Efficacy and safety of bevacizumab and etoposide combination in patients with recurrent malignant gliomas who have failed bevacizumab

Authors

  • Jose A. Carrillo UC Irvine, Department of Neurology and Chao Comprehensive Cancer Center UC Irvine Department of Neurological Surgery
  • Frank P.K. Hsu UC Irvine Department of Neurological Surgery
  • Johnny Delashaw UC Irvine Department of Neurological Surgery
  • Daniela Bota UC Irvine, Department of Neurology and Chao Comprehensive Cancer Center UC Irvine Department of Neurological Surgery

DOI:

https://doi.org/10.7175/rhc.v5i1.668

Keywords:

Bevacizumab, Etoposide, Malignant Gliomalioblastoma Multiforme, Malignant Glioma, GBM

Abstract

Despite recent advances in the treatment of malignant gliomas (World Health Organization grade III and grade IV tumors- Glioblastoma Multiforme, Anaplastic Astrocytoma and Anaplastic Oligodendroglioma), the overall prognosis remains poor. Tumor recurrence in malignant glioma is inevitable, and associated with reduced overall survival (OS). Bevacizumab is approved for use in progressive GBM as a second line treatment, and is associated with improvements in progression free survival (PFS). However, all GBM patients eventually recur on bevacizumab therapy, with a very short OS after bevacizumab failure. No FDA-approved therapy is available for this clinical setting. Etoposide crosses the blood-brain barrier and has activity in recurrent malignant gliomas. The use of bevacizumab with etoposide in recurrent malignant gliomas in the setting of bevacizumab resistance is evaluated in this review. Bevacizumab and etoposide combined therapy is associated with radiographic response and effectiveness in selected patients.

References

CBTRUS. CBTRUS statistical report: Primary brain and central nervous system tumors diagnosed in the United States in 2004-2008. In: Central Brain Tumor Registry of the United States. CBTRUS, 2012

Stupp R, Mason WP, van den Bent MJ, 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 Oncology 2009; 10: 459-466; http://dx.doi.org/10.1016/S1470-2045(09)70025-7

Stupp R, van den Bent MJ, Weller M, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. NEJM 2005; 352: 987-996; http://dx.doi.org/10.1056/NEJMoa043330

Schmidt NO, Hagel C, Ergun S, et al. Levels of Vascular Endothelial Growth Factor, Hepatocyte Growth Factor/Scatter Factor and Basic Fibroblast Growth Factor in Human Gliomas and Their Relation to Angiogenesis. International Journal of Cancer 1999; 84: 10-8; http://dx.doi.org/10.1002/(SICI)1097-0215(19990219)84:1<10::AID-IJC3>3.0.CO;2-L

Pietsch T, Valter MM, Wolf HK, et al. Expression and distribution of vascular endothelial growth factor protein in human brain tumors. Acta Neuropathol 1997; 93: 109-17; http://dx.doi.org/10.1007/s004010050591

Samoto K, Ikezaki K, Ono M. Expression of Vascular Endothelial Growth Factor and Its Possible Relation with Neovascularization in Human Brain Tumors. Cancer Res 1995; 55: 1189-93

Lamszus K, Ulbricht U, Matschke J, et al. Levels of Soluble Vascular Endothelial Growth Factor (VEGF) Receptor 1 in Astrocytic Tumors and Its Relation to Malignancy, Vascularity, and VEGF-A. Clin Cancer Res 2003; 9: 1399-405

Zhou YH, Tan F, Hess KR, et al. The Expression of PAX6, PTEN, Vascular Endothelial Growth Factor, and Epidermal Growth Factor Receptor in Gliomas: Relationship to Tumor Grade and Survival. Clin Cancer Res 2003; 9: 3369-75

Rubenstein JL, Ozawa T, Zhang M, et al. Anti-VEGF Antibody Treatment of Glioblastoma Prolongs Survival But Results in Increased Vascular Cooption. Neoplasia 2000; 2: 306-14; http://dx.doi.org/10.1038/sj.neo.7900102

Desjardins A, Reardon DA, Coan A, et al. Bevacizumab and daily temozolomide for recurrent glioblastoma. Cancer 2012; 118: 1302-12; http://dx.doi.org/10.1002/cncr.26381

Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev 2004; 25: 581-611; http://dx.doi.org/10.1210/er.2003-0027

Vredenburgh JJ, Desjardins A, Herndon JE 2nd, et al., Bevacizumab plus irinotecan in recurrent glioblastoma multiforme. J Clin Oncol 2007; 25: 4722-9; http://dx.doi.org/10.1200/JCO.2007.12.2440

Friedman HS, Prados MD, Wen PY, et al., Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J Clin Oncol 2009; 27: 4733-40; http://dx.doi.org/10.1200/JCO.2008.19.8721

Weller M, Cloughesy T, Perry JR, et al., Standards of care for treatment of recurrent glioblastoma--are we there yet? Neuro Oncol 2013; 15: 4-27; http://dx.doi.org/10.1093/neuonc/nos273

Kyritsis AP, Levin VA. An algorithm for chemotherapy treatment of recurrent glioma patients after temozolomide failure in the general oncology setting. Cancer Chemother Pharmacol 2011; 67: 971-83; http://dx.doi.org/10.1007/s00280-011-1617-9

Reardon DA, Desjardins A, Peters KB, et al., Phase 2 study of carboplatin, irinotecan, and bevacizumab for recurrent glioblastoma after progression on bevacizumab therapy. Cancer 2011; 117: 5351-8; http://dx.doi.org/10.1002/cncr.26188

Reardon DA, Desjardins A, Peters K, et al. Phase II study of metronomic chemotherapy with bevacizumab for recurrent glioblastoma after progression on bevacizumab therapy. J Neurooncol 2011; 103: 371-9; http://dx.doi.org/10.1007/s11060-010-0403-6

Kreisl TN, Kim L, Moore K, et al. Phase II trial of single-agent bevacizumab followed by bevacizumab plus irinotecan at tumor progression in recurrent glioblastoma. J Clin Oncol 2009; 27: 740-5; http://dx.doi.org/10.1200/JCO.2008.16.3055

Scott BJ, Quant EC, McNamara MB, et al. Bevacizumab salvage therapy following progression in high-grade glioma patients treated with VEGF receptor tyrosine kinase inhibitors. Neuro Oncol 2010; 12: 603-7; http://dx.doi.org/10.1093/neuonc/nop073

Clark AJ, Butowski NA, Chang SM, et al. Impact of bevacizumab chemotherapy on craniotomy wound healing. J Neurosurg 2011; 114: 1609-16; http://dx.doi.org/10.3171/2010.10.JNS101042

Clark AJ, Lamborn KR, Butowski NA, et al. Neurosurgical management and prognosis of patients with glioblastoma that progresses during bevacizumab treatment. Neurosurgery 2012; 70: 361-70; http://dx.doi.org/10.1227/NEU.0b013e3182314f9d

Kiya K, Uozumi T, Ogasawara H, et al. Penetration of etoposide into human malignant brain tumors after intravenous and oral administration. Cancer Chemother Pharmacol 1992; 29: 339-42; http://dx.doi.org/10.1007/BF00686001

Sevim H, Parkinson JF, McDonald KL. Etoposide-mediated glioblastoma cell death: dependent or independent on the expression of its target, topoisomerase II alpha? J Cancer Res Clin Oncol 2011; 137: 1705-12; http://dx.doi.org/10.1007/s00432-011-1046-5

Tirelli U, D’Incalci M, Canetta R, et al. Etoposide (VP-16-213) in Malignant Brain Tumors: A Phase II Study. Journal of Clinical Oncology 1984; 2: 432-7

Fulton D, Urtasun R, Forsyth P. Phase II study of prolonged oral therapy with etoposide (VP16) for patients with recurrent malignant glioma. J Neurooncol. 1996; 27: 149-55; http://dx.doi.org/10.1007/BF00177478

Korones DN, Benita-Weiss M, Coyle TE, et al. Phase I study of temozolomide and escalating doses of oral etoposide for adults with recurrent malignant glioma. Cancer 2003; 97: 1963-8; http://dx.doi.org/10.1002/cncr.11260

Jeremic B, Grujicic D, Jevremovic S, et al. Carboplatin and Etoposide Chemotherapy Regimen for Recurrent Malignant Glioma: A Phase II Study. J Clin Oncol 1992; 10: 1074-7

Watanabe K, Kanaya H, Fujiyama Y, et al. Combination chemotherapy using carboplatin (JM-8) and etoposide (JET therapy) for recurrent malignant gliomas: a phase II study. Acta Neurochir (Wien) 2002; 144: 1265-70; http://dx.doi.org/10.1007/s00701-002-1023-5

Franceschi E, Cavallo G, Scopece L, et al. Phase II trial of carboplatin and etoposide for patients with recurrent high-grade glioma. Br J Cancer 2004; 91: 1038-44

Sanson M, Monjour A, Sahmoud T, et al. Treatment of Recurrent Malignant Supratentorial Gliomas with Ifosfamide, Carboplatin and Etoposide: a Phase II Study. Eur J Cancer 1996; 32: 2229-35; http://dx.doi.org/10.1016/S0959-8049(96)00299-7

Aoki T, Mizutani T, Nojima K, et al. Phase II study of ifosfamide, carboplatin, and etoposide in patients with a first recurrence of glioblastoma multiforme. J Neurosurg 2010; 112: 50-6; http://dx.doi.org/10.3171/2009.5.JNS081738

Schäfer N, Tichy J, Thanendrarajan S, et al. Ifosfamide, carboplatin and etoposide in recurrent malignant glioma. Oncology 2011; 80: 330-2; http://dx.doi.org/10.1159/000330358

Kesari S, Schiff D, Doherty L, et al. Phase II study of metronomic chemotherapy for recurrent malignant gliomas in adults. Neuro Oncol 2007; 9: 354-63; http://dx.doi.org/10.1215/15228517-2007-006

Reardon DA, Desjardins A, Vredenburgh JJ, et al. Metronomic chemotherapy with daily, oral etoposide plus bevacizumab for recurrent malignant glioma: a phase II study. Br J Cancer 2009; 101: 1986-94; http://dx.doi.org/10.1038/sj.bjc.6605412

Fu BD, Linskey ME, Bota DA. Bevacizumab and etoposide combination chemotherapy in patients with recurrent malignant gliomas who failed bevacizumab. Drugs and Therapy Studies 2012; 2: 26-8; http://dx.doi.org/10.4081/dts.2012.e6

Francesconi AB, Dupre S, Matos M, et al. Carboplatin and etoposide combined with bevacizumab for the treatment of recurrent glioblastoma multiforme. J Clin Neurosci 2010; 17: 970-4; http://dx.doi.org/10.1016/j.jocn.2009.12.009

Reardon DA, Vredenburgh JJ, Coan A, et al. Phase I study of sunitinib and irinotecan for patients with recurrent malignant glioma. J Neurooncol 2011; 105: 621-7; http://dx.doi.org/10.1007/s11060-011-0631-4

Hegi ME, Diserens AC, Gorlia T, et al. MGMT Gene Silencing and Benefit from Temozolomide in Glioblastoma. N Engl J Med 2005; 352: 997-1003; http://dx.doi.org/10.1056/NEJMoa043331

Watanabe T, Katayama Y, Ogino A, et al. Preliminary Individualized Chemotherapy for Malignant Astrocytomas Based on O6-Methylguanine-Deoxyribonucleic Acid Methyltransferase Methylation Analysis. Neurol Med Chir 2006; 46: 387-4; http://dx.doi.org/10.2176/nmc.46.387

Clarke JL, Chang S. Pseudoprogression and Pseudoresponse: Challenges in Brain Tumor Imaging. Curr Neurol Neurosci Rep 2009; 9: 241-6; http://dx.doi.org/10.1007/s11910-009-0035-4

Brandsma D, van den Bent MJ. Pseudoprogression and pseudoresponse in the treatment of gliomas. Curr Opin Neurol 2009; 22: 633-8; http://dx.doi.org/10.1097/WCO.0b013e328332363e

Hygino da Cruz LC Jr, Rodriguez I, Domingues RC, et al. Pseudoprogression and pseudoresponse: imaging challenges in the assessment of posttreatment glioma. AJNR Am J Neuroradiol 2011; 32: 1978-85; http://dx.doi.org/10.3174/ajnr.A2397

Galanis E, Wu W, Cloughesy T, et al. Phase 2 trial design in neuro-oncology revisited: a report from the RANO group. Lancet Oncol 2012; 13: e196-204; http://dx.doi.org/10.1016/S1470-2045(11)70406-5

Macdonald DR, Cascino TL, Schold SC Jr, et al. Response Criteria for Phase II Studies of Supratentorial Malignant Glioma. J Clin Oncol 1990; 8: 1277-80

Downloads

Published

2014-01-30

Issue

Vol. 5 No. 1 (2014)

Section

Narrative reviews

License

Authors who publish with this journal agree to the following terms:
  1. Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution-NonCommercial 4.0 License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
  2. Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal. The Publication Agreement can be downloaded here, and should be signed by the Authors and sent to the Publisher when the article has been accepted for publication in this journal.
  3. Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
  4. Authors are permitted to post their work online after publication (the article must link to publisher version, in html format)