA
Papillary renal cell carcinoma. A clinical, radiologic, and pathologic study of 34 cases
Cancer
 , 
1976
, vol. 
38
 (pg. 
2469
-
80
)
2
Cromie
WJ
Davis
CJ
DeTure
FA
Atypical carcinoma of kidney, possibly originating from collecting duct epithelium
Urology
 , 
1979
, vol. 
13
 (pg. 
315
-
7
)
3
Fleming
S
Lewi
HJE
Collecting duct carcinoma of the kidney
Histopathology
 , 
1986
, vol. 
10
 (pg. 
1131
-
41
)
4
Mostofi
FK
Sesterhenn
IA
Sobin
LH
International histologic classification of tumors
Histological typing of kidney tumours
 , 
1981
No. 25
Geneva
WHO
5
Thoenes
W
Störkel
S
Rumpelt
HJ
Moll
R
Cytomorphological typing of renal cell carcinoma - a new approach
Eur Urol
 , 
1990
, vol. 
18
 (pg. 
6
-
9
)
6
Aizawa
Sh
Kikuchi
Y
Suzuki
M
Furusato
M
Renal cell carcinoma of lower nephron origin
Acta Pathol Jpn
 , 
1987
, vol. 
37
 (pg. 
567
-
74
)
7
Gohji
K
Minayoshi
K
Higuchi
A
Fujii
A
Gotoh
A
A case of papillary renal cell carcinoma suggestive of Bellini duct origin
Acta Urol Jpn
 , 
1994
, vol. 
40
 (pg. 
329
-
32
)
8
O'Brien
PK
Bedard
YC
A papillary adenocarcinoma of the renal pelvis in a young girl. A light- and electron-microscopic study
Am J Clin Pathol
 , 
1980
, vol. 
73
 (pg. 
427
-
33
)
9
Lack
EE
Cassady
JR
Sallan
SE
Renal cell carcinoma in childhood and adolescence. A clinical and pathological study of 17 cases
J Urol
 , 
1985
, vol. 
133
 (pg. 
822
-
8
)
10
Hai
MA
Diaz-Perez
R
Atypical carcinoma of kidney originating from collecting duct epithelium
Urology
 , 
1982
, vol. 
14
 (pg. 
89
-
92
)
11
Fleming
S
Symes
CE
The distribution of cytokeratin antigens in the kidney and in renal tumours
Histopathology
 , 
1987
, vol. 
11
 (pg. 
157
-
70
)
12
Kikuchi
Y
Lectin and immunohistochemical studies on acquired cystic kidney and associated renal cell carcinoma
Acta Pathol Jpn
 , 
1989
, vol. 
39
 (pg. 
373
-
80
)
13
Kennedy
SM
Merino
MJ
Linehan
WM
Roberts
JR
Robertson
CN
Neumann
RD
Collecting duct carcinoma of the kidney
Hum Pathol
 , 
1990
, vol. 
21
 (pg. 
449
-
56
)
14
Rumpelt
HJ
Störkel
S
Moll
R
Schärfe
T
Thoenes
W
Bellini duct carcinoma:further evidence for this rare variant of renal cell carcinoma
Histopathology
 , 
1991
, vol. 
18
 (pg. 
115
-
22
)
15
Dimopoulos
MA
Logothetis
CJ
Markowitz
A
Sella
A
Amato
R
Ro
J
Collecting duct carcinoma of the kidney
Br J Urol
 , 
1993
, vol. 
71
 (pg. 
388
-
91
)
16
Nomura
M
Nagaoka
A
Ueno
Y
Mitsuno
S
Sugita
A
Haratake
J
, et al.  . 
Bellini duct carcinoma: a case report
Nishinihon Hinyokika
 , 
1994
, vol. 
56
 (pg. 
1078
-
81
(in Japanese)
17
Carter
MD
Tha
S
McLoughlin
MG
Owen
DA
Collecting duct carcinoma of the kidney: a case report and review of the literature
J Urol
 , 
1992
, vol. 
147
 (pg. 
1096
-
8
)
18
Sekido
N
Hinotsu
S
Kawai
K
Matsuki
K
Akaza
H
Koiso
K
Bellini duct carcinoma accompanied by hemorrhagic renal cyst: a case report and review of the literature
Nishinihon Hinyokika
 , 
1995
, vol. 
57
 (pg. 
515
-
8
(in Japanese)