Skip to main content
Top
Published in: Archives of Gynecology and Obstetrics 5/2019

01-05-2019 | Ovarian Cancer | Gynecologic Oncology

High Ki-67 expression is significantly associated with poor prognosis of ovarian cancer patients: evidence from a meta-analysis

Authors: Dongmei Qiu, Wanqiu Cai, Zhiqiao Zhang, Hongyan Li, Dongmei Zhou

Published in: Archives of Gynecology and Obstetrics | Issue 5/2019

Login to get access

Abstract

Objective

The prognostic significance of Ki-67 expression in patients with ovarian cancer was controversial in various studies. Therefore, we carried out a meta-analysis to determine the prognostic significance of Ki-67 in ovarian cancer patients.

Methods

We searched PubMed, Cochrane Library, EMBASE, Web of Knowledge, China National Knowledge Infrastructure database and WanFang digital database for eligible studies from January 1, 1990 to June 1, 2017. The pooled hazard ratios and 95% confidence intervals were calculated to assess the prognostic significance of Ki-67 expression for overall survival in ovarian cancer patients.

Results

Finally, 38 eligible studies and 5004 ovarian cancer patients were included in the current study. The pooled hazard ratio was 1.35 (95% confidence interval 1.24–1.46, P = 0.001) for overall survival in ovarian cancer patients. The funnel plot bias was obviously asymmetrical and Egger’s test also detected significant publication bias (P = 0.001). The Contour-enhanced funnel plot with trim-and-fill method supplemented 11 dummy studies to balance the funnel plot and nine new supplementary studies were in area with statistical significance. Sensitivity analysis and cumulative meta-analysis further demonstrated that the association between high Ki-67 expression and poor overall survival of ovarian cancer patients was stable and reliable.

Conclusions

High Ki-67 expression is significantly related to poor overall survival and may serve as a prognostic biomarker for ovarian cancer patients.
Appendix
Available only for authorised users
Literature
3.
go back to reference Schluter C, Duchrow M, Wohlenberg C, Becker MH, Key G, Flad HD et al (1993) The cell proliferation-associated antigen of antibody Ki-67: a very large, ubiquitous nuclear protein with numerous repeated elements, representing a new kind of cell cycle-maintaining proteins. J Cell Biol 123:513–522CrossRefPubMed Schluter C, Duchrow M, Wohlenberg C, Becker MH, Key G, Flad HD et al (1993) The cell proliferation-associated antigen of antibody Ki-67: a very large, ubiquitous nuclear protein with numerous repeated elements, representing a new kind of cell cycle-maintaining proteins. J Cell Biol 123:513–522CrossRefPubMed
4.
go back to reference Cattoretti G, Becker MH, Key G, Duchrow M, Schluter C, Galle J et al (1992) Monoclonal antibodies against recombinant parts of the Ki-67 antigen (MIB 1 and MIB 3) detect proliferating cells in microwave-processed formalin-fixed paraffin sections. J Pathol 168:357–363CrossRefPubMed Cattoretti G, Becker MH, Key G, Duchrow M, Schluter C, Galle J et al (1992) Monoclonal antibodies against recombinant parts of the Ki-67 antigen (MIB 1 and MIB 3) detect proliferating cells in microwave-processed formalin-fixed paraffin sections. J Pathol 168:357–363CrossRefPubMed
5.
go back to reference Felix AS, Sherman ME, Hewitt SM, Gunja MZ, Yang HP, Cora RL et al (2015) Cell-cycle protein expression in a population-based study of ovarian and endometrial cancers. Front Oncol 5:25CrossRefPubMedPubMedCentral Felix AS, Sherman ME, Hewitt SM, Gunja MZ, Yang HP, Cora RL et al (2015) Cell-cycle protein expression in a population-based study of ovarian and endometrial cancers. Front Oncol 5:25CrossRefPubMedPubMedCentral
6.
go back to reference Hua M, Yan S, Deng Y, Xi Q, Liu R, Yang S et al (2015) CAP1 is overexpressed in human epithelial ovarian cancer and promotes cell proliferation. Int J Mol Med 35:941–949CrossRefPubMedPubMedCentral Hua M, Yan S, Deng Y, Xi Q, Liu R, Yang S et al (2015) CAP1 is overexpressed in human epithelial ovarian cancer and promotes cell proliferation. Int J Mol Med 35:941–949CrossRefPubMedPubMedCentral
7.
go back to reference Deng Y, Chen C, Hua M, Xi Q, Liu R, Yang S et al (2015) Annexin A2 plays a critical role in epithelial ovarian cancer. Arch Gynecol Obstet 292:175–182CrossRefPubMed Deng Y, Chen C, Hua M, Xi Q, Liu R, Yang S et al (2015) Annexin A2 plays a critical role in epithelial ovarian cancer. Arch Gynecol Obstet 292:175–182CrossRefPubMed
8.
go back to reference Battista MJ, Mantai N, Sicking I, Cotarelo C, Weyer V, Lebrecht A et al (2014) Ki-67 as an independent prognostic factor in an unselected cohort of patients with ovarian cancer: results of an explorative, retrospective study. Oncol Rep 31:2213–2219CrossRefPubMed Battista MJ, Mantai N, Sicking I, Cotarelo C, Weyer V, Lebrecht A et al (2014) Ki-67 as an independent prognostic factor in an unselected cohort of patients with ovarian cancer: results of an explorative, retrospective study. Oncol Rep 31:2213–2219CrossRefPubMed
9.
go back to reference Vallen MJ, Massuger LF, Ten DG, Bulten JV, Kuppevelt TH (2012) Highly sulfated chondroitin sulfates, a novel class of prognostic biomarkers in ovarian cancer tissue. Gynecol Oncol 127:202–209CrossRefPubMed Vallen MJ, Massuger LF, Ten DG, Bulten JV, Kuppevelt TH (2012) Highly sulfated chondroitin sulfates, a novel class of prognostic biomarkers in ovarian cancer tissue. Gynecol Oncol 127:202–209CrossRefPubMed
10.
go back to reference Kim H, Kim K, No JH, Jeon YT, Jeon HW, Kim YB (2012) Prognostic value of biomarkers related to drug resistance in patients with advanced epithelial ovarian cancer. Anticancer Res 32:589–594CrossRefPubMed Kim H, Kim K, No JH, Jeon YT, Jeon HW, Kim YB (2012) Prognostic value of biomarkers related to drug resistance in patients with advanced epithelial ovarian cancer. Anticancer Res 32:589–594CrossRefPubMed
11.
go back to reference Lu M, Xiang J, Xu F, Wang Y, Yin Y, Chen D (2012) The expression and significance of pThr32-FOXO3a in human ovarian cancer. Med Oncol 29:1258–1264CrossRefPubMed Lu M, Xiang J, Xu F, Wang Y, Yin Y, Chen D (2012) The expression and significance of pThr32-FOXO3a in human ovarian cancer. Med Oncol 29:1258–1264CrossRefPubMed
12.
go back to reference Lee JS, Choi YD, Choi C, Lee MC, Park CS, Min KW (2005) Expression of PTEN in ovarian epithelial tumors and its relation to tumor behavior and growth. Anal Quant Cytol Histol 27:202–210PubMed Lee JS, Choi YD, Choi C, Lee MC, Park CS, Min KW (2005) Expression of PTEN in ovarian epithelial tumors and its relation to tumor behavior and growth. Anal Quant Cytol Histol 27:202–210PubMed
13.
go back to reference Khalifeh I, Munkarah AR, Schimp V, Morris R, Lawrence WD, Ali-Fehmi R (2005) The impact of c-kit and ki-67 expression on patients prognosis in advanced ovarian serous carcinoma. Int J Gynecol Pathol 24:228–234CrossRefPubMed Khalifeh I, Munkarah AR, Schimp V, Morris R, Lawrence WD, Ali-Fehmi R (2005) The impact of c-kit and ki-67 expression on patients prognosis in advanced ovarian serous carcinoma. Int J Gynecol Pathol 24:228–234CrossRefPubMed
14.
go back to reference Ali-Fehmi R, Morris RT, Bandyopadhyay S, Che M, Schimp V, Malone JM et al (2005) Expression of cyclooxygenase-2 in advanced stage ovarian serous carcinoma: correlation with tumor cell proliferation, apoptosis, angiogenesis, and survival. Am J Obstet Gynecol 192:819–825CrossRefPubMed Ali-Fehmi R, Morris RT, Bandyopadhyay S, Che M, Schimp V, Malone JM et al (2005) Expression of cyclooxygenase-2 in advanced stage ovarian serous carcinoma: correlation with tumor cell proliferation, apoptosis, angiogenesis, and survival. Am J Obstet Gynecol 192:819–825CrossRefPubMed
15.
go back to reference Nakayama K, Takebayashi Y, Hata K, Fujiwaki R, Iida K, Fukumoto M et al (2004) Allelic loss at 19q12 and Xq11-12 predict an adverse clinical outcome in patients with mucinous ovarian tumours of low malignant potential. Br J Cancer 90:1204–1210CrossRefPubMedPubMedCentral Nakayama K, Takebayashi Y, Hata K, Fujiwaki R, Iida K, Fukumoto M et al (2004) Allelic loss at 19q12 and Xq11-12 predict an adverse clinical outcome in patients with mucinous ovarian tumours of low malignant potential. Br J Cancer 90:1204–1210CrossRefPubMedPubMedCentral
16.
go back to reference Layfield LJ, Saria EA, Berchuck A, Dodge RK, Thompson JK, Conlon DH et al (1997) Prognostic value of MIB-1 in advanced ovarian carcinoma as determined using automated immunohistochemistry and quantitative image analysis. J Surg Oncol 66:230–237CrossRefPubMed Layfield LJ, Saria EA, Berchuck A, Dodge RK, Thompson JK, Conlon DH et al (1997) Prognostic value of MIB-1 in advanced ovarian carcinoma as determined using automated immunohistochemistry and quantitative image analysis. J Surg Oncol 66:230–237CrossRefPubMed
17.
go back to reference Wang K, Li D, Sun L (2016) High levels of EGFR expression in tumor stroma are associated with aggressive clinical features in epithelial ovarian cancer. Onco Targets Ther 9:377–386CrossRefPubMedPubMedCentral Wang K, Li D, Sun L (2016) High levels of EGFR expression in tumor stroma are associated with aggressive clinical features in epithelial ovarian cancer. Onco Targets Ther 9:377–386CrossRefPubMedPubMedCentral
18.
go back to reference Masoumi-Moghaddam S, Amini A, Wei AQ, Robertson G, Morris DL (2015) Sprouty 1 predicts prognosis in human epithelial ovarian cancer. Am J Cancer Res 5:1531–1541PubMedPubMedCentral Masoumi-Moghaddam S, Amini A, Wei AQ, Robertson G, Morris DL (2015) Sprouty 1 predicts prognosis in human epithelial ovarian cancer. Am J Cancer Res 5:1531–1541PubMedPubMedCentral
19.
go back to reference Khandakar B, Mathur SR, Kumar L, Kumar S, Datta Gupta S, Iyer VK et al (2014) Tissue biomarkers in prognostication of serous ovarian cancer following neoadjuvant chemotherapy. Biomed Res Int 401245 Khandakar B, Mathur SR, Kumar L, Kumar S, Datta Gupta S, Iyer VK et al (2014) Tissue biomarkers in prognostication of serous ovarian cancer following neoadjuvant chemotherapy. Biomed Res Int 401245
20.
go back to reference Bachmayr-Heyda A, Aust S, Heinze G, Polterauer S, Grimm C, Braicu EI et al (2013) Prognostic impact of tumor infiltrating CD8+ T cells in association with cell proliferation in ovarian cancer patients–a study of the OVCAD consortium. BMC Cancer 13:422CrossRefPubMedPubMedCentral Bachmayr-Heyda A, Aust S, Heinze G, Polterauer S, Grimm C, Braicu EI et al (2013) Prognostic impact of tumor infiltrating CD8+ T cells in association with cell proliferation in ovarian cancer patients–a study of the OVCAD consortium. BMC Cancer 13:422CrossRefPubMedPubMedCentral
21.
go back to reference Heeran MC, Hogdall CK, Kjaer SK, Christensen L, Jensen A, Blaakaer J et al (2013) Prognostic value of tissue protein expression levels of MIB-1 (Ki-67) in Danish ovarian cancer patients. From the ‘MALOVA’ ovarian cancer study. APMIS 121:1177–1186CrossRefPubMed Heeran MC, Hogdall CK, Kjaer SK, Christensen L, Jensen A, Blaakaer J et al (2013) Prognostic value of tissue protein expression levels of MIB-1 (Ki-67) in Danish ovarian cancer patients. From the ‘MALOVA’ ovarian cancer study. APMIS 121:1177–1186CrossRefPubMed
22.
go back to reference Liu P, Sun YL, Du J, Hou XS, Meng H (2012) CD105/Ki67 coexpression correlates with tumor progression and poor prognosis in epithelial ovarian cancer. Int J Gynecol Cancer 22:586–592CrossRefPubMed Liu P, Sun YL, Du J, Hou XS, Meng H (2012) CD105/Ki67 coexpression correlates with tumor progression and poor prognosis in epithelial ovarian cancer. Int J Gynecol Cancer 22:586–592CrossRefPubMed
23.
go back to reference Katagiri A, Nakayama K, Rahman MT, Rahman M, Katagiri H, Nakayama N et al (2012) Loss of ARID1A expression is related to shorter progression-free survival and chemoresistance in ovarian clear cell carcinoma. Mod Pathol 25:282–288CrossRefPubMed Katagiri A, Nakayama K, Rahman MT, Rahman M, Katagiri H, Nakayama N et al (2012) Loss of ARID1A expression is related to shorter progression-free survival and chemoresistance in ovarian clear cell carcinoma. Mod Pathol 25:282–288CrossRefPubMed
24.
go back to reference Aune G, Stunes AK, Tingulstad S, Salvesen O, Syversen U, Torp SH (2011) The proliferation markers Ki-67/MIB-1, phosphohistone H3, and survivin may contribute in the identification of aggressive ovarian carcinomas. Int J Clin Exp Pathol 4:444–453PubMedPubMedCentral Aune G, Stunes AK, Tingulstad S, Salvesen O, Syversen U, Torp SH (2011) The proliferation markers Ki-67/MIB-1, phosphohistone H3, and survivin may contribute in the identification of aggressive ovarian carcinomas. Int J Clin Exp Pathol 4:444–453PubMedPubMedCentral
25.
go back to reference Kondoh E, Mori S, Yamaguchi K, Baba T, Matsumura NC, Barnett J et al (2010) Targeting slow-proliferating ovarian cancer cells. Int J Cancer 126:2448–2456PubMed Kondoh E, Mori S, Yamaguchi K, Baba T, Matsumura NC, Barnett J et al (2010) Targeting slow-proliferating ovarian cancer cells. Int J Cancer 126:2448–2456PubMed
26.
go back to reference Adams SF, Levine DA, Cadungog MG, Hammond R, Facciabene A, Olvera N et al (2009) Intraepithelial T cells and tumor proliferation: impact on the benefit from surgical cytoreduction in advanced serous ovarian cancer. Cancer 115:2891–2902CrossRefPubMed Adams SF, Levine DA, Cadungog MG, Hammond R, Facciabene A, Olvera N et al (2009) Intraepithelial T cells and tumor proliferation: impact on the benefit from surgical cytoreduction in advanced serous ovarian cancer. Cancer 115:2891–2902CrossRefPubMed
27.
go back to reference Kobel M, Kalloger SE, Boyd N, McKinney S, Mehl E, Palmer C et al (2008) Ovarian carcinoma subtypes are different diseases: implications for biomarker studies. PLoS Med V5:e232CrossRef Kobel M, Kalloger SE, Boyd N, McKinney S, Mehl E, Palmer C et al (2008) Ovarian carcinoma subtypes are different diseases: implications for biomarker studies. PLoS Med V5:e232CrossRef
28.
go back to reference Garcia-Velasco A, Mendiola C, Sanchez-Munoz A, Ballestin C, Colomer R, Cortes-Funes H (2008) Prognostic value of hormonal receptors, p53, ki67 and HER2/neu expression in epithelial ovarian carcinoma. Clin Transl Oncol 10:367–371CrossRefPubMed Garcia-Velasco A, Mendiola C, Sanchez-Munoz A, Ballestin C, Colomer R, Cortes-Funes H (2008) Prognostic value of hormonal receptors, p53, ki67 and HER2/neu expression in epithelial ovarian carcinoma. Clin Transl Oncol 10:367–371CrossRefPubMed
29.
go back to reference Tetu B, Popa I, Bairati I, L'Esperance S, Bachvarova M, Plante M et al (2008) Immunohistochemical analysis of possible chemoresistance markers identified by micro-arrays on serous ovarian carcinomas. Mod Pathol 21:1002–1010CrossRefPubMed Tetu B, Popa I, Bairati I, L'Esperance S, Bachvarova M, Plante M et al (2008) Immunohistochemical analysis of possible chemoresistance markers identified by micro-arrays on serous ovarian carcinomas. Mod Pathol 21:1002–1010CrossRefPubMed
30.
go back to reference Khouja MH, Baekelandt M, Nesland JM, Holm R (2007) The clinical importance of Ki-67, p16, p14, and p57 expression in patients with advanced ovarian carcinoma. Int J Gynecol Pathol 26:418–425CrossRefPubMed Khouja MH, Baekelandt M, Nesland JM, Holm R (2007) The clinical importance of Ki-67, p16, p14, and p57 expression in patients with advanced ovarian carcinoma. Int J Gynecol Pathol 26:418–425CrossRefPubMed
31.
go back to reference Yamamoto S, Tsuda H, Kita T, Maekawa K, Fujii K, Kudoh K et al (2007) Clinicopathological significance of WT1 expression in ovarian cancer: a possible accelerator of tumor progression in serous adenocarcinoma. Virchows Arch 451:27–35CrossRefPubMed Yamamoto S, Tsuda H, Kita T, Maekawa K, Fujii K, Kudoh K et al (2007) Clinicopathological significance of WT1 expression in ovarian cancer: a possible accelerator of tumor progression in serous adenocarcinoma. Virchows Arch 451:27–35CrossRefPubMed
32.
go back to reference Yamamoto S, Tsuda H, Yoshikawa T, Kudoh K, Kita T, Furuya K et al (2007) Clear cell adenocarcinoma associated with clear cell adenofibromatous components: a subgroup of ovarian clear cell adenocarcinoma with distinct clinicopathologic characteristics. Am J Surg Pathol 31:999–1006CrossRefPubMed Yamamoto S, Tsuda H, Yoshikawa T, Kudoh K, Kita T, Furuya K et al (2007) Clear cell adenocarcinoma associated with clear cell adenofibromatous components: a subgroup of ovarian clear cell adenocarcinoma with distinct clinicopathologic characteristics. Am J Surg Pathol 31:999–1006CrossRefPubMed
33.
go back to reference Green JA, Berns EM, Coens C, Luijk I, Thompson-Hehir JV, Diest P et al (2006) Alterations in the p53 pathway and prognosis in advanced ovarian cancer: a multi-factorial analysis of the EORTC Gynaecological Cancer group (study 55865). Eur J Cancer 42:2539–2548CrossRefPubMed Green JA, Berns EM, Coens C, Luijk I, Thompson-Hehir JV, Diest P et al (2006) Alterations in the p53 pathway and prognosis in advanced ovarian cancer: a multi-factorial analysis of the EORTC Gynaecological Cancer group (study 55865). Eur J Cancer 42:2539–2548CrossRefPubMed
34.
go back to reference Surowiak P, Materna V, Kaplenko I, Spaczynski M, Dietel M, Lage H et al (2006) Topoisomerase 1A, HER/2neu and Ki67 expression in paired primary and relapse ovarian cancer tissue samples. Histol Histopathol 21:713–720PubMed Surowiak P, Materna V, Kaplenko I, Spaczynski M, Dietel M, Lage H et al (2006) Topoisomerase 1A, HER/2neu and Ki67 expression in paired primary and relapse ovarian cancer tissue samples. Histol Histopathol 21:713–720PubMed
35.
go back to reference Kritpracha K, Hanprasertpong J, Chandeying V, Dechsukhum C, Geater A (2005) Survival analysis in advanced epithelial ovarian carcinoma in relation to proliferative index of MIB-1 immunostaining. J Obstet Gynaecol Res 31:268–276CrossRefPubMed Kritpracha K, Hanprasertpong J, Chandeying V, Dechsukhum C, Geater A (2005) Survival analysis in advanced epithelial ovarian carcinoma in relation to proliferative index of MIB-1 immunostaining. J Obstet Gynaecol Res 31:268–276CrossRefPubMed
36.
go back to reference Elie C, Geay JF, Morcos M, Tourneau A, Girre V, Broet P et al (2004) Lack of relationship between EGFR-1 immunohistochemical expression and prognosis in a multicentre clinical trial of 93 patients with advanced primary ovarian epithelial cancer (GINECO group). Br J Cancer 91:470–475CrossRefPubMedPubMedCentral Elie C, Geay JF, Morcos M, Tourneau A, Girre V, Broet P et al (2004) Lack of relationship between EGFR-1 immunohistochemical expression and prognosis in a multicentre clinical trial of 93 patients with advanced primary ovarian epithelial cancer (GINECO group). Br J Cancer 91:470–475CrossRefPubMedPubMedCentral
37.
go back to reference Camilleri-Broet S, Hardy-Bessard AC, Le Tourneau A, Paraiso D, Levrel O, Leduc B et al (2004) HER-2 overexpression is an independent marker of poor prognosis of advanced primary ovarian carcinoma: a multicenter study of the GINECO group. Ann Oncol 15:104–112CrossRefPubMed Camilleri-Broet S, Hardy-Bessard AC, Le Tourneau A, Paraiso D, Levrel O, Leduc B et al (2004) HER-2 overexpression is an independent marker of poor prognosis of advanced primary ovarian carcinoma: a multicenter study of the GINECO group. Ann Oncol 15:104–112CrossRefPubMed
38.
go back to reference Itamochi H, Kigawa J, Sugiyama T, Kikuchi Y, Suzuki M, Terakawa N (2002) Low proliferation activity may be associated with chemoresistance in clear cell carcinoma of the ovary. Obstet Gynecol 100:281–287PubMed Itamochi H, Kigawa J, Sugiyama T, Kikuchi Y, Suzuki M, Terakawa N (2002) Low proliferation activity may be associated with chemoresistance in clear cell carcinoma of the ovary. Obstet Gynecol 100:281–287PubMed
39.
go back to reference Sengupta PS, McGown AT, Bajaj V, Blackhall F, Swindell R, Bromley M et al (2000) P53 and related proteins in epithelial ovarian cancer. Eur J Cancer 36:2317–2328CrossRefPubMed Sengupta PS, McGown AT, Bajaj V, Blackhall F, Swindell R, Bromley M et al (2000) P53 and related proteins in epithelial ovarian cancer. Eur J Cancer 36:2317–2328CrossRefPubMed
40.
go back to reference Costa MJ, Hansen CL, Walls JE, Scudder SA (1999) Immunohistochemical markers of cell cycle control applied to ovarian and primary peritoneal surface epithelial neoplasms: p21(WAF1/CIP1) predicts survival and good response to platinin-based chemotherapy. Hum Pathol 30:640–647CrossRefPubMed Costa MJ, Hansen CL, Walls JE, Scudder SA (1999) Immunohistochemical markers of cell cycle control applied to ovarian and primary peritoneal surface epithelial neoplasms: p21(WAF1/CIP1) predicts survival and good response to platinin-based chemotherapy. Hum Pathol 30:640–647CrossRefPubMed
41.
go back to reference Anttila M, Kosma VM, Ji H, Wei-Ling X, Puolakka J, Juhola M et al (1998) Clinical significance of alpha-catenin, collagen IV, and Ki-67 expression in epithelial ovarian cancer. J Clin Oncol 16:2591–2600CrossRefPubMed Anttila M, Kosma VM, Ji H, Wei-Ling X, Puolakka J, Juhola M et al (1998) Clinical significance of alpha-catenin, collagen IV, and Ki-67 expression in epithelial ovarian cancer. J Clin Oncol 16:2591–2600CrossRefPubMed
42.
go back to reference Viale G, Maisonneuve P, Bonoldi E, Bacco A, Bevilacqua P, Panizzoni GA et al (1997) The combined evaluation of p53 accumulation and of Ki-67 (MIB1) labelling index provides independent information on overall survival of ovarian carcinoma patients. Ann Oncol V8:469–476CrossRef Viale G, Maisonneuve P, Bonoldi E, Bacco A, Bevilacqua P, Panizzoni GA et al (1997) The combined evaluation of p53 accumulation and of Ki-67 (MIB1) labelling index provides independent information on overall survival of ovarian carcinoma patients. Ann Oncol V8:469–476CrossRef
43.
go back to reference Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D et al (2000) Meta analysis of observational studies in epidemiology: a proposal for reporting. Meta analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283:2008–2012CrossRefPubMed Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D et al (2000) Meta analysis of observational studies in epidemiology: a proposal for reporting. Meta analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283:2008–2012CrossRefPubMed
44.
go back to reference Peters JL, Sutton AJ, Jones DR, Abrams KR, Rushton L (2008) Contour-enhanced meta analysis funnel plots help distinguish publication bias from other causes of asymmetry. J Clin Epidemiol 61:991–996CrossRefPubMed Peters JL, Sutton AJ, Jones DR, Abrams KR, Rushton L (2008) Contour-enhanced meta analysis funnel plots help distinguish publication bias from other causes of asymmetry. J Clin Epidemiol 61:991–996CrossRefPubMed
45.
go back to reference Wen S, Zhou W, Li CM, Hu J, Hu XM, Chen P et al (2015) Ki-67 as a prognostic marker in early-stage non-small cell lung cancer in Asian patients: a meta analysis of published studies involving 32 studies. BMC Cancer 15:520CrossRefPubMedPubMedCentral Wen S, Zhou W, Li CM, Hu J, Hu XM, Chen P et al (2015) Ki-67 as a prognostic marker in early-stage non-small cell lung cancer in Asian patients: a meta analysis of published studies involving 32 studies. BMC Cancer 15:520CrossRefPubMedPubMedCentral
46.
go back to reference Pan D, Wei K, Ling Y, Su S, Zhu M, Chen G (2015) The prognostic role of Ki-67/MIB-1 in cervical cancer: a systematic review with meta analysis. Med Sci Monit 21:882–889CrossRefPubMedPubMedCentral Pan D, Wei K, Ling Y, Su S, Zhu M, Chen G (2015) The prognostic role of Ki-67/MIB-1 in cervical cancer: a systematic review with meta analysis. Med Sci Monit 21:882–889CrossRefPubMedPubMedCentral
47.
go back to reference Pyo JS, Kang G, Sohn JH (2016) Ki-67labeling index can be used as a prognostic marker in gastrointestinal stromal tumor: asystematic review and meta analysis. Int J Biol Markers 31:204–210CrossRef Pyo JS, Kang G, Sohn JH (2016) Ki-67labeling index can be used as a prognostic marker in gastrointestinal stromal tumor: asystematic review and meta analysis. Int J Biol Markers 31:204–210CrossRef
Metadata
Title
High Ki-67 expression is significantly associated with poor prognosis of ovarian cancer patients: evidence from a meta-analysis
Authors
Dongmei Qiu
Wanqiu Cai
Zhiqiao Zhang
Hongyan Li
Dongmei Zhou
Publication date
01-05-2019
Publisher
Springer Berlin Heidelberg
Published in
Archives of Gynecology and Obstetrics / Issue 5/2019
Print ISSN: 0932-0067
Electronic ISSN: 1432-0711
DOI
https://doi.org/10.1007/s00404-019-05082-3

Other articles of this Issue 5/2019

Archives of Gynecology and Obstetrics 5/2019 Go to the issue