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Cell Proliferation in Prostate Cancer Patients with Lymph Node Metastasis: a Marker for Progression

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Cell Proliferation in Prostate Cancer Patients with Lymph Node Metastasis: a Marker for Progression 2820 Vol. 5, 2820–2823, October 1999 Clinical Cancer Research Cell Proliferation in Prostate Cancer Patients with Lymph Node Metastasis: A Marker for Progression Liang Cheng,1 Thomas M. Pisansky, expression in the primary cancer and lymph node metastasis Thomas J. Sebo, Bradley C. Leibovich, was associated with systemic progression-free survival in 5 Dharamdas M. Ramnani, Amy L. Weaver, univariate analysis (P 0.027 and 0.048, respectively) but was not significant after adjusting for nodal cancer volume Beth G. Scherer, Michael L. Blute, Horst Zincke, (P 5 0.52 and 0.17, respectively). Our data indicate that 2 and David G. Bostwick assessment of cell proliferation in nodal metastasis is pre- Departments of Pathology [L. C.] and Urology [L. C.], Indiana dictive of clinical outcome in prostate cancer patients with University School of Medicine, Indianapolis, Indiana 46202 and the regional lymph node metastasis. Division of Radiation Oncology [T. M. P.], the Departments of Pathology [T. J. S., D. M. R., D. G. B.], Urology [B. C. L., M. L. B., H. Z., D. G. B.] and the Section of Biostatistics [A. L. W., B. G. S.], INTRODUCTION Mayo Clinic, Rochester, Minnesota Prostate cancer is the most common noncutaneous malig- nancy and second leading cause of cancer-related mortality in the American male, accounting for 179,300 new cases and ABSTRACT 37,000 deaths in 1999 (1). About 10% of patients have pelvic The biological aggressiveness of lymph node-positive lymph node metastases at the time of diagnosis (2, 3), and many prostate cancer is closely linked to cancer volume in nodal received androgen deprivation (4) with radiotherapy (5) or sur- metastases. We evaluated MIB-1 (Ki-67) labeling index and gery (6–8). Despite the adverse prognostic significance of nodal bcl-2 expression in primary cancer and matched nodal me- involvement, the clinical outcome for these patients is variable tastases from 138 node-positive patients treated with radical (2). Additional factors are needed to more accurately determine prostatectomy and bilateral pelvic lymphadenectomy be- outcome in these patients. In this study, we sought to determine tween 1987 and 1992 at the Mayo Clinic. One hundred whether cell proliferation was associated with patient outcome. twenty-eight patients (93%) received androgen deprivation therapy within 90 days after radical prostatectomy. Mean patient age was 66 years (range, 51–78). The median fol- MATERIALS AND METHODS low-up was 6.7 years (range, 0.03–11). MIB-1 (Ki-67) label- Patients. The study group consisted initially of 269 pa- ing index was determined by digital image analysis, and tients who underwent radical prostatectomy and bilateral pelvic nodal cancer volume was determined by the grid method. lymphadenectomy between January 1987 and December 1992 at Systemic progression, defined as the presence of distant Mayo Clinic (2). All patients had regional lymph node metas- metastasis documented by biopsy or radiographic examina- tasis, and none had clinical evidence of distant metastases at the tion, was used as an outcome end point in the Cox propor- time of surgery. The final study population was limited to 138 tional hazard models. MIB-1 labeling index in nodal metas- patients with sufficient tissue in the primary cancer and metas- tases was predictive of systemic progression-free survival tasis for immunostaining. One hundred twenty-eight patients (P 5 0.001). The 8-year systemic progression-free survival (93%) received androgen deprivation therapy within 90 days was 100% for those with MIB-1 labeling index <3.5% com- after prostatectomy, and this consisted of orchiectomy or lutein- pared with 78% for those with MIB-1 labeling index >7.8%. izing hormone-releasing hormone agonist with or without an MIB-1 labeling index correlated with Gleason score, DNA antiandrogenic agent. After surgery, patients were evaluated ploidy, and nodal cancer volume (P < 0.001, 0.04, and quarterly for the first 2 years, semiannually for 2 additional 0.001, respectively). After controlling for nodal cancer years, and annually thereafter. Follow-up examinations included < 3 volume, MIB-1 labeling index remained significant in pre- physical examination, serum PSA measurement, chest radiog- dicting systemic progression-free survival (P 5 0.047). bcl-2 raphy, and computerized tomography of the abdomen and pelvis as clinically indicated. A radionuclide bone scan was conducted at least annually or as clinically indicated. Serum PSA was measured using the Hybritech Tandem-R assay (Hybrityech, Inc., San Diego, CA) in all patients. In those followed after Received 4/22/99; revised 7/12/99; accepted 7/15/99. The costs of publication of this article were defrayed in part by the surgery at another institution, PSA determination was performed payment of page charges. This article must therefore be hereby marked at Mayo Clinic by means of a mailed blood specimen; alterna- advertisement in accordance with 18 U.S.C. Section 1734 solely to tively, patients were contacted annually, and additional medical indicate this fact. Supported in part by Grant #IRG-84-002-16 from the information was obtained from the local physician, as necessary American Cancer Society (to. L. C.). 1 To whom requests for reprints should be addressed, at Department of (2, 6–10) Pathology, Indiana University School of Medicine, UH 3465, 550 North University Boulevard, Indianapolis, IN 46202. E-mail: lcheng@ iupui.edu. 2 Present address: Bostwick Laboratories, 6722 Patterson Avenue, Rich- mond, VA 23226. 3 The abbreviation used is: PSA, prostate-specific antigen. Downloaded from clincancerres.aacrjournals.org on October 2, 2021. © 1999 American Association for Cancer Research. Clinical Cancer Research 2821 Specimens. The radical prostatectomy and bilateral pel- Table 1 Characteristics of 138 prostate cancer patients with regional vic lymphadenectomy specimens were examined by frozen sec- lymph node metastasis tion at operation and subsequently by permanent sections, as No. of patients (%) described previously (2, 11–13) All histological evaluations Age (years) were performed without knowledge of the clinical outcome. ,60 27 (20) Briefly, the apex and base of the prostate were amputated or 60–69 67 (48) submitted as en face (shave) margins, and the prostate was $70 44 (32) serially sectioned perpendicular to the long axis of the gland Preoperative PSA (ng/ml) ,10 26 (20) from the apex to the tip of the seminal vesicles. After gross 10–19 29 (22) examination of the whole prostate slices, frozen sections were $20 76 (58) selected to encompass the cancer; the length, width, and height Pathologic stagea T 4 (3) were determined by microscopic examination of frozen sections. 2a T 9 (7) The number of cancer sections submitted for frozen examina- 2b T3a 18 (13) tions from the radical prostatectomy specimens varied from 8 to T3b 107 (77) 20 in this series, depending on cancer volume, prostate volume, Surgical margins and the preference of the pathologist. Approximately 14 prostate Positive 92 (67) blocks were examined per case, and the method of sampling Negative 45 (33) Gleason grade remained constant during the study period (2). #6 8 (6) The lymph nodes from the pelvic lymph node dissection 7 74 (54) were totally embedded. The median number of lymph nodes $8 56 (41) sampled was 14 (range, 4–33). Nodal cancer volume (size) was DNA ploidy Diploid 68 (50) determined in permanent sections by the grid method (2), and Tetraploid 48 (36) the total cancer volume of all positive nodes (nodal cancer Aneuploid 19 (14) volume) was used for statistical analysis. Number of positive nodes The 1997 Tumor-Node-Metastasis system was used for 1 61 (44) pathological staging (14). Grading of the primary cancer was 2–4 61 (44) $5 16 (12) performed according to the Gleason system (15). Prostatectomy Nodal cancer volume (ml)b specimens were examined for DNA ploidy in all patients by #0.02 19 (14) flow cytometry with the Hedley technique (16), and DNA 0.02–0.04 38 (28) histograms were classified as diploid, tetraploid, or aneuploid. 0.05–0.19 42 (30) $0.20 38 (28) (17) a Immunohistochemistry. For inclusion in the study, ad- Pathological staging according to the 1997 American Joint Com- mittee on Cancer (AJCC) cancer staging (14). equate tissue from both the primary cancer and matched nodal b Nodal cancer volume was measured by the grid method (2). metastases were required for immunostaining. Representative blocks of the primary cancer and paired lymph node metastases were selected from the same patient for immunostaining. Stain- ing was performed on 6-mm, formalin-fixed, paraffin-embedded for univariate associations of variables with systemic progres- sections using the avidin-biotin complex technique. Primary sion-free survival. Analysis of association of continuous vari- monoclonal antibodies were used for evaluation of MIB-1 la- ables with survival was performed using single degree of free- beling index (Ki-67; Immunotech, Westbrook, ME; dilution, dom (linear) terms in the Cox model. Nodal cancer volume was 1:50) and bcl-2 expression (Dako, Carpinteria, CA; dilution analyzed on the log base-2 scale because it was positively 1:20). 3,3-Diaminobenzidine was used as the chromogen, and skewed. To avoid bias, no arbitrary cutoff points were chosen 0.2% methyl green was used as the counterstain. Quantification for continuous variables in the Cox regression analysis (18). of MIB-1 (Ki-67) labeling was performed using the CAS 200 Continuous variables were split into three even groups (MIB-1) digital image analyzer and proliferation index software pro- for the purpose of illustration and estimating survival rates at 8 grams (Becton Dickinson, Cellular Imaging Systems, San Jose, years. The associations of MIB-1 labeling index and bcl-2 CA). At least 1000 cells were analyzed in each case. Immuno- expression with clinical and pathological findings were assessed , reactivity for bcl-2 was evaluated semiquantitatively on a 5% using the Spearman rank correlation coefficient.
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