Intra-arterial chemotherapy with osmotic blood-brain barrier disruption for aggressive oligodendroglial tumors: Results of a phase i study

Neurosurgery

Volumn 66, Issue 1, 2010, Pages 48-58

  Guillaume, Daniel J ^a   Doolittle, Nancy D ^b   Gahramanov, Seymur ^b   Hedrick, Nancy A ^b   Delashaw, Johnny B ^b   Neuwelt, Edward A ^c  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c PORTLAND VA MEDICAL CENTER   (United States)

Author keywords

Anaplastic oligodendroglioma; Blood brain barrier; Chemotherapy; Intra arterial chemotherapy; Oligoastrocytoma; Oligodendroglial tumors

Indexed keywords

CARBOPLATIN; ETOPOSIDE; MELPHALAN;

ADULT; ARTERY INJURY; ARTICLE; ASTROCYTOMA; BLOOD BRAIN BARRIER; CANCER RADIOTHERAPY; CHROMOSOME 19Q; CHROMOSOME 1P; CHROMOSOME DELETION; CLINICAL ARTICLE; CLINICAL TRIAL; DRUG DOSE ESCALATION; DRUG EFFICACY; DRUG SAFETY; FALSE ANEURYSM; FEMALE; HUMAN; KARNOFSKY PERFORMANCE STATUS; LEUKOPENIA; MALE; MAXIMUM TOLERATED DOSE; MULTIPLE CYCLE TREATMENT; NEUTROPENIA; NUCLEAR MAGNETIC RESONANCE IMAGING; OLIGODENDROGLIOMA; PHASE 1 CLINICAL TRIAL; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; SPEECH DISORDER; STATISTICAL ANALYSIS; THROMBOCYTOPENIA;

ADULT; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BLOOD-BRAIN BARRIER; BRAIN NEOPLASMS; CARBOPLATIN; CROSS-LINKING REAGENTS; DACARBAZINE; DISEASE-FREE SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; FOLLOW-UP STUDIES; HUMANS; INJECTIONS, INTRA-ARTERIAL; LOMUSTINE; MALE; MELPHALAN; MIDDLE AGED; OLIGODENDROGLIOMA; OSMOTIC PRESSURE; PROCARBAZINE; VINCRISTINE; YOUNG ADULT;

EID: 77249102549     PISSN: 0148396X     EISSN: None     Source Type: Journal    
DOI: 10.1227/01.NEU.0000363152.37594.F7     Document Type: Article

References (91)

1. Cairncross G, Berkey B, Shaw E, et al. Phase III trial of chemotherapy plus radiotherapy compared with radiotherapy alone for pure and mixed anaplastic oligodendroglioma: Intergroup Radiation Therapy Oncology Group Trial 9402. J Clin Oncol. 2006;24(18):2707-2714.
2. van den Bent MJ, Carpentier AF, Brandes AA, et al. Adjuvant procarbazine, lomustine, and vincristine improves progression-free survival but not overall survival in newly diagnosed anaplastic oligodendrogliomas and oligoastrocytomas: a randomized European Organisation for Research and Treatment of Cancer phase III trial. J Clin Oncol. 2006;24:2715-2722.
3. van den Bent MJ. Anaplastic oligodendroglioma and oligoastrocytoma. Neurol Clin. 2007;25(4):1089-1109.
4. Cairncross G, Macdonald D, Ludwin S, et al. Chemotherapy for anaplastic oligodendroglioma. National Cancer Institute of Canada Clinical Trials Group. J Clin Oncol 1994;12(10):2013-2021.
5. Soffietti R, Ruda R, Bradac GB, Schiffer D. PCV chemotherapy for recurrent oligodendrogliomas and oligoastrocytomas. Neurosurgery. 1998;43(5):1066-1073.
6. Brandes AA, Tosoni A, Cavallo G, et al. Correlations between O6-methylguanine DNA methyltransferase promoter methylation status, 1p and 19q deletions, and response to temozolomide in anaplastic and recurrent oligodendroglioma: a prospective GICNO study. J Clin Oncol. 2006;24(29):4746- 4753.
7. van den Bent MJ, Taphoorn MJ, Brandes AA, et al. Phase II study of first-line chemotherapy with temozolomide in recurrent oligodendroglial tumors: the European Organization for Research and Treatment of Cancer Brain Tumor Group Study 26971. J Clin Oncol. 2003;21(13):2525-2528.
8. Yung WK, Mechtler L, Gleason MJ. Intravenous carboplatin for recurrent malignant glioma: a phase II study. J Clin Oncol. 1991;9(5):860-864.
9. Rostomily RC, Spence AM, Duong D, McCormick K, Bland M, Berger MS. Multimodality management of recurrent adult malignant gliomas: results of a phase II multiagent chemotherapy study and analysis of cytoreductive surgery. Neurosurgery. 1994;35(3):378-388.
10. Salcman M. Resection and reoperation in neuro-oncology. Rationale and approach. Neurol Clin. 1985;3(4):831-842.
11. Brandes AA, Basso U, Vastola F, et al. Carboplatin and teniposide as third-line chemotherapy in patients with recurrent oligodendroglioma or oligoastrocytoma: a phase II study. Ann Oncol. 2003;14(2):1727-1731.
12. Brem H, Piantadosi S, Burger PC, et al. Placebo-controlled trial of safety and efficacy of intraoperative controlled delivery by biodegradable polymers of chemotherapy for recurrent gliomas. The Polymer-brain Tumor Treatment Group. Lancet. 1995;345(8956):1008-1012.
13. Chamberlain MC. Salvage chemotherapy with CPT-11 for recurrent glioblastoma multiforme. J Neurooncol. 2002;56(2):183-188.
14. Chamberlain MC, Glantz MJ. CPT-11 for recurrent temozolomide-refractory 1p19q co-deleted anaplastic oligodendroglioma. J Neurooncol. 2008;89(2):231-238.
15. Chamberlain MC, Tsao-Wei DD. Salvage chemotherapy with cyclophosphamide for recurrent, temozolomide-refractory glioblastoma multiforme. Cancer. 2004;100(6):1213-1220.
16. Jaeckle KA, Hess KR, Yung WK, et al. Phase II evaluation of temozolomide and 13-cis-retinoic acid for the treatment of recurrent and progressive malignant glioma: a North American Brain Tumor Consortium study. J Clin Oncol. 2003;21(12):2305-2311.
17. Longee DC, Friedman HS, Albright RE Jr, et al. Treatment of patients with recurrent gliomas with cyclophosphamide and vincristine. J Neurosurg. 1990;72(4):583-588.
18. Soffietti R, Nobile M, Rudà R, et al. Second-line treatment with carboplatin for recurrent or progressive oligodendroglial tumors after PCV (procarbazine, lomustine, and vincristine) chemotherapy. Cancer. 2004;100(4):807-813.
19. Triebels VH, Taphoorn MJ, Brandes AA, et al. Salvage PCV chemotherapy for temozolomide-resistant oligodendrogliomas. Neurology. 2004;63(5):904-906.
20. Angelov L, Doolittle ND, Kraemer DF, et al. Blood-brain barrier disruption and intra-arterial methotrexate-based therapy for newly diagnosed primary CNS lymphoma: a multi-institutional experience with 149 patients. J Clin Oncol. 2009; 27(21):3503-3509.
21. Correa DD, Maron L, Harder H, et al. Cognitive functions in primary central nervous system lymphoma: literature review and assessment guidelines. Ann Oncol. 2007;18(7):1145-1151.
22. Doolittle ND, Miner ME, Hall WA, et al. Safety and efficacy of a multicenter study using intraarterial chemotherapy in conjunction with osmotic opening of the blood-brain barrier for the treatment of patients with malignant brain tumors. Cancer. 2000;88(3):637-647.
23. Jahnke K, Kraemer DF, Knight KR, et al. Intraarterial chemotherapy and osmotic blood-brain barrier disruption for patients with embryonal and germ cell tumors of the central nervous system. Cancer. 2008;112(3):581-588.
24. McAllister LD, Doolittle ND, Guastadisegni PE, et al. Cognitive outcomes and long-term follow-up results after enhanced chemotherapy delivery for primary central nervous system lymphoma. Neurosurgery. 2000;46(1):51-60, discussion 60-61.
25. Muldoon LL, Soussain C, Jahnke K, et al. Chemotherapy delivery issues in central nervous system malignancy: a reality check. J Clin Oncol. 2007;25(16):2295-2305.
26. Neuwelt EA. Mechanisms of disease: the blood-brain barrier. Neurosurgery. 2004;54(1):131-140, discussion 141-142.
27. Neuwelt EA, Goldman DL, Dahlborg SA, et al. Primary CNS lymphoma treated with osmotic blood-brain barrier disruption: prolonged survival and preservation of cognitive function. J Clin Oncol. 1991;9(9):1580-1590.
28. Neuwelt EA, Guastadisegni PE, Varallyay P, Doolittle ND. Imaging changes and cognitive outcome in primary CNS lymphoma after enhanced chemotherapy delivery. AJNR Am J Neuroradiol. 2005;26(2):258-265.
29. Quencer RM, Neuwelt EA. Advances in the understanding of the blood-brain barrier in neuro-oncology. AJNR Am J Neuroradiol. 2002;23(10):1807-1810.
30. Doolittle ND, Jahnke K, Belanger R, et al. Potential of chemo-immunotherapy and radioimmunotherapy in relapsed primary central nervous system (CNS) lymphoma. Leuk Lymphoma. 2007;48(9):1712-1720.
31. Doolittle ND, Peereboom DM, Christoforidis GA, et al. Delivery of chemotherapy and antibodies across the blood-brain barrier and the role of chemoprotection, in primary and metastatic brain tumors: report of the Eleventh Annual Blood-Brain Barrier Consortium meeting. J Neurooncol. 2007;81(1):81-91.
32. Hall WA, Doolittle ND, Daman M, et al. Osmotic blood-brain barrier disruption chemotherapy for diffuse pontine gliomas. J Neurooncol. 2006;77(3):279-284.
33. Jahnke K, Doolittle ND, Muldoon LL, Neuwelt EA. Implications of the bloodbrain barrier in primary central nervous system lymphoma. Neurosurg Focus. 2006;21(5):E11.
34. Kraemer DF, Fortin D, Neuwelt EA. Chemotherapeutic dose intensification for treatment of malignant brain tumors: recent developments and future directions. Curr Neurol Neurosci Rep. 2002;2(3):216-224.
35. Neuwelt E, Abbott NJ, Abrey L, et al. Strategies to advance translational research into brain barriers. Lancet Neurol. 2008;7(1):84-96.
36. Williams PC, Henner WD, Roman-Goldstein S, et al. Toxicity and efficacy of carboplatin and etoposide in conjunction with disruption of the blood-brain tumor barrier in the treatment of intracranial neoplasms. Neurosurgery. 1995;37(1):17-27, discussion 27-28.
37. Doolittle ND, Murillo TP, Neuwelt EA. Blood-brain barrier disruption chemotherapy. In: Newton HB, ed. Handbook of Brain Tumor Chemotherapy. London, England: Elsevier; 2006:262-273.
38. Guidelines for the audiologic management of individuals receiving cochleotoxic drug therapy. ASHA. 1994;36:11-19.
39. van den Bent MJ, Kros JM, Heimans JJ, et al. Response rate and prognostic factors of recurrent oligodendroglioma treated with procarbazine, CCNU, and vincristine chemotherapy. Dutch Neuro-oncology Group. Neurology. 1998;51(4): 1140-1145.
40. Schabel FM Jr, Griswold DP Jr, Corbett TH, Laster WR Jr. Increasing the therapeutic response rates to anticancer drugs by applying the basic principles of pharmacology. Cancer. 1984;54(6):1160-1167.
41. Mohile NA, Forsyth P, Stewart D, et al. A phase II study of intensified chemotherapy alone as initial treatment for newly diagnosed anaplastic oligodendroglioma: an interim analysis. J Neurooncol. 2008;89(2):187-193.
42. Cloughesy TF, Gobin YP, Black KL, et al. Intra-arterial carboplatin chemotherapy for brain tumors: a dose escalation study based on cerebral blood flow. J Neurooncol. 1997;35(2):121-131.
43. Dropcho EJ, Rosenfeld SS, Morawetz RB, et al. Preradiation intracarotid cisplatin treatment of newly diagnosed anaplastic gliomas. The CNS Cancer Consortium. J Clin Oncol. 1992;10(3):452-458.
44. Fenstermacher JD, Cowles AL. Theoretic limitations of intracarotid infusions in brain tumor chemotherapy. Cancer Treat Rep. 1977;61(4):519-526.
45. Hirano Y, Mineura K, Mizoi K, Tomura N. Therapeutic results of intra-arterial chemotherapy in patients with malignant glioma. Int J Oncol. 1998;13(3):537-542.
46. Saris SC, Blasberg RG, Carson RE, et al. Intravascular streaming during carotid artery infusions. Demonstration in humans and reduction using diastole-phased pulsatile administration. J Neurosurg. 1991;74(5):763-772.
47. Bashir R, Hochberg FH, Linggood RM, Hottleman K. Pre-irradiation internal carotid artery BCNU in treatment of glioblastoma multiforme. J Neurosurg. 1988; 68(6):917-919.
48. Stewart DJ, Benjamin RS, Zimmerman S, et al. Clinical pharmacology of intraarterial cis-diamminedichloroplatinum (II). Cancer Res. 1983;43(2):917-920.
49. Assietti R, Olson JJ. Intra-arterial cisplatin in malignant brain tumors: incidence and severity of otic toxicity. J Neurooncol. 1996;27(3):251-258.
50. Hochberg FH, Pruitt AA, Beck DO, DeBrun G, Davis K. The rationale and methodology for intra-arterial chemotherapy with BCNU as treatment for glioblastoma. J Neurosurg. 1985;63(6):876-880.
51. Mahaley MS Jr, Hipp SW, Dropcho EJ, et al. Intracarotid cisplatin chemotherapy for recurrent gliomas. J Neurosurg. 1989;70(3):371-378.
52. Mortimer JE, Crowley J, Eyre H, Weiden P, Eltringham J, Stuckey WJ. A phase II randomized study comparing sequential and combined intraarterial cisplatin and radiation therapy in primary brain tumors. A Southwest Oncology Group study. Cancer. 1992;69(5):1220-1223.
53. Nakagawa H, Fujita T, Kubo S, et al. Selective intra-arterial chemotherapy with a combination of etoposide and cisplatin for malignant gliomas: preliminary report. Surg Neurol. 1994;41(1):19-27.
54. Shapiro WR, Green SB, Burger PC, et al. A randomized comparison of intraarterial versus intravenous BCNU, with or without intravenous 5-fluorouracil, for newly diagnosed patients with malignant glioma. J Neurosurg. 1992;76(5):772-781.
55. Stewart DJ, Belanger JM, Grahovac Z, et al. Phase I study of intracarotid administration of carboplatin. Neurosurgery. 1992;30(4):512-516, discussion 516-517.
56. Watne K, Hannisdal E, Nome O, Hager B, Hirschberg H. Combined intra-arterial and systemic chemotherapy for recurrent malignant brain tumors. Neurosurgery. 1992;30(2):223-227.
57. Barth RF, Yang W, Rotaru JH, et al. Boron neutron capture therapy of brain tumors: enhanced survival following intracarotid injection of either sodium borocaptate or boronophenylalanine with or without blood-brain barrier disruption. Cancer Res. 1997;57(6):1129-1136. (Pubitemid 27138613)
58. Black KL, Cloughesy T, Huang SC, et al. Intracarotid infusion of RMP-7, a bradykinin analog, and transport of gallium-68 ethylenediamine tetraacetic acid into human gliomas. J Neurosurg. 1997;86(4):603-609.
59. Kroll RA, Neuwelt EA. Outwitting the blood-brain barrier for therapeutic purposes: osmotic opening and other means. Neurosurgery. 1998;42(5):1083-1099; discussion 1099-1100.
60. Kroll RA, Pagel MA, Muldoon LL, Roman-Goldstein S, Fiamengo SA, Neuwelt EA. Improving drug delivery to intracerebral tumor and surrounding brain in a rodent model: a comparison of osmotic versus bradykinin modification of the blood-brain and/or blood-tumor barriers. Neurosurgery. 1998;43(4):879-886; discussion 886-889.
61. Matsukado K, Inamura T, Nakano S, Fukui M, Bartus RT, Black KL. Enhanced tumor uptake of carboplatin and survival in glioma-bearing rats by intracarotid infusion of bradykinin analog, RMP-7. Neurosurgery. 1996;39(1):125-133; discussion 133-134.
62. Neuwelt EA, Barnett PA, McCormick CI, Remsen LG, Kroll RA, Sexton G. Differential permeability of a human brain tumor xenograft in the nude rat: impact of tumor size and method of administration on optimizing delivery of biologically diverse agents. Clin Cancer Res. 1998;4(6):1549-1555.
63. Remsen LG, Pagel MA, McCormick CI, Fiamengo SA, Sexton G, Neuwelt EA. The influence of anesthetic choice, PaCO2, and other factors on osmotic blood-brain barrier disruption in rats with brain tumor xenografts. Anesth Analg. 1999;88(3):559-567.
64. Remsen LG, Trail PA, Hellstrom I, Hellstrom KE, Neuwelt EA. Enhanced delivery improves the efficacy of a tumor-specific doxorubicin immunoconjugate in a human brain tumor xenograft model. Neurosurgery. 2000;46(3):704-709.
65. Siegal T, Rubinstein R, Bokstein F, et al. In vivo assessment of the window of barrier opening after osmotic blood-brain barrier disruption in humans. J Neurosurg. 2000;92(4):599-605.
66. Kraemer DF, Fortin D, Doolittle ND, Neuwelt EA. Association of total dose intensity of chemotherapy in primary central nervous system lymphoma (human nonacquired immunodeficiency syndrome) and survival. Neurosurgery. 2001;48(5): 1033-1040; discussion 1040-1041.
67. Dahlborg SA, Henner WD, Crossen JR, et al. Non-AIDS primary CNS lymphoma: first example of a durable response in a primary brain tumor using enhanced chemotherapy delivery without cognitive loss and without radiotherapy. Cancer J Sci Am. 1996;2(3):166-174.
68. Friedman HS, Schold SC Jr, Mahaley MS Jr, et al. Phase II treatment of medulloblastoma and pineoblastoma with melphalan: clinical therapy based on experimental models of human medulloblastoma. J Clin Oncol. 1989;7(7):904-911.
69. Mahoney DH Jr, Strother D, Camitta B, et al. High-dose melphalan and cyclophosphamide with autologous bone marrow rescue for recurrent/progressive malignant brain tumors in children: a pilot pediatric oncology group study. J Clin Oncol. 1996;14(2):382-388.
70. Pritchard J, McElwain TJ, Graham-Pole J. High-dose melphalan with autologous marrow for treatment of advanced neuroblastoma. Br J Cancer. 1982;45(1):86-94.
71. Samuels BL, Bitran JD. High-dose intravenous melphalan: a review. J Clin Oncol. 1995;13(7):1786-1799.
72. Barnett PA, Roman-Goldstein S, Ramsey F, et al. Differential permeability and quantitative MR imaging of a human lung carcinoma brain xenograft in the nude rat. Am J Pathol. 1995;146(2):436-449.
73. Neuwelt EA, Frenkel EP, Rapoport S, Barnett P. Effect of osmotic blood-brain barrier disruption on methotrexate pharmacokinetics in the dog. Neurosurgery. 1980;7(1):36-43.
74. Doolittle ND, Muldoon LL, Brummett RE, et al. Delayed sodium thiosulfate as an otoprotectant against carboplatin-induced hearing loss in patients with malignant brain tumors. Clin Cancer Res. 2001;7(3):493-500.
75. Dickey DT, Muldoon LL, Doolittle ND, Peterson DR, Kraemer DF, Neuwelt EA. Effect of N-acetylcysteine route of administration on chemoprotection against cisplatininduced toxicity in rat models. Cancer Chemother Pharmacol. 2008;62(2):235-241.
76. Dickey DT, Muldoon LL, Kraemer DF, Neuwelt EA. Protection against cisplatininduced ototoxicity by N-acetylcysteine in a rat model. Hear Res. 2004;193(1-2):25-30.
77. Dickey DT, Wu YJ, Muldoon LL, Neuwelt EA. Protection against cisplatin-induced toxicities by N-acetylcysteine and sodium thiosulfate as assessed at the molecular, cellular, and in vivo levels. J Pharmacol Exp Ther. 2005;314(3):1052-1058.
78. Muldoon LL, Pagel MA, Kroll RA, et al. Delayed administration of sodium thiosulfate in animal models reduces platinum ototoxicity without reduction of antitumor activity. Clin Cancer Res. 2000;6(1):309-315.
79. Regine WF, Valentino J, Arnold SM, et al. High-dose intra-arterial cisplatin boost with hyperfractionated radiation therapy for advanced squamous cell carcinoma of the head and neck. J Clin Oncol. 2001;19(14):3333-3339.
80. Robbins KT, Homma A. Intra-arterial chemotherapy for head and neck cancer: experiences from three continents. Surg Oncol Clin N Am. 2009;17(4):919-933, xi.
81. Robbins KT, Kumar P, Regine WF, et al. Efficacy of targeted supradose cisplatin and concomitant radiation therapy for advanced head and neck cancer: the Memphis experience. Int J Radiat Oncol Biol Phys. 1997;38(2):263-271.
82. McLellan LI, Lewis AD, Hall DJ, Ansell JD, Wolf CR. Uptake and distribution of N-acetylcysteine in mice: tissue-specific effects on glutathione concentrations. Carcinogenesis. 1995;16(9):2099-2106.
83. Zhang K, Mack P, Wong KP. Glutathione-related mechanisms in cellular resistance to anticancer drugs. Int J Oncol. 1998;12(4):871-882.
84. Chen G, Zeller WJ. Augmentation of cisplatin (DDP) cytotoxicity in vivo by DLbuthionine sulfoximine (BSO) in DDP-sensitive and-resistant rat ovarian tumors and its relation to DNA interstrand cross links. Anticancer Res. 1991;11(6):2231-2237.
85. Grubbs EG, Ueno T, Abdel-Wahab O, et al. Modulation of resistance to regional chemotherapy in the extremity melanoma model. Surgery. 2004;136(2):210-218.
86. Harned TM, Kalous O, Neuwelt A, et al. Sodium thiosulfate administered six hours after cisplatin does not compromise antineuroblastoma activity. Clin Cancer Res. 2008;14(2):533-540.
87. Kobrinsky NL, Sjolander DE, Goldenberg JA, Ortmeier TC. Successful treatment of doxorubicin and cisplatin resistant hepatoblastoma in a child with Beckwith-Wiedemann syndrome with high dose acetaminophen and N-acetylcysteine rescue. Pediatr Blood Cancer. 2005;45(2):222-225.
88. Muldoon LL, Walker-Rosenfeld SL, Hale C, Purcell SE, Bennett LC, Neuwelt EA. Rescue from enhanced alkylator-induced cell death with low molecular weight sulfur-containing chemoprotectants. J Pharmacol Exp Ther. 2001;296(3):797-805.
89. Ozols RF, Louie KG, Plowman J, et al. Enhanced melphalan cytotoxicity in human ovarian cancer in vitro and in tumor-bearing nude mice by buthionine sulfoximine depletion of glutathione. Biochem Pharmacol. 1987;36(1):147-153.
90. Griffith OW. Mechanism of action, metabolism, and toxicity of buthionine sulfoximine and its higher homologs, potent inhibitors of glutathione synthesis. J Biol Chem. 1982;257(22):13704-13712.
91. Fischer LJ, Green MD, Harman AW. Levels of acetaminophen and its metabolites in mouse tissues after a toxic dose. J Pharmacol Exp Ther. 1981;219(2):281-286.