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Prostate cancer

Oncological outcomes of cribriform histology pattern in prostate cancer patients: a systematic review and meta-analysis

  • Bailar J, Mellinger GT, Gleason DF. Survival rates of patients with prostatic cancer, tumor stage, and differentiation—preliminary report. Cancer Chemother Rep. 1966;50:129–36.

    PubMed 

    Google Scholar
     

  • Epstein JI, Allsbrook WC, Amin MB, Egevad LL, Bastacky S, López Beltrán A, et al. The 2005 International Society of Urological Pathology (ISUP) Consensus Conference on Gleason Grading of Prostatic Carcinoma. Am J Surg Pathol. 2005;29:1228–42.

    PubMed 

    Google Scholar
     

  • Epstein JI, Amin MB, Reuter VE, Humphrey PA. 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. Am J Surg Pathol. 2017;41:e1–7.

    PubMed 

    Google Scholar
     

  • Kir G, Sarbay BC, Gumus E, Topal CS. The association of the cribriform pattern with outcome for prostatic adenocarcinomas. Pathol Res Pr. 2014;210:640–4.

    CAS 

    Google Scholar
     

  • Trudel D, Downes MR, Sykes J, Kron KJ, Trachtenberg J, Van Der Kwast TH. Prognostic impact of intraductal carcinoma and large cribriform carcinoma architecture after prostatectomy in a contemporary cohort. Eur J Cancer. 2014;50:1610–6.

    PubMed 

    Google Scholar
     

  • Kweldam CF, Wildhagen MF, Steyerberg EW, Bangma CH, van der Kwast TH, van Leenders GJLH. Cribriform growth is highly predictive for postoperative metastasis and disease-specific death in Gleason score 7 prostate cancer. Mod Pathol. 2015;28:457–64.

    PubMed 

    Google Scholar
     

  • Böker A, Kuczyk MA, Kramer MW, Merseburger AS, Krüger K, Imkamp F, et al. True incidence of gleason 6 pathology in patients with metastatic castration resistant prostate cancer (mCRPC). Adv Ther. 2017;34:171–9.

    PubMed 

    Google Scholar
     

  • De Nunzio C, Pastore AL, Lombardo R, Simone G, Leonardo C, Mastroianni R et al. The new Epstein gleason score classification significantly reduces upgrading in prostate cancer patients. Eur J Surg Oncol. 2018. https://doi.org/10.1016/j.ejso.2017.12.003.

  • Brassetti A, Lombardo R, Emiliozzi P, Cardi A, Antonio DV, Antonio I et al. Prostate-specific antigen density is a good predictor of upstaging and upgrading, according to the new grading system: the keys we are seeking may be already in our pocket. Urology. 2018. ihttps://doi.org/10.1016/j.urology.2017.07.071.

  • Awasthi S, Mahal BA, Park JY, Creed JH, Williams VL, Elkenawi A et al. Substantial Gleason reclassification in Black men with national comprehensive cancer network low-risk prostate cancer – A propensity score analysis. Prostate Cancer Prostatic Dis. 2022. https://doi.org/10.1038/S41391-022-00510-Z.

  • Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. PLOS Med. 2021;18:e1003583.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos M, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality if nonrandomized studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.htm 2022.

  • Au S, Villamil CF, Alaghehbandan R, Wang G. Prostatic ductal adenocarcinoma with cribriform architecture has worse prognostic features than non-cribriform-type. Ann Diagn Pathol. 2019;39:59–62.

    PubMed 

    Google Scholar
     

  • Elfandy H, Armenia J, Pederzoli F, Pullman E, Pertega-Gomes N, Schultz N, et al. Genetic and epigenetic determinants of aggressiveness in cribriform carcinoma of the prostate. Mol Cancer Res. 2019;17:446–56.

    CAS 
    PubMed 

    Google Scholar
     

  • Hollemans E, Verhoef EI, Bangma CH, Rietbergen J, Helleman J, Roobol MJ, et al. Large cribriform growth pattern identifies ISUP grade 2 prostate cancer at high risk for recurrence and metastasis. Mod Pathol. 2019;32:139–46.

    CAS 
    PubMed 

    Google Scholar
     

  • Hollemans E, Verhoef EI, Bangma CH, Schoots I, Rietbergen J, Helleman J, et al. Concordance of cribriform architecture in matched prostate cancer biopsy and radical prostatectomy specimens. Histopathology. 2019;75:338–45.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Luo X, Khurana JS, Jhala N, Zhao H, Wang H. The association of invasive cribriform lesions with adverse prostatic adenocarcinoma outcomes: an institutional experience, systematic review, and meta-analysis. Arch Pathol Lab Med. 2019;143:1012–21.

    CAS 
    PubMed 

    Google Scholar
     

  • Bernardino RM, Carvalho R, Severo L, Alves M, Papoila AL, Pinheiro LC. Prostate cancer with cribriform pattern: Exclusion criterion for active surveillance? Arch Ital DI Urol E Androl. 2020;92:235–8.

    CAS 

    Google Scholar
     

  • Flammia S, Frisenda M, Maggi M, Magliocca FM, Ciardi A, Panebianco V, et al. Cribriform pattern does not have a significant impact in Gleason Score ≥7/ISUP Grade ≥2 prostate cancers submitted to radical prostatectomy. Med (Baltim). 2020;99:e22156.

    CAS 

    Google Scholar
     

  • Gao J, Zhang Q, Fu Y, Wang W, Zhang C, Kan Y, et al. Combined clinical characteristics and multiparametric MRI parameters for prediction of cribriform morphology in intermediate-risk prostate cancer patients. Urol Oncol Semin Orig Investig. 2020;38:216–24.


    Google Scholar
     

  • Greenland NY, Cowan JE, Zhang L, Carroll PR, Chan E, Stohr BA, et al. Expansile cribriform Gleason pattern 4 has histopathologic and molecular features of aggressiveness and greater risk of biochemical failure compared to glomerulation Gleason pattern 4. Prostate. 2020;80:653–9.

    PubMed 

    Google Scholar
     

  • Haffner MC, Salles DC, Gao G, Epstein JI. Gleason pattern 4 with cribriform morphology on biopsy is associated with adverse clinicopathological findings in a prospective radical prostatectomy cohort. Hum Pathol. 2020;98:74–80.

    PubMed 

    Google Scholar
     

  • Spieker AJ, Gordetsky JB, Maris AS, Dehan LM, Denney JE, Arnold Egloff SA, et al. PTEN expression and morphological patterns in prostatic adenocarcinoma. Histopathology. 2021;79:1061–71.

    PubMed 

    Google Scholar
     

  • Hollemans E, Verhoef EI, Bangma CH, Rietbergen J, Helleman J, Roobol MJ, et al. Prostate carcinoma grade and length but not cribriform architecture at positive surgical margins are predictive for biochemical recurrence after radical prostatectomy. Am J Surg Pathol. 2020;44:191–7.

    PubMed 

    Google Scholar
     

  • Czaja RC, Tarima S, Wu R, Palagnmonthip W, Iczkowski KA. Comparative influence of cribriform growth and percent Gleason 4 in prostatic biopsies with Gleason 3+4 cancer. Ann Diagn Pathol. 2021;52:151725.

    PubMed 

    Google Scholar
     

  • da Paz AR, Billis A, Freitas LLL, Costa LBE, Barreto IS, Magna LA, et al. Prognostic significance of architectural subtypes of Gleason grade 4 prostate cancer in radical prostatectomy: A semiquantitative method of evaluation. Ann Diagn Pathol. 2021;50:151678.

    PubMed 

    Google Scholar
     

  • Hansum T, Hollemans E, Verhoef EI, Bangma CH, Rietbergen J, Osanto S, et al. Comedonecrosis Gleason pattern 5 is associated with worse clinical outcome in operated prostate cancer patients. Mod Pathol. 2021;34:2064–70.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hollemans E, Verhoef EI, Bangma CH, Rietbergen J, Osanto S, Pelger RCM, et al. Cribriform architecture in radical prostatectomies predicts oncological outcome in Gleason score 8 prostate cancer patients. Mod Pathol. 2021;34:184–93.

    PubMed 

    Google Scholar
     

  • Kryvenko ON, Iakymenko OA, De Lima Guido LP, Bhattu AS, Merhe A, Mouzannar A et al. Prostatic ductal adenocarcinoma controlled for tumor grade, stage, and margin status does not independently influence the likelihood of biochemical recurrence in localized prostate cancer after radical prostatectomy. Arch Pathol Lab Med. 2021. https://doi.org/10.5858/arpa.2021-0048-OA.

  • Ma C, Downes M, Jain R, Ientilucci M, Fleshner N, Perlis N, et al. Prevalence of adverse pathology features in grade group 2 prostatectomy specimens with syn‐ or metachronous metastatic disease. Prostate. 2022;82:345–51.

    PubMed 

    Google Scholar
     

  • Seyrek N, Hollemans E, Osanto S, Pelger RCM, Poel HG, Bekers E, et al. Cribriform architecture outperforms Gleason pattern 4 percentage and tertiary Gleason pattern 5 in predicting the outcome of Grade Group 2 prostate cancer patients. Histopathology. 2022;80:558–65.

    PubMed 

    Google Scholar
     

  • Dong F, Yang P, Wang C, Wu S, Xiao Y, McDougal WS, et al. Architectural heterogeneity and cribriform pattern predict adverse clinical outcome for Gleason grade 4 prostatic adenocarcinoma. Am J Surg Pathol. 2013;37:1855–61.

    PubMed 

    Google Scholar
     

  • Sarbay BC, Kir G, Topal CS, Gumus E. Significance of the cribriform pattern in prostatic adenocarcinomas. Pathol – Res Pr. 2014;210:554–7.


    Google Scholar
     

  • Bernardino RM, Carvalho R, Severo L, Alves M, Papoila AL, Pinheiro LC. Prostate cancer with cribriform pattern: Exclusion criterion for active surveillance? Arch Ital di Urol e Androl. 2020;92. https://doi.org/10.4081/aiua.2020.3.235.

  • Chua MLK, Lo W, Pintilie M, Murgic J, Lalonde E, Bhandari V, et al. A prostate cancer ‘nimbosus’: genomic instability and SChLAP1 dysregulation underpin aggression of intraductal and cribriform subpathologies. Eur Urol. 2017;72:665–74.

    CAS 
    PubMed 

    Google Scholar
     

  • van der Kwast TH, van Leenders GJ, Berney DM, Delahunt B, Evans AJ, Iczkowski KA, et al. ISUP consensus definition of cribriform pattern prostate cancer. Am J Surg Pathol. 2021;45:1118–26.

    PubMed 

    Google Scholar
     

  • Luo X, Khuran JS, Jhal N, Zhao OAQ, Wang H. The association of invasive cribriform lesions with adverse prostatic adenocarcinoma outcomes an institutional experience, systematic review, and meta-analysis. Arch Pathol Lab Med. 2019;143:1012–21.

    CAS 
    PubMed 

    Google Scholar
     

  • Taylor AS, Morgan TM, Wallington DG, Chinnaiyan AM, Spratt DE, Mehra R. Correlation between cribriform/intraductal prostatic adenocarcinoma and percent Gleason pattern 4 to a 22-gene genomic classifier. Prostate. 2020;80:146–52.

    CAS 
    PubMed 

    Google Scholar
     

  • Böttcher R, Kweldam CF, Livingstone J, Lalonde E, Yamaguchi TN, Huang V et al. Cribriform and intraductal prostate cancer are associated with increased genomic instability and distinct genomic alterations. BMC Cancer. 2018;18. https://doi.org/10.1186/s12885-017-3976-z.

  • Gordetsky JB, Schaffer K, Hurley PJ. Current conundrums with cribriform prostate cancer. Histopathology. 2022;80:1038–40.

    PubMed 

    Google Scholar
     

  • Ericson KJ, Wu SS, Lundy SD, Thomas LJ, Klein EA, McKenney JK. Diagnostic accuracy of prostate biopsy for detecting cribriform gleason pattern 4 carcinoma and intraductal carcinoma in paired radical prostatectomy specimens: implications for active surveillance. J Urol. 2020;203:311–9.

    PubMed 

    Google Scholar
     

  • Masoomian M, Downes MR, Sweet J, Cheung C, Evans AJ, Fleshner N, et al. Concordance of biopsy and prostatectomy diagnosis of intraductal and cribriform carcinoma in a prospectively collected data set. Histopathology. 2019;74:474–82.

    PubMed 

    Google Scholar
     

  • Mottet N, van den Bergh RCN, Briers E, Van den Broeck T, Cumberbatch MG, De Santis M, et al. EAU-EANM-ESTRO-ESUR-SIOG guidelines on prostate cancer—2020 update. Part 1: screening, diagnosis, and local treatment with curative intent. Eur Urol. 2021;79:243–62.

    CAS 
    PubMed 

    Google Scholar
     

  • van Leenders GJLH, van der Kwast TH, Grignon DJ, Evans AJ, Kristiansen G, Kweldam CF, et al. The 2019 international society of urological pathology (ISUP) consensus conference on grading of prostatic carcinoma. Am J Surg Pathol. 2020;44:e87–e99.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Numbere N, Teramoto Y, Gurung PMS, Wang Y, Yang Z, Miyamoto H. The clinical impact of unilateral versus bilateral invasion into the seminal vesicle in patients with prostate cancer undergoing radical prostatectomy. Arch Pathol Lab Med. 2021. https://doi.org/10.5858/arpa.2021-0265-OA.

  • Truong M, Feng C, Hollenberg G, Weinberg E, Messing EM, Miyamoto H, et al. A comprehensive analysis of cribriform morphology on magnetic resonance imaging/ultrasound fusion biopsy correlated with radical prostatectomy specimens. J Urol. 2018;199:106–13.

    PubMed 

    Google Scholar
     

  • Choy B, Pearce SM, Anderson BB, Shalhav AL, Zagaja G, Eggener SE, et al. Prognostic significance of percentage and architectural types of contemporary gleason pattern 4 prostate cancer in radical prostatectomy. Am J Surg Pathol. 2016;40:1400–6.

    PubMed 

    Google Scholar
     

  • Keefe DT, Schieda N, El Hallani S, Breau RH, Morash C, Robertson SJ, 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. Virchows Arch. 2015;467:437–42.

    PubMed 

    Google Scholar
     

  • Iczkowski KA, Torkko KC, Kotnis GR, Storey Wilson R, Huang W, Wheeler TM, et al. Digital quantification of five high-grade prostate cancer patterns, including the cribriform pattern, and their association with adverse outcome. Am J Clin Pathol. 2011;136:98–107.

    PubMed 

    Google Scholar