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Published in: BMC Cancer 1/2019

Open Access 01-12-2019 | Cystectomy | Research article

Clinicopathological factors in bladder cancer for cancer-specific survival outcomes following radical cystectomy: a systematic review and meta-analysis

Authors: Lijin Zhang, Bin Wu, Zhenlei Zha, Wei Qu, Hu Zhao, Jun Yuan

Published in: BMC Cancer | Issue 1/2019

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Abstract

Background

Assessing the prognostic significance of specific clinicopathological features plays an important role in surgical management after radical cystectomy. This study investigated the association between ten clinicopathological characteristics and cancer-specific survival (CSS) in patients with bladder cancer.

Methods

In accordance with the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) guidelines, a literature search was conducted through the PubMed, EMBASE and Web of Science databases using appropriate search terms from the dates of inception until November 2018. Pooled hazard ratios (HRs) with 95% confidence intervals (CIs) were calculated to evaluate the CSS. Fixed- or random-effects models were constructed according to existence of heterogeneity.

Results

Thirty-three articles met the eligibility criteria for this systematic review, which included 19,702 patients. The overall results revealed that CSS was associated with advanced age (old vs. young: pooled HR = 1.01; 95% CI:1.00–1.01; P < 0.001), higher tumor grade (3 vs. 1/2: pooled HR = 1.29; 95% CI:1.15–1.45; P < 0.001), higher pathological stage (3/4 vs. 1/2: pooled HR = 1.60; 95% CI:1.37–1.86; P < 0.001), lymph node metastasis (positive vs. negative: pooled HR = 1.51; 95% CI:1.37–1.67; P < 0.001), lymphovascular invasion (positive vs. negative: pooled HR = 1.36; 95% CI:1.28–1.45; P < 0.001), and soft tissue surgical margin (positive vs. negative: pooled HR = 1.42; 95% CI:1.30–1.56; P < 0.001). However, gender (male vs. female: pooled HR = 0.98; 95% CI: 0.96–1.01; P = 0.278), carcinoma in situ (positive vs. negative: pooled HR = 0.98; 95% CI: 0.88–1.10; P = 0.753), histology (transitional cell cancer vs variant: pooled HR = 0.90; 95% CI: 0.79–1.02; P = 0.089) and adjuvant chemotherapy (yes vs. no: pooled HR = 1.16; 95% CI: 1.00–1.34; P = 0.054) did not affect CSS after radical resection of bladder cancer.

Conclusions

Our results revealed that several clinicopathological characteristics can predict CSS risk after radical cystectomy. Prospective studies are needed to further confirm the predictive value of these variables for the prognosis of bladder cancer patients after radical cystectomy.
Appendix
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Literature
1.
Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61(2):69–90.CrossRef
2.
Burger M, Catto JW, Dalbagni G, Grossman HB, Herr H, Karakiewicz P, Kassouf W, Kiemeney LA, La Vecchia C, Shariat S, et al. Epidemiology and risk factors of urothelial bladder cancer. Eur Urol. 2013;63(2):234–41.CrossRef
3.
Aziz A, Gierth M, Fritsche HM, May M, Otto W, Denzinger S, Wieland WF, Merseburger A, Riedmiller H, Kocot A, et al. Oncological outcome of primary versus secondary muscle-invasive bladder cancer is comparable after radical cystectomy. Urol Int. 2013;91(1):97–102.CrossRef
4.
Sharma P, Zargar-Shoshtari K, Poch MA, Pow-Sang JM, Sexton WJ, Spiess PE, Gilbert SM. Surgical control and margin status after robotic and open cystectomy in high-risk cases: caution or equivalence? World J Urol. 2017;35(4):657–63.CrossRef
5.
Manoharan M, Katkoori D, Kishore TA, Jorda M, Luongo T, Soloway MS. Lymphovascular invasion in radical cystectomy specimen: is it an independent prognostic factor in patients without lymph node metastases? World J Urol. 2010;28(2):233–7.CrossRef
6.
Canter D, Guzzo TJ, Resnick MJ, Bergey MR, Sonnad SS, Tomaszewski J, VanArsdalen K, Malkowicz SB. A thorough pelvic lymph node dissection in presence of positive margins associated with better clinical outcomes in radical cystectomy patients. Urology. 2009;74(1):161–5.CrossRef
7.
Yafi FA, Aprikian AG, Chin JL, Fradet Y, Izawa J, Estey E, Fairey A, Rendon R, Cagiannos I, Lacombe L, et al. Impact of concomitant carcinoma in situ on upstaging and outcome following radical cystectomy for bladder cancer. World J Urol. 2014;32(5):1295–301.CrossRef
8.
Kanatani A, Nakagawa T, Kawai T, Naito A, Sato Y, Yoshida K, Nozaki K, Nagata M, Yamada Y, Azuma T, et al. Adjuvant chemotherapy is possibly beneficial for locally advanced or node-positive bladder cancer. Clinical genitourinary cancer. 2015;13(2):e107–12.CrossRef
9.
Sun M, Abdollah F, Bianchi M, Trinh QD, Shariat SF, Jeldres C, Tian Z, Hansen J, Briganti A, Graefen M et al: Conditional survival of patients with urothelial carcinoma of the urinary bladder treated with radical cystectomy. European journal of cancer (Oxford, England : 1990) 2012, 48(10):1503–1511.CrossRef
10.
Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. J Clin Epidemiol. 2009;62(10):e1–34.CrossRef
11.
Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25(9):603–5.CrossRef
12.
Mayr R, Gierth M, Zeman F, Reiffen M, Seeger P, Wezel F, Pycha A, Comploj E, Bonatti M, Ritter M, et al. Sarcopenia as a comorbidity-independent predictor of survival following radical cystectomy for bladder cancer. J Cachexia Sarcopenia Muscle. 2018;9(3):505–13.CrossRef
13.
Hodgson A, Xu B, Satkunasivam R, Downes MR. Tumour front inflammation and necrosis are independent prognostic predictors in high-grade urothelial carcinoma of the bladder. J Clin Pathol. 2018;71(2):154–60.CrossRef
14.
Muppa P, Gupta S, Frank I, Boorjian SA, Karnes RJ, Thompson RH, Thapa P, Tarrell RF, Herrera Hernandez LP, Jimenez RE, et al. Prognostic significance of lymphatic, vascular and perineural invasion for bladder cancer patients treated by radical cystectomy. Pathology. 2017;49(3):259–66.CrossRef
15.
Li G, Yu J, Song H, Zhu S, Sun L, Shang Z, Niu Y. Squamous differentiation in patients with superficial bladder urothelial carcinoma is associated with high risk of recurrence and poor survival. BMC Cancer. 2017;17(1):530.CrossRef
16.
Kang M, Balpukov UJ, Jeong CW, Kwak C, Kim HH, Ku JH. Can the preoperative neutrophil-to-lymphocyte ratio significantly predict the conditional survival probability in muscle-invasive bladder Cancer patients undergoing radical cystectomy? Clinical genitourinary cancer. 2017;15(3):e411–20.CrossRef
17.
Gorgel SN, Kose O, Koc EM, Ates E, Akin Y, Yilmaz Y. The prognostic significance of preoperatively assessed AST/ALT (De Ritis) ratio on survival in patients underwent radical cystectomy. Int Urol Nephrol. 2017;49(9):1577–83.CrossRef
18.
D'Andrea D, Moschini M, Soria F, Gust KM, Briganti A, Karakiewicz PI, Roupret M, Shariat SF. ABO blood group and rhesus factor are not associated with outcomes after radical cystectomy for non-metastatic urothelial carcinoma of the bladder. Anticancer Res. 2017;37(10):5747–53.PubMed
19.
Crozier J, Papa N, Perera M, Stewart M, Goad J, Sengupta S, Bolton D, Lawrentschuk N. Lymph node yield in node-negative patients predicts cancer specific survival following radical cystectomy for transitional cell carcinoma. Investigative and clinical urology. 2017;58(6):416–22.CrossRef
20.
Morizawa Y, Miyake M, Shimada K, Hori S, Tatsumi Y, Nakai Y, Anai S, Tanaka N, Konishi N, Fujimoto K. Neutrophil-to-lymphocyte ratio as a detection marker of tumor recurrence in patients with muscle-invasive bladder cancer after radical cystectomy. Urologic oncology. 2016;34(6):257.e211–57.CrossRef
21.
Liu J, Dai Y, Zhou F, Long Z, Li Y, Liu B, Xie D, Tang J, Tan J, Yao K, et al. The prognostic role of preoperative serum albumin/globulin ratio in patients with bladder urothelial carcinoma undergoing radical cystectomy. Urologic oncology. 2016;34(11):484.e481–8.CrossRef
22.
Bostrom PJ, Mirtti T, van Rhijn B, Fleshner NE, Finelli A, Laato M, Jewett MA, Moore MJ, Sridhar S, Nurmi M, et al. Benefit of adjuvant chemotherapy and pelvic lymph node dissection in pT3 and node positive bladder Cancer patients treated with radical cystectomy. Bladder cancer. 2016;2(2):263–72.CrossRef
23.
Alimi Q, Verhoest G, Kammerer-Jacquet SF, Mathieu R, Rioux-Leclercq N, Manunta A, Laguerre B, Guille F, Bensalah K, Peyronnet B. Role of routine computed tomography scan in the oncological follow up of patients treated by radical cystectomy for bladder cancer. International journal of urology : official journal of the Japanese Urological Association. 2016;23(10):840–6.CrossRef
24.
Soave A, John LM, Dahlem R, Minner S, Engel O, Schmidt S, Kluth LA, Fisch M, Rink M. The impact of tumor diameter and tumor necrosis on oncologic outcomes in patients with urothelial carcinoma of the bladder treated with radical cystectomy. Urology. 2015;86(1):92–8.CrossRef
25.
Raza SJ, Wilson T, Peabody JO, Wiklund P, Scherr DS, Al-Daghmin A, Dibaj S, Khan MS, Dasgupta P, Mottrie A, et al. Long-term oncologic outcomes following robot-assisted radical cystectomy: results from the international robotic cystectomy consortium. Eur Urol. 2015;68(4):721–8.CrossRef
26.
Ozcan C, Telli O, Ozturk E, Suer E, Gokce MI, Gulpinar O, Oztuna D, Baltaci S, Gogus C: The prognostic significance of preoperative leukocytosis and neutrophil-to-lymphocyte ratio in patients who underwent radical cystectomy for bladder cancer. Canadian Urological Association journal = Journal de l'Association des urologues du Canada 2015, 9(11–12):E789–E794.CrossRef
27.
Kwon T, Jeong IG, Lee J, Lee C, You D, Hong B, Hong JH, Ahn H, Kim CS. Adjuvant chemotherapy after radical cystectomy for bladder cancer: a comparative study using inverse-probability-of-treatment weighting. J Cancer Res Clin Oncol. 2015;141(1):169–76.CrossRef
28.
Ferro M, De Cobelli O, Buonerba C, Di Lorenzo G, Capece M, Bruzzese D, Autorino R, Bottero D, Cioffi A, Matei DV, et al. Modified Glasgow prognostic score is associated with risk of recurrence in bladder Cancer patients after radical cystectomy: a multicenter experience. Medicine. 2015;94(42):e1861.CrossRef
29.
Booth CM, Siemens DR, Wei X, Peng Y, Berman DM, Mackillop WJ. Pathological factors associated with survival benefit from adjuvant chemotherapy (ACT): a population-based study of bladder cancer. BJU Int. 2015;116(3):373–81.CrossRef
30.
Albisinni S, Rassweiler J, Abbou CC, Cathelineau X, Chlosta P, Fossion L, Gaboardi F, Rimington P, Salomon L, Sanchez-Salas R, et al. Long-term analysis of oncological outcomes after laparoscopic radical cystectomy in Europe: results from a multicentre study by the European Association of Urology (EAU) section of Uro-technology. BJU Int. 2015;115(6):937–45.CrossRef
31.
Kawai T, Enomoto Y, Morikawa T, Matsushita H, Kume H, Fukayama M, Yamaguchi H, Kakimi K, Homma Y. High expression of heat shock protein 105 predicts a favorable prognosis for patients with urinary bladder cancer treated with radical cystectomy. Molecular and clinical oncology. 2014;2(1):38–42.CrossRef
32.
Kaushik D, Frank I, Eisenberg MS, Cheville JC, Tarrell R, Thapa P, Thompson RH, Boorjian SA. Gender-specific survival following radical cystectomy for pT4 bladder cancer. World J Urol. 2014;32(6):1433–9.CrossRef
33.
Brunocilla E, Pernetti R, Schiavina R, Borghesi M, Vagnoni V, Rocca GC, Borgatti F, Concetti S, Martorana G. The number of nodes removed as well as the template of the dissection is independently correlated to cancer-specific survival after radical cystectomy for muscle-invasive bladder cancer. Int Urol Nephrol. 2013;45(3):711–9.CrossRef
34.
Otto W, May M, Fritsche HM, Dragun D, Aziz A, Gierth M, Trojan L, Herrmann E, Moritz R, Ellinger J, et al. Analysis of sex differences in cancer-specific survival and perioperative mortality following radical cystectomy: results of a large German multicenter study of nearly 2500 patients with urothelial carcinoma of the bladder. Gend Med. 2012;9(6):481–9.CrossRef
35.
Gondo T, Nakashima J, Ozu C, Ohno Y, Horiguchi Y, Namiki K, Yoshioka K, Ohori M, Hatano T, Tachibana M. Risk stratification of survival by lymphovascular invasion, pathological stage, and surgical margin in patients with bladder cancer treated with radical cystectomy. Int J Clin Oncol. 2012;17(5):456–61.CrossRef
36.
Yafi FA, Aprikian AG, Chin JL, Fradet Y, Izawa J, Estey E, Fairey A, Rendon R, Cagiannos I, Lacombe L, et al. Contemporary outcomes of 2287 patients with bladder cancer who were treated with radical cystectomy: a Canadian multicentre experience. BJU Int. 2011;108(4):539–45.CrossRef
37.
Rodriguez Faba O, Palou J, Rosales A, Breda A, Algaba F, Urdaneta G, Villavicencio H. Clinical predictive factors of poor outcome in patients with stage pT0 disease at radical cystectomy. J Urol. 2011;186(2):442–7.CrossRef
38.
Muramaki M, Miyake H, Kurahashi T, Takenaka A, Inoue TA, Fujisawa M. Prognostic significance of adjuvant cisplatin-based combination chemotherapy following radical cystectomy in patients with invasive bladder cancer. International journal of urology : official journal of the Japanese Urological Association. 2008;15(4):314–8.CrossRef
39.
Turkolmez K, Tokgoz H, Resorlu B, Kose K, Beduk Y. Muscle-invasive bladder cancer: predictive factors and prognostic difference between primary and progressive tumors. Urology. 2007;70(3):477–81.CrossRef
40.
Karam JA, Lotan Y, Karakiewicz PI, Ashfaq R, Sagalowsky AI, Roehrborn CG, Shariat SF. Use of combined apoptosis biomarkers for prediction of bladder cancer recurrence and mortality after radical cystectomy. The Lancet Oncology. 2007;8(2):128–36.CrossRef
41.
Stein JP, Lieskovsky G, Cote R, Groshen S, Feng AC, Boyd S, Skinner E, Bochner B, Thangathurai D, Mikhail M, et al. Radical cystectomy in the treatment of invasive bladder cancer: long-term results in 1,054 patients. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2001;19(3):666–75.CrossRef
42.
Tilki D, Reich O, Karakiewicz PI, Novara G, Kassouf W, Ergun S, Fradet Y, Ficarra V, Sonpavde G, Stief CG, et al. Validation of the AJCC TNM substaging of pT2 bladder cancer: deep muscle invasion is associated with significantly worse outcome. Eur Urol. 2010;58(1):112–7.CrossRef
43.
Rieken M, Shariat SF, Kluth L, Crivelli JJ, Abufaraj M, Foerster B, Mari A, Ilijazi D, Karakiewicz PI, Babjuk M, et al. Comparison of the EORTC tables and the EAU categories for risk stratification of patients with nonmuscle-invasive bladder cancer. Urologic oncology. 2018;36(1):8.e17–18.e24.CrossRef
44.
Warrick JI, Kaag M, Raman JD, Chan W, Tran T, Kunchala S, Shuman L, DeGraff D, Chen G. FOXA1 and CK14 as markers of luminal and basal subtypes in histologic variants of bladder cancer and their associated conventional urothelial carcinoma. Virchows Archiv : an international journal of pathology. 2017;471(3):337–45.CrossRef
45.
Shariat SF, Savage C, Chromecki TF, Sun M, Scherr DS, Lee RK, Lughezzani G, Remzi M, Marberger MJ, Karakiewicz PI, et al. Assessing the clinical benefit of nuclear matrix protein 22 in the surveillance of patients with nonmuscle-invasive bladder cancer and negative cytology: a decision-curve analysis. Cancer. 2011;117(13):2892–7.CrossRef
46.
Guo A, Wang X, Gao L, Shi J, Sun C, Wan Z. Bladder tumour antigen (BTA stat) test compared to the urine cytology in the diagnosis of bladder cancer: A meta-analysis. Canadian Urological Association journal = Journal de l'Association des urologues du Canada. 2014;8(5–6):E347–52.CrossRef
47.
Moschini M, Shariat SF, Abufaraj M, Soria F, Klatte T, Croce G, Mattei A, Damiano R, Salonia A, Montorsi F, et al. The presence of carcinoma in situ at radical cystectomy increases the risk of urothelial recurrence: Implications for follow-up schemes. Urologic oncology. 2017;35(4):151.e117–23.CrossRef
48.
Nuhn P, Bastian PJ, Novara G, Svatek RS, Karakiewicz PI, Skinner E, Fradet Y, Izawa JI, Kassouf W, Montorsi F, et al. Concomitant carcinoma in situ in cystectomy specimens is not associated with clinical outcomes after surgery. Urol Int. 2011;87(1):42–8.CrossRef
49.
Scosyrev E, Golijanin D, Wu G, Messing E. The burden of bladder cancer in men and women: analysis of the years of life lost. BJU Int. 2012;109(1):57–62.CrossRef
50.
Raghavan D, Bawtinhimer A, Mahoney J, Eckrich S, Riggs S. Adjuvant chemotherapy for bladder cancer-why does level 1 evidence not support it? Annals of oncology : official journal of the European Society for Medical Oncology. 2014;25(10):1930–4.CrossRef
51.
Egger M, Zellweger-Zahner T, Schneider M, Junker C, Lengeler C, Antes G. Language bias in randomised controlled trials published in English and German. Lancet (London, England). 1997;350(9074):326–9.CrossRef
Metadata
Title
Clinicopathological factors in bladder cancer for cancer-specific survival outcomes following radical cystectomy: a systematic review and meta-analysis
Authors
Lijin Zhang
Bin Wu
Zhenlei Zha
Wei Qu
Hu Zhao
Jun Yuan
Publication date
01-12-2019
Publisher
BioMed Central
Keyword
Cystectomy
Published in
BMC Cancer / Issue 1/2019
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-019-5924-6

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