Cited by 929Glioma Diagnosis and TreatmentPARP inhibition in cancer therapyCancer survivorship and care

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A phase II study of temozolomide vs. procarbazine in patients with glioblastoma multiforme at first relapse

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Yung, W K A, Albright, R E, Olson, J, Fredericks, R, Fink, K, Prados, M D, Brada, M, Spence, A, Hohl, R J, Shapiro, W, Glantz, M, Greenberg, H, Selker, R G, Vick, N A, Rampling, R, Friedman, H, Phillips, P, Bruner, J, Yue, N, Osoba, D, Zaknoen, S, Levin, V A·2000·British Journal of Cancer

DOI 10.1054/bjoc.2000.1316PMC PMC2363506

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Abstract

A randomized, multicentre, open-label, phase II study compared temozolomide (TMZ), an oral second-generation alkylating agent, and procarbazine (PCB) in 225 patients with glioblastoma multiforme at first relapse. Primary objectives were to determine progression-free survival (PFS) at 6 months and safety for TMZ and PCB in adult patients who failed conventional treatment. Secondary objectives were to assess overall survival and health-related quality of life (HRQL). TMZ was given orally at 200 mg/m(2)/day or 150 mg/m(2)/day (prior chemotherapy) for 5 days, repeated every 28 days. PCB was given orally at 150 mg/m(2)/day or 125 mg/m(2)/day (prior chemotherapy) for 28 days, repeated every 56 days. HRQL was assessed using the European Organization for Research and Treatment of Cancer Quality of Life Questionnaire (EORTC QLQ-C30 [+3]) and the Brain Cancer Module 20 (BCM20). The 6-month PFS rate for patients who received TMZ was 21%, which met the protocol objective. The 6-month PFS rate for those who received PCB was 8% (P = 0.008, for the comparison). Overall PFS significantly improved with TMZ, with a median PFS of 12.4 weeks in the TMZ group and 8.32 weeks in the PCB group (P = 0.0063). The 6-month overall survival rate for TMZ patients was 60% vs. 44% for PCB patients (P = 0.019). Freedom from disease progression was associated with maintenance of HRQL, regardless of treatment received. TMZ had an acceptable safety profile; most adverse events were mild or moderate in severity.

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The European Organization for Research and Treatment of Cancer QLQ-C30: A Quality-of-Life Instrument for Use in International Clinical Trials in Oncology
Aaronson, N. K., Ahmedzai, S., Bergman, B., Bullinger, M., Cull, A., Duez, N. J., Filiberti, A., Flechtner, H., Fleishman, S. B., Haes, J. C. J. M. D., et al. (1993) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/85.5.365 · Cited by 16,005 · cited 1×
“The European Organization for Research and Treatment of Cancer Quality of Life Questionnaire (EORTC-QLQ-C30 [+3]) (Aaronson et al, 1993; Osoba et al, 1997) and the Brain Cancer Module 20 (BCM20) (Osoba et al, 1996) questionnaires were used to measure HRQL. Questionnaires were administered on day 1…”
MethodSelf-citation
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“A 10-unit change on a 0–100 scale was deemed significant if it lasted for at least 8 weeks (Jaeschke et al, 1989; Juniper et al, 1994; King, 1996; Ware et al, 1998).”
The interpretation of scores from the EORTC quality of life questionnaire QLQ-C30
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Phase I trial of temozolomide (CCRG 81045: M&B 39831: NSC 362856)
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“TMZ has notable antitumour activity against recurrent GBM, recurrent anaplastic astrocytoma, and advanced malignant melanoma, and other refractory cancers (Newlands et al, 1992, 1996; O’Reilly et al, 1993; Bleehen et al, 1995; Bower et al, 1997).”
BackgroundResult
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Temozolomide in Patients with Glioblastoma at Second Relapse after First Line Nitrosourea-Procarbazine Failure: A Phase II Study
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“is generally considered efficacious. In our opinion both end points are worthy of attention, and should be reported in phase II studies.Among the recently introduced drugs, TMZ presents the most favourable toxicity profile, and has also demonstrated antitumor efficacy when administered at first relapse. Yung et al [”
Background
Drug Insight: temozolomide as a treatment for malignant glioma—impact of a recent trial
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Background
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Headache and Brain Tumor
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“TMZ [2–4] and irinotecan (CPT-11) [5–9] each have demonstrated clinical activity when administered separately to patients with MG.”
Self-citation
The combination of carmustine wafers and temozolomide for the treatment of malignant gliomas. A comprehensive review of the rationale and clinical experience
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“The majority of patients with high-grade gliomas receive temozolomide either as first-line treatment in combination with radiotherapy or at relapse, based on evidence from prospective trials demonstrating the clinical benefit of temozolomide in these settings [2, 3].”
Background
Continuous low-dose temozolomide and celecoxib in recurrent glioblastoma
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“On the other hand, in alternating, high-dose temozolomide procedures, leukopenia and thrombopenia seemed to be the major dose-limiting [2, 4 ] or even fatal [15] events.”
BackgroundResultInfluential
Perils of Evidence-Based Medicine
Williams, B. A. (2010) · Perspectives in biology and medicine · doi:10.1353/pbm.0.0132 · Cited by 57
Nanozeolite bioconjugates labeled with 223 Ra for targeted alpha therapy
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Historical Perspective on Surgery and Survival with Glioblastoma: How Far Have We Come?
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MGMT promoter hypermethylation correlates with a survival benefit from temozolomide in patients with recurrent anaplastic astrocytoma but not glioblastoma
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Novel Therapies in Glioblastoma
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“[34] W.”
Method
Report of the Jumpstarting Brain Tumor Drug Development Coalition and FDA clinical trials neuroimaging endpoint workshop (January 30, 2014, Bethesda MD)
Wen, P. Y., Cloughesy, T. F., Ellingson, B. M., Reardon, D. A., Fine, H. A., Abrey, L. E., Ballman, K. V., Bendszuz, M., Buckner, J. C., Chang, S. M., et al. (2014) · Neuro-Oncology · doi:10.1093/neuonc/nou226 · Cited by 53
Self-citation
MicroRNA as potential biomarkers in Glioblastoma
Areeb, Z., Stylli, S. S., Koldej, R. M., Ritchie, D. S., Siegal, T., Morokoff, A. P., Kaye, A. H., & Luwor, R. B. (2015) · Journal of Neuro-Oncology · doi:10.1007/s11060-015-1912-0 · Cited by 52
Response assessment of NovoTTF‐100A versus best physician's choice chemotherapy in recurrent glioblastoma
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“Objective response rates to alkylating chemotherapy are low, ranging 5–8% [1, 2].”
Background
Recurrent malignant glioma in adults
Tatter, S. B. (2002) · Current Treatment Options in Oncology · doi:10.1007/s11864-002-0070-8 · Cited by 52
“Cost effectiveness As an oral agent with some antitumor activity, temozolomide is likely to be cost effective [ 10 ].”
Background
A PK2/Bv8/PROK2 Antagonist Suppresses Tumorigenic Processes by Inhibiting Angiogenesis in Glioma and Blocking Myeloid Cell Infiltration in Pancreatic Cancer
Curtis, V. F., Wang, H., Yang, P., McLendon, R. E., Li, X., Zhou, Q., & Wang, X. (2013) · PLoS ONE · doi:10.1371/journal.pone.0054916 · Cited by 57
Cilengitide with metronomic temozolomide, procarbazine, and standard radiotherapy in patients with glioblastoma and unmethylated MGMT gene promoter in ExCentric, an open-label phase II trial
Khasraw, M., Lee, A., McCowatt, S., Kerestes, Z., Buyse, M. E., Back, M., Kichenadasse, G., Ackland, S. P., & Wheeler, H. (2016) · Journal of Neuro-Oncology · doi:10.1007/s11060-016-2094-0 · Cited by 52
Multicenter Phase IB Trial of Carboxyamidotriazole Orotate and Temozolomide for Recurrent and Newly Diagnosed Glioblastoma and Other Anaplastic Gliomas
Omuro, A. M. P., Beal, K. P., McNeill, K. A., Young, R. J., Thomas, A. A., Lin, X., Terziev, R., Kaley, T. J., DeAngelis, L. M., Daras, M., et al. (2018) · Journal of Clinical Oncology · doi:10.1200/jco.2017.76.9992 · Cited by 55
Therapeutic advances for glioblastoma multiforme: Current status and future prospects
Robins, H. I., Chang, S. M., Butowski, N. A., & Mehta, M. P. (2007) · Current Oncology Reports · doi:10.1007/bf02951428 · Cited by 51
“Thus, alternative endpoints, such as 6-month PFS, have evolved as meaningful surrogate markers for OS [ 29 ].”
Background
The Impact of Epigenetic Modifications on Adaptive Resistance Evolution in Glioblastoma
Wu, Q., Berglund, A., & Etame, A. B. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22158324 · Cited by 54
“The prognosis is markedly dismal in patients with recurrent GBM, whereby a highly resistant phenotype limits the effectiveness of additional chemotherapy [2,3].”
Background
Antitumor effect of humanized anti–interleukin-6 receptor antibody (tocilizumab) on glioma cell proliferation
Kudo, M., Jono, H., Shinriki, S., Yano, S., Nakamura, H., Makino, K., Hide, T., Muta, D., Ueda, M., Ota, K., et al. (2009) · Journal of neurosurgery · doi:10.3171/2008.12.jns081284 · Cited by 53
Progress on Antiangiogenic Therapy for Patients with Malignant Glioma
Ahluwalia, M. S., & Gladson, C. L. (2010) · Journal of Oncology · doi:10.1155/2010/689018 · Cited by 55
“at six months (PFS-6) was 43% for recurrent GBM patients and 59% for AG patients, and this was an improvement over the accepted PFS-6 standard of 15% for GBM patients and 31% for AG patients treated with temozolomide [79, 80].”
Result
Bevacizumab for glioblastoma: current indications, surgical implications, and future directions
Castro, B. A., & Aghi, M. K. (2014) · Neurosurgical FOCUS · doi:10.3171/2014.9.focus14516 · Cited by 52
Inhibiting kinases in malignant gliomas
Chi, A. S., & Wen, P. Y. (2007) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.11.4.473 · Cited by 51
“Most importantly, the trials did not show improvements in measures of progression or survival when compared with historical controls [4,5].”
Background
Novel human IgG2b/murine chimeric antitenascin monoclonal antibody construct radiolabeled with 131I and administered into the surgically created resection cavity of patients with malignant glioma: phase I trial results.
Reardon, D. A., Quinn, J. A., Akabani, G., Coleman, R. E., Friedman, A. H., Friedman, H. S., Herndon, J. E., McLendon, R. E., Pegram, C. N., Provenzale, J. M., et al. (2006) · PubMed · Cited by 51
Self-citation
Management of glioma in Victoria (1998–2000): retrospective cohort study
Rosenthal, M. A., Drummond, K. J., Dally, M. J., Murphy, M., Cher, L., Ashley, D. M., Thursfield, V. J., & Giles, G. G. (2006) · The Medical Journal of Australia · doi:10.5694/j.1326-5377.2006.tb00235.x · Cited by 51
Safety and pharmacokinetics of dose-intensive imatinib mesylate plus temozolomide: Phase 1 trial in adults with malignant glioma
Reardon, D. A., Desjardins, A., Vredenburgh, J. J., Sathornsumetee, S., Rich, J. N., Quinn, J. A., Lagattuta, T. F., Egorin, M. J., Gururangan, S., McLendon, R. E., et al. (2008) · Neuro-Oncology · doi:10.1215/15228517-2008-003 · Cited by 51
Self-citation
A phase II study of concurrent temozolomide and cis-retinoic acid with radiation for adult patients with newly diagnosed supratentorial glioblastoma
Butowski, N. A., Prados, M. D., Lamborn, K. R., Larson, D. A., Sneed, P. K., Wara, W. M., Malec, M. K., Rabbitt, J. E., Page, M., & Chang, S. M. (2005) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2004.08.023 · Cited by 50
Self-citation
Cost‐effectiveness of temozolomide for the treatment of newly diagnosed glioblastoma multiforme
Lamers, L. M., Stupp, R., van den Bent, M. J., Al, M., Gorlia, T., Wasserfallen, J., Mittmann, N., Seung, S. J., Crott, R., & Groot, C. A. U. (2008) · Cancer · doi:10.1002/cncr.23297 · Cited by 51
“There are trials showing 20% 6-month PFS in that situation.(8) So there is a clinical benefit, as we can also hypothesize in view of the superior survival of MGMT promoter methylated patients in the radiotherapy-only arm.”
BackgroundMethod
Development of luciferase tagged brain tumour models in mice for chemotherapy intervention studies
Kemper, E. M., Leenders, W. P. J., Küsters, B., Lyons, S. K., Buckle, T., Heerschap, A., Boogerd, W. J., Beijnen, J. H., & van Tellingen, O. (2006) · European Journal of Cancer · doi:10.1016/j.ejca.2006.07.013 · Cited by 51
Objective response rate targets for recurrent glioblastoma clinical trials based on the historic association between objective response rate and median overall survival
Ellingson, B. M., Wen, P. Y., Chang, S. M., van den Bent, M. J., Vogelbaum, M. A., Li, G., Li, S. J., Kim, J., Youssef, G., Wick, W., et al. (2023) · Neuro-Oncology · doi:10.1093/neuonc/noad002 · Cited by 50
Two phase II trials of temozolomide with interferon-α2b (pegylated and non-pegylated) in patients with recurrent glioblastoma multiforme
Groves, M. D., Puduvalli, V. K., GILBERT, M. R., Levin, V. A., Conrad, C. A., Liu, V., Hunter, K., Meyers, C., Hess, K. R., & Yung, W. K. A. (2009) · British Journal of Cancer · doi:10.1038/sj.bjc.6605189 · Cited by 50
“The PFS-6 results of 31 and 38% for IFN and PEG, respectively, compare favourably to the PFS-6 of 21% reported with standard (5-day every 28 days) dose TMZ in recurrent GBM (Yung et al, 2000).”
ResultSelf-citation
Key determinants of short-term and long-term glioblastoma survival: A 14-year retrospective study of patients from the Hermelin Brain Tumor Center at Henry Ford Hospital
Mazaris, P., Hong, X., Altshuler, D. B., Schultz, L. R., Poisson, L., Jain, R., Mikkelsen, T., Rosenblum, M. L., & Kalkanis, S. N. (2014) · Clinical Neurology and Neurosurgery · doi:10.1016/j.clineuro.2014.03.001 · Cited by 50
Progress and Prospects of Recurrent Glioma: A Recent Scientometric Analysis of the Web of Science in 2019
Chen, W., Lei, C., Liu, P., Liu, Y., Guo, X., Kong, Z., Wang, Y., Dai, C., Wang, Y., Ma, W., et al. (2019) · World Neurosurgery · doi:10.1016/j.wneu.2019.10.078 · Cited by 49
Therapeutic advances in the treatment of brain metastases.
Chang, J. E., Robins, H. I., & Mehta, M. P. (2007) · PubMed · Cited by 49
Current evidence of temozolomide and bevacizumab in treatment of gliomas
Nanegrungsunk, D., Onchan, W., Chattipakorn, N., & Chattipakorn, S. C. (2014) · Neurological Research · doi:10.1179/1743132814y.0000000423 · Cited by 50
Sunitinib administered prior to radiotherapy in patients with non-resectable glioblastoma: results of a Phase II study
Balañá, C., Gil‐Gil, M., Pérez, P., Reynés, G., Gallego, O. S., Ribalta, T., Capellades, J., González‐Ortiz, S., & Verger, E. (2014) · Targeted Oncology · doi:10.1007/s11523-014-0305-1 · Cited by 48
“Temozolomide showed superiority to the nitrosureas in early studies in relapsed glioblastoma patients [24] and is still the only drug that has demonstrated benefit as first-line treatment.”
Background
ACNU-based chemotherapy for recurrent glioma in the temozolomide era
Hertler, C., Roth, P., Wick, W., Steinbach, J. P., Linnebank, M., Weller, M., & Eisele, G. (2008) · Journal of Neuro-Oncology · doi:10.1007/s11060-008-9728-9 · Cited by 46
“In the registration trial, temozolomide given at recurrence in a conventional treatment schedule induced a progression-free survival of 11 weeks and a PFS-6 of 21% [16].”
Background
Advances in the treatment of newly diagnosed glioblastoma
Theeler, B. J., & Gilbert, M. R. (2015) · BMC Medicine · doi:10.1186/s12916-015-0536-8 · Cited by 48
“Temozolomide, an oral alkylating agent with good blood-brain barrier penetration, was developed in the 1990s and showed benefit in the recurrent setting in GBs and recurrent anaplastic gliomas gaining approval for this indication [8].”
Background
A phase II study of carboplatin and chronic high-dose tamoxifen in patients with recurrent malignant glioma
Tang, P., Roldán, G. B., Brasher, P. M. A., Fulton, D. S., Roa, W., Murtha, A. D., Cairncross, J. G., & Forsyth, P. A. (2006) · Journal of Neuro-Oncology · doi:10.1007/s11060-005-9104-y · Cited by 47
“By the time we accrued 27 patients it became clear that temozolomide was better tolerated regimen with a similar response rate for recurrent malignant gliomas and had become standard of care [34,35].”
Background
Bevacizumab/Irinotecan. Un nouveau traitement actif dans les gliomes de haut grade récidivants : résultats préliminaires d’une étude multicentrique de l’Anocef
Guiu, S., Taillibert, S., Chinot, O. L., Taillandier, L., Honnorat, J., Dietrich, P., Maire, J.-P., Guillamo, J., Guiu, B., Catry‐Thomas, I., et al. (2008) · Revue Neurologique · doi:10.1016/j.neurol.2008.04.003 · Cited by 47
The effect of temozolomide-based chemotherapy in patients with cerebral metastases from melanoma
Bafaloukos, D., Tsoutsos, D. A., Fountzilas, G., Linardou, H., Christodoulou, C., Kalofonos, H. P., Briassoulis, E., Panagiotou, P., Hatzichristou, H., & Gogas, H. J. (2004) · Melanoma Research · doi:10.1097/01.cmr.0000136707.60108.ab · Cited by 47
Brain tumor treatment: Chemotherapy and other new developments
Graham, C. A., & Cloughesy, T. F. (2004) · Seminars in Oncology Nursing · doi:10.1016/j.soncn.2004.07.006 · Cited by 47
Temozolomide in resistant or relapsed pediatric solid tumors
Sio, L. D., Milano, G. M., Castellano, A., Jenkner, A., Fidani, P., Dominici, C., & Donfrancesco, A. (2005) · Pediatric Blood & Cancer · doi:10.1002/pbc.20516 · Cited by 46
“Consistent with other reports [14,16,18], nausea and vomiting occurred most often after the first dose of TMZ”
Result
Local intracerebral administration of O6-benzylguanine combined with systemic chemotherapy with temozolomide of a patient suffering from a recurrent glioblastoma
Koch, D., Hundsberger, T., Boor, S., & Kaina, B. (2006) · Journal of Neuro-Oncology · doi:10.1007/s11060-006-9244-8 · Cited by 46
“Although a promising extension of average survival time was observed, only a minority of glioblastoma patients respond to O(6)-alkylating agents [1].”
Background
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Authors: Yung, W. K. A., Albright, R. E., Olson, J., Fredericks, R., Fink, K., Prados, M. D., Brada, M., Spence, A., Hohl, R. J., Shapiro, W., Glantz, M., Greenberg, H., Selker, R. G., Vick, N. A., Rampling, R., Friedman, H., Phillips, P., Bruner, J., Yue, N., Osoba, D., Zaknoen, S., & Levin, V. A.
Affiliations: The University of Texas MD Anderson Cancer Center (US)
Emory University (US)
University of Mississippi Medical Center (US)
The University of Texas Southwestern Medical Center (US)
University of California, San Francisco (US)
Royal Marsden NHS Foundation Trust (GB)
University of Washington (US)
University of Iowa Hospitals and Clinics (US)
Barrow Neurological Institute (US)
Memorial Hospital of Rhode Island (US)
University of Michigan (US)
Western Pennsylvania Hospital (US)
Evanston Hospital (US)
Beatson West of Scotland Cancer Centre (GB)
Duke University (US)
BC Cancer Agency (CA)
Merck & Co., Inc., Rahway, NJ, USA (United States) (US)
ORCID: Yung, W K A
Olson, J
Prados, M D
Glantz, M
Friedman, H
Levin, V A
Venue: British Journal of Cancer
Publisher: Springer Science and Business Media LLC
Published: 2000-09
Volume: 83
Issue: 5
Pages: 588-593
ISSN: 0007-0920 (ISSN-L)
1532-1827
DOI: 10.1054/bjoc.2000.1316
PMC: PMC2363506
OpenAlex: W1977392502
Cited by: 929
References: 27
Citations by year: 2026: 7 · 2025: 9 · 2024: 8 · 2023: 23 · 2022: 19 · 2021: 21 · 2020: 21 · 2019: 20 · 2018: 27 · 2017: 23 · 2016: 31 · 2015: 32 · 2014: 33 · 2013: 38 · 2012: 50
FWCI: 21.15
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
Locations: British Journal of Cancer (publishedVersion, cc-by-nc-sa)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
eScholarship (California Digital Library) (submittedVersion)
eScholarship (California Digital Library) (submittedVersion, cc-by)
Topics: Health Sciences › Medicine › Oncology › Glioma Diagnosis and Treatment
Health Sciences › Medicine › Oncology › PARP inhibition in cancer therapy
Health Sciences › Medicine › Oncology › Cancer survivorship and care
Keywords: temozolomide, procarbazine, glioblastoma, first relapse, progression-free survival, overall survival, health-related quality of life, alkylating agents, oral chemotherapy, treatment safety
MeSH terms: Temozolomide, Adult, Aged, Antineoplastic Agents, Brain Neoplasms, Dacarbazine, Female, Glioblastoma, Humans, Male, Middle Aged, Procarbazine, Prognosis, Quality of Life, Recurrence, Time Factors, Gliosarcoma, Disease-Free Survival, Antineoplastic Agents, Alkylating

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A phase II study of temozolomide vs. procarbazine in patients with glioblastoma multiforme at first relapse

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