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Upper Tract Urothelial Carcinoma: a Clinicopathologic Study Including Upper Tract Urothelial Carcinoma: A Clinicopathologic Study Including Microsatellite Instability Analysis Hagen Blaszyk, M.D., Linan Wang, M.D., Wolfgang Dietmaier, Ph.D., Ferdinand Hofstädter, M.D., Lawrence J. Burgart, M.D., John C. Cheville, M.D., Arndt Hartmann, M.D. Department of Laboratory Medicine and Pathology, Mayo Clinic and Foundation, Rochester, Minnesota (HB, LW, LJB, JCC); and Institute of Pathology, University of Regensburg, Regensburg, Germany (HB, WD, FH, AH) yposis colorectal cancer syndrome in some patients. Urothelial carcinoma of the renal pelvis and ureter These findings reinforce the importance of obtain- may develop as a manifestation of the hereditary ing cancer histories in patients with upper tract nonpolyposis colorectal cancer syndrome that is urothelial carcinoma to subsequently identify indi- characterized by mutations in a number of DNA viduals with the hereditary nonpolyposis colorectal mismatch repair genes and detectable as microsat- cancer syndrome and at-risk relatives for surveil- ellite instability. In this study, we examined micro- lance and management programs. satellite instability and the clinicopathologic fea- tures of urothelial carcinoma of the renal pelvis (n KEY WORDS: Family history, HNPCC, Microsatel- from 114 consecutive lites, Renal pelvis, Smoking, Ureter, Urothelial (53 ؍ and ureter (n (61 ؍ patients surgically treated from 1985–1992. Clinical carcinoma, data were obtained through chart review. Matched Mod Pathol 2002;15(8):790–797 normal and tumor DNA was extracted from paraffin-embedded tissue, and a panel of six micro- Urothelial carcinoma of the upper urinary tract (re- satellite loci was analyzed. The male–female ratio nal pelvis and ureter) is relatively uncommon, rep- was 2.8:1 with a median age of 70 years (range, 28 to resenting 5% of all urothelial cancers. During the 92 y). Microsatellite analysis was successful in 67 last two decades, the incidence of renal pelvic tu- tumors, and 21 (31.3%) patients had tumors that mors has remained stable, although there has been exhibited microsatellite instability. Patients with a slight increase in the incidence of ureteral cancer microsatellite-unstable tumors were significantly (1). Recently, the distribution of upper tract urothe- more likely to have additional nonurologic cancers lial carcinomas in the population has shifted to ؍ ؍ (P .015) including colorectal carcinoma (P .001) older patients, females, and non-white individuals. compared with patients with tumors that did not Similar to bladder carcinoma, smoking and occupa- exhibit microsatellite instability. In addition, pa- tional exposure to arylamines are well-established tients with microsatellite-unstable tumors showed risk factors for upper tract urothelial carcinoma ac- ؍ more colorectal cancers in their family (P .026) counting for the majority of cases (2). There are also and were more likely to have higher grade urothe- unusual exogenous carcinogenic factors unique to the ؍ lial carcinoma of the upper tract (P .028). Grade upper urothelial tract, including analgesic nephropa- and stage, but not microsatellite status, were the thy (3, 4) and Balkan nephropathy (5, 6). The 5-year strongest predictors of cancer-specific survival. This cancer-specific survival for upper tract urothelial car- study found the highest frequency of microsatellite cinoma in the United States approaches 75%, and instability in upper urothelial tract carcinomas re- stage and grade are the most powerful predictors of ported to date and highlights upper tract urothelial survival (1). Nephroureterectomy with excision of the carcinoma as a marker of the hereditary nonpol- ipsilateral ureteral orifice and bladder cuff en bloc is the standard treatment, and conservative manage- ment has evolved through the necessity for renal Copyright © 2002 by The United States and Canadian Academy of Pathology, Inc. preservation in some patients, particularly those with VOL. 15, NO. 8, P. 790, 2002 Printed in the U.S.A. Date of acceptance: May 1, 2002. low-grade and low-stage tumors (7). Address reprint requests to: Hagen Blaszyk, M.D., Department of Pathol- There is growing epidemiological and genetic ev- ogy, University of Regensburg Medical Center, PF 10 06 42, D-93042 Regensburg, Germany; e-mail: [email protected]; idence that some carcinomas of the upper urinary fax: 49-941-944-6602. tract develop as a manifestation of the hereditary DOI: 10.1097/01.MP.0000024263.25043.0C nonpolyposis colorectal cancer syndrome (HNPCC; 790 8). This syndrome is characterized by germline mu- or a large amount of stromal and inflammatory cells tations in a number of DNA mismatch repair genes, relative to tumor (15). Microdissected tissue sam- leading to tumor development in a number of or- ples were digested overnight with a proteinase gans and detectable as microsatellite instability in K–containing lysis buffer, and the lysate was further the DNA and loss of immunohistochemical staining processed using a standard column-based DNA pu- for the DNA mismatch repair enzymes in tumor rification kit (Qiagen, Hilden, Germany). Microsat- tissue (9, 10). Patients with HNPCC can develop a ellite analysis was performed using a panel of six number of extracolonic tumors, including cancers microsatellite loci, including five markers of the of the endometrium, ovaries, stomach, and urinary reference panel recommended by the National tract, particularly urothelial carcinoma of the renal Cancer Institute (16). In addition to the reference pelvis and ureter (8, 11). The aim of this study was panel markers (BAT25, BAT26, D2S123, D5S346, to characterize the clinicopathological features, in- and D17S250), the mononucleotide marker BAT40 cluding cancer histories, in a well-defined cohort of was used, because in our experience, it is the most patients with urothelial cancer of the upper urinary sensitive and specific for microsatellite instability tract, and to determine the frequency of microsat- among 31 markers used in colorectal cancer, and ellite instability in these upper tract urothelial the primer sequences have been described previ- carcinomas. ously (17). PCR amplifications were performed with 100 ng of purified genomic DNA in a final volume of 20 ␮L in an MJ Research Thermocycler (PTC100; MJ MATERIAL AND METHODS Research, Watertown, MA) and the polymerase chain reaction (PCR) products were electropho- Patient Characteristics resed through gels containing 6.7% polyacrylamide The study was approved by the Mayo Clinic In- and 50% urea. Microsatellite instability was defined stitutional Review Board. Patients had to have pro- by the presence of novel bands after PCR amplifi- vided research authorization to be included in the cation of tumor DNA that were not present in the study. The study cohort consisted of 114 consecu- PCR products of the corresponding normal DNA. tive patients surgically treated for urothelial carci- Tumor samples were included in the microsatellite noma of the upper tract (renal pelvis ϭ 61 and analysis only if at least five microsatellite loci could ureter ϭ 53) between 1985 and 1992. Clinical and be analyzed. All gels were evaluated independently epidemiological data were obtained through chart by two observers (AH, WD). A tumor was classified review without knowledge of the microsatellite sta- as microsatellite unstable if more than one of the tus. Pathologic features including pathologic stage six panel markers showed instability. Each paired (International Union Against Cancer; 12), histologic sample was analyzed at least twice to verify the grade (World Health Organization; 13) and growth results. architecture (papillary versus flat) were verified in- dependently through microscopic slide review (AH, HB). The patients were seen for regular outpatient Statistical Analyses visits for Ն7 years, and/or were followed by yearly Cancer-specific survival was estimated by the questionnaires sent to their primary physician. method of Kaplan and Meier (18) and compared between patients with various tumor stages and histologic grades, and between patients with Molecular Analyses microsatellite-stable and -unstable tumors by the Matched normal and tumor DNA was extracted exact log-rank statistics (StatXact; 19). Because the from paraffin-embedded tissue for the microsatel- number of deaths was relatively small (n ϭ 33), lite analysis as described previously (14). In brief, exact P values were computed for the log-rank sta- 10-␮m histologic tissue sections were deparaf- tistics. The frequencies of events in the patient his- finized and stained with methylene blue for approx- tories and family histories were compared by the imately 15 seconds. Tumor cell aggregates were Fisher exact test using the StatXact software pack- separated from surrounding stromal cells by micro- age statistics (19). All P values resulted from two- dissection under an inverted microscope at 40ϫ sided tests. magnification. The microdissected tissue samples contained Ն80% tumor cells. Renal parenchyma without tumor infiltration, lamina propria, muscu- RESULTS laris propria of the ureter, or adipose tissue sur- rounding ureter or renal pelvis served as the normal Clinicopathological Characteristics tissue sample. Microdissection using laser micro- The study cohort consisted of 114 consecutive dissection (PALM) was performed in cases where patients with surgically resected urothelial carci- there was low tumor content, limited normal tissue, noma of the upper urinary tract (renal pelvis and Upper Tract Urothelial Cancer
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