Development and validation of an interferon signature predicting prognosis and treatment response for glioblastoma

References

• Morgan LL. The epidemiology of glioma in adults: a “state of the science” review. Neuro-Oncology. 2015;17:623–624. doi:10.1093/neuonc/nou358.
   PubMed Web of Science ®Google Scholar
• Quail DF, Joyce JA. The microenvironmental landscape of brain tumors. Cancer Cell. 2017;31:326–341. doi:10.1016/j.ccell.2017.02.009.
   PubMed Web of Science ®Google Scholar
• Han S, Wang C, Qin X, Xia J, Wu A. LPS alters the immuno-phenotype of glioma and glioma stem-like cells and induces in vivo antitumor immunity via TLR4. J Exp Clin Cancer Res. 2017;36:83. doi:10.1186/s13046-017-0552-y.
   PubMed Web of Science ®Google Scholar
• Han S, Zhang C, Li Q, Dong J, Liu Y, Huang Y, Jiang T, Wu A. Tumour-infiltrating CD4(+) and CD8(+) lymphocytes as predictors of clinical outcome in glioma. Br J Cancer. 2014;110:2560–2568. doi:10.1038/bjc.2014.162.
   PubMed Web of Science ®Google Scholar
• Zhang CB, Cheng W, Ren X, Wang Z, Liu X, Li G, Han S, Jiang T, Wu A. Tumor purity as an underlying key factor in Glioma. Clin Cancer Res. 2017;23:6279–6291. doi:10.1158/1078-0432.CCR-16-2598.
   PubMed Web of Science ®Google Scholar
• Cheng W, Ren X, Zhang C, Cai J, Liu Y, Han S, Wu A. Bioinformatic profiling identifies an immune-related risk signature for glioblastoma. Neurology. 2016;86:2226–2234. doi:10.1212/WNL.0000000000002770.
   PubMed Web of Science ®Google Scholar
• Zitvogel L, Galluzzi L, Kepp O, Smyth MJ, Kroemer G. Type I interferons in anticancer immunity. Nat Rev Immunol. 2015;15:405–414. doi:10.1038/nri3845.
   PubMed Web of Science ®Google Scholar
• Parker BS, Rautela J, Hertzog PJ. Antitumour actions of interferons: implications for cancer therapy. Nat Rev Cancer. 2016;16:131–144. doi:10.1038/nrc.2016.14.
   PubMed Web of Science ®Google Scholar
• Payne MJ, Argyropoulou K, Fau - Lorigan P, Lorigan P, Fau - McAleer JJ, McAleer J, Fau - Farrugia D, Farrugia D, Fau - Davidson N, Davidson N, et al. Phase II pilot study of intravenous high-dose interferon with or without maintenance treatment in melanoma at high risk of recurrence. J Clin Oncol. 2014;32:185–190. doi:10.1200/JCO.2013.49.8717.
   PubMed Web of Science ®Google Scholar
• De Palma M, Mazzieri R, Fau - Politi LS, Politi L, Fau - Pucci F, Pucci F, Fau - Zonari E, Zonari E, Fau - Sitia G, Sitia G, et al. Tumor-targeted interferon-alpha delivery by Tie2-expressing monocytes inhibits tumor growth and metastasis. Cancer Cell. 2008;14:299–311. doi:10.1016/j.ccr.2008.09.004.
   PubMed Web of Science ®Google Scholar
• Hervas-Stubbs S, Perez-Gracia JL, Rouzaut A, Sanmamed MF, Le Bon A, Melero I. Direct effects of type I interferons on cells of the immune system. Clin Cancer Res. 2011;17:2619–2627. doi:10.1158/1078-0432.CCR-10-1114.
   PubMed Web of Science ®Google Scholar
• Natsume A, Ishii D, Wakabayashi T, Tsuno T, Hatano H, Mizuno M, Yoshida J. IFN-beta down-regulates the expression of DNA repair gene MGMT and sensitizes resistant glioma cells to temozolomide. Cancer Res. 2005;65:7573–7579. doi:10.1158/0008-5472.CAN-05-0036.
   PubMed Web of Science ®Google Scholar
• Qian J, Wang C, Wang B, Yang J, Wang Y, Luo F, Xu J, Zhao C, Liu R, Chu Y. The IFN-gamma/PD-L1 axis between T cells and tumor microenvironment: hints for glioma anti-PD-1/PD-L1 therapy. J Neuroinflammation. 2018;15(1):290. doi:10.1186/s12974-018-1330-2.
   Google Scholar
• Silginer M, Nagy S, Happold C, Schneider H, Weller M, Roth P. Autocrine activation of the IFN signaling pathway may promote immune escape in glioblastoma. Neuro-Oncology. 2017;19:1338–1349. doi:10.1093/neuonc/nox051.
   PubMed Web of Science ®Google Scholar
• Lesinski GB, Zimmerer JM, Kreiner M, Trefry J, Bill MA, Young GS. Modulation of SOCS protein expression influences the interferon responsiveness of human melanoma cells. BMC Cancer. 2010;10:142. doi:10.1186/1471-2407-10-663.
   PubMed Web of Science ®Google Scholar
• Ludigs K, Jandus C, Utzschneider DT, Staehli F, Bessoles S, Dang AT, Rota G, Castro W, Zehn D, Vivier E, et al. NLRC5 shields T lymphocytes from NK-cell-mediated elimination under inflammatory conditions. Nat Commun. 2016;7:10554. doi:10.1038/ncomms10554.
   PubMed Web of Science ®Google Scholar
• Reu FJ, Bae SI, Cherkassky L, Leaman DW, Lindner D, Beaulieu N. Overcoming resistance to interferon-induced apoptosis of renal carcinoma and melanoma cells by DNA demethylation. J Clin Oncol. 2006;24:3771–3779. doi:10.1200/JCO.2005.03.4074.
   PubMed Web of Science ®Google Scholar
• Tsuno T, Mejido J, Zhao T, Schmeisser H, Morrow A, Zoon KC. IRF9 is a key factor for eliciting the antiproliferative activity of IFN-alpha. J Immunother. 2009;803–816.
   PubMed Web of Science ®Google Scholar
• Zitzmann K, Brand S, De Toni EN, Baehs S, Goke B, Meinecke J, Spottl G, Meyer HH, Auernhammer CJ. SOCS1 silencing enhances antitumor activity of type I IFNs by regulating apoptosis in neuroendocrine tumor cells. Cancer Res. 2007;67:5025–5032. doi:10.1158/0008-5472.CAN-06-2575.
   PubMed Web of Science ®Google Scholar
• Yang Y, Zhou Y, Hou J, Bai C, Li Z, Fan J, Ng IOL, Zhou W, Sun H, Dong Q, et al. Hepatic IFIT3 predicts interferon-alpha therapeutic response in patients of hepatocellular carcinoma. Hepatology. 2017;66:152–166. doi:10.1002/hep.29156.
   PubMed Web of Science ®Google Scholar
• Cheon H, Borden EC, Stark GR. Interferons and their stimulated genes in the tumor microenvironment. Semin Oncol. 2014;41:156–173. doi:10.1053/j.seminoncol.2014.02.002.
   PubMed Web of Science ®Google Scholar
• Dalpke A, Heeg K, Bartz H, Baetz A. Regulation of innate immunity by suppressor of cytokine signaling (SOCS) proteins. Immunobiology. 2008;213:225–235. doi:10.1016/j.imbio.2007.10.008.
   PubMed Web of Science ®Google Scholar
• Lupfer C, Kanneganti TD. The expanding role of NLRs in antiviral immunity. Immunol Rev. 2013;255:13–24. doi:10.1111/imr.12089.
   PubMed Web of Science ®Google Scholar
• Ozato K, Tailor P, Kubota T. The interferon regulatory factor family in host defense: mechanism of action. J Biol Chem. 2007;282:20065–20069. doi:10.1074/jbc.R700003200.
   PubMed Web of Science ®Google Scholar
• Melguizo C, Prados J, Gonzalez B, Ortiz R, Concha A, Alvarez PJ, Badet L, Hauet T. MGMT promoter methylation status and MGMT and CD133 immunohistochemical expression as prognostic markers in glioblastoma patients treated with temozolomide plus radiotherapy. J Transl Med. 2012;10:250. doi:10.1186/1479-5876-10-233.
   PubMed Web of Science ®Google Scholar
• Brown SD, Warren RL, Gibb EA, Martin SD, Spinelli JJ, Nelson BH, Holt RA. Neo-antigens predicted by tumor genome meta-analysis correlate with increased patient survival. Genome Res. 2014;24:743–750. doi:10.1101/gr.165985.113.
   PubMed Web of Science ®Google Scholar
• Rutledge WC, Kong J, Gao J, Gutman DA, Cooper LA, Appin C, Park Y, Scarpace L, Mikkelsen T, Cohen ML, et al. Tumor-infiltrating lymphocytes in glioblastoma are associated with specific genomic alterations and related to transcriptional class. Clin Cancer Res. 2013;19:4951–4960. doi:10.1158/1078-0432.CCR-13-0551.
   PubMed Web of Science ®Google Scholar
• Meisen WH, Wohleb ES, Jaime-Ramirez AC, Bolyard C, Yoo JY, Russell L, Hardcastle J, Dubin S, Muili K, Yu J, et al. the impact of macrophage- and microglia-secreted TNFalpha on oncolytic HSV-1 therapy in the glioblastoma tumor microenvironment. Clin Cancer Res. 2015;21:3274–3285. doi:10.1158/1078-0432.CCR-14-3118.
   PubMed Web of Science ®Google Scholar
• Vo DN, Alexia C, Allende-Vega N, Morschhauser F, Houot R, Menard C, Hoadley KA, Print C, Knowlton N, Black MA, et al. NK cell activation and recovery of NK cell subsets in lymphoma patients after obinutuzumab and lenalidomide treatment. Oncoimmunology. 2018;7:e1409322. doi:10.1080/2162402X.2018.1490854.
   PubMed Web of Science ®Google Scholar
• Doucette T, Rao G, Rao A, Shen L, Aldape K, Wei J, Dziurzynski K, Gilbert M, Heimberger AB. Immune heterogeneity of glioblastoma subtypes: extrapolation from the cancer genome atlas. Cancer Immunol Res. 2013;1:112–122. doi:10.1158/2326-6066.CIR-13-0028.
   PubMed Web of Science ®Google Scholar
• Chawla-Sarkar M, Lindner D, Fau - Liu YF, Liu Y, Fau - Williams BR, Williams B, Fau - Sen GC, Sen G, Fau - Silverman RH, Silverman R, et al. Apoptosis and interferons: role of interferon-stimulated genes as mediators of apoptosis. Apoptosis. 2003;8:237–249.
   PubMed Web of Science ®Google Scholar
• De Beuckelaer A, Grooten J, De Koker S. Type I interferons modulate CD8(+) T cell immunity to mRNA vaccines. Trends Mol Med. 2017;23:216–226. doi:10.1016/j.molmed.2017.01.006.
   PubMed Web of Science ®Google Scholar
• Happold C, Roth P, Silginer M, Florea AM, Lamszus K, Frei K, Deenen R, Reifenberger G, Weller M. Interferon-beta induces loss of spherogenicity and overcomes therapy resistance of glioblastoma stem cells. Mol Cancer Ther. 2014;13:948–961. doi:10.1158/1535-7163.MCT-13-0772.
   PubMed Web of Science ®Google Scholar
• Kito T, Kuroda E, Fau - Yokota A, Yamashita U. Enhancement of macrophage cytotoxicity against murine gliomas by interferon beta: increase in nitric oxide production in response to glioma-derived soluble factors. J Neurosurg. 2002;97:619–626. doi:10.3171/jns.2002.97.3.0619.
   PubMed Web of Science ®Google Scholar
• Takano S, Ishikawa E, Matsuda M, Yamamoto T, Matsumura A. Interferon-beta inhibits glioma angiogenesis through downregulation of vascular endothelial growth factor and upregulation of interferon inducible protein 10. Int J Oncol. 2014;45:1837–1846. doi:10.3892/ijo.2014.2620.
   PubMed Web of Science ®Google Scholar
• Wang Q, Hu B, Hu X, Kim H, Squatrito M, Scarpace L, deCarvalho AC, Lyu S, Li P, Li Y, et al. tumor evolution of glioma-intrinsic gene expression subtypes associates with immunological changes in the microenvironment. Cancer Cell. 2018;33:152. doi:10.1016/j.ccell.2017.12.012.
   PubMed Web of Science ®Google Scholar
• Yang K, Guan S, Zhang H, Chen Z. Induction of interleukin 6 impairs the anti-HBV efficiency of IFN-α in human hepatocytes through upregulation of SOCS3. J Med Virol. 2019;91:803–812. doi:10.1002/jmv.25382.
   PubMed Web of Science ®Google Scholar
• Yu C-F, Peng W-M, Schlee M, Barchet W, Eis-Hübinger AM, Kolanus W, Geyer M, Schmitt S, Steinhagen F, Oldenburg J, et al. SOCS1 and SOCS3 Target IRF7 degradation to suppress TLR7-mediated type I IFN Production of Human plasmacytoid dendritic cells. J Immunol. 2018;200:4024–4035. doi:10.4049/jimmunol.1700510.
   PubMed Web of Science ®Google Scholar
• Cui J, Zhu L, Xia X, Wang HY, Legras X, Hong J, Ji J, Shen P, Zheng S, Chen ZJ, et al. NLRC5 negatively regulates the NF-kappaB and type I interferon signaling pathways. Cell. 2010;141:483–496. doi:10.1016/j.cell.2010.03.040.
   PubMed Web of Science ®Google Scholar
• Fekete T, Bencze D, Szabo A, Csoma E, Biro T, Bacsi A, Pazmandi K. Regulatory NLRs Control the RLR-Mediated Type I Interferon and Inflammatory Responses in Human Dendritic Cells. Front Immunol. 2018;9:2314. doi:10.3389/fimmu.2018.02314.
   PubMed Web of Science ®Google Scholar
• Weiss CM, Trobaugh DW, Sun C, Lucas TM, Diamond MS, Ryman KD, Klimstra WB.The interferon-induced exonuclease ISG20 exerts antiviral activity through upregulation of type i interferon response proteins. mSphere. 2018;3.
   Web of Science ®Google Scholar
• Zheng C, Zheng Z, Zhang Z, Meng J, Liu Y, Ke X, Hu Q, Wang H. IFIT5 positively regulates NF-κB signaling through synergizing the recruitment of IκB kinase (IKK) to TGF-β-activated kinase 1 (TAK1).. Cell Signal. 2015;27:2343–2354. doi:10.1016/j.cellsig.2015.08.018.
   PubMed Web of Science ®Google Scholar
• Paul A, Tang TH, Ng SK. Interferon regulatory factor 9 structure and regulation. Front Immunol. 2018;9:1831. doi:10.3389/fimmu.2018.01831.
   PubMed Web of Science ®Google Scholar
• Wu Z, Wang L, Xu X, Lin G, Mao H, Ran X, Zhang T, Huang K, Wang H, Huang Q, et al. Interaction of IRF9 and STAT2 synergistically up-regulates IFN and PKR transcription in Ctenopharyngodon idella. Mol Immunol. 2017;85:273–282. doi:10.1016/j.molimm.2017.03.013.
   PubMed Web of Science ®Google Scholar
• Martini M, Pallini R, Luongo G, Cenci T, Lucantoni C, Larocca LM. Prognostic relevance of SOCS3 hypermethylation in patients with glioblastoma multiforme. Int J Cancer. 2008;123:2955–2960. doi:10.1002/ijc.23805.
   PubMed Web of Science ®Google Scholar
• Lin S-L, Wu S-M, Chung I-H, Lin Y-H, Chen C-Y, Chi H-C, Lin T-K, Yeh C-T, Lin K-H. Stimulation of interferon-stimulated gene 20 by thyroid hormone enhances angiogenesis in liver cancer. Neoplasia. 2018;20:57–68. doi:10.1016/j.neo.2017.10.007.
   PubMed Web of Science ®Google Scholar
• Lou Y-J, Pan X-R, Jia P-M, Li D, Xiao S, Zhang Z-L, Chen S-J, Chen Z, Tong J-H. IRF-9/STAT2 [corrected] functional interaction drives retinoic acid-induced gene G expression independently of STAT1. Cancer Res. 2009;69:3673–3680. doi:10.1158/0008-5472.CAN-08-4922.
   PubMed Web of Science ®Google Scholar
• Yoshihama S, Vijayan S, Sidiq T, Kobayashi KS. NLRC5/CITA: a key player in cancer immune surveillance. Trends in Cancer. 2017;3:28–38. doi:10.1016/j.trecan.2016.12.003.
   PubMed Web of Science ®Google Scholar
• Lo U-G, Bao J, Cen J, Yeh H-C, Luo J, Tan W, Hsieh J-T. Interferon-induced IFIT5 promotes epithelial-to-mesenchymal transition leading to renal cancer invasion. Am J Clin Exp Urol. 2019;7:31–45.
   PubMed Web of Science ®Google Scholar
• Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P, et al. STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2019;47:D607–D613. doi:10.1093/nar/gky1131.
   PubMed Web of Science ®Google Scholar
• Shukla S, Evans JR, Malik R, Feng FY, Dhanasekaran SM, Cao X, Chen G, Beer DG, Jiang H, Chinnaiyan AM. Development of a RNA-Seq based prognostic signature in lung Adenocarcinoma. J Natl Cancer Inst. 2017;109(1).
   Google Scholar
• Amankulor NM, Kim Y, Arora S, Kargl J, Szulzewsky F, Hanke M, Margineantu DH, Rao A, Bolouri H, Delrow J, et al. Mutant IDH1 regulates the tumor-associated immune system in gliomas. Genes Dev. 2017;31:774–786. doi:10.1101/gad.294991.116.
   PubMed Web of Science ®Google Scholar
• Cheng W, Ren X, Zhang C, Cai J, Han S, Wu A. Gene expression profiling stratifies IDH1-mutant glioma with distinct prognoses. Mol Neurobiol. 2017;54:5996–6005. doi:10.1007/s12035-016-0150-6.
   PubMed Web of Science ®Google Scholar
• Rooney MS, Shukla SA, Wu CJ, Getz G, Hacohen N. Molecular and genetic properties of tumors associated with local immune cytolytic activity. Cell. 2015;160:48–61. doi:10.1016/j.cell.2014.12.033.
   PubMed Web of Science ®Google Scholar
• Zhou W, Ke SQ, Huang Z, Flavahan W, Fang X, Paul J, Wu L, Sloan AE, McLendon RE, Li X, et al. Periostin secreted by glioblastoma stem cells recruits M2 tumour-associated macrophages and promotes malignant growth. Nat Cell Biol. 2015;17:170–182. doi:10.1038/ncb3090.
   PubMed Web of Science ®Google Scholar
• Young JS, Dayani F, Morshed RA, Okada H, Aghi MK Immunotherapy for high grade gliomas: A clinical update and practical considerations for neurosurgeons. World neurosurgery 2019124 397–409 doi:10.1016/j.wneu.2018.12.222
   Google Scholar
• Zhu X, McDowell MM, Newman WC, Mason GE, Greene S, Tamber MS. Severe cerebral edema following nivolumab treatment for pediatric glioblastoma: case report. J Neurosurg Pediatr. 2017;19:249–253. doi:10.3171/2016.8.PEDS16326.
   PubMed Web of Science ®Google Scholar
• Sippel TR, White J, Fau - Nag K, Tsvankin V, Klaassen M, Kleinschmidt-DeMasters BK, Waziri A. Neutrophil degranulation and immunosuppression in patients with GBM: restoration of cellular immune function by targeting arginase I. Clin Cancer Res. 2011;17:6992–7002. doi:10.1158/1078-0432.CCR-11-1107.
   PubMed Web of Science ®Google Scholar
• Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol. 2011;11:723–737. doi:10.1038/nri3073.
   PubMed Web of Science ®Google Scholar
• Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest. 2012;122:787–795. doi:10.1172/JCI59643.
   PubMed Web of Science ®Google Scholar
• Benci JL, Xu B, Qiu Y, Wu TJ, Dada H, Twyman-Saint Victor C, Cucolo L, Lee DSM, Pauken KE, Huang AC, et al. Tumor interferon signaling regulates a multigenic resistance program to immune checkpoint blockade. Cell. 2016;167:1540–1554. doi:10.1016/j.cell.2016.11.022.
   PubMed Web of Science ®Google Scholar
• Minn AJ, Wherry EJ. Combination cancer therapies with immune checkpoint blockade: convergence on interferon signaling. Cell. 2016;165:272–275. doi:10.1016/j.cell.2016.03.031.
   PubMed Web of Science ®Google Scholar
• Bowman RL, Wang Q, Carro A, Verhaak RGW, Squatrito M. GlioVis data portal for visualization and analysis of brain tumor expression datasets. Neuro-Oncology. 2017;19:139–141. doi:10.1093/neuonc/now247.
   PubMed Web of Science ®Google Scholar
• Tripathi S, Pohl MO, Zhou Y, Rodriguez-Frandsen A, Wang G, Stein DA, Moulton H, DeJesus P, Che J, Mulder LF, et al. Meta- and orthogonal integration of influenza “OMICs” data defines a role for ubr4 in virus budding. Cell Host Microbe. 2015;18:723–735. doi:10.1016/j.chom.2015.11.002.
   PubMed Web of Science ®Google Scholar
• Bindea G, Mlecnik B, Hackl H, Charoentong P, Tosolini M, Kirilovsky A, Fridman W-H, Pagès F, Trajanoski Z, Galon J. ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics. 2009;25:1091–1093. doi:10.1093/bioinformatics/btp101.
   PubMed Web of Science ®Google Scholar
• Hänzelmann S, Castelo R, Fau - Guinney J. GSVA: gene set variation analysis for microarray and RNA-seq data. BMC Bioinformatics. 2013;14:7. doi:10.1186/1471-2105-14-7.
   PubMed Web of Science ®Google Scholar
• Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005;102:15545–15550. doi:10.1073/pnas.0506580102.
   PubMed Web of Science ®Google Scholar
• Bindea G, Mlecnik B, Tosolini M, Kirilovsky A, Waldner M, Obenauf AC, Angell H, Fredriksen T, Lafontaine L, Berger A, et al. Spatiotemporal dynamics of intratumoral immune cells reveal the immune landscape in human cancer. Immunity. 2013;39:782–795. doi:10.1016/j.immuni.2013.10.003.
   PubMed Web of Science ®Google Scholar
• Becht E, Giraldo NA, Lacroix L, Buttard B, Elarouci N, Petitprez F, Selves J, Laurent-Puig P, Sautès-Fridman C, Fridman WH, et al. Estimating the population abundance of tissue-infiltrating immune and stromal cell populations using gene expression. Genome Biol. 2016;17:218. doi:10.1186/s13059-016-1070-5.
   PubMed Web of Science ®Google Scholar
• Newman AM, Liu CL, Green MR, Gentles AJ, Feng W, Xu Y, Hoang CD, Diehn M, Alizadeh AA. Robust enumeration of cell subsets from tissue expression profiles. Nat Methods. 2015;12:453–457. doi:10.1038/nmeth.3337.
   PubMed Web of Science ®Google Scholar
• Remmele W, Schicketanz KH. Immunohistochemical determination of estrogen and progesterone receptor content in human breast cancer. Computer-assisted image analysis (QIC score) vs. subjective grading (IRS). Pathol Res Pract. 1993;189:862–866. doi:10.1016/S0344-0338(11)81095-2.
   PubMed Web of Science ®Google Scholar
• Lossos IS, Czerwinski D, Fau - Alizadeh AA, Alizadeh A, Fau - Wechser MA, Wechser M, Fau - Tibshirani R, Tibshirani R, Fau - Botstein D, Botstein D, et al. Prediction of survival in diffuse large-B-cell lymphoma based on the expression of six genes. N Engl J Med. 2004;350:1828–1837. doi:10.1056/NEJMoa032520.
   PubMed Web of Science ®Google Scholar
• Wang Y, Li J, Xia Y, Gong R, Wang K, Yan Z, Wan X, Liu G, Wu D, Shi L, et al. Prognostic nomogram for intrahepatic cholangiocarcinoma after partial hepatectomy. J Clin Oncol. 2013;31:1188–1195. doi:10.1200/JCO.2012.41.5984.
   PubMed Web of Science ®Google Scholar