Top

World Journal of Urology

Published in:

Open Access 01-11-2018 | Original Article

Surgical margin status and its impact on prostate cancer prognosis after radical prostatectomy: a meta-analysis

Authors: Lijin Zhang, Bin Wu, Zhenlei Zha, Hu Zhao, Jun Yuan, Yuefang Jiang, Wei Yang

Published in: World Journal of Urology | Issue 11/2018

Abstract

Background and purpose

Positive surgical margins (PSMs) correlate with adverse outcomes in numerous solid tumours. However, the prognostic value of PSMs in prostate cancer (PCa) patients who underwent radical prostatectomy remains unclear. Herein, we performed a meta-analysis to evaluate the association between PSMs and the prognostic value for biochemical recurrence-free survival (BRFS), cancer-specific survival (CSS), overall survival (OS), cancer-specific mortality (CSM) and overall mortality (OM) in PCa patients.

Materials and methods

According to the PRISMA statement, online databases PubMed, EMBASE and Web of Science were searched to identify relevant studies published prior to February 2018. The hazard ratios (HRs) and 95% confidence intervals (95% CIs) were calculated to evaluate the relationship between PSMs and PCa.

Results

Ultimately, 32 cohort studies that met the eligibility criteria and involved 141,222 patients (51–65,633 per study) were included in this meta-analysis. The results showed that PSMs were significantly predictive of poorer BRFS (HR = 1.35, 95% CI 1.28–1.48, p < 0.001), CSS (HR = 1.49, 95% CI 1.16–1.90, p = 0.001) and OS (HR = 1.11, 95% CI 1.02–1.20, p = 0.014). In addition, PSMs were significantly associated with higher risk of CSM (HR = 1.23, 95% CI 1.16–1.30, p < 0.001) and OM (HR = 1.09, 95% CI 1.02–1.16, p = 0.009) in patients with PCa.

Conclusions

Our study suggests that the presence of a histopathologic PSM is associated with the clinical outcomes BRFS, CSS, OS, CSM and OM in patients with PCa, and PSMs could serve as a poor prognostic factor for patients with PCa.

Available only for authorised users

Siegel RL, Miller KD, Jemal A (2017) Cancer statistics, 2017. CA Cancer J Clin 67(1):7–30. https://doi.org/10.3322/caac.21387 CrossRef

Edwards BK, Noone AM, Mariotto AB, Simard EP, Boscoe FP, Henley SJ, Jemal A, Cho H, Anderson RN, Kohler BA, Eheman CR, Ward EM (2014) Annual report to the nation on the status of cancer, 1975–2010, featuring prevalence of comorbidity and impact on survival among persons with lung, colorectal, breast, or prostate cancer. Cancer 120(9):1290–1314. https://doi.org/10.1002/cncr.28509 CrossRefPubMed

Loeb S, Feng Z, Ross A, Trock BJ, Humphreys EB, Walsh PC (2011) Can we stop prostate specific antigen testing 10 years after radical prostatectomy? J Urol 186(2):500–505. https://doi.org/10.1016/j.juro.2011.03.116 CrossRefPubMedPubMedCentral

Eastham JA, Kattan MW, Riedel E, Begg CB, Wheeler TM, Gerigk C, Gonen M, Reuter V, Scardino PT (2003) Variations among individual surgeons in the rate of positive surgical margins in radical prostatectomy specimens. J Urol 170(6 Pt 1):2292–2295. https://doi.org/10.1097/01.ju.0000091100.83725.51 CrossRefPubMed

Vis AN, Schroder FH, van der Kwast TH (2006) The actual value of the surgical margin status as a predictor of disease progression in men with early prostate cancer. Eur Urol 50(2):258–265. https://doi.org/10.1016/j.eururo.2005.11.030 CrossRefPubMed

Swindle P, Eastham JA, Ohori M, Kattan MW, Wheeler T, Maru N, Slawin K, Scardino PT (2008) Do margins matter? The prognostic significance of positive surgical margins in radical prostatectomy specimens. J Urol 179(5 Suppl):S47–S51. https://doi.org/10.1016/j.juro.2008.03.137 CrossRefPubMed

Pfitzenmaier J, Pahernik S, Tremmel T, Haferkamp A, Buse S, Hohenfellner M (2008) Positive surgical margins after radical prostatectomy: do they have an impact on biochemical or clinical progression? BJU Int 102(10):1413–1418. https://doi.org/10.1111/j.1464-410X.2008.07791.x CrossRefPubMed

Mithal P, Howard LE, Aronson WJ, Terris MK, Cooperberg MR, Kane CJ, Amling C, Freedland SJ (2016) Positive surgical margins in radical prostatectomy patients do not predict long-term oncological outcomes: results from the Shared Equal Access Regional Cancer Hospital (SEARCH) cohort. BJU Int 117(2):244–248. https://doi.org/10.1111/bju.13181 CrossRef

Hull GW, Rabbani F, Abbas F, Wheeler TM, Kattan MW, Scardino PT (2002) Cancer control with radical prostatectomy alone in 1000 consecutive patients. J Urol 167(2 Pt 1):528–534CrossRef

10.

Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. J Clin Epidemiol 62(10):e1–34. https://doi.org/10.1016/j.jclinepi.2009.06.006 CrossRef

11.

Stang A (2010) Critical evaluation of the Newcastle–Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25(9):603–605. https://doi.org/10.1007/s10654-010-9491-z CrossRef

12.

Kliment J Jr, Elias B, Baluchova K, Kliment J Sr (2017) The long-term outcomes of radical prostatectomy for very high-risk prostate cancer pT3b-T4 N0-1 on definitive histopathology. Cent Euro J Urol 70(1):13–19. https://doi.org/10.5173/ceju.2017.897 CrossRef

13.

Fujimura T, Fukuhara H, Taguchi S, Yamada Y, Sugihara T, Nakagawa T, Niimi A, Kume H, Igawa Y, Homma Y (2017) Robot-assisted radical prostatectomy significantly reduced biochemical recurrence compared to retro pubic radical prostatectomy. BMC Cancer 17(1):454. https://doi.org/10.1186/s12885-017-3439-6 CrossRefPubMedPubMedCentral

14.

Heering M, Berg KD, Brasso K, Iversen P, Roder MA (2017) Radical prostatectomy in Denmark: survival analysis and temporal trends in clinicopathological parameters with up to 20 years of follow-up. Surg Oncol 26(1):21–27. https://doi.org/10.1016/j.suronc.2016.12.002 CrossRefPubMed

15.

Zhang YD, Wang J, Wu CJ, Bao ML, Li H, Wang XN, Tao J, Shi HB (2016) An imaging-based approach predicts clinical outcomes in prostate cancer through a novel support vector machine classification. Oncotarget 7(47):78140–78151. https://doi.org/10.18632/oncotarget.11293 CrossRefPubMedPubMedCentral

16.

Xu N, Chen HJ, Chen SH, Xue XY, Chen H, Zheng QS, Wei Y, Li XD, Huang JB, Cai H, Sun XL (2016) Reduced Connexin 43 expression is associated with tumor malignant behaviors and biochemical recurrence-free survival of prostate cancer. Oncotarget 7(41):67476–67484. https://doi.org/10.18632/oncotarget.11231 CrossRefPubMedPubMedCentral

17.

Moschini M, Sharma V, Zattoni F, Boorjian SA, Frank I, Gettman MT, Thompson RH, Tollefson MK, Kwon ED, Karnes RJ (2016) Risk stratification of pN+ prostate cancer after radical prostatectomy from a large single institutional series with long-term followup. J Urol 195(6):1773–1778. https://doi.org/10.1016/j.juro.2015.12.074 CrossRefPubMed

18.

Abdel Raheem A, Kim DK, Santok GD, Alabdulaali I, Chung BH, Choi YD, Rha KH (2016) Stratified analysis of 800 Asian patients after robot-assisted radical prostatectomy with a median 64 months of follow up. Int J Urol 23(9):765–774. https://doi.org/10.1111/iju.13151 CrossRefPubMed

19.

Moris L, Van den Broeck T, Tosco L, Van Baelen A, Gontero P, Karnes RJ, Everaerts W, Albersen M, Bastian PJ, Chlosta P, Claessens F, Chun FK, Graefen M, Gratzke C, Kneitz B, Marchioro G, Salas RS, Tombal B, Van Der Poel H, Walz JC, De Meerleer G, Bossi A, Haustermans K, Montorsi F, Van Poppel H, Spahn M, Briganti A, Joniau S (2016) Impact of lymph node burden on survival of high-risk prostate cancer patients following radical prostatectomy and pelvic lymph node dissection. Front Surg 3:65. https://doi.org/10.3389/fsurg.2016.00065 CrossRefPubMedPubMedCentral

20.

Boehm K, Larcher A, Tian Z, Mandel P, Schiffmann J, Karakiewicz PI, Graefen M, Huland H, Tilki D (2016) Low other cause mortality rates reflect good patient selection in patients with prostate cancer treated with radical prostatectomy. J Urol 196(1):82–88. https://doi.org/10.1016/j.juro.2016.01.122 CrossRefPubMed

21.

Maxeiner A, Magheli A, Johrens K, Kilic E, Braun TL, Kempkensteffen C, Hinz S, Stephan C, Miller K, Busch J (2016) Significant reduction in positive surgical margin rate after laparoscopic radical prostatectomy by application of the modified surgical margin recommendations of the 2009 international society of urological pathology consensus. BJU Int 118(5):750–757. https://doi.org/10.1111/bju.13451 CrossRefPubMed

22.

Eminaga O, Wei W, Hawley SJ, Auman H, Newcomb LF, Simko J, Hurtado-Coll A, Troyer DA, Carroll PR, Gleave ME, Lin DW, Nelson PS, Thompson IM, True LD, McKenney JK, Feng Z, Fazli L, Brooks JD (2016) MUC1 expression by immunohistochemistry is associated with adverse pathologic features in prostate cancer: a multi-institutional study. PLoS One 11(11):e0165236. https://doi.org/10.1371/journal.pone.0165236 CrossRefPubMedPubMedCentral

23.

Liu B, Miyake H, Nishikawa M, Tei H, Fujisawa M (2015) Expression profile of autophagy-related markers in localized prostate cancer: correlation with biochemical recurrence after radical prostatectomy. Urology 85(6):1424–1430. https://doi.org/10.1016/j.urology.2015.03.006 CrossRefPubMed

24.

Kim SH, Kim SH, Joung JY, Lee GK, Hong EK, Kang KM, Yu A, Nam BH, Chung J, Seo HK, Park WS, Lee KH (2015) Overexpression of ERG and wild-type PTEN are associated with favorable clinical prognosis and low biochemical recurrence in prostate cancer. PLoS One 10(4):e0122498. https://doi.org/10.1371/journal.pone.0122498 CrossRefPubMedPubMedCentral

25.

Jeong BC, Chalfin HJ, Lee SB, Feng Z, Epstein JI, Trock BJ, Partin AW, Humphreys E, Walsh PC, Han M (2015) The relationship between the extent of extraprostatic extension and survival following radical prostatectomy. Eur Urol 67(2):342–346. https://doi.org/10.1016/j.eururo.2014.06.015 CrossRefPubMed

26.

Rouanne M, Rode J, Campeggi A, Allory Y, Vordos D, Hoznek A, Abbou CC, De La Taille A, Salomon L (2014) Long-term impact of positive surgical margins on biochemical recurrence after radical prostatectomy: ten years of follow-up. Scand J Urol 48(2):131–137. https://doi.org/10.3109/21681805.2013.813067 CrossRefPubMed

27.

Park J, Yoo DS, Song C, Park S, Park S, Kim SC, Cho Y, Ahn H (2014) Comparison of oncological outcomes between retropubic radical prostatectomy and robot-assisted radical prostatectomy: an analysis stratified by surgical experience. World J Urol 32(1):193–199. https://doi.org/10.1007/s00345-013-1168-2 CrossRefPubMed

28.

Knoedler JJ, Karnes RJ, Thompson RH, Rangel LJ, Bergstralh EJ, Boorjian SA (2014) The association of tumor volume with mortality following radical prostatectomy. Prostate Cancer Prostatic Dis 17(2):144–148. https://doi.org/10.1038/pcan.2013.61 CrossRefPubMed

29.

Touijer KA, Mazzola CR, Sjoberg DD, Scardino PT, Eastham JA (2014) Long-term outcomes of patients with lymph node metastasis treated with radical prostatectomy without adjuvant androgen-deprivation therapy. Eur Urol 65(1):20–25. https://doi.org/10.1016/j.eururo.2013.03.053 CrossRefPubMed

30.

Fairey AS, Daneshmand S, Skinner EC, Schuckman A, Cai J, Lieskovsky G (2014) Long-term cancer control after radical prostatectomy and bilateral pelvic lymph node dissection for pT3bN0M0 prostate cancer in the prostate-specific antigen era. Urol Oncol 32(2):85–91. https://doi.org/10.1016/j.urolonc.2013.03.005 CrossRefPubMed

31.

Sukumar S, Rogers CG, Trinh QD, Sammon J, Sood A, Stricker H, Peabody JO, Menon M, Diaz-Insua M (2014) Oncological outcomes after robot-assisted radical prostatectomy: long-term follow-up in 4803 patients. BJU Int 114(6):824–831. https://doi.org/10.1111/bju.12404 CrossRefPubMed

32.

McNeill SA, Good DW, Stewart GD, Stolzenburg JU (2014) Five-year oncological outcomes of endoscopic extraperitoneal radical prostatectomy (EERPE) for prostate cancer: results from a medium-volume UK centre. BJU Int 113(3):449–457. https://doi.org/10.1111/bju.12260 CrossRefPubMed

33.

Zhong WD, Liang YX, Lin SX, Li L, He HC, Bi XC, Han ZD, Dai QS, Ye YK, Chen QB, Wang YS, Zeng GH, Zhu G, Zhang Z, Chen ZN, Wu CL (2012) Expression of CD147 is associated with prostate cancer progression. Int J Cancer 130(2):300–308. https://doi.org/10.1002/ijc.25982 CrossRefPubMed

34.

Mitchell CR, Boorjian SA, Umbreit EC, Rangel LJ, Carlson RE, Karnes RJ (2012) 20-Year survival after radical prostatectomy as initial treatment for cT3 prostate cancer. BJU Int 110(11):1709–1713. https://doi.org/10.1111/j.1464-410X.2012.11372.x CrossRef

35.

Min SH, Park YH, Lee SB, Ku JH, Kwak C, Kim HH (2012) Impact of prostate size on pathologic outcomes and prognosis after radical prostatectomy. Korean J Urol 53(7):463–466. https://doi.org/10.4111/kju.2012.53.7.463 CrossRefPubMedPubMedCentral

36.

Lewinshtein D, Teng B, Valencia A, Gibbons R, Porter CR (2012) The long-term outcomes after radical prostatectomy of patients with pathologic Gleason 8–10 disease. Adv Urol 2012:428098. https://doi.org/10.1155/2012/428098 CrossRefPubMed

37.

Joniau S, Hsu CY, Gontero P, Spahn M, Van Poppel H (2012) Radical prostatectomy in very high-risk localized prostate cancer: long-term outcomes and outcome predictors. Scand J Urol Nephrol 46(3):164–171. https://doi.org/10.3109/00365599.2011.637956 CrossRef

38.

Dorin RP, Daneshmand S, Lassoff MA, Cai J, Skinner DG, Lieskovsky G (2012) Long-term outcomes of open radical retropubic prostatectomy for clinically localized prostate cancer in the prostate-specific antigen era. Urology 79(3):626–631. https://doi.org/10.1016/j.urology.2011.09.051 CrossRefPubMed

39.

Oh JJ, Lee SC, Jeong CW, Yoon CY, Jeong SJ, Hong SK, Byun SS, Rho YK, Choe G, Lee SE (2011) The prognostic significance of percentage of tumour involvement according to disease risk group in men treated with radical prostatectomy. Asian J Androl 13(6):828–832. https://doi.org/10.1038/aja.2011.111 CrossRefPubMed

40.

Ku JH, Moon KC, Cho SY, Kwak C, Kim HH (2011) Serum prostate-specific antigen value adjusted for non-cancerous prostate tissue volume in patients undergoing radical prostatectomy: a new predictor of biochemical recurrence in localized or locally advanced prostate cancer. Asian J Androl 13(2):248–253. https://doi.org/10.1038/aja.2010.152 CrossRefPubMed

41.

Villari D, Nesi G, Della Melina A, Palli D, Ceroti M, Castigli M, Filocamo MT, Li Marzi V, Nicita G (2010) Radical retropubic prostatectomy for prostate cancer with microscopic bladder neck involvement: survival and prognostic implications. BJU Int 105(7):946–950. https://doi.org/10.1111/j.1464-410X.2009.08914.x CrossRefPubMed

42.

Wright JL, Dalkin BL, True LD, Ellis WJ, Stanford JL, Lange PH, Lin DW (2010) Positive surgical margins at radical prostatectomy predict prostate cancer specific mortality. J Urol 183(6):2213–2218. https://doi.org/10.1016/j.juro.2010.02.017 CrossRefPubMedPubMedCentral

43.

Mackinnon AC, Yan BC, Joseph LJ, Al-Ahmadie HA (2009) Molecular biology underlying the clinical heterogeneity of prostate cancer: an update. Arch Pathol Lab Med 133(7):1033–1040. https://doi.org/10.1043/1543-2165-133.7.1033 CrossRefPubMed

44.

Lee T, Hoogenes J, Wright I, Matsumoto ED, Shayegan B (2017) Utility of preoperative 3 Tesla pelvic phased-array multiparametric magnetic resonance imaging in prediction of extracapsular extension and seminal vesicle invasion of prostate cancer and its impact on surgical margin status: experience at a Canadian academic tertiary care centre. Can Urol Assoc J 11(5):e174–e178. https://doi.org/10.5489/cuaj.4211 CrossRefPubMedPubMedCentral

45.

Luchini C, Fleischmann A, Boormans JL, Fassan M (2017) Extranodal extension of lymph node metastasis influences recurrence in prostate cancer: a systematic review and meta-analysis. Sci Rep 7(1):2374. https://doi.org/10.1038/s41598-017-02577-4 CrossRefPubMedPubMedCentral

46.

Dell’Atti L (2016) Prognostic significance of perineural invasion in patients who underwent radical prostatectomy for localized prostate cancer. J BUON 21(5):1219–1223PubMed

47.

Stephenson AJ, Kattan MW, Eastham JA, Bianco FJ Jr, Yossepowitch O, Vickers AJ, Klein EA, Wood DP, Scardino PT (2009) Prostate cancer-specific mortality after radical prostatectomy for patients treated in the prostate-specific antigen era. J Clin Oncol 27(26):4300–4305. https://doi.org/10.1200/jco.2008.18.2501 CrossRefPubMedPubMedCentral

48.

Fontenot PA, Mansour AM (2013) Reporting positive surgical margins after radical prostatectomy: time for standardization. BJU Int 111(8):E290–E299. https://doi.org/10.1111/j.1464-410X.2012.11640.x CrossRefPubMed

49.

Alkhateeb S, Alibhai S, Fleshner N, Finelli A, Jewett M, Zlotta A, Nesbitt M, Lockwood G, Trachtenberg J (2010) Impact of positive surgical margins after radical prostatectomy differs by disease risk group. J Urol 183(1):145–150. https://doi.org/10.1016/j.juro.2009.08.132 CrossRefPubMed

50.

Yossepowitch O, Briganti A, Eastham JA, Epstein J, Graefen M, Montironi R, Touijer K (2014) Positive surgical margins after radical prostatectomy: a systematic review and contemporary update. Eur Urol 65(2):303–313. https://doi.org/10.1016/j.eururo.2013.07.039 CrossRefPubMed

Title: Surgical margin status and its impact on prostate cancer prognosis after radical prostatectomy: a meta-analysis
Authors: Lijin Zhang
Bin Wu
Zhenlei Zha
Hu Zhao
Jun Yuan
Yuefang Jiang
Wei Yang
Publication date: 01-11-2018
Publisher: Springer Berlin Heidelberg
Published in: World Journal of Urology / Issue 11/2018
Print ISSN: 0724-4983
Electronic ISSN: 1433-8726
DOI: https://doi.org/10.1007/s00345-018-2333-4

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Surgical margin status and its impact on prostate cancer prognosis after radical prostatectomy: a meta-analysis

Abstract

Background and purpose

Materials and methods

Results

Conclusions

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Background and purpose

Materials and methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 11/2018

Perioperative outcomes and complications of intracorporeal vs extracorporeal urinary diversion after robot-assisted radical cystectomy for bladder cancer: a real-life, multi-institutional french study

Molecularly-driven precision medicine for advanced bladder cancer

Pseudoprogression and hyperprogression during immune checkpoint inhibitor therapy for urothelial and kidney cancer

A placebo-controlled efficacy study of the intravesical immunomodulators TMX-101 and TMX-202 in an orthotopic bladder cancer rat model

Immunotherapy for bladder cancer: the fight is on

Overall survival in patients with residual disease after radical cystectomy and neoadjuvant chemotherapy