Skip to main content
Top
Published in: World Journal of Surgical Oncology 1/2014

Open Access 01-12-2014 | Research

The impact of cyclin D1 overexpression on the prognosis of bladder cancer: a meta-analysis

Authors: Baoming Ren, Wenjun Li, Yanping Yang, Songdi Wu

Published in: World Journal of Surgical Oncology | Issue 1/2014

Login to get access

Abstract

Background

To evaluate the relationship between cyclin D1 overexpression and bladder cancer prognosis.

Methods

A systematic literature search up to July 27, 2013 was carried out in PubMed and Wanfang databases, and the references of retrieved articles were screened. The hazard ratios (HRs) and their 95% CIs were used to combine the data. Heterogeneity and publication bias were also evaluated.

Results

A total of 15 studies containing 2,591 cases were included. We found that increased cyclin D1 levels were significantly correlated with progression-free survival with a pooled HR estimate of 0.54 (95% CI: 0.32–0.92). There was a significant degree of heterogeneity (I2 = 93.8%, P <0.001). Moreover, subgroup analysis indicated that elevated cyclin D1 levels were significantly associated with overall survival in muscle-invasive bladder patients (HR: 0.95, 95% CI: 0.91–0.99), without a significant heterogeneity in the data (I2 = 0.0%, P = 0.456).

Conclusions

Increased cyclin D1 expression level detected by immunohistochemistry is associated with good progression-free survival for bladder cancer. Because of the limited number of studies, further well-designed prospective studies are warranted to confirm the findings from our study.
Appendix
Available only for authorised users
Literature
1.
go back to reference Ploeg M, Aben KK, Kiemeney LA: The present and future burden of urinary bladder cancer in the world. World J Urol. 2009, 27: 289-293. 10.1007/s00345-009-0383-3.PubMedCentralCrossRefPubMed Ploeg M, Aben KK, Kiemeney LA: The present and future burden of urinary bladder cancer in the world. World J Urol. 2009, 27: 289-293. 10.1007/s00345-009-0383-3.PubMedCentralCrossRefPubMed
2.
go back to reference Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D: Global cancer statistics. CA Cancer J Clin. 2011, 61: 69-90. 10.3322/caac.20107.CrossRefPubMed Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D: Global cancer statistics. CA Cancer J Clin. 2011, 61: 69-90. 10.3322/caac.20107.CrossRefPubMed
3.
go back to reference Baumgart E, Cohen MS, Silva Neto B, Jacobs MA, Wotkowicz C, Rieger-Christ KM, Biolo A, Zeheb R, Loda M, Libertino JA, Summerhayes IC: Identification and prognostic significance of an epithelial-mesenchymal transition expression profile in human bladder tumors. Clin Cancer Res. 2007, 13: 1685-1694. 10.1158/1078-0432.CCR-06-2330.CrossRefPubMed Baumgart E, Cohen MS, Silva Neto B, Jacobs MA, Wotkowicz C, Rieger-Christ KM, Biolo A, Zeheb R, Loda M, Libertino JA, Summerhayes IC: Identification and prognostic significance of an epithelial-mesenchymal transition expression profile in human bladder tumors. Clin Cancer Res. 2007, 13: 1685-1694. 10.1158/1078-0432.CCR-06-2330.CrossRefPubMed
4.
go back to reference Shariat SF, Bolenz C, Karakiewicz PI, Fradet Y, Ashfaq R, Bastian PJ, Nielsen ME, Capitanio U, Jeldres C, Rigaud J, Müller SC, Lerner SP, Montorsi F, Sagalowsky AI, Cote RJ, Lotan Y: p53 expression in patients with advanced urothelial cancer of the urinary bladder. BJU Int. 2010, 105: 489-495. 10.1111/j.1464-410X.2009.08742.x.CrossRefPubMed Shariat SF, Bolenz C, Karakiewicz PI, Fradet Y, Ashfaq R, Bastian PJ, Nielsen ME, Capitanio U, Jeldres C, Rigaud J, Müller SC, Lerner SP, Montorsi F, Sagalowsky AI, Cote RJ, Lotan Y: p53 expression in patients with advanced urothelial cancer of the urinary bladder. BJU Int. 2010, 105: 489-495. 10.1111/j.1464-410X.2009.08742.x.CrossRefPubMed
5.
go back to reference Fauconnet S, Bernardini S, Lascombe I, Boiteux G, Clairotte A, Monnien F, Chabannes E, Bittard H: Expression analysis of VEGF-A and VEGF-B: relationship with clinicopathological parameters in bladder cancer. Oncol Rep. 2009, 21: 1495-1504.CrossRefPubMed Fauconnet S, Bernardini S, Lascombe I, Boiteux G, Clairotte A, Monnien F, Chabannes E, Bittard H: Expression analysis of VEGF-A and VEGF-B: relationship with clinicopathological parameters in bladder cancer. Oncol Rep. 2009, 21: 1495-1504.CrossRefPubMed
6.
go back to reference Strauss M, Lukas J, Bartek J: Unrestricted cell cycling and cancer. Nat Med. 1995, 1: 1245-1246. 10.1038/nm1295-1245.CrossRefPubMed Strauss M, Lukas J, Bartek J: Unrestricted cell cycling and cancer. Nat Med. 1995, 1: 1245-1246. 10.1038/nm1295-1245.CrossRefPubMed
7.
go back to reference Niehans GA, Kratzke RA, Froberg MK, Aeppli DM, Nguyen PL, Geradts J: G1 checkpoint protein and p53 abnormalities occur in most invasive transitional cell carcinomas of the urinary bladder. Br J Cancer. 1999, 80: 1175-1184. 10.1038/sj.bjc.6990483.PubMedCentralCrossRefPubMed Niehans GA, Kratzke RA, Froberg MK, Aeppli DM, Nguyen PL, Geradts J: G1 checkpoint protein and p53 abnormalities occur in most invasive transitional cell carcinomas of the urinary bladder. Br J Cancer. 1999, 80: 1175-1184. 10.1038/sj.bjc.6990483.PubMedCentralCrossRefPubMed
8.
go back to reference Moher D, Liberati A, Tetzlaff J, Altman DG: Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009, 6: e1000097-10.1371/journal.pmed.1000097.PubMedCentralCrossRefPubMed Moher D, Liberati A, Tetzlaff J, Altman DG: Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009, 6: e1000097-10.1371/journal.pmed.1000097.PubMedCentralCrossRefPubMed
9.
go back to reference Parmar MK, Torri V, Stewart L: Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med. 1998, 17: 2815-2834. 10.1002/(SICI)1097-0258(19981230)17:24<2815::AID-SIM110>3.0.CO;2-8.CrossRefPubMed Parmar MK, Torri V, Stewart L: Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med. 1998, 17: 2815-2834. 10.1002/(SICI)1097-0258(19981230)17:24<2815::AID-SIM110>3.0.CO;2-8.CrossRefPubMed
10.
go back to reference DerSimonian R, Laird N: Meta-analysis in clinical trials. Control Clin Trials. 1986, 7: 177-188. 10.1016/0197-2456(86)90046-2.CrossRefPubMed DerSimonian R, Laird N: Meta-analysis in clinical trials. Control Clin Trials. 1986, 7: 177-188. 10.1016/0197-2456(86)90046-2.CrossRefPubMed
11.
go back to reference Begg CB, Mazumdar M: Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994, 50: 1088-1101. 10.2307/2533446.CrossRefPubMed Begg CB, Mazumdar M: Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994, 50: 1088-1101. 10.2307/2533446.CrossRefPubMed
12.
go back to reference Egger M, Davey Smith G, Schneider M, Minder C: Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997, 315: 629-634. 10.1136/bmj.315.7109.629.PubMedCentralCrossRefPubMed Egger M, Davey Smith G, Schneider M, Minder C: Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997, 315: 629-634. 10.1136/bmj.315.7109.629.PubMedCentralCrossRefPubMed
13.
go back to reference Shin KY, Kong G, Kim WS, Lee TY, Woo YN, Lee JD: Overexpression of cyclin D1 correlates with early recurrence in superficial bladder cancers. Br J Cancer. 1997, 75: 1788-1792. 10.1038/bjc.1997.305.PubMedCentralCrossRefPubMed Shin KY, Kong G, Kim WS, Lee TY, Woo YN, Lee JD: Overexpression of cyclin D1 correlates with early recurrence in superficial bladder cancers. Br J Cancer. 1997, 75: 1788-1792. 10.1038/bjc.1997.305.PubMedCentralCrossRefPubMed
14.
go back to reference Liukkonen T, Lipponen P, Raitanen M, Kaasinen E, Ala-Opas M, Rajala P, Kosma VM: Evaluation of p21WAF1/CIP1 and cyclin D1 expression in the progression of superficial bladder cancer. Finbladder Group. Urol Res. 2000, 28: 285-292. 10.1007/s002400000116.CrossRefPubMed Liukkonen T, Lipponen P, Raitanen M, Kaasinen E, Ala-Opas M, Rajala P, Kosma VM: Evaluation of p21WAF1/CIP1 and cyclin D1 expression in the progression of superficial bladder cancer. Finbladder Group. Urol Res. 2000, 28: 285-292. 10.1007/s002400000116.CrossRefPubMed
15.
go back to reference Takagi Y, Takashi M, Koshikawa T, Sakata T, Ohshima S: Immunohistochemical demonstration of cyclin D1 in bladder cancers as an inverse indicator of invasiveness but not an independent prognostic factor. Int J Urol. 2000, 7: 366-372. 10.1046/j.1442-2042.2000.00212.x.CrossRefPubMed Takagi Y, Takashi M, Koshikawa T, Sakata T, Ohshima S: Immunohistochemical demonstration of cyclin D1 in bladder cancers as an inverse indicator of invasiveness but not an independent prognostic factor. Int J Urol. 2000, 7: 366-372. 10.1046/j.1442-2042.2000.00212.x.CrossRefPubMed
16.
go back to reference Tut VM, Braithwaite KL, Angus B, Neal DE, Lunec J, Mellon JK: Cyclin D1 expression in transitional cell carcinoma of the bladder: correlation with p53, waf1, pRb and Ki67. Br J Cancer. 2001, 84: 270-275. 10.1054/bjoc.2000.1557.PubMedCentralCrossRefPubMed Tut VM, Braithwaite KL, Angus B, Neal DE, Lunec J, Mellon JK: Cyclin D1 expression in transitional cell carcinoma of the bladder: correlation with p53, waf1, pRb and Ki67. Br J Cancer. 2001, 84: 270-275. 10.1054/bjoc.2000.1557.PubMedCentralCrossRefPubMed
17.
go back to reference Sgambato A, Migaldi M, Faraglia B, De Aloysio G, Ferrari P, Ardito R, De Gaetani C, Capelli G, Cittadini A, Trentini GP: Cyclin D1 expression in papillary superficial bladder cancer: its association with other cell cycle-associated proteins, cell proliferation and clinical outcome. Int J Cancer. 2002, 97: 671-678. 10.1002/ijc.10055.CrossRefPubMed Sgambato A, Migaldi M, Faraglia B, De Aloysio G, Ferrari P, Ardito R, De Gaetani C, Capelli G, Cittadini A, Trentini GP: Cyclin D1 expression in papillary superficial bladder cancer: its association with other cell cycle-associated proteins, cell proliferation and clinical outcome. Int J Cancer. 2002, 97: 671-678. 10.1002/ijc.10055.CrossRefPubMed
18.
go back to reference Lopez-Beltran A, Luque RJ, Alvarez-Kindelan J, Quintero A, Merlo F, Requena MJ, Montironi R: Prognostic factors in survival of patients with stage Ta and T1 bladder urothelial tumors: the role of G1-S modulators (p53, p21Waf1, p27Kip1, cyclin D1, and cyclin D3), proliferation index, and clinicopathologic parameters. Am J Clin Pathol. 2004, 122: 444-452. 10.1309/LTFU3UUMBY095HUM.CrossRefPubMed Lopez-Beltran A, Luque RJ, Alvarez-Kindelan J, Quintero A, Merlo F, Requena MJ, Montironi R: Prognostic factors in survival of patients with stage Ta and T1 bladder urothelial tumors: the role of G1-S modulators (p53, p21Waf1, p27Kip1, cyclin D1, and cyclin D3), proliferation index, and clinicopathologic parameters. Am J Clin Pathol. 2004, 122: 444-452. 10.1309/LTFU3UUMBY095HUM.CrossRefPubMed
19.
go back to reference Mhawech P, Greloz V, Oppikofer C, Szalay-Quinodoz I, Herrmann F: Expression of cell cycle proteins in T1a and T1b urothelial bladder carcinoma and their value in predicting tumor progression. Cancer. 2004, 100: 2367-2375. 10.1002/cncr.20306.CrossRefPubMed Mhawech P, Greloz V, Oppikofer C, Szalay-Quinodoz I, Herrmann F: Expression of cell cycle proteins in T1a and T1b urothelial bladder carcinoma and their value in predicting tumor progression. Cancer. 2004, 100: 2367-2375. 10.1002/cncr.20306.CrossRefPubMed
20.
go back to reference Galmozzi F, Rubagotti A, Romagnoli A, Carmignani G, Perdelli L, Gatteschi B, Boccardo F: Prognostic value of cell cycle regulatory proteins in muscle-infiltrating bladder cancer. J Cancer Res Clin Oncol. 2006, 132: 757-764. 10.1007/s00432-006-0123-7.CrossRefPubMed Galmozzi F, Rubagotti A, Romagnoli A, Carmignani G, Perdelli L, Gatteschi B, Boccardo F: Prognostic value of cell cycle regulatory proteins in muscle-infiltrating bladder cancer. J Cancer Res Clin Oncol. 2006, 132: 757-764. 10.1007/s00432-006-0123-7.CrossRefPubMed
21.
go back to reference Yurakh AO, Ramos D, Calabuig-Farinas S, Lopez-Guerrero JA, Rubio J, Solsona E, Romanenko AM, Vozianov AF, Pellin A, Llombart-Bosch A: Molecular and immunohistochemical analysis of the prognostic value of cell-cycle regulators in urothelial neoplasms of the bladder. Eur Urol. 2006, 50: 506-515. 10.1016/j.eururo.2006.03.027. discussion 515CrossRefPubMed Yurakh AO, Ramos D, Calabuig-Farinas S, Lopez-Guerrero JA, Rubio J, Solsona E, Romanenko AM, Vozianov AF, Pellin A, Llombart-Bosch A: Molecular and immunohistochemical analysis of the prognostic value of cell-cycle regulators in urothelial neoplasms of the bladder. Eur Urol. 2006, 50: 506-515. 10.1016/j.eururo.2006.03.027. discussion 515CrossRefPubMed
22.
go back to reference Shariat SF, Ashfaq R, Sagalowsky AI, Lotan Y: Association of cyclin D1 and E1 expression with disease progression and biomarkers in patients with nonmuscle-invasive urothelial cell carcinoma of the bladder. Urol Oncol. 2007, 25: 468-475. 10.1016/j.urolonc.2006.09.011.CrossRefPubMed Shariat SF, Ashfaq R, Sagalowsky AI, Lotan Y: Association of cyclin D1 and E1 expression with disease progression and biomarkers in patients with nonmuscle-invasive urothelial cell carcinoma of the bladder. Urol Oncol. 2007, 25: 468-475. 10.1016/j.urolonc.2006.09.011.CrossRefPubMed
23.
go back to reference Lee K, Jung ES, Choi YJ, Lee KY, Lee A: Expression of pRb, p53, p16 and cyclin D1 and their clinical implications in urothelial carcinoma. J Korean Med Sci. 2010, 25: 1449-1455. 10.3346/jkms.2010.25.10.1449.PubMedCentralCrossRefPubMed Lee K, Jung ES, Choi YJ, Lee KY, Lee A: Expression of pRb, p53, p16 and cyclin D1 and their clinical implications in urothelial carcinoma. J Korean Med Sci. 2010, 25: 1449-1455. 10.3346/jkms.2010.25.10.1449.PubMedCentralCrossRefPubMed
24.
go back to reference Levidou G, Saetta AA, Karlou M, Thymara I, Pratsinis H, Pavlopoulos P, Isaiadis D, Diamantopoulou K, Patsouris E, Korkolopoulou P: D-type cyclins in superficial and muscle-invasive bladder urothelial carcinoma: correlation with clinicopathological data and prognostic significance. J Cancer Res Clin Oncol. 2010, 136: 1563-1571. 10.1007/s00432-010-0814-y.CrossRefPubMed Levidou G, Saetta AA, Karlou M, Thymara I, Pratsinis H, Pavlopoulos P, Isaiadis D, Diamantopoulou K, Patsouris E, Korkolopoulou P: D-type cyclins in superficial and muscle-invasive bladder urothelial carcinoma: correlation with clinicopathological data and prognostic significance. J Cancer Res Clin Oncol. 2010, 136: 1563-1571. 10.1007/s00432-010-0814-y.CrossRefPubMed
25.
go back to reference Behnsawy HM, Miyake H, Abdalla MA, Sayed MA, Ahmed Ael F, Fujisawa M: Expression of cell cycle-associated proteins in non-muscle-invasive bladder cancer: correlation with intravesical recurrence following transurethral resection. Urol Oncol. 2011, 29: 495-501. 10.1016/j.urolonc.2009.08.002.CrossRefPubMed Behnsawy HM, Miyake H, Abdalla MA, Sayed MA, Ahmed Ael F, Fujisawa M: Expression of cell cycle-associated proteins in non-muscle-invasive bladder cancer: correlation with intravesical recurrence following transurethral resection. Urol Oncol. 2011, 29: 495-501. 10.1016/j.urolonc.2009.08.002.CrossRefPubMed
26.
go back to reference Olsson H, Hultman P, Monsef N, Rosell J, Jahnson S: Immunohistochemical evaluation of cell cycle regulators: impact on predicting prognosis in stage t1 urinary bladder cancer. ISRN Urol. 2012, 2012: 379081-PubMedCentralPubMed Olsson H, Hultman P, Monsef N, Rosell J, Jahnson S: Immunohistochemical evaluation of cell cycle regulators: impact on predicting prognosis in stage t1 urinary bladder cancer. ISRN Urol. 2012, 2012: 379081-PubMedCentralPubMed
27.
go back to reference Fristrup N, Birkenkamp-Demtroder K, Reinert T, Sanchez-Carbayo M, Segersten U, Malmstrom PU, Palou J, Alvarez-Mugica M, Pan CC, Ulhoi BP, Borre M, Ørntoft TF, Dyrskjøt L: Multicenter validation of cyclin D1, MCM7, TRIM29, and UBE2C as prognostic protein markers in non-muscle-invasive bladder cancer. Am J Pathol. 2013, 182: 339-349. 10.1016/j.ajpath.2012.10.017.CrossRefPubMed Fristrup N, Birkenkamp-Demtroder K, Reinert T, Sanchez-Carbayo M, Segersten U, Malmstrom PU, Palou J, Alvarez-Mugica M, Pan CC, Ulhoi BP, Borre M, Ørntoft TF, Dyrskjøt L: Multicenter validation of cyclin D1, MCM7, TRIM29, and UBE2C as prognostic protein markers in non-muscle-invasive bladder cancer. Am J Pathol. 2013, 182: 339-349. 10.1016/j.ajpath.2012.10.017.CrossRefPubMed
28.
29.
go back to reference Jirawatnotai S, Hu Y, Michowski W, Elias JE, Becks L, Bienvenu F, Zagozdzon A, Goswami T, Wang YE, Clark AB, Kunkel TA, van Harn T, Xia B, Correll M, Quackenbush J, Livingston DM, Gygi SP, Sicinski P: A function for cyclin D1 in DNA repair uncovered by protein interactome analyses in human cancers. Nature. 2011, 474: 230-234. 10.1038/nature10155.PubMedCentralCrossRefPubMed Jirawatnotai S, Hu Y, Michowski W, Elias JE, Becks L, Bienvenu F, Zagozdzon A, Goswami T, Wang YE, Clark AB, Kunkel TA, van Harn T, Xia B, Correll M, Quackenbush J, Livingston DM, Gygi SP, Sicinski P: A function for cyclin D1 in DNA repair uncovered by protein interactome analyses in human cancers. Nature. 2011, 474: 230-234. 10.1038/nature10155.PubMedCentralCrossRefPubMed
30.
go back to reference Xu XL, Chen SZ, Chen W, Zheng WH, Xia XH, Yang HJ, Li B, Mao WM: The impact of cyclin D1 overexpression on the prognosis of ER-positive breast cancers: a meta-analysis. Breast Cancer Res Treat. 2013, 139: 329-339. 10.1007/s10549-013-2563-5.CrossRefPubMed Xu XL, Chen SZ, Chen W, Zheng WH, Xia XH, Yang HJ, Li B, Mao WM: The impact of cyclin D1 overexpression on the prognosis of ER-positive breast cancers: a meta-analysis. Breast Cancer Res Treat. 2013, 139: 329-339. 10.1007/s10549-013-2563-5.CrossRefPubMed
31.
go back to reference Zhao J, Li L, Wei S, Gao Y, Chen Y, Wang G, Wu Z: Clinicopathological and prognostic role of cyclin D1 in esophageal squamous cell carcinoma: a meta-analysis. Dis Esophagus. 2012, 25: 520-526. 10.1111/j.1442-2050.2011.01278.x.CrossRefPubMed Zhao J, Li L, Wei S, Gao Y, Chen Y, Wang G, Wu Z: Clinicopathological and prognostic role of cyclin D1 in esophageal squamous cell carcinoma: a meta-analysis. Dis Esophagus. 2012, 25: 520-526. 10.1111/j.1442-2050.2011.01278.x.CrossRefPubMed
32.
go back to reference Rainsbury JW, Ahmed W, Williams HK, Roberts S, Paleri V, Mehanna H: Prognostic biomarkers of survival in oropharyngeal squamous cell carcinoma: systematic review and meta-analysis. Head Neck. 2013, 35: 1048-1055. 10.1002/hed.22950.CrossRefPubMed Rainsbury JW, Ahmed W, Williams HK, Roberts S, Paleri V, Mehanna H: Prognostic biomarkers of survival in oropharyngeal squamous cell carcinoma: systematic review and meta-analysis. Head Neck. 2013, 35: 1048-1055. 10.1002/hed.22950.CrossRefPubMed
Metadata
Title
The impact of cyclin D1 overexpression on the prognosis of bladder cancer: a meta-analysis
Authors
Baoming Ren
Wenjun Li
Yanping Yang
Songdi Wu
Publication date
01-12-2014
Publisher
BioMed Central
Published in
World Journal of Surgical Oncology / Issue 1/2014
Electronic ISSN: 1477-7819
DOI
https://doi.org/10.1186/1477-7819-12-55

Other articles of this Issue 1/2014

World Journal of Surgical Oncology 1/2014 Go to the issue