Skip to main content
Top
Published in: Cancer Cell International 1/2019

Open Access 01-12-2019 | Hepatocellular Carcinoma | Primary research

Prognostic role of PD-L1 for HCC patients after potentially curative resection: a meta-analysis

Authors: Gao-Min Liu, Xu-Gang Li, Yao-Min Zhang

Published in: Cancer Cell International | Issue 1/2019

Login to get access

Abstract

Background

A series of studies has investigated the prognostic role and clinical significance of programmed death ligand 1 (PD-L1) in hepatocellular carcinoma (HCC). However, the results were inconsistent. We aimed to clarify the prognostic role of PD-L1 and relationship between PD-L1 expression and several important clinicopathological features.

Methods

PubMed, EMBASE and the Science Citation Index Expanded were systematically searched. All cohort or case–control studies comparing the prognosis and clinical features between the high PD-L1 and low PD-L1 groups were included. Publication bias was evaluated using funnel plots and Begg’s test. Subgroup analysis, sensitivity analysis and meta-regression analysis were performed.

Results

Seventeen studies including 2979 patients were eligible. The overall survival (OS) was not significantly different between the high and low PD-L1 groups (hazard ratio [HR]: 1.27; 95% confidence interval [CI] 0.98–1.65: P = 0.07) with significant heterogeneity (P < 0.001; I2 = 81%). The recurrence-free survival (RFS) was not significantly different between the high and low PD-L1 groups (HR: 1.22; 95% CI 0.97–1.53; P = 0.09) with significant heterogeneity (P < 0.001; I2 = 78%). The expression of PD-L1 was found to be significantly correlated with alpha-fetoprotein, hepatitis history, and tumour-infiltrating lymphocytes. Begg’s test found no significant publication bias for OS and RFS. Sensitivity analysis established the robustness of our results. Subgroup analysis and meta-regression analysis found the region of research as a significant contributor to inter-study heterogeneity in RFS, indicating some racial differences in the prognostic role of PD-L1.

Conclusions

Our study found no significant prognostic role of PD-L1 in HCC patients after potential curative hepatectomy based on our included studies. The expression of PD-L1 was significantly correlated with AFP, hepatitis history, and TILs. The prognostic role of PD-L1 in HCC warrants further investigation.
Appendix
Available only for authorised users
Literature
1.
go back to reference Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics 2012. CA: Cancer J Clin. 2015;65(2):87–108. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics 2012. CA: Cancer J Clin. 2015;65(2):87–108.
2.
go back to reference El-Serag HB. Epidemiology of viral hepatitis and hepatocellular carcinoma. Gastroenterology. 2012;142(6):1264–73.CrossRef El-Serag HB. Epidemiology of viral hepatitis and hepatocellular carcinoma. Gastroenterology. 2012;142(6):1264–73.CrossRef
3.
go back to reference Makarovarusher OV, Medinaecheverz J, Duffy AG, Greten TF. The yin and yang of evasion and immune activation in HCC. J Hepatol. 2015;62(6):1420.CrossRef Makarovarusher OV, Medinaecheverz J, Duffy AG, Greten TF. The yin and yang of evasion and immune activation in HCC. J Hepatol. 2015;62(6):1420.CrossRef
4.
go back to reference Keir ME, Butte MJ, Freeman GJ, Sharpe AH. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol. 2009;26(1):677–704.CrossRef Keir ME, Butte MJ, Freeman GJ, Sharpe AH. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol. 2009;26(1):677–704.CrossRef
5.
go back to reference Kudo M. Immune checkpoint inhibition in hepatocellular carcinoma: basics and ongoing clinical trials. Oncology. 2017;92(Suppl 1):50.CrossRef Kudo M. Immune checkpoint inhibition in hepatocellular carcinoma: basics and ongoing clinical trials. Oncology. 2017;92(Suppl 1):50.CrossRef
6.
go back to reference Melero I, Crocenzi TS, Welling TH, Yau TC, Yeo W, Chopra A, Grosso J, Lang L, Anderson J, Dela Cruz CM. Phase I/II safety and antitumor activity of nivolumab in patients with advanced hepatocellular carcinoma (HCC): CA209-040. J Clin Oncol. 2015;33(18_suppl):LBA101.CrossRef Melero I, Crocenzi TS, Welling TH, Yau TC, Yeo W, Chopra A, Grosso J, Lang L, Anderson J, Dela Cruz CM. Phase I/II safety and antitumor activity of nivolumab in patients with advanced hepatocellular carcinoma (HCC): CA209-040. J Clin Oncol. 2015;33(18_suppl):LBA101.CrossRef
7.
go back to reference Chang H, Jung W, Kim A, Kim HK, Kim WB, Kim JH, Kim BH. Expression and prognostic significance of programmed death protein 1 and programmed death ligand-1, and cytotoxic T lymphocyte-associated molecule-4 in hepatocellular carcinoma. APMIS. 2017;125(8):690–8.CrossRef Chang H, Jung W, Kim A, Kim HK, Kim WB, Kim JH, Kim BH. Expression and prognostic significance of programmed death protein 1 and programmed death ligand-1, and cytotoxic T lymphocyte-associated molecule-4 in hepatocellular carcinoma. APMIS. 2017;125(8):690–8.CrossRef
8.
go back to reference Gao Q, Wang XY, Qiu SJ, Yamato I, Sho M, Nakajima Y, Zhou J, Li BZ, Shi YH, Xiao YS, et al. Overexpression of PD-L1 significantly associates with tumor aggressiveness and postoperative recurrence in human hepatocellular carcinoma. Clin Cancer Res. 2009;15(3):971–9.CrossRef Gao Q, Wang XY, Qiu SJ, Yamato I, Sho M, Nakajima Y, Zhou J, Li BZ, Shi YH, Xiao YS, et al. Overexpression of PD-L1 significantly associates with tumor aggressiveness and postoperative recurrence in human hepatocellular carcinoma. Clin Cancer Res. 2009;15(3):971–9.CrossRef
9.
go back to reference Jung HI, Jeong D, Ji S, Ahn TS, Bae SH, Chin S, Chung JC, Kim HC, Lee MS, Baek MJ. Overexpression of PD-L1 and PD-L2 is associated with poor prognosis in patients with hepatocellular carcinoma. Cancer Res Treat. 2017;49(1):246–54.CrossRef Jung HI, Jeong D, Ji S, Ahn TS, Bae SH, Chin S, Chung JC, Kim HC, Lee MS, Baek MJ. Overexpression of PD-L1 and PD-L2 is associated with poor prognosis in patients with hepatocellular carcinoma. Cancer Res Treat. 2017;49(1):246–54.CrossRef
10.
go back to reference Semaan A, Dietrich D, Bergheim D, Dietrich J, Kalff JC, Branchi V, Matthaei H, Kristiansen G, Fischer HP, Goltz D. CXCL12 expression and PD-L1 expression serve as prognostic biomarkers in HCC and are induced by hypoxia. Virchows Archiv. 2017;470(2):185–96.CrossRef Semaan A, Dietrich D, Bergheim D, Dietrich J, Kalff JC, Branchi V, Matthaei H, Kristiansen G, Fischer HP, Goltz D. CXCL12 expression and PD-L1 expression serve as prognostic biomarkers in HCC and are induced by hypoxia. Virchows Archiv. 2017;470(2):185–96.CrossRef
11.
go back to reference Wu K, Kryczek I, Chen L, Zou W, Welling TH. Kupffer cell suppression of CD8+ T cells in human hepatocellular carcinoma is mediated by B7-H1/programmed death-1 interactions. Can Res. 2009;69(20):8067–75.CrossRef Wu K, Kryczek I, Chen L, Zou W, Welling TH. Kupffer cell suppression of CD8+ T cells in human hepatocellular carcinoma is mediated by B7-H1/programmed death-1 interactions. Can Res. 2009;69(20):8067–75.CrossRef
12.
go back to reference Gu XB, Gao XS, Xiong W, Guo W, Han LJ, Bai Y, Peng C, Cui M, Xie M. Increased programmed death ligand-1 expression predicts poor prognosis in hepatocellular carcinoma patients. OncoTargets Ther. 2016;9:4805–13.CrossRef Gu XB, Gao XS, Xiong W, Guo W, Han LJ, Bai Y, Peng C, Cui M, Xie M. Increased programmed death ligand-1 expression predicts poor prognosis in hepatocellular carcinoma patients. OncoTargets Ther. 2016;9:4805–13.CrossRef
13.
go back to reference Chen CL, Pan QZ, Zhao JJ, Wang Y, Li YQ, Wang QJ, Pan K, Weng DS, Jiang SS, Tang Y, et al. PD-L1 expression as a predictive biomarker for cytokine-induced killer cell immunotherapy in patients with hepatocellular carcinoma. Oncoimmunology. 2016;5(7):e1176653.CrossRef Chen CL, Pan QZ, Zhao JJ, Wang Y, Li YQ, Wang QJ, Pan K, Weng DS, Jiang SS, Tang Y, et al. PD-L1 expression as a predictive biomarker for cytokine-induced killer cell immunotherapy in patients with hepatocellular carcinoma. Oncoimmunology. 2016;5(7):e1176653.CrossRef
14.
go back to reference Kan G, Dong W. The expression of PD-L1 APE1 and P53 in hepatocellular carcinoma and its relationship to clinical pathology. Eur Rev Med Pharmacol Sci. 2015;19(16):3063–71.PubMed Kan G, Dong W. The expression of PD-L1 APE1 and P53 in hepatocellular carcinoma and its relationship to clinical pathology. Eur Rev Med Pharmacol Sci. 2015;19(16):3063–71.PubMed
15.
go back to reference Sideras K, Biermann K, Verheij J, Takkenberg BR, Mancham S, Hansen BE, Schutz HM, de Man RA, Sprengers D, Buschow SI, et al. PD-L1, galectin-9 and CD8(+) tumor-infiltrating lymphocytes are associated with survival in hepatocellular carcinoma. Oncoimmunology. 2017;6(2):e1273309.CrossRef Sideras K, Biermann K, Verheij J, Takkenberg BR, Mancham S, Hansen BE, Schutz HM, de Man RA, Sprengers D, Buschow SI, et al. PD-L1, galectin-9 and CD8(+) tumor-infiltrating lymphocytes are associated with survival in hepatocellular carcinoma. Oncoimmunology. 2017;6(2):e1273309.CrossRef
16.
go back to reference Higgins JPTGS, editor. Cochrane handbook for systematic reviews of interventions version 5.1.0. Oxford: The Cochrane Collaboration; 2011 (updated March 2011). Higgins JPTGS, editor. Cochrane handbook for systematic reviews of interventions version 5.1.0. Oxford: The Cochrane Collaboration; 2011 (updated March 2011).
17.
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(7):e1000097.CrossRef Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097.CrossRef
18.
go back to reference Tierney JF, Stewart LA, Ghersi D, Burdett S, Sydes MR. Practical methods for incorporating summary time-to-event data into meta-analysis. Trials. 2007;8:16.CrossRef Tierney JF, Stewart LA, Ghersi D, Burdett S, Sydes MR. Practical methods for incorporating summary time-to-event data into meta-analysis. Trials. 2007;8:16.CrossRef
19.
go back to reference Calderaro J, Rousseau B, Amaddeo G, Mercey M, Charpy C, Costentin C, Luciani A, Zafrani ES, Laurent A, Azoulay D, et al. PD-L1 expression in hepatocellular carcinoma: relationship with clinical and pathological features. Hepatology. 2016;64:624A.CrossRef Calderaro J, Rousseau B, Amaddeo G, Mercey M, Charpy C, Costentin C, Luciani A, Zafrani ES, Laurent A, Azoulay D, et al. PD-L1 expression in hepatocellular carcinoma: relationship with clinical and pathological features. Hepatology. 2016;64:624A.CrossRef
20.
go back to reference Huang CY, Wang Y, Luo GY, Han F, Li YQ, Zhou ZG, Xu GL. Relationship between PD-L1 expression and CD8+ T-cell immune responses in hepatocellular carcinoma. J Immunother. 2017;40(9):323–33.PubMed Huang CY, Wang Y, Luo GY, Han F, Li YQ, Zhou ZG, Xu GL. Relationship between PD-L1 expression and CD8+ T-cell immune responses in hepatocellular carcinoma. J Immunother. 2017;40(9):323–33.PubMed
21.
go back to reference Umemoto Y, Okano S, Matsumoto Y, Nakagawara H, Matono R, Yoshiya S, Yamashita YI, Yoshizumi T, Ikegami T, Soejima Y, et al. Prognostic impact of programmed cell death 1 ligand 1 expression in human leukocyte antigen class I-positive hepatocellular carcinoma after curative hepatectomy. J Gastroenterol. 2014;50(1):65–75.CrossRef Umemoto Y, Okano S, Matsumoto Y, Nakagawara H, Matono R, Yoshiya S, Yamashita YI, Yoshizumi T, Ikegami T, Soejima Y, et al. Prognostic impact of programmed cell death 1 ligand 1 expression in human leukocyte antigen class I-positive hepatocellular carcinoma after curative hepatectomy. J Gastroenterol. 2014;50(1):65–75.CrossRef
22.
go back to reference Chang B, Shen L, Wang K, Jin J, Huang T, Chen Q, Li W, Wu P. High number of PD-1 positive intratumoural lymphocytes predicts survival benefit of cytokine-induced killer cells for hepatocellular carcinoma patients. Liver Int. 2018;38(8):1449–58.CrossRef Chang B, Shen L, Wang K, Jin J, Huang T, Chen Q, Li W, Wu P. High number of PD-1 positive intratumoural lymphocytes predicts survival benefit of cytokine-induced killer cells for hepatocellular carcinoma patients. Liver Int. 2018;38(8):1449–58.CrossRef
23.
go back to reference Gabrielson A, Wu YN, Wang HK, Jiang JJ, Kallakury B, Gatalica Z, Reddy S, Kleiner D, Fishbein T, Johnson L, et al. Intratumoral CD3 and CD8 T-cell densities associated with relapse-free survival in HCC. Cancer Immunol Res. 2016;4(5):419–30.CrossRef Gabrielson A, Wu YN, Wang HK, Jiang JJ, Kallakury B, Gatalica Z, Reddy S, Kleiner D, Fishbein T, Johnson L, et al. Intratumoral CD3 and CD8 T-cell densities associated with relapse-free survival in HCC. Cancer Immunol Res. 2016;4(5):419–30.CrossRef
24.
go back to reference Xie QK, Zhao YJ, Pan T, Lyu N, Mu LW, Li SL, Shi MD, Zhang ZF, Zhou PH, Zhao M. Programmed death ligand 1 as an indicator of pre-existing adaptive immune responses in human hepatocellular carcinoma. Oncoimmunology. 2016;5(7):e1181252.CrossRef Xie QK, Zhao YJ, Pan T, Lyu N, Mu LW, Li SL, Shi MD, Zhang ZF, Zhou PH, Zhao M. Programmed death ligand 1 as an indicator of pre-existing adaptive immune responses in human hepatocellular carcinoma. Oncoimmunology. 2016;5(7):e1181252.CrossRef
25.
go back to reference Dai X, Pi G, Yang SL, Chen GG, Liu LP, Dong HH. Association of PD-L1 and HIF-1α coexpression with poor prognosis in hepatocellular carcinoma. Transl Oncol. 2018;11(2):559–66.CrossRef Dai X, Pi G, Yang SL, Chen GG, Liu LP, Dong HH. Association of PD-L1 and HIF-1α coexpression with poor prognosis in hepatocellular carcinoma. Transl Oncol. 2018;11(2):559–66.CrossRef
26.
go back to reference Hu K, Wang ZM, Li JN, Zhang S, Xiao ZF, Tao YM. CLEC1B expression and PD-L1 expression predict clinical outcome in hepatocellular carcinoma with tumor hemorrhage. Transl Oncol. 2018;11(2):552–8.CrossRef Hu K, Wang ZM, Li JN, Zhang S, Xiao ZF, Tao YM. CLEC1B expression and PD-L1 expression predict clinical outcome in hepatocellular carcinoma with tumor hemorrhage. Transl Oncol. 2018;11(2):552–8.CrossRef
27.
go back to reference Liu CQ, Xu J, Zhou ZG, Jin LL, Yu XJ, Xiao G, Lin J, Zhuang SM, Zhang YJ, Zheng L. Expression patterns of programmed death ligand 1 correlate with different microenvironments and patient prognosis in hepatocellular carcinoma. Br J Cancer. 2018;119(1):80–8.CrossRef Liu CQ, Xu J, Zhou ZG, Jin LL, Yu XJ, Xiao G, Lin J, Zhuang SM, Zhang YJ, Zheng L. Expression patterns of programmed death ligand 1 correlate with different microenvironments and patient prognosis in hepatocellular carcinoma. Br J Cancer. 2018;119(1):80–8.CrossRef
28.
go back to reference Ioannidis JPA, Trikalinos TA. The appropriateness of asymmetry tests for publication bias in meta-analyses: a large survey. CMAJ. 2007;176(8):1091–6.CrossRef Ioannidis JPA, Trikalinos TA. The appropriateness of asymmetry tests for publication bias in meta-analyses: a large survey. CMAJ. 2007;176(8):1091–6.CrossRef
29.
go back to reference Xiang X, Yu PC, Long D, Liao XL, Zhang S, You XM, Zhong JH, Li LQ. Prognostic value of PD-L1 expression in patients with primary solid tumors. Oncotarget. 2018;9(4):5058–72.CrossRef Xiang X, Yu PC, Long D, Liao XL, Zhang S, You XM, Zhong JH, Li LQ. Prognostic value of PD-L1 expression in patients with primary solid tumors. Oncotarget. 2018;9(4):5058–72.CrossRef
30.
go back to reference Wang X, Teng FF, Kong L, Yu JM. PD-L1 expression in human cancers and its association with clinical outcomes. OncoTargets Ther. 2016;9:5023–39.CrossRef Wang X, Teng FF, Kong L, Yu JM. PD-L1 expression in human cancers and its association with clinical outcomes. OncoTargets Ther. 2016;9:5023–39.CrossRef
31.
go back to reference Dai C, Wang M, Lu J, Dai ZM, Lin S, Yang PT, Tian T, Liu XH, Min WL, Dai ZJ. Prognostic and predictive values of PD-L1 expression in patients with digestive system cancer: a meta-analysis. OncoTargets Ther. 2017;10:3625–34.CrossRef Dai C, Wang M, Lu J, Dai ZM, Lin S, Yang PT, Tian T, Liu XH, Min WL, Dai ZJ. Prognostic and predictive values of PD-L1 expression in patients with digestive system cancer: a meta-analysis. OncoTargets Ther. 2017;10:3625–34.CrossRef
32.
go back to reference Coelho MA, Trécesson SDC, Rana S, Zecchin D, Moore C, Molina-Arcas M, East P, Spencer-Dene B, Nye E, Barnouin K. Oncogenic RAS signaling promotes tumor immunoresistance by stabilizing PD-L1 mRNA. Immunity. 2017;47(6):1083–99.CrossRef Coelho MA, Trécesson SDC, Rana S, Zecchin D, Moore C, Molina-Arcas M, East P, Spencer-Dene B, Nye E, Barnouin K. Oncogenic RAS signaling promotes tumor immunoresistance by stabilizing PD-L1 mRNA. Immunity. 2017;47(6):1083–99.CrossRef
33.
go back to reference Zhou J, Liu M, Sun H, Feng Y, Xu L, Chan AWH, Tong JH, Wong J, Chong CCN, Lai PBS, et al. Hepatoma-intrinsic CCRK inhibition diminishes myeloid-derived suppressor cell immunosuppression and enhances immune-checkpoint blockade efficacy. Gut. 2018;67(5):931–44.CrossRef Zhou J, Liu M, Sun H, Feng Y, Xu L, Chan AWH, Tong JH, Wong J, Chong CCN, Lai PBS, et al. Hepatoma-intrinsic CCRK inhibition diminishes myeloid-derived suppressor cell immunosuppression and enhances immune-checkpoint blockade efficacy. Gut. 2018;67(5):931–44.CrossRef
34.
go back to reference Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJ, Robert L, Chmielowski B, Spasic M, Henry G, Ciobanu V. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature. 2014;515(7528):568.CrossRef Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJ, Robert L, Chmielowski B, Spasic M, Henry G, Ciobanu V. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature. 2014;515(7528):568.CrossRef
35.
go back to reference Ribas A, Wolchok JD. Cancer immunotherapy using checkpoint blockade. Science. 2018;359(6382):1350–5.CrossRef Ribas A, Wolchok JD. Cancer immunotherapy using checkpoint blockade. Science. 2018;359(6382):1350–5.CrossRef
36.
go back to reference Schumacher TN, Schreiber RD. Neoantigens in cancer immunotherapy. Science. 2015;348(6230):69–74.CrossRef Schumacher TN, Schreiber RD. Neoantigens in cancer immunotherapy. Science. 2015;348(6230):69–74.CrossRef
37.
go back to reference Haynes D. B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion. Nat Med. 1999;5(12):1365–9.CrossRef Haynes D. B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion. Nat Med. 1999;5(12):1365–9.CrossRef
38.
go back to reference Taube JM, Anders RA, Young GD, Xu H, Sharma R, McMiller TL, Chen S, Klein AP, Pardoll DM, Topalian SL, et al. Colocalization of inflammatory response with B7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape. Sci Transl Med. 2012;4(127):127ra137.CrossRef Taube JM, Anders RA, Young GD, Xu H, Sharma R, McMiller TL, Chen S, Klein AP, Pardoll DM, Topalian SL, et al. Colocalization of inflammatory response with B7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape. Sci Transl Med. 2012;4(127):127ra137.CrossRef
39.
go back to reference He J, Zhang Y, Kang S, Shen J, He J, Jiang L, Wang W, Guo Z, Peng G, Chen G, et al. Prognostic significance of programmed cell death 1 (PD-1) or PD-1 ligand 1 (PD-L1) expression in epithelial-originated cancer: a meta-analysis. Medicine. 2015;94(6):e515.CrossRef He J, Zhang Y, Kang S, Shen J, He J, Jiang L, Wang W, Guo Z, Peng G, Chen G, et al. Prognostic significance of programmed cell death 1 (PD-1) or PD-1 ligand 1 (PD-L1) expression in epithelial-originated cancer: a meta-analysis. Medicine. 2015;94(6):e515.CrossRef
40.
go back to reference Pyo JS, Kang G, Kim JY. Prognostic role of PD-L1 in malignant solid tumors: a meta-analysis. Int J Biol Mark. 2017;32(1):e68–74.CrossRef Pyo JS, Kang G, Kim JY. Prognostic role of PD-L1 in malignant solid tumors: a meta-analysis. Int J Biol Mark. 2017;32(1):e68–74.CrossRef
41.
go back to reference Wang Q, Liu F, Liu L. Prognostic significance of PD-L1 in solid tumor: an updated meta-analysis. Medicine. 2017;96(18):e6369.CrossRef Wang Q, Liu F, Liu L. Prognostic significance of PD-L1 in solid tumor: an updated meta-analysis. Medicine. 2017;96(18):e6369.CrossRef
42.
go back to reference Zhong JH, Luo CP, Zhang CY, Li LQ. Strengthening the case that elevated levels of programmed death ligand 1 predict poor prognosis in hepatocellular carcinoma patients. J Hepatocell Carcinoma. 2017;4:11–3.CrossRef Zhong JH, Luo CP, Zhang CY, Li LQ. Strengthening the case that elevated levels of programmed death ligand 1 predict poor prognosis in hepatocellular carcinoma patients. J Hepatocell Carcinoma. 2017;4:11–3.CrossRef
44.
go back to reference Zeng Z, Shi F, Zhou L, Zhang MN, Chen Y, Chang XJ, Lu YY, Bai WL, Qu JH, Wang CP, et al. Upregulation of circulating PD-L1/PD-1 is associated with poor post-cryoablation prognosis in patients with HBV-related hepatocellular carcinoma. PLoS ONE. 2011;6(9):e23621.CrossRef Zeng Z, Shi F, Zhou L, Zhang MN, Chen Y, Chang XJ, Lu YY, Bai WL, Qu JH, Wang CP, et al. Upregulation of circulating PD-L1/PD-1 is associated with poor post-cryoablation prognosis in patients with HBV-related hepatocellular carcinoma. PLoS ONE. 2011;6(9):e23621.CrossRef
45.
go back to reference Dai XM, Xue J, Hu JL, Yang SL, Chen GG, Lai PBS, Yu C, Zeng C, Fang XF, Pan XL, et al. Positive expression of programmed death ligand 1 in peritumoral liver tissue is associated with poor survival after curative resection of hepatocellular carcinoma. Transl Oncol. 2017;10(4):511–7.CrossRef Dai XM, Xue J, Hu JL, Yang SL, Chen GG, Lai PBS, Yu C, Zeng C, Fang XF, Pan XL, et al. Positive expression of programmed death ligand 1 in peritumoral liver tissue is associated with poor survival after curative resection of hepatocellular carcinoma. Transl Oncol. 2017;10(4):511–7.CrossRef
46.
go back to reference Finkelmeier F, Canli Ö, Tal A, Pleli T, Trojan J, Schmidt M, Kronenberger B, Zeuzem S, Piiper A, Greten FR, et al. High levels of the soluble programmed death-ligand (sPD-L1) identify hepatocellular carcinoma patients with a poor prognosis. Eur J Cancer. 2016;59:152–9.CrossRef Finkelmeier F, Canli Ö, Tal A, Pleli T, Trojan J, Schmidt M, Kronenberger B, Zeuzem S, Piiper A, Greten FR, et al. High levels of the soluble programmed death-ligand (sPD-L1) identify hepatocellular carcinoma patients with a poor prognosis. Eur J Cancer. 2016;59:152–9.CrossRef
Metadata
Title
Prognostic role of PD-L1 for HCC patients after potentially curative resection: a meta-analysis
Authors
Gao-Min Liu
Xu-Gang Li
Yao-Min Zhang
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Cancer Cell International / Issue 1/2019
Electronic ISSN: 1475-2867
DOI
https://doi.org/10.1186/s12935-019-0738-9

Other articles of this Issue 1/2019

Cancer Cell International 1/2019 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine