Prostate cancer with cribriform morphology: diagnosis, aggressiveness, molecular pathology and possible relationships with intraductal carcinoma

ABSTRACT Introduction: The Gleason grading system is one of the most important prognostic factors in prostate cancer (PCa). From the 2005 to the 2014 conference organized by the International Society of Urological Pathology (ISUP), the histological criteria for the Gleason patterns were improved, resulting in the shrinkage of the Gleason pattern (GP) 3 and expansion of the GP 4. Areas Covered: Cribriform, fused, ill-defined and glomeruloid glands are part of the morphologic spectrum of the current GP 4. Cribriform, derived from the Latin word cribrum (i.e. sieve), was introduced by Gleason to describe glands composed of a solid sheet with perforations or lumina. Cribriform morphology has a worse prognosis compared with the other, non-cribriform, GP4 morphologies. A practical implication is that a cribriform growth precludes a patient from selecting an active surveillance (AS) protocol. Expert commentary: The presence of these four growth patterns should be incorporated into the current Grade Group (GG) system. Enhancing our understanding of cribriform tumor behavior will lead to correctly identifying and treating those patients that will die because of PCa, while sparing treatment in those who do not require it.

[1]  Hong Wang,et al.  Intraductal carcinoma of the prostate can evade androgen deprivation, with emergence of castrate‐tolerant cells , 2018, BJU international.

[2]  Charlotte F. Kweldam,et al.  On cribriform prostate cancer , 2018, Translational andrology and urology.

[3]  Takafumi N. Yamaguchi,et al.  Cribriform and intraductal prostate cancer are associated with increased genomic instability and distinct genomic alterations , 2018, BMC Cancer.

[4]  P. Humphrey,et al.  Proliferation index of different Gleason pattern 4 histomorphologies and associated pattern 3 adenocarcinoma of the prostate. , 2017, Human pathology.

[5]  T. H. van der Kwast,et al.  A Prostate Cancer "Nimbosus": Genomic Instability and SChLAP1 Dysregulation Underpin Aggression of Intraductal and Cribriform Subpathologies. , 2017, European urology.

[6]  J. Z. Lee,et al.  Cribriform pattern is risk factor of biochemical recurrence in positive surgical margin patients , 2017 .

[7]  T. H. van der Kwast,et al.  Intraductal Carcinoma of the Prostate: Anonymous to Ominous. , 2017, European urology.

[8]  J. Cheville,et al.  Adverse Disease Features in Gleason Score 3 + 4 "Favorable Intermediate-Risk" Prostate Cancer: Implications for Active Surveillance. , 2017, European urology.

[9]  K. Iczkowski,et al.  The New Realization About Cribriform Prostate Cancer , 2017, Advances in anatomic pathology.

[10]  E. Messing,et al.  Impact of Gleason Subtype on Prostate Cancer Detection Using Multiparametric Magnetic Resonance Imaging: Correlation with Final Histopathology , 2017, The Journal of urology.

[11]  K. Iczkowski,et al.  PTEN loss and p27 loss differ among morphologic patterns of prostate cancer, including cribriform. , 2017, Human pathology.

[12]  T. H. van der Kwast,et al.  Improving the Rotterdam European Randomized Study of Screening for Prostate Cancer Risk Calculator for Initial Prostate Biopsy by Incorporating the 2014 International Society of Urological Pathology Gleason Grading and Cribriform growth. , 2017, European urology.

[13]  T. H. van der Kwast,et al.  Distinct DNA methylation alterations are associated with cribriform architecture and intraductal carcinoma in Gleason pattern 4 prostate tumors. , 2017, Oncology letters.

[14]  D. Nieboer,et al.  Presence of invasive cribriform or intraductal growth at biopsy outperforms percentage grade 4 in predicting outcome of Gleason score 3+4=7 prostate cancer , 2017, Modern Pathology.

[15]  T. Cenci,et al.  SOCS3 Immunohistochemical Expression Seems to Support the 2005 and 2014 International Society of Urological Pathology (ISUP) Modified Gleason Grading System , 2017, The Prostate.

[16]  Mahul B Amin,et al.  Contemporary Gleason Grading of Prostatic Carcinoma: An Update With Discussion on Practical Issues to Implement the 2014 International Society of Urological Pathology (ISUP) Consensus Conference on Gleason Grading of Prostatic Carcinoma , 2017, The American journal of surgical pathology.

[17]  M. Roobol,et al.  Biopsy undergrading in men with Gleason score 6 and fatal prostate cancer in the European Randomized study of Screening for Prostate Cancer Rotterdam , 2017, International journal of urology : official journal of the Japanese Urological Association.

[18]  Y. Tsao,et al.  NRIP/DCAF6 stabilizes the androgen receptor protein by displacing DDB2 from the CUL4A-DDB1 E3 ligase complex in prostate cancer , 2017, Oncotarget.

[19]  Wei Li,et al.  Gleason Score 7 Prostate Cancers Emerge through Branched Evolution of Clonal Gleason Pattern 3 and 4 , 2017, Clinical Cancer Research.

[20]  J. Schalken,et al.  Blood-based and urinary prostate cancer biomarkers: a review and comparison of novel biomarkers for detection and treatment decisions , 2016, Prostate Cancer and Prostatic Diseases.

[21]  M. Haider,et al.  Determination of the Association Between T2-weighted MRI and Gleason Sub-pattern: A Proof of Principle Study. , 2016, Academic radiology.

[22]  C. Morash,et al.  Perineural invasion on biopsy is associated with upstaging at radical prostatectomy in Gleason score 3 + 4 = 7 prostate cancer , 2016, Pathology international.

[23]  A. Shalhav,et al.  Prognostic Significance of Percentage and Architectural Types of Contemporary Gleason Pattern 4 Prostate Cancer in Radical Prostatectomy , 2016, The American journal of surgical pathology.

[24]  Esther I Verhoef,et al.  Prostate cancer outcomes of men with biopsy Gleason score 6 and 7 without cribriform or intraductal carcinoma. , 2016, European journal of cancer.

[25]  K. Iczkowski,et al.  Outcome of Gleason 3 + 5 = 8 Prostate Cancer Diagnosed on Needle Biopsy: Prognostic Comparison with Gleason 4 + 4 = 8. , 2016, The Journal of urology.

[26]  Ziding Feng,et al.  Histologic Grading of Prostatic Adenocarcinoma Can Be Further Optimized: Analysis of the Relative Prognostic Strength of Individual Architectural Patterns in 1275 Patients From the Canary Retrospective Cohort , 2016, The American journal of surgical pathology.

[27]  Daan Nieboer,et al.  Gleason grade 4 prostate adenocarcinoma patterns: an interobserver agreement study among genitourinary pathologists , 2016, Histopathology.

[28]  John T. Wei,et al.  Prognostic Value of Percent Gleason Grade 4 at Prostate Biopsy in Predicting Prostatectomy Pathology and Recurrence. , 2016, The Journal of urology.

[29]  C. Morash,et al.  Utility of Gleason pattern 4 morphologies detected on transrectal ultrasound (TRUS)-guided biopsies for prediction of upgrading or upstaging in Gleason score 3 + 4 = 7 prostate cancer , 2016, Virchows Archiv.

[30]  Esther I Verhoef,et al.  Disease-specific survival of patients with invasive cribriform and intraductal prostate cancer at diagnostic biopsy , 2016, Modern Pathology.

[31]  B. Delahunt,et al.  The 2014 International Society of Urological Pathology (ISUP) Consensus Conference on Gleason Grading of Prostatic Carcinoma: Definition of Grading Patterns and Proposal for a New Grading System , 2015, The American journal of surgical pathology.

[32]  Toyonori Tsuzuki,et al.  Diagnosis of “Poorly Formed Glands” Gleason Pattern 4 Prostatic Adenocarcinoma on Needle Biopsy: An Interobserver Reproducibility Study Among Urologic Pathologists With Recommendations , 2015, The American journal of surgical pathology.

[33]  C. Morash,et al.  Cribriform morphology predicts upstaging after radical prostatectomy in patients with Gleason score 3 + 4 = 7 prostate cancer at transrectal ultrasound (TRUS)-guided needle biopsy , 2015, Virchows Archiv.

[34]  Rodolfo Montironi,et al.  Not all gleason pattern 4 prostate cancers are created equal: A study of latent prostatic carcinomas in a cystoprostatectomy and autopsy series , 2015, The Prostate.

[35]  P. Zhang,et al.  The presence and clinical implication of intraductal carcinoma of prostate in metastatic castration resistant prostate cancer , 2015, The Prostate.

[36]  T. Kamoto,et al.  Expression of human kallikrein 1-related peptidase 4 (KLK4) and MET phosphorylation in prostate cancer tissue: immunohistochemical analysis , 2015, Human Cell.

[37]  Ewout W Steyerberg,et al.  Cribriform growth is highly predictive for postoperative metastasis and disease-specific death in Gleason score 7 prostate cancer , 2015, Modern Pathology.

[38]  B. Sarbay,et al.  The association of the cribriform pattern with outcome for prostatic adenocarcinomas. , 2014, Pathology, research and practice.

[39]  B. Sarbay,et al.  Significance of the cribriform pattern in prostatic adenocarcinomas. , 2014, Pathology, research and practice.

[40]  Fang-Ming Deng,et al.  Gleason Score 3 + 4=7 Prostate Cancer With Minimal Quantity of Gleason Pattern 4 on Needle Biopsy Is Associated With Low-risk Tumor in Radical Prostatectomy Specimen , 2014, The American journal of surgical pathology.

[41]  T. H. van der Kwast,et al.  Prognostic impact of intraductal carcinoma and large cribriform carcinoma architecture after prostatectomy in a contemporary cohort. , 2014, European journal of cancer.

[42]  T. Tsuzuki,et al.  Prognostic value of intraductal carcinoma of the prostate in radical prostatectomy specimens , 2014, The Prostate.

[43]  Ping Yang,et al.  Architectural Heterogeneity and Cribriform Pattern Predict Adverse Clinical Outcome for Gleason Grade 4 Prostatic Adenocarcinoma , 2013, The American journal of surgical pathology.

[44]  C. Magi-Galluzzi,et al.  Incidence and clinicopathological characteristics of intraductal carcinoma detected in prostate biopsies: a prospective cohort study , 2013, Histopathology.

[45]  J. Epstein,et al.  Gleason score 7 adenocarcinoma of the prostate with lymph node metastases: analysis of 184 radical prostatectomy specimens. , 2013, Archives of pathology & laboratory medicine.

[46]  P. Nelson,et al.  Abstract 1086: MYC overexpression combined with Pten loss generates genomic instability and rapid metastasis in a new mouse model of lethal prostate adenocarcinoma. , 2013 .

[47]  D. Berney,et al.  Standardization of Gleason grading among 337 European pathologists , 2013, Histopathology.

[48]  Janet E Cowan,et al.  Do Adenocarcinomas of the Prostate With Gleason Score (GS)⩽6 Have the Potential to Metastasize to Lymph Nodes? , 2012, The American journal of surgical pathology.

[49]  T. H. van der Kwast,et al.  Biopsy diagnosis of intraductal carcinoma is prognostic in intermediate and high risk prostate cancer patients treated by radiotherapy. , 2012, European journal of cancer.

[50]  Wei Huang,et al.  Digital quantification of five high-grade prostate cancer patterns, including the cribriform pattern, and their association with adverse outcome. , 2011, American journal of clinical pathology.

[51]  J. Epstein,et al.  Intraductal carcinoma of the prostate without invasive carcinoma on needle biopsy: emphasis on radical prostatectomy findings. , 2010, The Journal of urology.

[52]  Jaya M Satagopan,et al.  TMPRSS2–ERG gene fusion is associated with low Gleason scores and not with high-grade morphological features , 2010, Modern Pathology.

[53]  J. Epstein,et al.  A pathological reassessment of organ-confined, Gleason score 6 prostatic adenocarcinomas that progress after radical prostatectomy. , 2009, Human pathology.

[54]  Arul M Chinnaiyan,et al.  Prevalence of TMPRSS2-ERG Fusion Prostate Cancer among Men Undergoing Prostate Biopsy in the United States , 2009, Clinical Cancer Research.

[55]  Ximing J. Yang,et al.  Grading of Invasive Cribriform Carcinoma on Prostate Needle Biopsy: An Interobserver Study among Experts in Genitourinary Pathology , 2008, The American journal of surgical pathology.

[56]  J. Epstein,et al.  Immunohistochemical Antibody Cocktail Staining (p63/HMWCK/AMACR) of Ductal Adenocarcinoma and Gleason Pattern 4 Cribriform and Noncribriform Acinar Adenocarcinomas of the Prostate , 2007, The American journal of surgical pathology.

[57]  J. Epstein,et al.  Intraductal carcinoma of the prostate on needle biopsy: histologic features and clinical significance , 2006, Modern Pathology.

[58]  L. Egevad,et al.  The 2005 International Society of Urological Pathology (ISUP) Consensus Conference on Gleason Grading of Prostatic Carcinoma , 2005, The American journal of surgical pathology.

[59]  D. Ornstein Pathology and Genetics: Tumours of the Urinary System and Male Genital Organs , 2004 .

[60]  D. Bostwick,et al.  Detection of chromosomal anomalies and c-myc gene amplification in the cribriform pattern of prostatic intraepithelial neoplasia and carcinoma by fluorescence in situ hybridization. , 1997, Modern pathology : an official journal of the United States and Canadian Academy of Pathology, Inc.

[61]  T. Stamey,et al.  Cribriform adenocarcinoma of the prostate , 1986, Cancer.

[62]  J. Epstein,et al.  Adverse Pathologic Findings for Men Electing Immediate Radical Prostatectomy: Defining a Favorable Intermediate-Risk Group , 2018, JAMA oncology.

[63]  E. Messing,et al.  A Comprehensive Analysis of Cribriform Morphology on Magnetic Resonance Imaging/Ultrasound Fusion Biopsy Correlated with Radical Prostatectomy Specimens , 2018, The Journal of urology.

[64]  T. H. van der Kwast,et al.  Evaluation of ERG and PTEN protein expression in cribriform architecture prostate carcinomas. , 2017, Pathology, research and practice.

[65]  D. Gleason Classification of prostatic carcinomas. , 1966, Cancer chemotherapy reports.