Effectiveness of antiangiogenic drugs in glioblastoma patients: A systematic review and meta-analysis of randomized clinical trials

Critical Reviews in Oncology/Hematology

Volumn 111, Issue , 2017, Pages 94-102

  Lombardi, Giuseppe ^a   Pambuku, Ardi ^a   Bellu, Luisa ^a   Farina, Miriam ^a   Della Puppa, Alessandro ^b   Denaro, Luca ^c   Zagonel, Vittorina ^a  

^a VENETO INSTITUTE OF ONCOLOGY IOV IRCCS   (Italy)

^b UNIVERSITY HOSPITAL OF PADOVA   (Italy)

^c UNIVERSITY OF PADOVA   (Italy)

Author keywords

Antiangiogenic drugs; Bevacizumab; Chemotherapy; Glioblastoma

Indexed keywords

ANGIOGENESIS INHIBITOR; BEVACIZUMAB; CEDIRANIB; CILENGITIDE; DASATINIB; ENZASTAURIN; FOTEMUSTINE; IRINOTECAN; LOMUSTINE; TEMOZOLOMIDE; TEMSIROLIMUS; VANDETANIB; ANTINEOPLASTIC AGENT;

CANCER COMBINATION CHEMOTHERAPY; CANCER RECURRENCE; DRUG RESPONSE; GLIOBLASTOMA; HUMAN; OVERALL SURVIVAL; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PROGRESSION FREE SURVIVAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SYSTEMATIC REVIEW; TREATMENT OUTCOME; BRAIN NEOPLASMS; DISEASE FREE SURVIVAL; META ANALYSIS; NEOVASCULARIZATION, PATHOLOGIC; VASCULARIZATION;

ANGIOGENESIS INHIBITORS; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BRAIN NEOPLASMS; DISEASE-FREE SURVIVAL; GLIOBLASTOMA; HUMANS; NEOVASCULARIZATION, PATHOLOGIC; RANDOMIZED CONTROLLED TRIALS AS TOPIC;

EID: 85014072446     PISSN: 10408428     EISSN: 18790461     Source Type: Journal    
DOI: 10.1016/j.critrevonc.2017.01.018     Document Type: Review

References (51)

1. Barlesi, F., Scherpereel, A., Rittmeyer, A., Pazzola, A., Ferrer Tur, N., Kim, J.H., et al. Randomized phase III trial of maintenance bevacizumab with or without pemetrexed after first-line induction with bevacizumab, cisplatin, and pemetrexed in advanced nonsquamous non-small-cell lung cancer: AVAPERL (MO22089). J. Clin. Oncol. 31 (2013), 3004–3011.
2. Batchelor, T.T., Mulholland, P., Neyns, B., Nabors, L.B., Campone, M., Wick, A., et al. Phase III randomized trial comparing the efficacy of cediranib as monotherapy, and in combination with lomustine, versus lomustine alone in patients with recurrent glioblastoma. J. Clin. Oncol. 31 (2013), 3212–3218.
3. Batchelor, T.T., Gerstner, E.R., Emblem, K.E., Duda, D.G., Kalpathy-Cramer, J., Snuderl, M., et al. Improved tumor oxygenation and survival in glioblastoma patients who show increased blood perfusion after cediranib and chemoradiation. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 19059–19064.
4. Brandes, A.A., Finocchiaro, G., Zagonel, V., Reni, M., Fabi, A., Caserta, C., et al. Final results from the randomized phase II trial avareg (ML25739) with bevacizumab or fotemustine in recurrent GBM. Neuro-Oncol. 16 (2014), v8–v22.
5. Chauffert, B., Feuvret, L., Bonnetain, F., Taillandier, L., Frappaz, D., Taillia, H., et al. Randomized phase II trial of irinotecan and bevacizumab as neo-adjuvant and adjuvant to temozolomide-based chemoradiation compared with temozolomide-chemoradiation for unresectable glioblastoma: final results of the TEMAVIR study from ANOCEFdagger. Ann. Oncol. 25 (2014), 1442–1447.
6. Chinot, O.L., Wick, W., Mason, W., Henriksson, R., Saran, F., Nishikawa, R., et al. Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N. Engl. J. Med. 370 (2014), 709–722.
7. Chinot, O.L., Nishikawa, R., Mason, W., Henriksson, R., Saran, F., Cloughesy, T., et al. Upfront bevacizumab may extend survival for glioblastoma patients who do not receive second-line therapy: an exploratory analysis of AVAglio. Neuro Oncol. 18 (2016), 1313–1318.
8. Corroyer-Dulmont, A., Peres, E.A., Petit, E., Guillamo, J.S., Varoqueaux, N., Roussel, S., et al. Detection of glioblastoma response to temozolomide combined with bevacizumab based on muMRI and muPET imaging reveals [18F]-fluoro-L-thymidine as an early and robust predictive marker for treatment efficacy. Neuro Oncol. 15 (2013), 41–56.
9. DerSimonian, R., Laird, N., Meta-analysis in clinical trials revisited. Contemp. Clin. Trials 45 (2015), 139–145.
10. Di Stefano, A.L., Labussiere, M., Lombardi, G., Eoli, M., Bianchessi, D., Pasqualetti, F., et al. VEGFA SNP rs2010963 is associated with vascular toxicity in recurrent glioblastomas and longer response to bevacizumab. J. Neurooncol. 121 (2015), 499–504.
11. Duval, S., The Trim and Fill Method. 2005, John Wiley & Sons Ltd, Cheichester.
12. Fischer, I., Gagner, J.P., Law, M., Newcomb, E.W., Zagzag, D., Angiogenesis in gliomas: biology and molecular pathophysiology. Brain Pathol. 15 (2005), 297–310.
13. Friedman, H.S., Prados, M.D., Wen, P.Y., Mikkelsen, T., Schiff, D., Abrey, L.E., et al. Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J. Clin. Oncol. 27 (2009), 4733–4740.
14. Gallego Perez-Larraya, J., Lahutte, M., Petrirena, G., Reyes-Botero, G., Gonzalez-Aguilar, A., Houillier, C., et al. Response assessment in recurrent glioblastoma treated with irinotecan-bevacizumab: comparative analysis of the Macdonald, RECIST, RANO, and RECIST + F criteria. Neuro Oncol. 14 (2012), 667–673.
15. Gasparini, G., Longo, R., Toi, M., Ferrara, N., Angiogenic inhibitors: a new therapeutic strategy in oncology. Nat. Clin. Pract. Oncol. 2 (2005), 562–577.
16. Gasparini, G., Longo, R., Fanelli, M., Teicher, B.A., Combination of antiangiogenic therapy with other anticancer therapies: results, challenges, and open questions. J. Clin. Oncol. 23 (2005), 1295–1311.
17. Giantonio, B.J., Catalano, P.J., Meropol, N.J., O'Dwyer, P.J., Mitchell, E.P., Alberts, S.R., et al. Bevacizumab in combination with oxaliplatin, fluorouracil, and leucovorin (FOLFOX4) for previously treated metastatic colorectal cancer: results from the Eastern Cooperative Oncology Group Study E3200. J. Clin. Oncol. 25 (2007), 1539–1544.
18. Gilbert, M.R., Dignam, J.J., Armstrong, T.S., Wefel, J.S., Blumenthal, D.T., Vogelbaum, M.A., et al. A randomized trial of bevacizumab for newly diagnosed glioblastoma. N. Engl. J. Med. 370 (2014), 699–708.
19. Hartmann, C., Hentschel, B., Wick, W., Capper, D., Felsberg, J., Simon, M., et al. Patients with IDH1 wild type anaplastic astrocytomas exhibit worse prognosis than IDH1-mutated glioblastomas, and IDH1 mutation status accounts for the unfavorable prognostic effect of higher age: implications for classification of gliomas. Acta Neuropathol. 120 (2010), 707–718.
20. Herrlinger, U., Schafer, N., Steinbach, J.P., Weyerbrock, A., Hau, P., Goldbrunner, R., et al. The randomized, multicenter glarius trial investigating bevacizumab/irinotecan vs standard temozolomide in newly diagnosed, MGMT-non-methylated glioblastoma patients: final survival results and quality of life. Neuro-Oncol. 16 (2014), ii1–ii2.
21. Jakobsen, J.N., Hasselbalch, B., Stockhausen, M.T., Lassen, U., Poulsen, H.S., Irinotecan and bevacizumab in recurrent glioblastoma multiforme. Expert Opin. Pharmacother. 12 (2011), 825–833.
22. Khasraw, M., Ameratunga, M.S., Grant, R., Wheeler, H., Pavlakis, N., Antiangiogenic therapy for high-grade glioma. Cochrane Database Syst. Rev., 2014, CD008218 CD008218.
23. Kreisl, T.N., Kim, L., Moore, K., Duic, P., Royce, C., Stroud, I., et al. Phase II trial of single-agent bevacizumab followed by bevacizumab plus irinotecan at tumor progression in recurrent glioblastoma. J. Clin. Oncol. 27 (2009), 740–745.
24. Laack, N.N., Galanis, E., Anderson, S.K., Leinweber, C., Giannini, C., Randomized, placebo-controlled, phase II study of dasatinib with standard chemo-radiotherapy for newly diagnosed glioblastoma, NCCTG N0877 (alliance). J. Clin Oncol, 33, 2015 suppl, abstr 2013.
25. Labussiere, M., Cheneau, C., Prahst, C., Gallego Perez-Larraya, J., Farina, P., Lombardi, G., et al. Angiopoietin-2 may Be involved in the resistance to bevacizumab in recurrent glioblastoma. Cancer Invest. 34 (2016), 39–44.
26. Lee, E.Q., Kaley, T.J., Duda, D.G., Schiff, D., Lassman, A.B., Wong, E.T., et al. A multicenter, phase II, randomized, noncomparative clinical trial of radiation and temozolomide with or without vandetanib in newly diagnosed glioblastoma patients. Clin. Cancer Res. 21 (2015), 3610–3618.
27. Levin, V.A., Crafts, D.C., Norman, D.M., Hoffer, P.B., Spire, J.P., Wilson, C.B., Criteria for evaluating patients undergoing chemotherapy for malignant brain tumors. J. Neurosurg. 47 (1977), 329–335.
28. Lu-Emerson, C., Duda, D.G., Emblem, K.E., Taylor, J.W., Gerstner, E.R., Loeffler, J.S., et al. Lessons from anti-vascular endothelial growth factor and anti-vascular endothelial growth factor receptor trials in patients with glioblastoma. J. Clin. Oncol. 33 (2015), 1197–1213.
29. Macdonald, D.R., Cascino, T.L., Schold, S.C. Jr., Cairncross, J.G., Response criteria for phase II studies of supratentorial malignant glioma. J. Clin. Oncol. 8 (1990), 1277–1280.
30. Manegold, C., Dingemans, A.C., Gray, J.E., Nakagawa, K., Nicolson, M., Peters, S., et al. The potential of combined immunotherapy and antiangiogenesis for the synergistic treatment of advanced NSCLC. J. Thorac. Oncol. 12:2 (2017), 194–207.
31. Nabors, L.B., Fink, K.L., Mikkelsen, T., Grujicic, D., Tarnawski, R., Nam do, H., et al. Two cilengitide regimens in combination with standard treatment for patients with newly diagnosed glioblastoma and unmethylated MGMT gene promoter: results of the open-label, controlled, randomized phase II CORE study. Neuro Oncol. 17 (2015), 708–717.
32. Norden, A.D., Drappatz, J., Wen, P.Y., Antiangiogenic therapies for high-grade glioma. Nat. Rev. Neurol. 5 (2009), 610–620.
33. Parmar, M.K., Torri, V., Stewart, L., Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat. Med. 17 (1998), 2815–2834.
34. Piao, Y., Liang, J., Holmes, L., Henry, V., Sulman, E., de Groot, J.F., Acquired resistance to anti-VEGF therapy in glioblastoma is associated with a mesenchymal transition. Clin. Cancer Res. 19 (2013), 4392–4403.
35. Sandmann, T., Bourgon, R., Garcia, J., Li, C., Cloughesy, T., Chinot, O.L., et al. Patients with proneural glioblastoma may derive overall survival benefit from the addition of bevacizumab to first-line radiotherapy and temozolomide: retrospective analysis of the AVAglio trial. J. Clin. Oncol. 33:25 (2015), 2735–2744.
36. Sathornsumetee, S., Cao, Y., Marcello, J.E., Herndon, J.E. 2nd, McLendon, R.E., Desjardins, A., et al. Tumor angiogenic and hypoxic profiles predict radiographic response and survival in malignant astrocytoma patients treated with bevacizumab and irinotecan. J. Clin. Oncol. 26 (2008), 271–278.
37. Schaub, C., Schafer, N., Mack, F., Stuplich, M., Kebir, S., Niessen, M., et al. The earlier the better? Bevacizumab in the treatment of recurrent MGMT-non-methylated glioblastoma. J. Cancer Res. Clin. Oncol. 142 (2016), 1825–1829.
38. Stupp, R., Mason, W.P., van den Bent, M.J., Weller, M., Fisher, B., Taphoorn, M.J., et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 352 (2005), 987–996.
39. Stupp, R., Hegi, M.E., Mason, W.P., van den Bent, M.J., Taphoorn, M.J., Janzer, R.C., et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 10 (2009), 459–466.
40. Stupp, R., Hegi, M.E., Gorlia, T., Erridge, S.C., Perry, J., Hong, Y.K., et al. Cilengitide combined with standard treatment for patients with newly diagnosed glioblastoma with methylated MGMT promoter (CENTRIC EORTC 26071-22072 study): a multicentre, randomised, open-label, phase 3 trial. Lancet Oncol. 15 (2014), 1100–1108.
41. Taal, W., Oosterkamp, H.M., Walenkamp, A.M., Dubbink, H.J., Beerepoot, L.V., Hanse, M.C., et al. Single-agent bevacizumab or lomustine versus a combination of bevacizumab plus lomustine in patients with recurrent glioblastoma (BELOB trial): a randomised controlled phase 2 trial. Lancet Oncol. 15 (2014), 943–953.
42. Tabouret, E., Boudouresque, F., Barrie, M., Matta, M., Boucard, C., Loundou, A., et al. Association of matrix metalloproteinase 2 plasma level with response and survival in patients treated with bevacizumab for recurrent high-grade glioma. Neuro Oncol. 16 (2014), 392–399.
43. Tabouret, E., Boudouresque, F., Farina, P., Barrie, M., Bequet, C., Sanson, M., et al. MMP2 and MMP9 as candidate biomarkers to monitor bevacizumab therapy in high-grade glioma. Neuro Oncol. 17 (2015), 1174–1176.
44. Tierney, J.F., Stewart, L.A., Ghersi, D., Burdett, S., Sydes, M.R., Practical methods for incorporating summary time-to-event data into meta-analysis. Trials, 8, 2007, 16.
45. Vredenburgh, J.J., Desjardins, A., Herndon, J.E., 2nd Marcello, J., Reardon, D.A., Quinn, J.A., et al. Bevacizumab plus irinotecan in recurrent glioblastoma multiforme. J. Clin. Oncol. 25 (2007), 4722–4729.
46. Wen, P.Y., Kesari, S., Malignant gliomas in adults. N. Engl. J. Med. 359 (2008), 492–507.
47. Wen, P.Y., Macdonald, D.R., Reardon, D.A., Cloughesy, T.F., Sorensen, A.G., Galanis, E., et al. Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J. Clin. Oncol. 28 (2010), 1963–1972.
48. Wick, W., Puduvalli, V.K., Chamberlain, M.C., van den Bent, M.J., Carpentier, A.F., Cher, L.M., et al. Phase III study of enzastaurin compared with lomustine in the treatment of recurrent intracranial glioblastoma. J. Clin. Oncol. 28 (2010), 1168–1174.
49. Wick, W., Gorlia, T., Van Den bent, M.J., Vetch, C.J., Steuve, J., Brandes, A.A., et al. Radiation therapy and concurrent plus adjuvant temsirolimus (CCI-779) versus chemoirradiation with temozolomide in newly diagnosed glioblastoma without methylation of MGMT gene promoter. J. Clin. Oncol., 32, 2014, 5s (suppl; abstr 2037).
50. Wick, W., Brandes, A.A., Gorlia, T., Bendszus, M., Sahm, F., Taal, W., et al. Phase III trial exploring the combination of bevacizumab and lomustine in patients with first recurrence of a glioblastoma: the EORTC 26101 trial. Neuro-Oncol., 17, 2015, v1.
51. Wong, M.L., Prawira, A., Kaye, A.H., Hovens, C.M., Tumour angiogenesis: its mechanism and therapeutic implications in malignant gliomas. J. Clin. Neurosci. 16 (2009), 1119–1130.