Evaluating the efficacy and safety of trebananib in treating ovarian cancer and non-ovarian cancer patients: a meta-analysis and systematic review

References

• Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–249. doi: 10.3322/caac.21660
   PubMed Web of Science ®Google Scholar
• Ferrari F, Giannini A. Approaches to prevention of gynecological malignancies. BMC Womens Health. 2024;24(1):254. doi: 10.1186/s12905-024-03100-4
   PubMed Web of Science ®Google Scholar
• Ghose A, Bolina A, Mahajan I, et al. Hereditary ovarian cancer: towards a cost-effective prevention strategy. Int J Environ Res Public Health. 2022;19(19):12057. doi: 10.3390/ijerph191912057
   PubMed Web of Science ®Google Scholar
• Giannini A, Di Dio C, Di Donato V, et al. PARP inhibitors in newly diagnosed and recurrent ovarian cancer. Am J Clin Oncol. 2023;46(9):414–419. doi: 10.1097/coc.0000000000001024
   PubMed Web of Science ®Google Scholar
• Folkman J. Role of angiogenesis in tumor growth and metastasis. Semin Oncol. 2002;29(6 Suppl 16):15–18. doi: 10.1053/sonc.2002.37263
   PubMed Web of Science ®Google Scholar
• Bergers G, Benjamin LE. Tumorigenesis and the angiogenic switch. Nat Rev Cancer. 2003;3(6):401–410. doi: 10.1038/nrc1093
   PubMed Web of Science ®Google Scholar
• Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–674. doi: 10.1016/j.cell.2011.02.013
   PubMed Web of Science ®Google Scholar
• Sherwood LM, Parris EE, Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med. 1971;285(21):1182–1186. doi: 10.1056/nejm197111182852108
   PubMed Web of Science ®Google Scholar
• Integrated genomic analyses of ovarian carcinoma. Nature. 2011;474(7353):609–615. doi: 10.1038/nature10166
   PubMed Web of Science ®Google Scholar
• Ioannidou E, Moschetta M, Shah S, et al. Angiogenesis and anti-angiogenic treatment in prostate cancer: mechanisms of action and molecular targets. Int J Mol Sci. 2021;22(18):9926. doi: 10.3390/ijms22189926
   PubMed Web of Science ®Google Scholar
• Keck PJ, Hauser SD, Krivi G, et al. Vascular permeability factor, an endothelial cell mitogen related to PDGF. Sci (New York, NY). 1989;246(4935):1309–1312. doi: 10.1126/science.2479987
   Google Scholar
• Leung DW, Cachianes G, Kuang WJ, et al. Vascular endothelial growth factor is a secreted angiogenic mitogen. Sci (New Y, NY). 1989;246(4935):1306–1309. doi: 10.1126/science.2479986
   PubMed Web of Science ®Google Scholar
• Hurwitz H, Fehrenbacher L, Novotny W, et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med. 2004;350(23):2335–2342. doi: 10.1056/NEJMoa032691
   PubMed Web of Science ®Google Scholar
• Faivre S, Demetri G, Sargent W, et al. Molecular basis for sunitinib efficacy and future clinical development. Nat Rev Drug Discov. 2007;6(9):734–745. doi: 10.1038/nrd2380
   PubMed Web of Science ®Google Scholar
• Wilhelm S, Carter C, Lynch M, et al. Discovery and development of sorafenib: a multikinase inhibitor for treating cancer. Nat Rev Drug Discov. 2006;5(10):835–844. doi: 10.1038/nrd2130
   PubMed Web of Science ®Google Scholar
• Su J, Wang M, Fu Y, et al. Efficacy and safety of multi-kinase inhibitors in patients with radioiodine-refractory differentiated thyroid cancer: a systematic review and meta-analysis of clinical trials. Expert Rev Anticancer Ther. 2022;22(9):999–1008. doi: 10.1080/14737140.2022.2102000
   PubMed Web of Science ®Google Scholar
• Burger RA, Brady MF, Bookman MA, et al. Risk factors for GI adverse events in a phase III randomized trial of bevacizumab in first-line therapy of advanced ovarian cancer: a gynecologic oncology group study. J Clin Oncol. 2014;32(12):1210–1217. doi: 10.1200/jco.2013.53.6524
   PubMed Web of Science ®Google Scholar
• Dempke WCM, Heinemann V. Resistance to EGF-R (erbB-1) and VEGF-R modulating agents. Eur J Cancer. 2009;45(7):1117–1128. doi: 10.1016/j.ejca.2008.11.038
   PubMed Web of Science ®Google Scholar
• Eklund L, Olsen BR. Tie receptors and their angiopoietin ligands are context-dependent regulators of vascular remodeling. Exp Cell Res. 2006;312(5):630–641. doi: 10.1016/j.yexcr.2005.09.002
   PubMed Web of Science ®Google Scholar
• Parmar D, Apte M. Angiopoietin inhibitors: A review on targeting tumor angiogenesis. Eur J Pharmacol. 2021;899:174021. doi: 10.1016/j.ejphar.2021.174021
   PubMed Web of Science ®Google Scholar
• Robson EJ, Ghatage P. AMG 386: profile of a novel angiopoietin antagonist in patients with ovarian cancer. Expert Opin Investig Drugs. 2011;20(2):297–304. doi: 10.1517/13543784.2011.549125
   PubMed Web of Science ®Google Scholar
• Coxon A, Bready J, Min H, et al. Context-dependent role of angiopoietin-1 inhibition in the suppression of angiogenesis and tumor growth: implications for AMG 386, an angiopoietin-1/2-neutralizing peptibody. Mol Cancer Ther. 2010;9(10):2641–2651. doi: 10.1158/1535-7163.Mct-10-0213
   PubMed Web of Science ®Google Scholar
• Monk BJ, Minion L, Lambrechts S, et al. Incidence and management of edema associated with trebananib (AMG 386). Gynecol Oncol. 2013;130(3):636–641. doi: 10.1016/j.ygyno.2013.05.023
   PubMed Web of Science ®Google Scholar
• Karlan BY, Oza AM, Richardson GE, et al. Randomized, double-blind, placebo-controlled phase II study of AMG 386 combined with weekly paclitaxel in patients with recurrent ovarian cancer. J Clin Oncol. 2012;30(4):362–371. doi: 10.1200/jco.2010.34.3178
   PubMed Web of Science ®Google Scholar
• Rini B, Szczylik C, Tannir NM, et al. AMG 386 in combination with sorafenib in patients with metastatic clear cell carcinoma of the kidney: a randomized, double-blind, placebo-controlled, phase 2 study. Cancer. 2012;118(24):6152–6161. doi: 10.1002/cncr.27632
   PubMed Web of Science ®Google Scholar
• Eatock MM, Tebbutt NC, Bampton CL, et al. Phase II randomized, double-blind, placebo-controlled study of AMG 386 (trebananib) in combination with cisplatin and capecitabine in patients with metastatic gastro-oesophageal cancer [Article]. Ann Oncol. 2013;24(3):710–718. doi: 10.1093/annonc/mds502
   PubMed Web of Science ®Google Scholar
• Peeters M, Strickland AH, Lichinitser M, et al. A randomised, double-blind, placebo-controlled phase 2 study of trebananib (AMG 386) in combination with FOLFIRI in patients with previously treated metastatic colorectal carcinoma. Br J Cancer. 2013;108(3):503–511. doi: 10.1038/bjc.2012.594
   PubMed Web of Science ®Google Scholar
• Monk BJ, Poveda A, Vergote I, et al. Anti-angiopoietin therapy with trebananib for recurrent ovarian cancer (TRINOVA-1): a randomised, multicentre, double-blind, placebo-controlled phase 3 trial. Lancet Oncol. 2014;15(8):799–808. doi: 10.1016/S1470-2045(14)70244-X
   PubMed Web of Science ®Google Scholar
• Diéras V, Wildiers H, Jassem J, et al. Trebananib (AMG 386) plus weekly paclitaxel with or without bevacizumab as first-line therapy for HER2-negative locally recurrent or metastatic breast cancer: a phase 2 randomized study. Breast. 2015;24(3):182‐190. doi: 10.1016/j.breast.2014.11.003
   Web of Science ®Google Scholar
• Marth C, Vergote I, Scambia G, et al. ENGOT-ov-6/TRINOVA-2: randomised, double-blind, phase 3 study of pegylated liposomal doxorubicin plus trebananib or placebo in women with recurrent partially platinum-sensitive or resistant ovarian cancer. Eur J Cancer. 2017;70:111–121. doi: 10.1016/j.ejca.2016.09.004
   PubMed Web of Science ®Google Scholar
• Vergote I, Scambia G, O’Malley DM, et al. Trebananib or placebo plus carboplatin and paclitaxel as first-line treatment for advanced ovarian cancer (TRINOVA-3/ENGOT-ov2/GOG-3001): a randomised, double-blind, phase 3 trial. Lancet Oncol. 2019;20(6):862–876. doi: 10.1016/s1470-2045(19)30178-0
   PubMed Web of Science ®Google Scholar
• Lee EQ, Zhang P, Wen PY, et al. NRG/RTOG 1122: a phase 2, double-blinded, placebo-controlled study of bevacizumab with and without trebananib in patients with recurrent glioblastoma or gliosarcoma. Cancer. 2020;126(12):2821–2828. doi: 10.1002/cncr.32811
   PubMed Web of Science ®Google Scholar
• Yancopoulos GD, Davis S, Gale NW, et al. Vascular-specific growth factors and blood vessel formation. Nature. 2000;407(6801):242–248. doi: 10.1038/35025215
   PubMed Web of Science ®Google Scholar
• Sato TN, Tozawa Y, Deutsch U, et al. Distinct roles of the receptor tyrosine kinases tie-1 and tie-2 in blood vessel formation. Nature. 1995;376(6535):70–74. doi: 10.1038/376070a0
   PubMed Web of Science ®Google Scholar
• Leong A, Kim M. The Angiopoietin-2 and TIE pathway as a therapeutic target for enhancing antiangiogenic therapy and immunotherapy in patients with advanced cancer. Int J Mol Sci. 2020;21(22):8689. doi: 10.3390/ijms21228689
   PubMed Web of Science ®Google Scholar
• Etoh T, Inoue H, Tanaka S, et al. Angiopoietin-2 is related to tumor angiogenesis in gastric carcinoma: possible in vivo regulation via induction of proteases. Cancer Res. 2001;61(5):2145–2153.
   PubMed Web of Science ®Google Scholar
• Ahmad SA, Liu W, Jung YD, et al. The effects of angiopoietin-1 and -2 on tumor growth and angiogenesis in human colon cancer. Cancer Res. 2001;61(4):1255–1259.
   PubMed Web of Science ®Google Scholar
• Itatani Y, Kawada K, Yamamoto T, et al. Resistance to anti-angiogenic therapy in cancer—alterations to anti-VEGF pathway. Int J Mol Sci. 2018;19(4):1232. doi: 10.3390/ijms19041232
   PubMed Web of Science ®Google Scholar
• Eklund L, Kangas J, Saharinen P. Angiopoietin-Tie signalling in the cardiovascular and lymphatic systems. Clin Sci (Lond). 2017;131(1):87–103. doi: 10.1042/cs20160129
   PubMed Web of Science ®Google Scholar
• Brindle NP, Saharinen P, Alitalo K. Signaling and functions of angiopoietin-1 in vascular protection. Circ Res. 2006;98(8):1014–1023. doi: 10.1161/01.Res.0000218275.54089.12
   PubMed Web of Science ®Google Scholar
• Aliyuda F, Moschetta M, Ghose A, et al. Advances in ovarian cancer treatment beyond PARP inhibitors. Curr Cancer Drug Targets. 2023;23(6):433–446. doi: 10.2174/1568009623666230209121732
   PubMed Web of Science ®Google Scholar
• Liang X, Xu F, Li X, et al. VEGF signal system: the application of antiangiogenesis. Curr Med Chem. 2014;21(7):894–910. doi: 10.2174/09298673113206660264
   PubMed Web of Science ®Google Scholar
• Kloepper J, Riedemann L, Amoozgar Z, et al. Ang-2/VEGF bispecific antibody reprograms macrophages and resident microglia to anti-tumor phenotype and prolongs glioblastoma survival. Proc Natl Acad Sci U S A. 2016;113(16):4476–4481. doi: 10.1073/pnas.1525360113
   PubMed Web of Science ®Google Scholar
• Wang HL, Deng CS, Lin J, et al. Expression of angiopoietin-2 is correlated with vascularization and tumor size in human colorectal adenocarcinoma. Tohoku J Exp Med. 2007;213(1):33–40. doi: 10.1620/tjem.213.33
   PubMed Web of Science ®Google Scholar
• Helfrich I, Edler L, Sucker A, et al. Angiopoietin-2 levels are associated with disease progression in metastatic malignant melanoma. Clin Cancer Res. 2009;15(4):1384–1392. doi: 10.1158/1078-0432.Ccr-08-1615
   PubMed Web of Science ®Google Scholar
• Sfiligoi C, de Luca A, Cascone I, et al. Angiopoietin-2 expression in breast cancer correlates with lymph node invasion and short survival. Int J Cancer. 2003;103(4):466–474. doi: 10.1002/ijc.10851
   PubMed Web of Science ®Google Scholar
• Monk BJ, Poveda A, Vergote I, et al. Anti-angiopoietin therapy with trebananib for recurrent ovarian cancer (TRINOVA-1): a randomised, multicentre, double-blind, placebo-controlled phase 3 trial. Lancet Oncol. 2014;15(8):799–808. doi: 10.1016/s1470-2045(14)70244-x
   PubMed Web of Science ®Google Scholar
• Eskens FA, Verweij J. The clinical toxicity profile of vascular endothelial growth factor (VEGF) and vascular endothelial growth factor receptor (VEGFR) targeting angiogenesis inhibitors; a review. Eur J Cancer. 2006;42(18):3127–3139. doi: 10.1016/j.ejca.2006.09.015
   PubMed Web of Science ®Google Scholar
• Savaliya M, Surati D, Surati R, et al. Posterior reversible encephalopathy syndrome after Pazopanib therapy. Diseases. 2023;11(2):76. doi: 10.3390/diseases11020076
   PubMedGoogle Scholar
• Gotink KJ, Verheul HM. Anti-angiogenic tyrosine kinase inhibitors: what is their mechanism of action? Angiogenesis. 2010;13(1):1–14. doi: 10.1007/s10456-009-9160-6
   PubMed Web of Science ®Google Scholar
• Lynch TJ, Bell DW, Sordella R, et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med. 2004;350(21):2129–2139. doi: 10.1056/NEJMoa040938
   PubMed Web of Science ®Google Scholar
• Pao W, Miller V, Zakowski M, et al. EGF receptor gene mutations are common in lung cancers from “never smokers” and are associated with sensitivity of tumors to gefitinib and erlotinib. Proc Natl Acad Sci USA. 2004;101(36):13306–13311. doi: 10.1073/pnas.0405220101
   PubMed Web of Science ®Google Scholar
• Bueno MJ, Mouron S, Quintela-Fandino M. Personalising and targeting antiangiogenic resistance: a complex and multifactorial approach. Br J Cancer. 2017;116(9):1119–1125. doi: 10.1038/bjc.2017.69
   PubMed Web of Science ®Google Scholar
• Pepper MS, Ferrara N, Orci L, et al. Potent synergism between vascular endothelial growth factor and basic fibroblast growth factor in the induction of angiogenesis in vitro. Biochem Biophys Res Commun. 1992;189(2):824–831. doi: 10.1016/0006-291x(92)92277-5
   PubMed Web of Science ®Google Scholar
• Oliner J, Min H, Leal J, et al. Suppression of angiogenesis and tumor growth by selective inhibition of angiopoietin-2. Cancer Cell. 2004;6(5):507–516. doi: 10.1016/j.ccr.2004.09.030
   PubMed Web of Science ®Google Scholar
• Lu KV, Chang JP, Parachoniak CA, et al. VEGF inhibits tumor cell invasion and mesenchymal transition through a MET/VEGFR2 complex. Cancer Cell. 2012;22(1):21–35. doi: 10.1016/j.ccr.2012.05.037
   PubMed Web of Science ®Google Scholar
• Choueiri TK, Escudier B, Powles T, et al. Cabozantinib versus everolimus in advanced renal-cell carcinoma. N Engl J Med. 2015;373(19):1814–1823. doi: 10.1056/NEJMoa1510016
   PubMed Web of Science ®Google Scholar
• Augustin HG, Koh GY, Thurston G, et al. Control of vascular morphogenesis and homeostasis through the angiopoietin–Tie system. Nat Rev Mol Cell Biol. 2009;10(3):165–177. doi: 10.1038/nrm2639
   PubMed Web of Science ®Google Scholar
• Ghose A, Gullapalli SVN, Chohan N, et al. Applications of proteomics in ovarian cancer: dawn of a new era. Proteomes. 2022;10(2):16. doi: 10.3390/proteomes10020016
   PubMed Web of Science ®Google Scholar
• Khan KA, Kerbel RS. Improving immunotherapy outcomes with anti-angiogenic treatments and vice versa. Nat Rev Clin Oncol. 2018;15(5):310–324. doi: 10.1038/nrclinonc.2018.9
   PubMed Web of Science ®Google Scholar
• Tian L, Goldstein A, Wang H, et al. Mutual regulation of tumour vessel normalization and immunostimulatory reprogramming. Nature. 2017;544(7649):250–254. doi: 10.1038/nature21724
   PubMed Web of Science ®Google Scholar
• Shrimali RK, Yu Z, Theoret MR, et al. Antiangiogenic agents can increase lymphocyte infiltration into tumor and enhance the effectiveness of adoptive immunotherapy of cancer. Cancer Res. 2010;70(15):6171–6180. doi: 10.1158/0008-5472.Can-10-0153
   PubMed Web of Science ®Google Scholar
• Allen E, Jabouille A, Rivera LB, et al. Combined antiangiogenic and anti–PD-L1 therapy stimulates tumor immunity through HEV formation. Sci Transl Med. 2017;9(385). doi: 10.1126/scitranslmed.aak9679
   Web of Science ®Google Scholar
• Hodi FS, Lawrence D, Lezcano C, et al. Bevacizumab plus ipilimumab in patients with metastatic melanoma. Cancer Immunol Res. 2014;2(7):632–642. doi: 10.1158/2326-6066.Cir-14-0053
   PubMed Web of Science ®Google Scholar
• Motzer RJ, Escudier B, McDermott DF, et al. Nivolumab versus everolimus in advanced renal-cell carcinoma. N Engl J Med. 2015;373(19):1803–1813. doi: 10.1056/NEJMoa1510665
   PubMed Web of Science ®Google Scholar
• Brown JE, Royle KL, Gregory W, et al. Temporary treatment cessation versus continuation of first-line tyrosine kinase inhibitor in patients with advanced clear cell renal cell carcinoma (STAR): an open-label, non-inferiority, randomised, controlled, phase 2/3 trial. Lancet Oncol. 2023;24(3):213–227. doi: 10.1016/s1470-2045(22)00793-8
   PubMed Web of Science ®Google Scholar
• Hatfield SM, Kjaergaard J, Lukashev D, et al. Immunological mechanisms of the antitumor effects of supplemental oxygenation. Sci Transl Med. 2015;7(277):277ra30. doi: 10.1126/scitranslmed.aaa1260
   PubMed Web of Science ®Google Scholar
• Huang Y, Yuan J, Righi E, et al. Vascular normalizing doses of antiangiogenic treatment reprogram the immunosuppressive tumor microenvironment and enhance immunotherapy. Proc Natl Acad Sci U S A. 2012;109(43):17561–17566. doi: 10.1073/pnas.1215397109
   PubMed Web of Science ®Google Scholar
• Coffelt SB, Tal AO, Scholz A, et al. Angiopoietin-2 regulates gene expression in TIE2-expressing monocytes and augments their inherent proangiogenic functions. Cancer Res. 2010;70(13):5270–5280. doi: 10.1158/0008-5472.Can-10-0012
   PubMed Web of Science ®Google Scholar
• Scholz A, Lang V, Henschler R, et al. Angiopoietin-2 promotes myeloid cell infiltration in a β₂-integrin-dependent manner. Blood. 2011;118(18):5050–5059. doi: 10.1182/blood-2011-03-343293
   PubMed Web of Science ®Google Scholar
• Wu X, Giobbie-Hurder A, Liao X, et al. Angiopoietin-2 as a biomarker and target for immune checkpoint therapy. Cancer Immunol Res. 2017;5(1):17–28. doi: 10.1158/2326-6066.Cir-16-0206
   PubMed Web of Science ®Google Scholar
• Schmittnaegel M, De Palma M. Reprogramming tumor blood vessels for enhancing immunotherapy. Trends Cancer. 2017;3(12):809–812. doi: 10.1016/j.trecan.2017.10.002
   PubMed Web of Science ®Google Scholar
• Burger RA, Brady MF, Bookman MA, et al. Incorporation of bevacizumab in the primary treatment of ovarian cancer. N Engl J Med. 2011;365(26):2473–2483. doi: 10.1056/NEJMoa1104390
   PubMed Web of Science ®Google Scholar
• Jayson GC, Kerbel R, Ellis LM, et al. Antiangiogenic therapy in oncology: current status and future directions. Lancet. 2016;388(10043):518–529. doi: 10.1016/s0140-6736(15)01088-0
   PubMed Web of Science ®Google Scholar
• Simpkins F, Belinson JL, Rose PG. Avoiding bevacizumab related gastrointestinal toxicity for recurrent ovarian cancer by careful patient screening. Gynecol Oncol. 2007;107(1):118–123. doi: 10.1016/j.ygyno.2007.06.004
   PubMed Web of Science ®Google Scholar