Phase II study of metronomic chemotherapy with bevacizumab for recurrent glioblastoma after progression on bevacizumab therapy

Journal of Neuro-Oncology

Volumn 103, Issue 2, 2011, Pages 371-379

  Reardon, David A ^a   Desjardins, Annick ^a   Peters, Katherine ^a   Gururangan, Sridharan ^a   Sampson, John ^a   Rich, Jeremy N ^a   McLendon, Roger ^a   Herndon II, James E ^a   Marcello, Jennifer ^a   Threatt, Stevie ^a   Friedman, Allan H ^a   Vredenburgh, James J ^a   Friedman, Henry S ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Angiogenesis; Bevacizumab; Glioblastoma; Metronomic chemotherapy; Vascular endothelial growth factor

Indexed keywords

BEVACIZUMAB; CARBOPLATIN; ETOPOSIDE; IRINOTECAN; TEMOZOLOMIDE;

ADULT; ANTINEOPLASTIC ACTIVITY; ARTICLE; BRAIN HEMORRHAGE; CANCER COMBINATION CHEMOTHERAPY; CLINICAL ARTICLE; CONTROLLED STUDY; DIARRHEA; DRUG DOSE REDUCTION; DRUG DOSE REGIMEN; DRUG EFFICACY; DRUG RESPONSE; DRUG SAFETY; DRUG TOLERABILITY; DRUG TREATMENT FAILURE; DRUG WITHDRAWAL; FATIGUE; FEMALE; GLIOBLASTOMA; HEADACHE; HEMATOLOGIC DISEASE; HISTOLOGY; HUMAN; INFECTION; LOW DRUG DOSE; MALE; MUCOSA INFLAMMATION; MULTIPLE CYCLE TREATMENT; NAUSEA; NEUTROPENIA; NUCLEAR MAGNETIC RESONANCE IMAGING; OPEN STUDY; OVERALL SURVIVAL; PATIENT COMPLIANCE; PHASE 2 CLINICAL TRIAL; PROGRESSION FREE SURVIVAL; RANDOMIZED CONTROLLED TRIAL; RASH; TREATMENT DURATION; TUMOR RECURRENCE;

ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BRAIN NEOPLASMS; DACARBAZINE; DISEASE-FREE SURVIVAL; ETOPOSIDE; FEMALE; GLIOBLASTOMA; HUMANS; KAPLAN-MEIER ESTIMATE; KARNOFSKY PERFORMANCE STATUS; MALE; MIDDLE AGED; NEOPLASM RECURRENCE, LOCAL;

EID: 79959812904     PISSN: 0167594X     EISSN: 15737373     Source Type: Journal    
DOI: 10.1007/s11060-010-0403-6     Document Type: Article

References (56)

1. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987-996 (Pubitemid 40349501)
2. Wong ET, Hess KR, Gleason MJ, Jaeckle KA, Kyritsis AP, Prados MD, Levin VA, Yung WK (1999) Outcomes and prognostic factors in recurrent glioma patients enrolled onto phase II clinical trials. J Clin Oncol 17:2572-2578 (Pubitemid 29368260)
3. Ballman KV, Buckner JC, Brown PD, Giannini C, Flynn PJ, LaPlant BR, Jaeckle KA (2007) The relationship between six-month progression-free survival and 12-month overall survival end points for phase II trials in patients with glioblastoma multiforme. Neuro-oncology 9:29-38 (Pubitemid 46543486)
4. Lamborn KR, Yung WK, Chang SM, Wen PY, Cloughesy TF, Deangelis LM, Robins HI, Lieberman FS, Fine HA, Fink KL, Junck L, Abrey L, Gilbert MR, Mehta M, Kuhn JG, Aldape KD, Hibberts J, Peterson PM, Prados MD (2008) Progression-free survival: an important end point in evaluating therapy for recurrent high-grade gliomas. Neuro-oncology 10:162-170
5. Friedman HS, Prados MD, Wen PY, Mikkelsen T, Schiff D, Abrey LE, Yung WK, Paleologos N, Nicholas MK, Jensen R, Vredenburgh J, Huang J, Zheng M, Cloughesy T (2009) Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J Clin Oncol 27:4733-4740
6. Kreisl TN, Kim L, Moore K, Duic P, Royce C, Stroud I, Garren N, Mackey M, Butman JA, Camphausen K, Park J, Albert PS, Fine HA (2009) Phase II trial of single-agent bevacizumab followed by bevacizumab plus irinotecan at tumor progression in recurrent glioblastoma. J Clin Oncol 27:740-745
7. Reardon DA, Desjardins A, Vredenburgh JJ, Gururangan S, Sampson JH, Sathornsumetee S, McLendon RE, Herndon JE II, Marcello JE, Norfleet J, Friedman AH, Bigner DD, Friedman HS (2009) Metronomic chemotherapy with daily, oral etoposide plus bevacizumab for recurrent malignant glioma: a phase II study. Br J Cancer 101:1986-1994
8. Vredenburgh JJ, Desjardins A, Herndon JE II, Marcello J, Reardon DA, Quinn JA, Rich JN, Sathornsumetee S, Gururangan S, Sampson J, Wagner M, Bailey L, Bigner DD, Friedman AH, Friedman HS (2007) Bevacizumab plus irinotecan in recurrent glioblastoma multiforme. J Clin Oncol 25:4722-4729 (Pubitemid 350086473)
9. Kerbel RS, Kamen BA (2004) The anti-angiogenic basis of metronomic chemotherapy. Nat Rev Cancer 4(6):423-436 (Pubitemid 38745528)
10. Laquente B, Lacasa C, Ginesta MM, Casanovas O, Figueras A, Galan M, Ribas IG, Germa JR, Capella G, Vinals F (2008) Antiangiogenic effect of gemcitabine following metronomic administration in a pancreas cancer model. Mol Cancer Ther 7:638-647 (Pubitemid 351482146)
11. Browder T, Butterfield CE, Kraling BM, Shi B, Marshall B, O'Reilly MS, Folkman J (2000) Antiangiogenic scheduling of chemotherapy improves efficacy against experimental drug-resistant cancer. Cancer Res 60:1878-1886
12. Choi LM, Rood B, Kamani N, La Fond D, Packer RJ, Santi MR, Macdonald TJ (2008) Feasibility of metronomic maintenance chemotherapy following high-dose chemotherapy for malignant central nervous system tumors. Pediatr Blood Cancer 50:970-975 (Pubitemid 351500173)
13. Herrlinger U, Rieger J, Steinbach JP, Nagele T, Dichgans J, Weller M (2005) UKT-04 trial of continuous metronomic low-dose chemotherapy with methotrexate and cyclophosphamide for recurrent glioblastoma. J Neurooncol 71:295-299 (Pubitemid 40372960)
14. Kesari S, Schiff D, Doherty L, Gigas DC, Batchelor TT, Muzikansky A, O'Neill A, Drappatz J, Chen-Plotkin AS, Ramakrishna N, Weiss SE, Levy B, Bradshaw J, Kracher J, Laforme A, Black PM, Folkman J, Kieran M, Wen PY (2007) Phase II study of metronomic chemotherapy for recurrent malignant gliomas in adults. Neuro-oncology 9:354-363 (Pubitemid 47169667)
15. Tuettenberg J, Grobholz R, Korn T, Wenz F, Erber R, Vajkoczy P (2005) Continuous low-dose chemotherapy plus inhibition of cyclooxygenase-2 as an antiangiogenic therapy of glioblastoma multiforme. J Cancer Res Clin Oncol 131:31-40
16. Young SD, Whissell M, Noble JC, Cano PO, Lopez PG, Germond CJ (2006) Phase II clinical trial results involving treatment with low-dose daily oral cyclophosphamide, weekly vinblastine, and rofecoxib in patients with advanced solid tumors. Clin Cancer Res 12:3092-3098 (Pubitemid 43837356)
17. Ma J, Waxman DJ (2008) Modulation of the antitumor activity of metronomic cyclophosphamide by the angiogenesis inhibitor axitinib. Mol Cancer Ther 7:79-89
18. Rapisarda A, Zalek J, Hollingshead M, Braunschweig T, Uranchimeg B, Bonomi CA, Borgel SD, Carter JP, Hewitt SM, Shoemaker RH, Melillo G (2004) Schedule-dependent inhibition of hypoxia-inducible factor-1 alpha protein accumulation, angiogenesis, and tumor growth by topotecan in U251-HRE glioblastoma xenografts. Cancer Res 64:6845-6848 (Pubitemid 39330988)
19. Bello L, Carrabba G, Giussani C, Lucini V, Cerutti F, Scaglione F, Landre J, Pluderi M, Tomei G, Villani R, Carroll RS, Black PM, Bikfalvi A (2001) Low-dose chemotherapy combined with an antiangiogenic drug reduces human glioma growth in vivo. Cancer Res 61:7501-7506 (Pubitemid 32995040)
20. Bertolini F, Paul S, Mancuso P, Monestiroli S, Gobbi A, Shaked Y, Kerbel RS (2003) Maximum tolerable dose and low-dose metronomic chemotherapy have opposite effects on the mobilization and viability of circulating endothelial progenitor cells. Cancer Res 63:4342-4346 (Pubitemid 36951001)
21. Bocci G, Nicolaou KC, Kerbel RS (2002) Protracted low-dose effects on human endothelial cell proliferation and survival in vitro reveal a selective antiangiogenic window for various chemotherapeutic drugs. Cancer Res 62:6938-6943 (Pubitemid 35424084)
22. Klement G, Baruchel S, Rak J, Man S, Clark K, Hicklin DJ, Bohlen P, Kerbel RS (2000) Continuous low-dose therapy with vinblastine and VEGF receptor-2 antibody induces sustained tumor regression without overt toxicity. J Clin Invest 105:R15-24
23. Perry JR, Rizek P, Cashman R, Morrison M, Morrison T (2008) Temozolomide rechallenge in recurrent malignant glioma by using a continuous temozolomide schedule: the "rescue" approach. Cancer 113:2152-2157
24. Kong DS, Lee JI, Kim WS, Son MJ, Lim do H, Kim ST, Park K, Kim JH, Eoh W, Nam DH (2006) A pilot study of metronomic temozolomide treatment in patients with recurrent temozolomide-refractory glioblastoma. Oncol Rep 16:1117-1121
25. Chamberlain MC (1997) Recurrent supratentorial malignant gliomas in children. Long-term salvage therapy with oral etoposide. Arch Neurol 54:554-558
26. Chamberlain MC, Grafe MR (1995) Recurrent chiasmatic-hypothalamic glioma treated with oral etoposide. J Clin Oncol 13:2072-2076
27. Fulton D, Urtasun R, Forsyth P (1996) Phase II study of prolonged oral therapy with etoposide (VP16) for patients with recurrent malignant glioma. J Neurooncol 27:149-155 (Pubitemid 26052650)
28. Davidson A, Gowing R, Lowis S, Newell D, Lewis I, Dicks-Mireaux C, Pinkerton CR (1997) Phase II study of 21 day schedule oral etoposide in children. New Agents Group of the United Kingdom Children's Cancer Study Group (UKCCSG). Eur J Cancer 33:1816-1822
29. Yung WK, Albright RE, Olson J, Fredericks R, Fink K, Prados MD, Brada M, Spence A, Hohl RJ, Shapiro W, Glantz M, Greenberg H, Selker RG, Vick NA, Rampling R, Friedman H, Phillips P, Bruner J, Yue N, Osoba D, Zaknoen S, Levin VA (2000) A phase II study of temozolomide vs procarbazine in patients with glioblastoma multiforme at first relapse. Br J Cancer 83:588-593 (Pubitemid 30636298)
30. Pocock SJ (1982) Interim analyses for randomized clinical trials: the group sequential approach. Biometrics 38:153-162
31. Pope WB, Xia Q, Das A, Hambleton J, Kim H, Brown M, Goldin J, Cloughesy T (2009) Patterns of progression in patients with glioblastoma at first or second relapse treated with bevacizumab alone or in combination with irinotecan in the brain study. Neurooncology 11:626 (Article no. 270)
32. Ferrara N, Hillan KJ, Gerber HP, Novotny W (2004) Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nat Rev Drug Discov 3:391-400 (Pubitemid 38618122)
33. Damber JE, Vallbo C, Albertsson P, Lennernas B, Norrby K (2006) The anti-tumour effect of low-dose continuous chemotherapy may partly be mediated by thrombospondin. Cancer Chemother Pharmacol 58:354-360 (Pubitemid 43800739)
34. Grothey A, Sugrue MM, Purdie DM, Dong W, Sargent D, Hedrick E, Kozloff M (2008) Bevacizumab beyond first progression is associated with prolonged overall survival in metastatic colorectal cancer: results from a large observational cohort study (BRiTE). J Clin Oncol 26:5326-5334
35. Bekaii-Saab TS, Bendell JC, Cohn AL, Hurwitx H, Kozloff M, Roach N, Texcan H, Feng S, Sing AP, Grothey A (2010) Bevacizumab (BV) plus chemotherapy (CT) in second-line metastatic colorectal cancer (mCRC): initial results from ARIES, a second BV observational cohort study (OCS). In: Grunberg SM (ed) Proceedings of the annual meeting of the society of clinical oncology. American Society of Clinical Oncology, Chicago, IL, p 284
36. Zuniga RM, Torcuator R, Jain R, Anderson J, Doyle T, Schultz L, Mikkelsen T (2010) Rebound tumour progression after the cessation of bevacizumab therapy in patients with recurrent high-grade glioma. J Neurooncol 99(2):237-242
37. Drevs J, Fakler J, Eisele S, Medinger M, Bing G, Esser N, Marme D, Unger C (2004) Antiangiogenic potency of various chemotherapeutic drugs for metronomic chemotherapy. Anticancer Res 24:1759-1763 (Pubitemid 38954706)
38. Needle MN, Molloy PT, Geyer JR, Herman-Liu A, Belasco JB, Goldwein JW, Sutton L, Phillips PC (1997) Phase II study of daily oral etoposide in children with recurrent brain tumors and other solid tumors. Med Pediatr Oncol 29:28-32 (Pubitemid 27194736)
39. Andre N, Rome A, Coze C, Padovani L, Pasquier E, Camoin L, Gentet JC (2008) Metronomic etoposide/cyclophosphamide/celecoxib regimen given to children and adolescents with refractory cancer: a preliminary monocentric study. Clin Ther 30:1336-1340
40. Correale P, Cerretani D, Remondo C, Martellucci I, Marsili S, La Placa M, Sciandivasci A, Paolelli L, Pascucci A, Rossi M, Di Bisceglie M, Giorgi G, Gotti G, Francini G (2006) A novel metronomic chemotherapy regimen of weekly platinum and daily oral etoposide in high-risk non-small cell lung cancer patients. Oncol Rep 16:133-140
41. Sterba J, Valik D, Mudry P, Kepak T, Pavelka Z, Bajciova V, Zitterbart K, Kadlecova V, Mazanek P (2006) Combined biodifferentiating and antiangiogenic oral metronomic therapy is feasible and effective in relapsed solid tumors in children: single-center pilot study. Onkologie 29:308-313 (Pubitemid 44022404)
42. Twardowski PW, Smith-Powell L, Carroll M, VanBalgooy J, Ruel C, Frankel P, Synold TW (2008) Biologic markers of angiogenesis: circulating endothelial cells in patients with advanced malignancies treated on phase I protocol with metronomic chemotherapy and celecoxib. Cancer Invest 26:53-59
43. Lam T, Hetherington JW, Greenman J, Little S, Maraveyas A (2007) Metronomic chemotherapy dosing-schedules with estramustine and temozolomide act synergistically with anti-VEGFR-2 antibody to cause inhibition of human umbilical venous endothelial cell growth. Acta Oncol 46:1169-1177 (Pubitemid 350058876)
44. Kurzen H, Schmitt S, Naher H, Mohler T (2003) Inhibition of angiogenesis by non-toxic doses of temozolomide. Anticancer Drugs 14:515-522 (Pubitemid 37083156)
45. Tolcher AW, Gerson SL, Denis L, Geyer C, Hammond LA, Patnaik A, Goetz AD, Schwartz G, Edwards T, Reyderman L, Statkevich P, Cutler DL, Rowinsky EK (2003) Marked inactivation of O6-alkylguanine-DNA alkyltransferase activity with protracted temozolomide schedules. Br J Cancer 88:1004-1011 (Pubitemid 36560766)
46. Perry JR, Belanger K, Mason WP, Fulton D, Kavan P, Easaw J, Shields C, Kirby S, Macdonald DR, Eisenstat DD, Thiessen B, Forsyth P, Pouliot JF (2010) Phase II trial of continuous dose-intense temozolomide in recurrent malignant glioma: RESCUE study. J Clin Oncol 28:2051-2057
47. Iwamoto FM, Abrey LE, Beal K, Gutin PH, Rosenblum MK, Reuter VE, DeAngelis LM, Lassman AB (2009) Patterns of relapse and prognosis after bevacizumab failure in recurrent glioblastoma. Neurology 73:1200-1206
48. Quant EC, Norden AD, Drappatz J, Muzikansky A, Doherty L, Lafrankie D, Ciampa A, Kesari S, Wen PY (2009) Role of a second chemotherapy in recurrent malignant glioma patients who progress on bevacizumab. Neuro-oncology 11:550-555
49. de Groot JF, Fuller G, Kumar AJ, Piao Y, Eterovic K, Ji Y, Conrad CA (2010) Tumor invasion after treatment of glioblastoma with bevacizumab: radiographic and pathologic correlation in humans and mice. Neuro-oncology 12: 233-242
50. Norden AD, Young GS, Setayesh K, Muzikansky A, Klufas R, Ross GL, Ciampa AS, Ebbeling LG, Levy B, Drappatz J, Kesari S, Wen PY (2008) Bevacizumab for recurrent malignant gliomas: efficacy, toxicity, and patterns of recurrence. Neurology 70:779-787
51. Rubenstein JL, Kim J, Ozawa T, Zhang M, Westphal M, Deen DF, Shuman MA (2000) Anti-VEGF antibody treatment of glioblastoma prolongs survival but results in increased vascular cooption. Neoplasia 2:306-314
52. Batchelor TT, Sorensen AG, di Tomaso E, Zhang WT, Duda DG, Cohen KS, Kozak KR, Cahill DP, Chen PJ, Zhu M, Ancukiewicz M, Mrugala MM, Plotkin S, Drappatz J, Louis DN, Ivy P, Scadden DT, Benner T, Loeffler JS, Wen PY, Jain RK (2007) AZD2171, a Pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 11:83-95 (Pubitemid 46075199)
53. Fernando NT, Koch M, Rothrock C, Gollogly LK, D'Amore PA, Ryeom S, Yoon SS (2008) Tumor escape from endogenous, extracellular matrix-associated angiogenesis inhibitors by upregulation of multiple proangiogenic factors. Clin Cancer Res 14:1529-1539 (Pubitemid 351413938)
54. Ebos JM, Lee CR, Christensen JG, Mutsaers AJ, Kerbel RS (2007) Multiple circulating proangiogenic factors induced by sunitinib malate are tumor-independent and correlate with antitumor efficacy. Proc Natl Acad Sci U S A 104:17069-17074 (Pubitemid 350210993)
55. Shojaei F, Ferrara N (2008) Refractoriness to antivascular endothelial growth factor treatment: role of myeloid cells. Cancer Res 68:5501-5504
56. Rapisarda A, Melillo G (2009) Role of the hypoxic tumor microenvironment in the resistance to anti-angiogenic therapies. Drug Resist Updat 12:74-80