EUROPEAN UROLOGY 58 (2010)

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1 EUROPEAN UROLOGY 58 (2010) available at journal homepage: Editorial Original Gleason System Versus 2005 ISUP Modified Gleason System: The Importance of Indicating Which System Is Used in the Patient s Pathology and Clinical Reports Rodolfo Montironi a, *, Liang Cheng b, Antonio Lopez-Beltran c, Marina Scarpelli a, Roberta Mazzucchelli a, Gregor Mikuz d, Ziya Kirkali e, Francesco Montorsi f a Section of Pathological Anatomy, Polytechnic University of the Marche Region, School of Medicine, United Hospitals, Ancona, Italy b Department of Pathology and Laboratory Medicine, Indiana University School of Medicine, Indianapolis, Indiana, USA c Department of Pathology, Reina Sofia University Hospital and Faculty of Medicine, Cordoba, Spain d Department of Pathology, University of Innsbruck School of Medicine, Innsbruck, Austria e Department of Urology, School of Medicine, Dokuz Eylül University, Izmir, Turkey f Department of Urology, University Vita-Salute, Scientific Institute H San Raffaele, Milan, Italy 1. Introduction The Gleason grading system of prostatic carcinoma (PCa) is the quintessential prognostic factor in predicting findings in radical prostatectomy, biochemical failure, local recurrences, lymph node or distant metastasis in patients receiving no treatment, radiation therapy, radical prostatectomy, and other therapies, including cryotherapy and high-intensity focal ultrasound therapy [1 8]. Clinicians use various tools, such as Partin tables or Kattan nomograms, to predict outcomes such as the pathologic stage or prognosis following radical prostatectomy or radiotherapy [9 14]. All of these tools incorporate the Gleason score. 2. Original Gleason system Donald F. Gleason created a unique grading system for PCa in 1966, based solely on the architectural pattern of the tumour and using a 5-point scale; patterns 1, 2, and 3 represent tumours that most closely resemble normal prostatic glands, and patterns 4 and 5 tumours show increasingly abnormal glandular architecture (Table 1) [15 17]. An innovative aspect of this system was that rather than assigning the worst grade as the grade of the carcinoma, the grade was defined as the sum of the two most common patterns and reported as the Gleason score. 3. Gleason s modifications By 1974, Gleason and Mellinger [18] and the Veterans Administration Cooperative Urological Research Group expanded their study of the original Gleason system to 1032 men. Gleason pattern 4 was described in a figure legend as raggedly infiltrating, fused-glandular tumour, frequently with pale cells, may resemble hypernephroma of kidney. The Gleason system was further refined in 1977 by Mellinger, who described the papillary and cribriform tumour under Gleason pattern 3 as having a smooth and usually rounded edge [19]. In describing the breakdown of Gleason patterns among 2911 cases, Gleason pattern 1 was seen in 3.5%, pattern 2 in 24.4%, pattern 3 in 87.7%, pattern 4 in 12.1%, and pattern 5 in 22.6% [19]. These percentages added up to approximately 15% because 50% of the tumours showed at least two different patterns. In 1977, Gleason provided additional comments concerning the application of the Gleason system: Grading is performed under low magnification [20]. He also stated: An occasional small area of fused glands did not change a pattern 3 tumour to pattern 4. A small focus of disorganised cells did not change a pattern 3 or 4 tumour to pattern 5. The only comment relating to tertiary patterns was that occasionally, small areas of a third pattern were observed. * Corresponding author. Pathological Anatomy, Polytechnic University of the Marche Region, School of Medicine, United Hospitals, Via Conca 71, I Torrette, Ancona, Italy. address: r.montironi@univpm.it (R. Montironi) /$ see back matter # 2010 European Association of Urology. Published by Elsevier B.V. All rights reserved. doi: /j.eururo

2 370 EUROPEAN UROLOGY 58 (2010) Table 1 The five patterns according to the original Gleason five Pattern Description 1 Very well-differentiated, small, closely packed, uniform glands in essentially circumscribed masses. 2 Similar to pattern 1 but with moderate variation in size and shape of glands and more atypia in the individual cells; cribriform pattern may be present, still essentially circumscribed, but more loosely arranged. 3 Similar to pattern 2 but marked irregularity in size and shape of glands, with tiny glands or individual cells invading stroma away from circumscribed masses or solid cords and masses with easily identifiable glandular differentiation within most of them. 4 Large clear cells growing in a diffuse pattern resembling hypernephroma; may show gland formation. 5 Very poorly differentiated tumours; usually solid masses or diffuse growth with little or no differentiation into glands. 4. Changes of prostate carcinoma since the late 1960s PCa has changed dramatically since the late 1960s when the Gleason grading system was described. In the 1960s, there was no screening for PCa other than by digital rectal examination (DRE) because serum prostate-specific antigen (PSA) had not yet been discovered. In Gleason s 1974 study, the vast majority of men had advanced disease with either local extension out of the prostate on DRE or distant metastases. Only 6% of patients had nonpalpable tumour diagnosed by transurethral resection, and 8% of patients were diagnosed with a localised nodule on DRE [18]. The method of obtaining prostate tissue was also different from today s practice. Typically, only a couple of thick-gauge needle biopsies were directed into an area of palpable abnormality, usually perineally. The use of 18-gauge thin biopsy needles and the concept of sextant needle biopsies to sample the prostate more extensively were not developed until the 1980s [21]. Consequently, the grading of prostate cancer in thin cores and in multiple cores from different sites of the prostate was not an issue in Gleason s era. In the 1960s, radical prostatectomy was relatively uncommon, prostates were not as often removed intact, and glands were not processed in their entirety or as extensively and systematically to the degree currently seen. Further issues relating to radical prostatectomy specimens, such as the grading of multiple nodules within the same prostate as well as variants and variations of PCa or dealing with tertiary patterns, were not addressed within the original Gleason system. The Gleason system also predated the use of immunohistochemistry. It is likely that, with immunostaining for basal cells, many of Gleason s original = 2 PCa would today be regarded as adenosis (atypical adenomatous hyperplasia), that is, a benign lesion. Similarly, many of the cases in 1966 diagnosed as cribriform Gleason pattern 3 carcinoma would probably be referred to currently as cribriform high-grade prostatic intraepithelial neoplasia, if labelled with basal cell markers [22]. 5. Forty years after the inception of the Gleason system It is remarkable that nearly 40 yr after its inception, the Gleason system remains one of the most powerful prognostic factors in PCa. In part, this system has remained timely by minor adaptations to accommodate the changing practice of medicine [23 28]. However, certain aspects of the original Gleason system are interpreted differently in today s practice. With such changes have come variations in applying the Gleason system among pathologists, with some differences that are regional in nature and others that are dependent on other demographic factors. For example, it was demonstrated that pathologists >50 yr of age tended to diagnose Gleason score 4 on needle biopsy with a statistically significantly higher frequency than younger pathologists, who were trained to do so rarely, if ever [25]. The assigning of an overall score to needle biopsy specimens with different grades on different cores is more of a phenomenon practiced in Europe than in the United States [25] ISUP Modified Gleason System The International Society of Urological Pathology (ISUP) convened a conference in 2005 in San Antonio, Texas, in an attempt to achieve consensus in controversial areas relating to the Gleason system (Tables 2 and 3). This conference led to what is called the 2005 ISUP Modified Gleason System [29]. It is outside the scope of this editorial to describe individually all of the features included in the 2005 ISUP Modified Gleason System. Interested readers are referred to Epstein et al. [29]. We briefly mention that the general theme of the changes to patterns 3 and 4 was to limit the definition of pattern 3 carcinoma and widen the scope of pattern 4 carcinoma. As in Gleason s original description, pattern 3 carcinomas were composed of discrete, circumscribed, and infiltrative glands with well-formed glandular lumina. In the 2005 ISUP Modified Gleason System, very small wellformed glands were still considered within the spectrum of Gleason pattern 3; however, a departure from the original Gleason system was that individual cells would not be allowed within Gleason pattern 3. A further area of divergence from the original Gleason system was the controversial area of cribriform Gleason pattern 3. Within Gleason s original illustrations of pattern 3, he depicts large cribriform glands with rounded and smooth contours. It is important to note that Gleason never conducted any studies that specifically addressed the prognostic differences between the rounded glands he considered cribriform pattern 3 and the irregular glands he also called cribriform pattern 3. At the ISUP 2005 conference, it was the consensus that almost all of these cribriform patterns be diagnosed as Gleason pattern 4.

3 EUROPEAN UROLOGY 58 (2010) Table 2 Controversial areas relating to the Gleason system [29] General applications of the Gleason grading system Gleason patterns Grading variants and variations of acinar adenocarcinoma of the prostate Reporting secondary patterns of lower grade when present to a limited extent Reporting secondary patterns of higher grade when present to a limited extent Tertiary Gleason patterns Percent pattern 4 5 Radical prostatectomy specimens with separate tumour nodules Needle biopsy with different cores showing different grades The consensus panel required extremely stringent criteria for the diagnosis of cribriform pattern 3 and included only rounded well-circumscribed glands of the same size of normal glands. Cribriform Gleason pattern 3 PCa should morphologically resemble cribriform high-grade prostatic intraepithelial neoplasia (Fig. 1a) yet show diagnostic features of infiltrating carcinoma such as (1) glands negative for basal cell markers; (2) back-to-back glands, ruling out high-grade prostatic intraepithelial neoplasia; or (3) glands exhibiting pathognomonic features of carcinoma such as perineural invasion or extraprostatic extension. In contrast, pattern 4, which originally was limited to fused or irregularly contoured cribriform structures, was widened in scope. With rare exceptions, almost all cribriform morphologies were accepted as Gleason pattern 4 (Fig. 1b). Although not included in Gleason s original depictions, a consensus was reached that ill-defined glands with poorly formed glandular lumina, a pattern that often accompanies fused glands, warranted a diagnosis of Gleason pattern Upgrading with the 2005 ISUP Modified Gleason System The most immediate result of limiting the definition of Gleason pattern 3 and expanding the definition of pattern 4 is Gleason grade migration or upgrading, both in needle biopsies and radical prostatectomy specimens. In many settings, Gleason pattern 3 PCa, previously the most common pattern, has become less common than pattern 4. In one recent study comparing the original and modified Gleason systems on needle biopsy material, Gleason score 6 cancers decreased from 48% to 22% of the total, whereas Gleason score 7 cancers increased from 25% to 68%. Not surprisingly, the magnitude of this shift depends somewhat on the study population, and it is less dramatic in clinical settings with a greater proportion of early stage disease, as seen in a study by Billis et al. [24] where the proportion of needle biopsies with a Gleason score of 6 was 68%, decreasing to 49% using the modified grading scheme. Correspondingly, Gleason 7 went from 26% to 39% with application of the modified grade criteria. There are clinical consequences with the upgrading in the Gleason score, for instance, in the type of therapy Table 3 The five patterns according to the 2005 International Society of Urological Pathology Modified Gleason System Pattern Description 1 Circumscribed nodule of closely packed but separate, uniform, rounded to oval, medium-sized acini (larger glands than pattern 3). 2 Like pattern 1, fairly circumscribed, yet at the edge of the tumour nodule there may be minimal infiltration. Glands are more loosely arranged and not quite as uniform as Gleason pattern 1. 3 Discrete glandular units. Typically smaller glands than seen in Gleason pattern 1 or 2. Infiltrates in and among non-neoplastic prostate acini. Marked variation in size and shape. Smoothly circumscribed small cribriform nodules of tumour. 4 Fused microacinar glands. Ill-defined glands with poorly formed glandular lumina. Large cribriform glands. Cribriform glands with an irregular border. Hypernephromatoid. 5 Essentially no glandular differentiation, composed of solid sheets, cords, or single cells. Comedocarcinoma with central necrosis surrounded by papillary, cribriform, or solid masses. Fig. 1 Adenocarcinoma of the prostate with (A) Gleason pattern 3 and (B) Gleason pattern 4.

4 372 EUROPEAN UROLOGY 58 (2010) Table 4 Differences between the original Gleason system and the 2005 International Society of Urological Pathology (ISUP) Modified Gleason System * Original Gleason system A diagnosis of GS <4 is possible on NB. A partial cribriform pattern, large cribriform, is diagnosed as Gleason pattern 3. The same GS is used for NB and RP specimens. High-grade tumour of small quantity (<5%) on NB should be excluded based on GS (5% threshold rule). Tumours on NB should be graded by listing the primary and secondary patterns (ie, excluding tertiary pattern). The GS of RP specimens should be assigned based on the primary and secondary patterns. Separate or overall scoring is used to assess all grades of NB specimens. The grade of the largest portion should be assigned even if the second largest portion is of higher grade ISUP Modified Gleason System GS of NB specimens <4 is rarely if ever made. Most cribriform patterns would be diagnosed as Gleason pattern 4; specimens with only rare cribriform lesions would satisfy the diagnostic criteria for cribriform pattern 3. Different GS is used for NB and RP specimens. High-grade tumour of any quantity on NB should be included within the GS. For the tertiary pattern on NB specimens, both the primary pattern and the highest grade should be recorded. For RP specimens, the pathologist should assign the GS based on the primary and secondary patterns with a comment on the tertiary pattern. When NB specimens show different grades in separate cores, individual GS should be assigned to these cores (separate scoring). When RP specimens show different grades in separate tumour nodules, a separate GS should be assigned to each of the dominant tumour nodules. GS = Gleason score; NB = needle biopsy; RP = radical prostatectomy. * Adapted from Uemura et al. [37]. offered to an individual patient with PCa [30 36]. As an example, patients with high-grade tumours in the biopsy could be discouraged from undergoing active surveillance. The true test of the validity of the 2005 ISUP Modified Gleason System is its correlation with patient outcomes. Few studies have been published. For instance, Uemura et al. [37] found that the 2005 ISUP modified Gleason score of needle biopsy specimens was significantly associated with biochemical recurrence-free survival after radical prostatectomy. They concluded that the ISUP system is clinically useful for determining the most appropriate treatments for patients with early stage PCa [37]. However, it will be some time until studies with sufficient follow-up periods are published. 8. Conclusions The differences between the original Gleason system and the 2005 ISUP Modified Gleason System (Table 4) make it difficult to compare data sets assessing patient outcomes in PCa over time. Urologists and uropathologists have to be aware of the impact on patient prognosis and treatment of the Gleason system used. The pathology report and the clinical records must clearly indicate which system is adopted for each individual patient. Conflicts of interest: The authors have nothing to disclose. References [1] Campos-Fernandes J-L, Bastien L, Nicolaiew N, et al. Prostate cancer detection rate in patients with repeated extended 21-sample needle biopsy. Eur Urol 2009;55: [2] Chun FK-H, Karakiewicz PI, Briganti A. Prostate cancer diagnosis: importance of individualized risk stratification models over PSA alone. Eur Urol 2008;54: [3] Haese A, de la Taille A, van Poppel H, et al. Clinical utility of the PCA3 urine assay in European men scheduled for repeat biopsy. Eur Urol 2008;54: [4] Heidenreich A, Richter S, Thüer D, Pfister D. Prognostic parameters, complications, and oncologic and functional outcome of salvage radical prostatectomy for locally recurrent prostate cancer after 21st-century radiotherapy. Eur Urol 2010;57: [5] Patel A. Editorial comment on: prognostic parameters, complications, and oncologic and functional outcome of salvage radical prostatectomy for locally recurrent prostate cancer after 21stcentury radiotherapy. Eur Urol 2010;57:444. [6] Schellhammer PF. Re: Pathologic characteristics of cancers detected in the Prostate Cancer Prevention Trial: implications for prostate cancer detection and chemoprevention. Eur Urol 2009;55: [7] Walz J, Chun FKH, Klein EA, et al. Risk-adjusted hazard rates of biochemical recurrence for prostate cancer patients after radical prostatectomy. Eur Urol 2009;55: [8] Ward JF. Editorial comment on: prognostic parameters, complications, and oncologic and functional outcome of salvage radical prostatectomy for locally recurrent prostate cancer after 21stcentury radiotherapy. Eur Urol 2010;57: [9] Briganti A, Karakiewicz PI, Joniau S, Van Poppel H. The motion: nomograms should become a routine tool in determining prostate cancer prognosis. Eur Urol 2009;55: [10] Capitanio U, Jeldres C, Shariat SF, Karakiewicz P. Clinicians are most familiar with nomograms and rate their clinical usefulness highest, look-up tables are second best. Eur Urol 2008;54: [11] Catto JWF. More nomograms or better evidence of efficacy: what do we need in urologic oncology? Eur Urol 2008;54:11 2. [12] DiBlasio CJ, Rhee AC, Cho D, et al. Predicting clinical end points: treatment nomograms in prostate cancer. Semin Oncol 2003;30: [13] Partin AW, Kattan MW, Subong EN, et al. Combination of prostatespecific antigen, clinical stage, and Gleason score to predict pathological stage of localized prostate cancer. A multi-institutional update. JAMA 1997;277: [14] Vickers AJ, Bianco FJ, Gonen M, et al. Effects of pathologic stage on the learning curve for radical prostatectomy: evidence that recurrence in organ-confined cancer is largely related to inadequate surgical technique. Eur Urol 2008;53: [15] Bailar III JC, Mellinger GT, Gleason DF. Survival rates of patients with prostatic cancer, tumor stage, and differentiation preliminary report. Cancer Chemother Rep 1966;50:

5 EUROPEAN UROLOGY 58 (2010) [16] Gleason DF. Classification of prostatic carcinomas. Cancer Chemother Rep 1966;50: [17] Mellinger GT, Gleason D, Bailar III J. The histology and prognosis of prostatic cancer. J Urol 1967;97: [18] Gleason DF, Mellinger GT. Prediction of prognosis for prostatic adenocarcinoma by combined histological grading and clinical staging. J Urol 1974;11: [19] Mellinger GT. Prognosis of prostatic carcinoma. Recent Results Cancer Res 1977;60: [20] Gleason DF. Histological grading and clinical staging of prostatic carcinoma. In: Tannenbaum M, ed. Urologic pathology. The prostate. Philadelphia, PA: Lea and Feibiger; p [21] Hodge KK, McNeal JE, Terris MK, Stamey TA. Random systematic versus directed ultrasound guided transrectal core biopsies of the prostate. J Urol 1989;142:71 4. [22] Amin MB, Schultz DS, Zarbo RJ. Analysis of cribriform morphology in prostatic neoplasia using antibody to high-molecular-weight cytokeratins. Arch Pathol Lab Med 1994;118: [23] Amin M, Boccon-Gibod L, Egevad L, et al. Prognostic and predictive factors and reporting of prostate carcinoma in prostate needle biopsy specimens. Scand J Urol Nephrol Suppl 2005;216: [24] Billis A, Guimaraes MS, Freitas LL, Meirelles L, Magna LA, Ferreira U. The impact of the 2005 International Society of Urological Pathology consensus conference on standard Gleason grading of prostatic carcinoma in needle biopsies. J Urol 2008;180: [25] Egevad L, Allsbrook WC, Epstein JI. Current practice of Gleason grading among genitourinary pathologists. Hum Pathol 2005;36: 5 9. [26] Harnden P, Shelley MD, Coles B, Staffurth J, Mason MD. Should the Gleason grading system for prostate cancer be modified to account for high-grade tertiary components? A systematic review and meta-analysis. Lancet Oncol 2007;8: [27] Helpap B, Egevad L. The significance of modified Gleason grading of prostatic carcinoma in biopsy and radical prostatectomy specimens. Virchows Arch 2006;449: [28] Montironi R, Vela Navarrete R, Lopez-Beltran A, Mazzucchelli R, Mikuz G, Bono AV. Histopathology reporting of prostate needle biopsies update. Virchows Arch 2006;449:1 13. [29] Epstein JI, Allsbrook Jr WC, Amin MB, Egevad LL, ISUP Grading Committee. The 2005 International Society of Urological Pathology (ISUP) consensus conference on Gleason grading of prostatic carcinoma. Am J Surg Pathol 2005;29: [30] Albertson PC. Editorial comment on: insignificant prostate cancer and active surveillance: from definition to clinical implications. Eur Urol 2009;55: [31] Aus G. Editorial comment on: insignificant prostate cancer and active surveillance: from definition to clinical implications. Eur Urol 2009;55:1331. [32] Bastian PJ, Carter BH, Bjartell A, et al. Insignificant prostate cancer and active surveillance: from definition to clinical implications. Eur Urol 2009;55: [33] Cohen MS, Hanley RS, Kurteva T, et al. Comparing the Gleason prostate biopsy and Gleason prostatectomy grading system: the Lahey Clinic Medical Center experience and an international metaanalysis. Eur Urol 2008;54: [34] Heidenreich A. Identification of high-risk prostate cancer: role of prostate-specific antigen, PSA doubling time, and PSA velocity. Eur Urol 2008;54: [35] Ladjevardi S, Sandblom G, Berglund A, Varenhorst E. Tumour grade, treatment, and relative survival in a population-based cohort of men with potentially curable prostate cancer. Eur Urol 2010;57: [36] Lee MC, Dong F, Stephenson AJ, Jones JS, Magi-Galluzzi C, Klein EA. The Epstein criteria predict for organ-confined but not insignificant disease and a high likelihood of cure at radical prostatectomy. Eur Urol 2010;58:90 5. [37] Uemura H, Hoshino K, Sasaki T, et al. Usefulness of the 2005 International Society of Urologic Pathology Gleason grading system in prostate biopsy and radical prostatectomy specimens. BJU Int 2009;103:

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