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Originally published as JCO Early Release 10.1200/JCO.2004.09.046 on December 9 2003

Journal of Clinical Oncology, Vol 22, No 1 (January 1), 2004: pp. 23-30
© 2004 American Society of Clinical Oncology.
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A Randomized Controlled Trial of Fluorouracil Plus Leucovorin, Irinotecan, and Oxaliplatin Combinations in Patients With Previously Untreated Metastatic Colorectal Cancer

Richard M. Goldberg, Daniel J. Sargent, Roscoe F. Morton, Charles S. Fuchs, Ramesh K. Ramanathan, Stephen K. Williamson, Brian P. Findlay, Henry C. Pitot, Steven R. Alberts

From the North Central Cancer Treatment Group, Divisions of Hematology/Oncology and Medical Oncology, University of North Carolina at Chapel Hill, Chapel Hill, NC; North Central Cancer Treatment Group, Division of Biostatistics, Mayo Clinic, Rochester, MN; North Central Cancer Treatment Group, Iowa Oncology Research Association Community Clinical Oncology Program, Des Moines, IA; Cancer and Acute Leukemia Group B, Department of Oncology, Dana-Farber Cancer Institute, Boston, MA; Eastern Cooperative Oncology Group, Division of Medical Oncology, University of Pittsburgh Cancer Institute, Pittsburgh, PA; Southwestern Oncology Group, Division of Hematology and Oncology, University of Kansas Medical Center, Kansas City, KS; National Cancer Institute of Canada, St Catharines, Ontario, Canada.

Address reprint requests to Richard M. Goldberg, MD, Division of Hematology/Oncology, University of North Carolina at Chapel Hill, CB#7305, 3009 Old Clinic Building, Chapel Hill, NC 27599-7305; e-mail: goldberg{at}med.unc.edu

PURPOSE: Three agents with differing mechanisms of action are available for treatment of advanced colorectal cancer: fluorouracil, irinotecan, and oxaliplatin. In this study, we compared the activity and toxicity of three different two-drug combinations in patients with metastatic colorectal cancer who had not been treated previously for advanced disease.

PATIENTS AND METHODS: Patients were concurrently randomly assigned to receive irinotecan and bolus fluorouracil plus leucovorin (IFL, control combination), oxaliplatin and infused fluorouracil plus leucovorin (FOLFOX), or irinotecan and oxaliplatin (IROX). The primary end point was time to progression, with secondary end points of response rate, survival time, and toxicity.

RESULTS: A total of 795 patients were randomly assigned between May 1999 and April 2001. A median time to progression of 8.7 months, response rate of 45%, and median survival time of 19.5 months were observed for FOLFOX. These results were significantly superior to those observed for IFL for all end points (6.9 months, 31%, and 15.0 months, respectively) or for IROX (6.5 months, 35%, and 17.4 months, respectively) for time to progression and response. The FOLFOX regimen had significantly lower rates of severe nausea, vomiting, diarrhea, febrile neutropenia, and dehydration. Sensory neuropathy and neutropenia were more common with the regimens containing oxaliplatin.

CONCLUSION: The FOLFOX regimen of oxaliplatin and infused fluorouracil plus leucovorin was active and comparatively safe. It should be considered as a standard therapy for patients with advanced colorectal cancer.

Supported by National Institutes of Health grants CA25224, CA32102, CA38926, CA21115, and CA77202, Pharmacia Corp, and Sanofi-Synthelabo. Pharmacia and Sanofi-Synthelabo provided irinotecan and oxaliplatin, respectively, for this study, and both approved the study protocol.

Presented in part at the 2001 (May 12-15, 2001, San Francisco, CA), 2002 (May 18-21, 2002, Orlando, FL), and 2003 (May 31-June 3, 2003, Chicago, IL) Annual Meetings of the American Society of Clinical Oncology.

Nothing in this article implies endorsement of the products of Pharmacia (Pfizer) Corp or Sanofi-Synthelabo.

Authors' disclosures of potential conflicts of interest are found at the end of this article.


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Positron Emission Tomography Detection of Distant Metastatic or Synchronous Disease in Patients with Locally Advanced Rectal Cancer Receiving Preoperative Chemoradiation
Ann. Surg. Oncol., March 1, 2008; 15(3): 704 - 711.
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E. Van Cutsem, C. Verslype, P. Beale, S. Clarke, R. Bugat, A. Rakhit, S. H. Fettner, U. Brennscheidt, A. Feyereislova, and J.-P Delord
A phase Ib dose-escalation study of erlotinib, capecitabine and oxaliplatin in metastatic colorectal cancer patients
Ann. Onc., February 1, 2008; 19(2): 332 - 339.
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J. Tabernero, P. Pfeiffer, and A. Cervantes
Administration of Cetuximab Every 2 Weeks in the Treatment of Metastatic Colorectal Cancer: An Effective, More Convenient Alternative to Weekly Administration?
Oncologist, February 1, 2008; 13(2): 113 - 119.
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A. Lievre, J.-B. Bachet, V. Boige, A. Cayre, D. Le Corre, E. Buc, M. Ychou, O. Bouche, B. Landi, C. Louvet, et al.
KRAS Mutations As an Independent Prognostic Factor in Patients With Advanced Colorectal Cancer Treated With Cetuximab
J. Clin. Oncol., January 20, 2008; 26(3): 374 - 379.
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A. Grothey, E. E. Hedrick, R. D. Mass, S. Sarkar, S. Suzuki, R. K. Ramanathan, H. I. Hurwitz, R. M. Goldberg, and D. J. Sargent
Response-Independent Survival Benefit in Metastatic Colorectal Cancer: A Comparative Analysis of N9741 and AVF2107
J. Clin. Oncol., January 10, 2008; 26(2): 183 - 189.
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V. Boige, D. Malka, D. Elias, M. Castaing, T. De Baere, D. Goere, C. Dromain, M. Pocard, and M. Ducreux
Hepatic Arterial Infusion of Oxaliplatin and Intravenous LV5FU2 in Unresectable Liver Metastases from Colorectal Cancer after Systemic Chemotherapy Failure
Ann. Surg. Oncol., January 1, 2008; 15(1): 219 - 226.
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 The OncologistHome page
T. M. Pawlik, R. D. Schulick, and M. A. Choti
Expanding Criteria for Resectability of Colorectal Liver Metastases
Oncologist, January 1, 2008; 13(1): 51 - 64.
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Y. Inaba, H. Yamaura, Y. Sato, M. Najima, H. Shimamoto, H. Nishiofuku, T. Ura, and K. Muro
Central Venous Access Port-related Complications in Outpatient Chemotherapy for Colorectal Cancer
Jpn. J. Clin. Oncol., December 4, 2007; (2007) hym118v1.
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 J Oncol Pharm PractHome page
N. Kitada, T. Dan, K. Takara, T. Tsuji, H. Yamasaki, T. Yokoyama, and M. Watari
Oxaliplatin-induced hypersensitivity reaction displaying marked elevation of immunoglobulin E
Journal of Oncology Pharmacy Practice, December 1, 2007; 13(4): 233 - 235.
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Y. Becouarn, P. Senesse, S. Thezenas, E. Boucher, A. Adenis, L. Cany, J. H. Jacob, F. Cvitkovic, C. Montoto-Grillot, and M. Ychou
A randomized phase II trial evaluating safety and efficacy of an experimental chemotherapy regimen (irinotecan + oxaliplatin, IRINOX) and two standard arms (LV5 FU2 + irinotecan or LV5 FU2 + oxaliplatin) in first-line metastatic colorectal cancer: a study of the Digestive Group of the Federation Nationale des Centres de Lutte Contre le Cancer
Ann. Onc., December 1, 2007; 18(12): 2000 - 2005.
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M. Buyse, T. Burzykowski, K. Carroll, S. Michiels, D. J. Sargent, L. L. Miller, G. L. Elfring, J.-P. Pignon, and P. Piedbois
Progression-Free Survival Is a Surrogate for Survival in Advanced Colorectal Cancer
J. Clin. Oncol., November 20, 2007; 25(33): 5218 - 5224.
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J. Tabernero, E. Van Cutsem, E. Diaz-Rubio, A. Cervantes, Y. Humblet, T. Andre, J.-L. Van Laethem, P. Soulie, E. Casado, C. Verslype, et al.
Phase II Trial of Cetuximab in Combination With Fluorouracil, Leucovorin, and Oxaliplatin in the First-Line Treatment of Metastatic Colorectal Cancer
J. Clin. Oncol., November 20, 2007; 25(33): 5225 - 5232.
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D. J. Jonker, C. J. O'Callaghan, C. S. Karapetis, J. R. Zalcberg, D. Tu, H.-J. Au, S. R. Berry, M. Krahn, T. Price, R. J. Simes, et al.
Cetuximab for the Treatment of Colorectal Cancer
N. Engl. J. Med., November 15, 2007; 357(20): 2040 - 2048.
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J. A. Sloan, L. Berk, J. Roscoe, M. J. Fisch, E. G. Shaw, G. Wyatt, G. R. Morrow, and A. C. Dueck
Integrating Patient-Reported Outcomes Into Cancer Symptom Management Clinical Trials Supported by the National Cancer Institute Sponsored Clinical Trials Networks
J. Clin. Oncol., November 10, 2007; 25(32): 5070 - 5077.
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L. A. Lambert and P. F. Mansfield
Cytoreductive Surgery and Perioperative Intraperitoneal Chemotherapy for Colorectal Carcinomatosis: If at First You Don't Succeed...
Ann. Surg. Oncol., November 1, 2007; 14(11): 3037 - 3039.
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P. Kornprat, W. R. Jarnagin, R. P. DeMatteo, Y. Fong, L. H. Blumgart, and M. D'Angelica
Role of Intraoperative Thermoablation Combined With Resection in the Treatment of Hepatic Metastasis From Colorectal Cancer
Arch Surg, November 1, 2007; 142(11): 1087 - 1092.
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E. Bajetta, L. Celio, E. Ferrario, M. Di Bartolomeo, A. Denaro, K. Dotti, M. Mancin, R. Bajetta, A. Colombo, and S. Pusceddu
Capecitabine plus oxaliplatin and irinotecan regimen every other week: a phase I/II study in first-line treatment of metastatic colorectal cancer
Ann. Onc., November 1, 2007; 18(11): 1810 - 1816.
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C. S. Fuchs, J. Marshall, E. Mitchell, R. Wierzbicki, V. Ganju, M. Jeffery, J. Schulz, D. Richards, R. Soufi-Mahjoubi, B. Wang, et al.
Randomized, Controlled Trial of Irinotecan Plus Infusional, Bolus, or Oral Fluoropyrimidines in First-Line Treatment of Metastatic Colorectal Cancer: Results From the BICC-C Study
J. Clin. Oncol., October 20, 2007; 25(30): 4779 - 4786.
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J. S. Tomlinson, W. R. Jarnagin, R. P. DeMatteo, Y. Fong, P. Kornprat, M. Gonen, N. Kemeny, M. F. Brennan, L. H. Blumgart, and M. D'Angelica
Actual 10-Year Survival After Resection of Colorectal Liver Metastases Defines Cure
J. Clin. Oncol., October 10, 2007; 25(29): 4575 - 4580.
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P. A. Tang, S. M. Bentzen, E. X. Chen, and L. L. Siu
Surrogate End Points for Median Overall Survival in Metastatic Colorectal Cancer: Literature-Based Analysis From 39 Randomized Controlled Trials of First-Line Chemotherapy
J. Clin. Oncol., October 10, 2007; 25(29): 4562 - 4568.
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R. Porschen, H.-T. Arkenau, S. Kubicka, R. Greil, T. Seufferlein, W. Freier, A. Kretzschmar, U. Graeven, A. Grothey, A. Hinke, et al.
Phase III Study of Capecitabine Plus Oxaliplatin Compared With Fluorouracil and Leucovorin Plus Oxaliplatin in Metastatic Colorectal Cancer: A Final Report of the AIO Colorectal Study Group
J. Clin. Oncol., September 20, 2007; 25(27): 4217 - 4223.
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E. Diaz-Rubio, J. Tabernero, A. Gomez-Espana, B. Massuti, J. Sastre, M. Chaves, A. Abad, A. Carrato, B. Queralt, J. J. Reina, et al.
Phase III Study of Capecitabine Plus Oxaliplatin Compared With Continuous-Infusion Fluorouracil Plus Oxaliplatin As First-Line Therapy in Metastatic Colorectal Cancer: Final Report of the Spanish Cooperative Group for the Treatment of Digestive Tumors Trial
J. Clin. Oncol., September 20, 2007; 25(27): 4224 - 4230.
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 Ann. Surg. Oncol.Home page
T. Liersch, J. Meller, M. Bittrich, B. Kulle, H. Becker, and D. M. Goldenberg
Update of Carcinoembryonic Antigen Radioimmunotherapy with 131I-Labetuzumab After Salvage Resection of Colorectal Liver Metastases: Comparison of Outcome to a Contemporaneous Control Group
Ann. Surg. Oncol., September 1, 2007; 14(9): 2577 - 2590.
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T. Yoshino, N. Boku, Y. Onozawa, S. Hironaka, A. Fukutomi, Y. Yamaguchi, N. Hasuike, K. Yamazaki, N. Machida, and H. Ono
Efficacy and Safety of an Irinotecan plus Bolus 5-Fluorouracil and L-Leucovorin Regimen for Metastatic Colorectal Cancer in Japanese Patients: Experience in a Single Institution in Japan
Jpn. J. Clin. Oncol., September 1, 2007; 37(9): 686 - 691.
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T. Andre, E. Quinaux, C. Louvet, P. Colin, E. Gamelin, O. Bouche, E. Achille, P. Piedbois, N. Tubiana-Mathieu, A. Boutan-Laroze, et al.
Phase III Study Comparing a Semimonthly With a Monthly Regimen of Fluorouracil and Leucovorin As Adjuvant Treatment for Stage II and III Colon Cancer Patients: Final Results of GERCOR C96.1
J. Clin. Oncol., August 20, 2007; 25(24): 3732 - 3738.
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G. K. Dy, J. E. Krook, E. M. Green, D. J. Sargent, T. Delaunoit, R. F. Morton, C. S. Fuchs, R. K. Ramanathan, S. K. Williamson, B. P. Findlay, et al.
Impact of Complete Response to Chemotherapy on Overall Survival in Advanced Colorectal Cancer: Results From Intergroup N9741
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A. de Gramont, M. Buyse, J. C. Abrahantes, T. Burzykowski, E. Quinaux, A. Cervantes, A. Figer, G. Lledo, M. Flesch, L. Mineur, et al.
Reintroduction of Oxaliplatin Is Associated With Improved Survival in Advanced Colorectal Cancer
J. Clin. Oncol., August 1, 2007; 25(22): 3224 - 3229.
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 Ann. Surg. Oncol.Home page
L. Bijelic, T. D. Yan, and P. H. Sugarbaker
Failure Analysis of Recurrent Disease Following Complete Cytoreduction and Perioperative Intraperitoneal Chemotherapy in Patients with Peritoneal Carcinomatosis from Colorectal Cancer
Ann. Surg. Oncol., August 1, 2007; 14(8): 2281 - 2288.
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N. Fuse, T. Doi, A. Ohtsu, S. Takeuchi, T. Kojima, K. Taku, M. Tahara, M. Muto, M. Asaka, and S. Yoshida
Feasibility of Oxaliplatin and Infusional Fluorouracil/Leucovorin (FOLFOX4) for Japanese Patients with Unresectable Metastatic Colorectal Cancer
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N. Boku, A. Ohtsu, I. Hyodo, K. Shirao, Y. Miyata, K. Nakagawa, T. Tamura, K. Hatake, and Y. Tanigawara
Phase II Study of Oxaliplatin in Japanese Patients with Metastatic Colorectal Cancer Refractory to Fluoropyrimidines
Jpn. J. Clin. Oncol., June 1, 2007; 37(6): 440 - 445.
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S. L. Spunt, B. B. Freeman III, C. A. Billups, V. McPherson, R. B. Khan, C. B. Pratt, and C. F. Stewart
Phase I Clinical Trial of Oxaliplatin in Children and Adolescents With Refractory Solid Tumors
J. Clin. Oncol., June 1, 2007; 25(16): 2274 - 2280.
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S. R. Land, J. A. Kopec, R. S. Cecchini, P. A. Ganz, H. S. Wieand, L. H. Colangelo, K. Murphy, J. P. Kuebler, T. E. Seay, B. M. Needles, et al.
Neurotoxicity From Oxaliplatin Combined With Weekly Bolus Fluorouracil and Leucovorin As Surgical Adjuvant Chemotherapy for Stage II and III Colon Cancer: NSABP C-07
J. Clin. Oncol., June 1, 2007; 25(16): 2205 - 2211.
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P. E. Goss, J. N. Ingle, S. Martino, N. J. Robert, H. B. Muss, M. J. Piccart, M. Castiglione, D. Tu, L. E. Shepherd, K. I. Pritchard, et al.
Efficacy of Letrozole Extended Adjuvant Therapy According to Estrogen Receptor and Progesterone Receptor Status of the Primary Tumor: National Cancer Institute of Canada Clinical Trials Group MA.17
J. Clin. Oncol., May 20, 2007; 25(15): 2006 - 2011.
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