Multilocular Cystic Renal Cell Carcinoma A Report of 45 Cases of a Kidney Tumor of Low Malignant Potential
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1 Anatomic Pathology / MULTILOCULAR CYSTIC RENAL CELL CARCINOMA Multilocular Cystic Renal Cell Carcinoma A Report of 45 Cases of a Kidney Tumor of Low Malignant Potential Sueli Suzigan, MD, 1 Antonio López-Beltrán, MD, PhD, 2 Rodolfo Montironi, MD, FRCPath, 3 Ricardo Drut, MD, 4 Ana Romero, MD, 2 Tomayoshi Hayashi, MD, 5 Ana L.C. Gentili, MD, 6 Paulo S.P. Fonseca, MD, 7 Ines detorres, MD, 8 Athanase Billis, MD, 9 Lucia C. Japp, MD, 10 Enrico Bollito, MD, 11 Ferran Algaba, MD, 12 and Maria J. Requena-Tapias, MD 13 Key Words: Cystic renal cell carcinoma; Multilocular cystic carcinoma; Clear cell renal cell carcinoma; Low-grade cystic carcinoma Abstract The 2004 World Health Organization (WHO) classification of kidney tumors recognizes multilocular cystic renal cell carcinoma (MCRCC) as a rare variant of clear cell renal cell carcinoma with a good prognosis. Available information on its clinical significance is limited. The study cohort included 45 MCRCC cases classified according to 2004 WHO criteria obtained through a multi-institutional international search. Most patients had unilateral MCRCC with no side predominance that was found incidentally; 62% were men, but women had tumors at an earlier age (P =.385). MCRCC occurred slightly more often in men than in women (1.7:1). At diagnosis, 82% of patients had stage T1 and 16%, stage T2; 1 patient had stage T3. The Fuhrman grade was 1 (62%) or 2 (38%), with smaller tumors ( 4 cm) most likely Fuhrman grade 1 (P =.911). All 45 patients were alive with no evidence of disease at mean follow-up of 66.1 months, confirming an extremely good prognosis after surgery and a 5-year disease-specific survival rate of 100%. To rename this tumor as multilocular cystic renal cell neoplasm of low malignant potential might help urologists approach the patients conservatively. Multilocular cystic renal cell carcinoma (MCRCC), also known as multilocular clear cell renal cell carcinoma (RCC) and multicystic clear cell carcinoma, is a rare cystic tumor of the kidney with an excellent outcome. 1-7 Diagnostic criteria for MCRCC were defined by the 2004 World Health Organization (WHO) classification of kidney tumors based on previous reports and the suggestions of Eble and Bonsib. 1,8 The true incidence is unknown because no strict criteria were defined previously. Some reports suggest that cystic renal cell carcinomas (crcc, a category including MCRCC, unilocular cystic RCC, RCC with extensive cystic necrosis, and cystic RCC characterized by a unilocular cyst with one or a few isolated mural tumor nodules) might represent 3% to 14% of RCC Studies have focused on unilocular and multilocular crcc with variable proportions of a solid clear cell component but usually with no more than 25% and no evidence of tumor necrosis. 2-6 Although each of these studies reported that patients with crcc had a better prognosis than patients with solid clear cell RCC, some concern persists about the true clinical significance of the diagnosis of MCRCC in a given patient and its malignant potential. 9 This is in part because of the lack of reports on large series of cases defined according to the more restrictive 2004 WHO criteria. MCRCC is considered a distinct subtype of clear cell RCC in the 2004 WHO classification based on the characteristic gross features with a multilocular cystic appearance and a variegated, yellowish solid component limited to small areas with no expansive nodules or necrosis. 1,18-27 Histologic examination reveals cysts lined by occasionally flattened cuboidal clear cells and septa that contain aggregates of epithelial cells with clear cytoplasm; tumors usually are Fuhrman grade 1. 1 Because there is little difference between nuclear grades 1 and Downloaded from Am J Clin Pathol 2006;125:
2 Suzigan et al / MULTILOCULAR CYSTIC RENAL CELL CARCINOMA 2 in conventional clear cell RCC in terms of outcome, we found a reasonable expansion of the criteria to include lowgrade tumors (Fuhrman grade 1 or 2). An important issue is the differential diagnosis of MCRCC, which in adults includes multicystic kidney, segmental cystic disease, cystic nephroma, and other crccs, including cystic necrosis in RCC (pseudocystic necrotic carcinoma). 9,17,28-32 The difficulties of differential diagnosis might be responsible as a confounding factor for the variable outcome observed in some series in which other crccs are incorporated into the analysis in addition to true MCRCC; therefore, some controversy exists in the literature concerning its malignant potential. Likewise, the recent finding of VHL gene mutations in MCRCC supports its classification as a type of clear cell RCC. 32 This article reports the clinical and pathologic findings in a series of 45 cases of MCRCC diagnosed according to the 2004 WHO criteria to better define their clinical significance. Materials and Methods For this retrospective, observational study, the sample series was obtained through an international and multi-institutional search including centers from Brazil, Argentina, Japan, Spain, and Italy. Surgical pathology files of the participating institutions were reviewed from January 1987 to December 2004, and cases of MCRCC that met the inclusion criteria were obtained; this included meeting the 2004 WHO 1 diagnostic criteria Table 1 and available follow-up data. Clinical and demographic information obtained through the hospital records included clinical manifestations, treatment, and follow-up. Gross features were recorded in each case from pathology reports and photographs of the gross specimens. Pathologic evaluation consisted of reassessing all original histologic material by at least 3 dedicated pathologists (S.S., A.L.B., and I.T.) blinded to the clinical outcomes of the patients. Nuclear grade was determined according to the Fuhrman system, and tumor stage was assessed according to Table 1 Main Pathologic Features of Multilocular Cystic Renal Cell Carcinoma According to the 2004 World Health Organization Classification of Kidney Tumors 1 Gross features Multilocular cystic appearance and encapsulated Yellowish solid component limited to small areas No expansive nodules Tumor necrosis absent Microscopic features Cysts lined by cuboidal clear cells or flattened epithelium Septa containing aggregates of epithelial cells with clear cytoplasm Low Fuhrman grade the 2002 revision of the TNM system. 33 Tumor size was measured according to the longest diameter. Radiologic and operative surgical information and pathology reports were used to assess the extent of disease. The end point of the study was disease-specific survival determined from the date of nephrectomy to the date of last follow-up. In addition to descriptive statistics, bivariate and multivariate analysis was undertaken using contingency table methods and tested for significance by using the Fisher exact test and χ 2 analysis. All statistical analysis was performed using SPSS for Windows software (SPSS, Chicago, IL). A P value of.05 or less was considered indicative of a statistically significant difference. All were 2-sided tests. Results Table 2 shows the clinical and pathologic variables of the 45 cases that met gross and microscopic criteria for MCRCC Image 1. 1 The mean age at diagnosis was 54.3 years (range, years). There were 28 men (62%) with a mean age of 56.3 years (range, years), and 17 (38%) women (mean age, 51.1 years; range, years); 50% of the patients were 52 years old or younger Figure 1. MCRCC occurred slightly more often in men than in women (1.7:1), and it was found incidentally during evaluation for an unrelated condition in 51% of the cases. All cases except 1 were unilateral at diagnosis, and in 22 patients (49%), the tumor was in the left kidney (P =.794). Two patients had multifocal tumors and 1 patient had bilateral MCRCC. Tumor size was similar in men and women (mean, 4.9 cm; range, 1-14 cm), but the tumors occurred at a somewhat earlier age in women (P =.385; Figure 1). In 25 patients (56%), the tumors were smaller than 4 cm (Figure 1). A total of 28 cases (women, 11 [65%]; men, 17 [61%]) were Fuhrman grade 1, and 17 (women, 6 [35%]; men, 11 [39%]) were Fuhrman grade 2 (P =.173). Of the tumors smaller than 4 cm, 68% were Fuhrman grade 1 (Figure 1; P =.911). Of the 45 patients, 24 (53%) had stage T1a, 13 (29%) had stage T1b, 7 (16%) had stage T2, and 1 (2%) had stage T3a disease (renal sinus fat involvement) (P =.186); smaller tumors ( 4 cm) were most likely Fuhrman grade 1 (P =.911). None of the patients had Fuhrman grade 3 or 4, stage T4, renal vein neoplastic thrombus, or metastatic disease at diagnosis; all cases were N0 M0. All patients were alive with no evidence of recurrent disease at a mean follow-up of 66.1 months (range, 1 month to 17.9 years; Figure 1). The Fuhrman grade and TNM stage were unrelated to clinical variables included in the analysis (tumor size, age at diagnosis, sex, side of tumor location, and TNM stage; P >.05). Table 2 shows a comparison of the main findings in our case series with those in other series reported in the literature. 218 Am J Clin Pathol 2006;125: Downloaded 218 from
3 Anatomic Pathology / ORIGINAL ARTICLE Table 2 Main Clinical and Pathologic Findings in Recent Series of MCRCC * Fuhrman Grade (%) Stage (%) Mean Right-Sided Incidental NED at Age Male Tumors Presentation Mean Follow- Study (y) (%) (%) (%) T1 T2 T3 Size (cm) up (%) Corica et al, (n = 24) Nassir et al, (n = 12) Murad et al, (n = 6) Brinker et al, (n = 7) Present study, 2005 (n = 45) MCRCC, multilocular cystic renal cell carcinoma; NED, no evidence of disease. * None of the reported cases in these series had Fuhrman grade 4, stage T4, renal vein thrombus, or metastatic disease at diagnosis. Corica et al 3 and Nassir et al 5 included cases with less than 25% solid growth as their criteria for MCRCC; Murad et al 26 accepted cases with less than 10% solid growth. Brinker et al 30 and the present series followed more strict criteria as recommended by the 2004 World Health Organization classification of kidney tumors, accepting cases with no grossly visible expansive nodules (see the text). A B C D Image 1 (Case 32) A, Gross presentation in a case of multilocular cystic renal cell carcinoma. B and C, Histologic examination revealed thin septa lined up by cuboidal clear cells (B) with small groups of cells forming solid areas in the septum (C) (B and C, H&E, 200). D, Tumor cells show low Fuhrman grade (H&E, 400). Downloaded from Am J Clin Pathol 2006;125:
4 Suzigan et al / MULTILOCULAR CYSTIC RENAL CELL CARCINOMA A B No. of Cases No. of Cases C Men Women Age (y) <4 >4 to 7 >7 Tumor Size (cm) F1 F2 No. of Cases Follow-up (y) Figure 1 Age vs sex (A), follow-up (B), and Fuhrman grade vs tumor size (C) in 45 cases of multilocular cystic renal cell carcinoma. Discussion MCRCC is considered a distinct subtype of clear cell RCC in the 2004 WHO classification based on the characteristic gross and microscopic features. 1 No tumor with these features has ever recurred or metastasized. 1,13 Therefore, the use of these somewhat more restrictive criteria should be adopted in daily practice. Low Fuhrman grade and stage are characteristic features of MCRCC, with only rare cases considered to be stage T3, 3 as seen in our series including 1 stage T3 case and other reported series such that by Corica et al 3 that included 12.5% of cases in stage T3. In their series, 92% of patients had no evidence of disease at a mean follow-up of 77.6 months (Table 2), in contrast with our series, in which 100% of patients were alive without evidence of disease at a mean follow-up of 66.1 months. This minor finding of aggressiveness in the report by Corica et al 3 might be related to the criteria for accepting cases in their study because cases of MCRCC with up to 25% solid nodules were included. This criterion was modified in the 2004 WHO classification, and solid expansive nodules are no longer accepted for the diagnosis of MCRCC. 1 In fact, a recent series of 12 cases of MCRCC by Nassir et al 5 showed patients with no evidence of disease at a mean follow-up of 42.5 months, confirming our results on the excellent prognosis of MCRCC with no solid component. A notable difference between MCRCC and conventional RCC is the absence of nodal or metastatic spread at diagnosis in MCRCC. 9,14,17,31 According to most authors, it seems that in general, crcc has a better outcome than noncystic conventional RCC. 15,31 Evidence supporting this includes that crcc in general is of low Fuhrman grade and stage at diagnosis and the mean tumor size is less than 5 cm, compared with 7.4 cm in the recent study by Han et al. 31 Because at diagnosis crccs tend to be smaller tumors and have a lower T stage and nuclear grade, these lesions may be more amenable to nephron-sparing surgery. 2,31 This seems to be particularly agreeable in MCRCC, which seems to be the end of the spectrum of crccs composed exclusively of cysts and showing an excellent outcome. In these cases, the clear cell component is limited to small aggregates within the septa. All cases in our series and most reported cases of MCRCC were N0 M0 at diagnosis, further suggesting a tumor of low malignant potential. 1-7,17,31 A number of reasons might help explain the improved outcome for predominantly crcc: (1) Compared with solid RCC these MCRCCs contain fewer malignant cells, which seem to be proliferating at a slower rate, as shown in our cases by the observed very low mitotic rate. (2) The majority of these tumors are Fuhrman grade 1 or 2, a finding that carries a better prognosis by itself. To our knowledge, our study reports the largest series of MCRCCs in the English literature that incorporated the recent 2004 WHO diagnostic criteria. 220 Am J Clin Pathol 2006;125: Downloaded 220 from
5 Anatomic Pathology / ORIGINAL ARTICLE Although somewhat limited by the relatively small number of patients and short follow-up, it allows confirmation that the 5- year disease-related survival is excellent for patients with MCRCC. Our results indicate that MCRCC is an important subtype of crcc that can be cured by surgical resection. 1 Of our patients, 100% had no evidence of disease at a mean of about 66.1 months after surgery. Patient outcome was not affected adversely by large tumor size or advanced stage that was observed occasionally in our cases. Thus, patients with MCRCC might benefit from nephron-sparing surgery. Owing to the limited available follow-up in our series and in other reported series, it remains to be proven whether the excellent 5- year outcome observed in MCRCC persists in a longer followup period. It is our belief that MCRCC should be renamed and reclassified to indicate the most probably benign nature of this tumor. Multilocular cystic renal cell neoplasm of low malignant potential seems to be an appropriate term for this lesion. From the 1 Laborclin Laboratory, São José do Rio Prêto, Brazil; 2 Unit of Anatomic Pathology, Cordoba University Medical School and Reina Sofia University Hospital, Cordoba, Spain; 3 Institute of Pathological Anatomy and Histopathology, Polytechnic University of the Marche Region, Ancona, Italy; 4 Pathology Service, Sor María Ludovica Children s Hospital, La Plata, Argentina; 5 Department of Pathology, Nagasaki University Hospital, Nagasaki, Japan; 6 Lins Laboratory of Histopathology and Cytopathology, Lins, Brazil; 7 Anápolis Center for Anatomic Pathology and Cytopathology, Anápolis, Brazil; 8 Pathology Service, Val d Hebron University Hospital, Barcelona, Spain; 9 Department of Pathology, Unicamp, Campinas, Brazil; 10 Department of Pathology, Sarah Hospital, Brasília, Brazil; 11 Department of Pathology, San Luigi Gonzaga Hospital, Turin, Italy; 12 Department of Pathology, Puigvert Foundation and Department of Morphology, Autonomous University, Barcelona, Spain; and 13 Urology Service, Reina Sofia University Hospital, Cordoba, Spain. Supported by grant FIS 03/0952 from the Ministry of Health, Madrid, Spain. Presented in part at the Sixth Latin American Virtual Congress of Anatomic Pathology, Burgos, Spain, March 1, Address correspondence to Dr López-Beltrán: Unit of Anatomical Pathology, Faculty of Medicine, Avda. Menendez Pidal s/n, E-14004, Cordoba. Spain. None of the 45 cases of MCRCC reported in this article have been published in the English literature. References 1. Eble JN. Multilocular cystic renal cell carcinoma. In: Eble JN, Sauter G, Epstein JI, et al, eds. Pathology and Genetics of Tumours of the Urinary System and Male Genital Organs. Lyon, France: IARC Press; World Health Organization Classification of Tumours. 2. Bloom TL, Gray-Sears CL, Williams TR, et al. Multilocular cystic renal cell carcinoma with osseous metaplasia in a 25- year-old woman. Urology. 2003;61: Corica FA, Iczkowski KA, Cheng L, et al. Cystic renal cell carcinoma is cured by resection: a study of 24 cases with longterm followup. J Urol. 1999;161: Murphy WM, Grignon DJ, Perlman EJ. Tumors of the Kidney, Bladder, and Related Urinary Structures. Washington, DC: American Registry of Pathology; 2004: AFIP Atlas of Tumor Pathology; Fourth Series, Fascicle Nassir A, Jollimore J, Gupta R, et al. Multilocular cystic renal cell carcinoma: a series of 12 cases and review of the literature. Urology. 2002;60: Bielsa O, Lloreta J, Gelabert-Mas A. Cystic renal cell carcinoma: pathological features, survival and implications for treatment. J Urol. 1998;82: Koga S, Nishikido M, Hayashy T, et al. Outcome of surgery in cystic renal cell carcinoma. Urology. 2000;56: Eble JN, Bonsib SM. Extensively cystic renal neoplasms: cystic nephroma, cystic partially differentiated nephroblastoma, multilocular cystic renal cell carcinoma and cystic hamartoma of renal pelvis. Semin Diagn Pathol. 1998;15: Truong LD, Choi YJ, Shen SS, et al. Renal cystic neoplasms and renal neoplasms associated with cystic renal disease: pathogenetic and molecular links. Adv Anat Pathol. 2003;10: Kim JC, Kim KH, Lee JW. CT and US findings of multilocular cystic renal cell carcinoma. Korean J Radiol. 2000;1: Tosaka A, Yoshida K, Kobayashi N, et al. A report of two cases of multilocular cystic renal cell carcinoma: review of 51 cases reported and the results of a prognostic survey [in Japanese]. Hinyokika Kiyo. 1992;38: Agrons GA, Wagner BJ, Davidson AJ, et al. Multilocular cystic renal tumor in children: radiologic-pathologic correlation. Radiographics. 1995;15: Lopez-Beltran A, Scarpelli M, Montironi R WHO classification of the renal tumours of the adults. Eur Urol. In press. 14. Fuhrman SA, Lasky LC, Limas C. Prognostic significance of morphologic parameters in renal cell carcinoma. Am J Surg Pathol. 1982;6: Bostwick DG, Eble JN. Diagnosis and classification of renal cell carcinoma. Urol Clin North Am. 1999;26: Suzigan S, Müller MEA, Lima WS, et al. Brazilian primary renal tumors: clinical and pathological review of 137 cases with emphasis on renal cortical epithelial neoplasms. Available at 2001; COMUNICACION-E/002/index.htm. Accessed March 1, Sakurai M, Sugimura Y, Satani H, et al. Multilocular cystic renal cell carcinoma: a report of two cases [in Japanese]. Hinyokika Kiyo. 1993;39: Desligneres S. Clear cell unilocular and multilocular cystic renal tumors and in situ clear cell intratubular carcinoma. J Urol. 1993;99: Geller E, Smergel EM, Lowry PA. Renal neoplasms of childhood. Radiol Clin North Am. 1997;35: Castillo OA, Boyle ET Jr, Kramer SA. Multilocular cysts of kidney: a study of 29 patients and review of literature. Urology. 1991;37: Levy P, Helenon O, Merran S, et al. Cystic tumors of the kidney in adults: radio-histopathologic correlations. J Radiol. 1999;80: Taxy JB, Fray F, Marshall FF. 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6 Suzigan et al / MULTILOCULAR CYSTIC RENAL CELL CARCINOMA 23. Takeuchi T, Tanaka T, Tokuyama H, et al. Multilocular cystic renal adenocarcinoma: a case report and review of the literature. J Surg Oncol. 1984;25: Laperriere J, Filion R, Houde M, et al. Renal cell carcinoma presenting as multilocular cystic mass. Urology. 1986;28: Sherman ME, Silverman ML, Balogh K, et al. Multilocular renal cyst: a hamartoma with potential for neoplastic transformation? Arch Pathol Lab Med. 1987;111: Murad T, Komaiko W, Oyasu R, et al. Multilocular cystic renal cell carcinoma. Am J Clin Pathol. 1991;95: Koga S, Yamasaki A, Nishikido M, et al. Multiloculated renal cell carcinoma. Int Urol Nephrol. 1991;23: Yamamoto H, Maruyama T, Kuwae H, et al. Bilateral multilocular cystic renal cell carcinoma: a case report [in Japanese]. Hinyokika Kiyo. 1996;42: Ooi GC, Sagar G, Lynch D, et al. Cystic renal cell carcinoma: radiological features and clinico-pathological correlation. Clin Radiol. 1996;51: Brinker DA, Amin MB, De Peralta-Venturina M, et al. Extensively necrotic cystic renal cell carcinoma. Am J Surg Pathol. 2000;24: Han K, Janzen NK, McWhorter VC, et al. Cystic renal cell carcinoma: biology and clinical behavior. Urol Oncol. 2004;22: Grignon DJ, Bismar TA, Bianco F, et al. VHL gene mutations in multilocular cystic renal cell carcinoma: evidence in support of its classification as a type of clear cell renal cell carcinoma [abstract]. Mod Pathol. 2004;17(suppl 1):154A. 33. Greene FL, Page DL, Fleming ID, et al (American Joint Committee on Cancer). AJCC Cancer Staging Manual. 6th ed. New York, NY: Springer; Am J Clin Pathol 2006;125: Downloaded 222 from
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