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Effect of First-Line Chemotherapy Combined With Cetuximab or Bevacizumab on Overall Survival in Patients With KRAS Wild-Type Advanced or Metastatic Colorectal Cancer: A Randomized Clinical Trial
Open accessAbstract
Importance: Combining biologic monoclonal antibodies with chemotherapeutic cytotoxic drugs provides clinical benefit to patients with advanced or metastatic colorectal cancer, but the optimal choice of the initial biologic therapy in previously untreated patients is unknown. Objective: To determine if the addition of cetuximab vs bevacizumab to the combination of leucovorin, fluorouracil, and oxaliplatin (mFOLFOX6) regimen or the combination of leucovorin, fluorouracil, and irinotecan (FOLFIRI) regimen is superior as first-line therapy in advanced or metastatic KRAS wild-type (wt) colorectal cancer. Design, Setting, and Participants: Patients (≥18 years) enrolled at community and academic centers throughout the National Clinical Trials Network in the United States and Canada (November 2005-March 2012) with previously untreated advanced or metastatic colorectal cancer whose tumors were KRAS wt chose to take either the mFOLFOX6 regimen or the FOLFIRI regimen as chemotherapy and were randomized to receive either cetuximab (n = 578) or bevacizumab (n = 559). The last date of follow-up was December 15, 2015. Interventions: Cetuximab vs bevacizumab combined with either mFOLFOX6 or FOLFIRI chemotherapy regimen chosen by the treating physician and patient. Main Outcomes and Measures: The primary end point was overall survival. Secondary objectives included progression-free survival and overall response rate, site-reported confirmed or unconfirmed complete or partial response. Results: Among 1137 patients (median age, 59 years; 440 [39%] women), 1074 (94%) of patients met eligibility criteria. As of December 15, 2015, median follow-up for 263 surviving patients was 47.4 months (range, 0-110.7 months), and 82% of patients (938 of 1137) experienced disease progression. The median overall survival was 30.0 months in the cetuximab-chemotherapy group and 29.0 months in the bevacizumab-chemotherapy group with a stratified hazard ratio (HR) of 0.88 (95% CI, 0.77-1.01; P = .08). The median progression-free survival was 10.5 months in the cetuximab-chemotherapy group and 10.6 months in the bevacizumab-chemotherapy group with a stratified HR of 0.95 (95% CI, 0.84-1.08; P = .45). Response rates were not significantly different, 59.6% vs 55.2% for cetuximab and bevacizumab, respectively (difference, 4.4%, 95% CI, 1.0%-9.0%, P = .13). Conclusions and Relevance: Among patients with KRAS wt untreated advanced or metastatic colorectal cancer, there was no significant difference in overall survival between the addition of cetuximab vs bevacizumab to chemotherapy as initial biologic treatment. Trial Registration: clinicaltrials.gov identifier: NCT00265850.
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“Also, patients with metastatic colorectal cancer and related intestinal malignancies tend to receive similar treatments and live for many months with relatively stable health (median overall survival >2 years) [44], facilitating study completion and potentially derivation of durable benefit from the intervention.”
From Being present: A single-arm feasibility study of audio-based mindfulness meditation for colorectal cancer patients and caregivers (2018) · cites this paper as [44]
Experimental — accuracy not yet measuredThe check wasn’t confident either way, so it gives no verdict — never disputed.
In the citing paper
“Although a higher percentage of men enrolled compared to most prior mindfulness interventions for integrative cancer care [34], the evaluable study sample included a greater proportion of younger (age <50), female, White and Latino or Hispanic patients relative to the underlying population [44, 53].”
From Being present: A single-arm feasibility study of audio-based mindfulness meditation for colorectal cancer patients and caregivers (2018) · cites this paper as [44]
Experimental — accuracy not yet measuredIn the citing paper
“This trial demonstrated that patients in the cetuximab plus chemotherapy group had slightly higher overall survival versus patients in the bevacizumab plus chemotherapy group (30.0 months versus 29.0 months).”
From Update on Targeted Therapy and Immunotherapy for Metastatic Colorectal Cancer (2024) · cites this paper as [65]
In the citing paper
“Similar to the FIRE-3 trial, median progression-free survival and response rates were similar between groups.”
From Update on Targeted Therapy and Immunotherapy for Metastatic Colorectal Cancer (2024) · cites this paper as [65]
In the citing paper
“Similarly, the CALGB/SWOG 80405 trial showed that both cetuximab and bevacizumab provided comparable outcomes when combined with chemotherapy in the overall population, but the benefit of anti-EGFR therapy was again limited to RAS wild-type tumors [21].”
From RAS Mutations in Advanced Colorectal Cancer: Mechanisms, Clinical Implications, and Novel Therapeutic Approaches (2025) · cites this paper as [21]
In the citing paper
“however, it must be noted here that this pooled analysis also included patients who had received a nonstandard treatment regimen, including FUFIRI, FUFOX, and mIROX as induction chemotherapies and bevacizumab monotherapy or observation alone as maintenance therapies in clinical trials [22,23].”
From The Prognostic Impact of KRAS G12C Mutation in Patients with Metastatic Colorectal Cancer: A Multicenter Retrospective Observational Study (2021) · cites this paper as [22]
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“Hurdles race for CAR T ‐cell therapy in digestive tract cancer”
Kronig, M.-N., Wehrli, M., Salas‐Benito, D., & Maus, M. V. (2023) · Immunological Reviews · doi:10.1111/imr.13273 · Cited by 20
Effect of Time to Surgery of Colorectal Liver Metastases on Survival
Chen, E. Y.-S., Mayo, S. C., Sutton, T. L., Kearney, M., Kardosh, A., Vaccaro, G. M., Billingsley, K. G., & Lopez, C. D. (2020) · Journal of Gastrointestinal Cancer · doi:10.1007/s12029-020-00372-5 · Cited by 19
Karani, A., Felismino, T. C., Diniz, L. A., de Macêdo, M. P., Silva, V. S. E., & de Mello, C. A. L. (2020) · ecancermedicalscience · doi:10.3332/ecancer.2020.1069 · Cited by 18
“It is noteworthy that 94% of our patients had a left-side primary tumour and it is known that patients with a left-sided tumour have prolonged survival when treated with anti-EGFR in the first line as demonstrated by many prospective trials [5, 6].”
BackgroundFeasibility of MRI Radiomics for Predicting KRAS Mutation in Rectal Cancer
Guo, X., Yang, W.-Q., Yang, Q., Yuan, Z., Liu, Y., Niu, X., & Xu, H. (2020) · Current Medical Science · doi:10.1007/s11596-020-2298-6 · Cited by 19
Lai, E., Cascinu, S., & Scartozzi, M. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.637823 · Cited by 19
Liu, T., Jiang, S., Teng, X., Zhong, L., Liu, M., Jin, Y., & Dong, M. (2023) · Immunopharmacology and Immunotoxicology · doi:10.1080/08923973.2022.2112222 · Cited by 17
Zhang, X., Di, Y., Wang, Y., Qin, J., Ye, L., Wen, X., Ke, Z., Wang, Z., & He, W. (2025) · The EMBO Journal · doi:10.1038/s44318-025-00416-1 · Cited by 19
“…chemotherapy and targeted therapy remains unsatisfactory in patients with mCRC (Douillard et al, 2010; Heinemann et al, 2014; Mayer et al, 2015; Venook et al, 2017), and the relapse rate is as high as 68% within three years after curative resection of metastatic tumors (Galjart et al, 2016).”
Primary Tumor Sidedness Predicts Bevacizumab Benefit in Metastatic Colorectal Cancer Patients
You, X.-H., Wen, C., Xia, Z., Sun, F., Li, Y., Wang, W., Fang, Z., Chen, Q.-G., Zhang, L., Jiang, Y.-H., et al. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00723 · Cited by 17
Pan, B., Yue, Y., Ding, W., Sun, L., Xu, M., & Wang, S. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1161382 · Cited by 17
Ramon, L., David, C., Fontaine, K., Lallet, E., Marcaillou, C., Martin‐Lannerée, S., Decaulne, V., Vazart, C., Gélibert, A.-H., Abdelali, R. B., et al. (2018) · Biomarker Insights · doi:10.1177/1177271918763357 · Cited by 17
Treatment sequencing for simultaneous colorectal liver metastases
Krell, R. W., & D'Angelica, M. I. (2019) · Journal of Surgical Oncology · doi:10.1002/jso.25424 · Cited by 18
Dai, D., Zhou, B., Zhong, Y., Jin, H., & Wang, X. (2019) · Oncology Letters · doi:10.3892/ol.2019.11024 · Cited by 17
Tougeron, D., Emambux, S., Favot, L., Lecomte, T., Wierzbicka-Hainaut, E., Samimi, M., Frouin, É., Azzopardi, N., Chevrier, J., Serres, L., et al. (2020) · OncoImmunology · doi:10.1080/2162402x.2020.1848058 · Cited by 17
Fischer, L. E., Stintzing, S., von Weikersthal, L. F., Modest, D. P., Decker, T. W., Kiani, A., Kaiser, F., Al-Batran, S.-E., Heintges, T., Lerchenmuller, C. A., et al. (2022) · British Journal of Cancer · doi:10.1038/s41416-022-01854-y · Cited by 17
Li, M., Mulkey, F. A., Jiang, C., O’Neil, B. H., Schneider, B. P., Shen, F., Friedman, P. N., Momozawa, Y., Kubo, M., Niedzwiecki, D., et al. (2018) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-17-1523 · Cited by 17
“This trial has been described previously in detail (14).”
MethodSelf-citationShuford, R. A., Cairns, A., & Moaven, O. (2020) · Cancers · doi:10.3390/cancers12113481 · Cited by 17
“Similarly, the CALGB/SWOG 80405 trial showed overall improved outcomes, especially in left-sided primary KRAS wt CRC with improved OS (OS for all-sided lesions was 30 months with cetuximab plus chemotherapy versus 29 months with bevacizumab plus chemotherapy, the finding was not statistically significant) in this popu…”
ResultHe, X., Jiao, X., Liu, K., Qin, B., Wu, Y., Ling, Y., Liu, J., Xu, A., Song, K., & Zang, Y. (2021) · JCO Precision Oncology · doi:10.1200/po.20.00534 · Cited by 17
“With advances in combining chemotherapy with vascular endothelial growth factor or epidermal growth factor receptor inhibitors, the median overall survival for patients with metastatic colorectal carcinoma (mCRC) is approximately 30 months.(3) Recent next-generation sequencing (NGS) has uncovered several novel potenti…”
BackgroundNegative Predictive Biomarkers in Colorectal Cancer: PRESSING Ahead
Sundar, R., Tan, I. B. H., & Chee, C. E. (2019) · Journal of Clinical Oncology · doi:10.1200/jco.19.01977 · Cited by 17
Innovation in cancer pharmacotherapy through integrative consideration of germline and tumor genomes
Tremmel, R., Hübschmann, D., Schaeffeler, E., Pirmann, S., Fröhling, S., & Schwab, M. (2024) · Pharmacological Reviews · doi:10.1124/pharmrev.124.001049 · Cited by 17
Arai, H., Elliott, A., Millstein, J., Xiu, J., Ou, F., Innocenti, F., Wang, J., Battaglin, F., Jayachandran, P., Kawanishi, N. K., et al. (2021) · Oncogene · doi:10.1038/s41388-021-02074-z · Cited by 16
“S1B): a cohort from Caris CODEai (a real-world clinico-genomic data platform that integrates molecular data collected at Caris Life Sciences with cancer treatment information and clinical outcomes data obtained from insurance claims data; including 224 patients with available NGS data); and one from the phase III Canc…”
MethodSelf-citationWang, C., Sandhu, J. S., & Fakih, M. (2022) · The Oncologist · doi:10.1093/oncolo/oyab028 · Cited by 16
Colorectal cancer: Review of signaling pathways and associated therapeutic strategies
Leiphrakpam, P. D., Rajappa, S. J., Krishnan, M., Batra, R., Murthy, S. S., & Are, C. (2023) · Journal of Surgical Oncology · doi:10.1002/jso.27295 · Cited by 17
Waldstein, S., Spengler, M., Pinchuk, I. V., & Yee, N. S. (2023) · Journal of Personalized Medicine · doi:10.3390/jpm13071114 · Cited by 20
Optimizing Treatment Strategy for Oligometastases/Oligo-Recurrence of Colorectal Cancer
Yokoi, R., Tajima, J. Y., Fukada, M., Hayashi, H., Kuno, M., Asai, R., Sato, Y., Yasufuku, I., Kiyama, S., Tanaka, Y., et al. (2023) · Cancers · doi:10.3390/cancers16010142 · Cited by 17
Takashima, A., Alfonso, P. G., Manneh, R., Beşen, A. A., Hong, Y. S., Cuyle, P.-J. A., Yanez, P. E., Burge, M., Yoshino, T., Kim, T. W., et al. (2024) · European Journal of Cancer · doi:10.1016/j.ejca.2024.114036 · Cited by 17
Karaoğlan, B. B., Öz, D. K., Araz, M., Akyol, C., & Utkan, G. (2024) · Current Oncology Reports · doi:10.1007/s11912-024-01548-z · Cited by 16
Cha, Y., Kim, S. Y., Yeo, H. Y., Baek, J. Y., Choi, M. K., Jung, K. H., Dong, S. M., & Chang, H. J. (2018) · Neoplasia · doi:10.1016/j.neo.2018.11.010 · Cited by 16
“Since the adoption of anti-EGFR and anti-VEGF(R) antibodies in 2004, the median survival time of patients with metastatic CRC has reached 30 months [2].”
Apatinib as an optional treatment in metastatic colorectal cancer
Li, A., Wang, K., Xu, A., Wang, G., Miao, Y., Sun, Z., & Zhang, J. (2019) · Medicine · doi:10.1097/md.0000000000016919 · Cited by 16
“0 months.([4]) Although most patients will experience undesired progressive disease, it is necessary to explore effective treatment options for these patients.”
BackgroundTo treat or not to treat: a clinical series of retinal arterial macroaneurysms
Cho, W., Chiang, W., Chen, C.-H., & Kuo, H. (2020) · Medicine · doi:10.1097/md.0000000000019077 · Cited by 16
Gootjes, E. C., van der Stok, E. P., Buffart, T. E., Bakkerus, L., Labots, M., Zonderhuis, B. M., Tuynman, J. B., Meijerink, M. R., van de Ven, P. M., Haasbeek, C. J. A., et al. (2020) · The Oncologist · doi:10.1634/theoncologist.2019-0693 · Cited by 16
“These patients primarily receive palliative systemic treatment consisting of combination chemotherapy with agents targeting VEGF or EGFR [17, 18].”
BackgroundWang, Y., Dong, J., Quan, Q., Liu, S., Chen, X., Cai, X., Qiu, H., Zhang, B., & Guo, G. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2020.581051 · Cited by 16
Zhang, Y., Li, C., Jia, R., Gao, R., Zhao, Y., Ji, Q., Cai, J., Li, Q., & Wang, Y. (2021) · Biomaterials Science · doi:10.1039/d1bm00160d · Cited by 15
RetractedDiagnostic and therapeutic biomarkers in colorectal cancer: a review.
de Assis, J. V., Coutinho, L. A., Oyeyemi, I. T., Oyeyemi, O. T., & Grenfell, R. F. Q. (2022) · PubMed Central · Cited by 16
Khakoo, S. S., Chau, I., Pedley, I. D., Ellis, R. E., Steward, W. P., Harrison, M., Baijal, S., Tahir, S., Ross, P. J., Raouf, S., et al. (2019) · Clinical Colorectal Cancer · doi:10.1016/j.clcc.2019.07.003 · Cited by 16
Liu, R., Zhao, X., Guo, W., Huang, M., Qiu, L., Zhang, W., Zhang, Z., Li, W., Zhu, X., & Chen, Z. (2019) · Clinical & Translational Oncology · doi:10.1007/s12094-019-02215-7 · Cited by 16
Joharatnam‐Hogan, N., Wilson, W., Shiu, K., Fusai, G., Davidson, B. R., Hochhauser, D., Bridgewater, J. A., & Khan, K. H. (2020) · Cancers · doi:10.3390/cancers12123545 · Cited by 16
Avallone, A., Giuliani, F., Stefano, A. D., Santabarbara, G., Nasti, G., Montesarchio, V., Rosati, G., Cassata, A., Leo, S., Romano, C., et al. (2024) · Journal of Clinical Oncology · doi:10.1200/jco.24.00979 · Cited by 15
The treatment of rectal cancer with synchronous liver metastases: A matter of strategy
Gelsomino, F., Spallanzani, A., & Garajová, I. (2019) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2019.05.004 · Cited by 15
Liu, S., Wang, L., Li, S., Meng, X., Sun, B., Zhang, X., Zhang, L., Liu, Y., Lin, M., Zhang, H., et al. (2019) · Biomaterials Science · doi:10.1039/c9bm01017c · Cited by 15
Bai, L., Zhang, P., Zhou, K., Liao, W., & Li, Q. (2019) · Cancer Management and Research · doi:10.2147/cmar.s219318 · Cited by 15
“In addition, unlike in the CALGB/SWOG80405 trial, it seemed that patients with right-sided, BRAF wt mCRC could benefit from the addition of cetuximab to first-line FOLFOX-4 in the TAILOR trial.(9,10) Although therapy with cetuximab plus FOLFOX-4 shows certain advantages, health care costs increased significantly in th…”
MethodAdes, S., Pulluri, B., Holmes, C. E., Lal, I., Kumar, S., & Littenberg, B. (2022) · Cancer Medicine · doi:10.1002/cam4.4581 · Cited by 15
Walker, B. S., Billingsley, K. G., Sutton, T. L., Kolbeck, K. J., Korngold, E. K., Nabavizadeh, N., Dewey, E. N., Herzig, D. O., Lopez, C. D., & Mayo, S. C. (2022) · Journal of Surgical Oncology · doi:10.1002/jso.26911 · Cited by 15
Cann, C., LaPelusa, M. B., Cimino, S. K., & Eng, C. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.1176950 · Cited by 16
Metadata
- Authors
- Venook, A. P., Niedzwiecki, D., Lenz, H.-J., Innocenti, F., Fruth, B., Meyerhardt, J. A., Schrag, D., Greene, C., O'Neil, B. H., Atkins, J. N., Berry, S., Polite, B. N., O'Reilly, E. M., Goldberg, R. M., Hochster, H. S., Schilsky, R. L., Bertagnolli, M. M., El-Khoueiry, A. B., Watson, P., Benson, A. B., Mulkerin, D. L., Mayer, R. J., & Blanke, C.
- Affiliations
- University of California, San Francisco (US)
- Duke University (US)
- University of Southern California (US)
- University of North Carolina at Chapel Hill (US)
- Mayo Clinic (US)
- Dana-Farber/Partners CancerCare, Boston, Massachusetts
- Indiana University, Simon Cancer Center, Indianapolis
- Southeastern Medical Oncology Center (US)
- Sunnybrook Health Science Centre (CA)
- University of Chicago Comprehensive Cancer Center, Chicago, Illinois
- Memorial Sloan Kettering Cancer Center (US)
- The Ohio State University Comprehensive Cancer Center – Arthur G. James Cancer Hospital and Richard J. Solove Research Institute (US)
- Department of Medical Oncology, Yale University School of Medicine, New Haven, Connecticut
- American Society of Clinical Oncology (US)
- Brigham and Women's Hospital (US)
- Kinston Medical Specialists (US)
- Northwestern University (US)
- University of Wisconsin–Madison (US)
- Oregon Health & Science University (US)
- ORCID
- Venue
- JAMA
- Publisher
- American Medical Association (AMA)
- Published
- 2017-06-20
- Volume
- 317
- Issue
- 23
- Pages
- 2392
- ISSN
- 0002-9955 (ISSN-L)
- 0098-7484
- PMC
- PMC5545896
- OpenAlex
- W2712978371
- Cited by
- 898
- References
- 24
- Citations by year
- 2026: 66 · 2025: 76 · 2024: 87 · 2023: 104 · 2022: 118 · 2021: 118 · 2020: 122 · 2019: 107 · 2018: 82 · 2017: 16
- FWCI
- 39.43
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- JAMA (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institutes of Health (UL1TR001863)
- National Cancer Institute (U10CA180882, K05CA169384, U10CA180820, U10CA180791, U10CA180888, U10CA180836, U10CA180790, U10CA180830, U10CA180795, U10CA180850, R01CA149222, U10CA180838, U10CA180867, U10CA180821, U10CA180799)
- National Center for Advancing Translational Sciences
- Topics
- Health Sciences › Medicine › Oncology › Colorectal Cancer Treatments and Studies
- Health Sciences › Medicine › Oncology › Colorectal Cancer Surgical Treatments
- Health Sciences › Medicine › Surgery › Intraperitoneal and Appendiceal Malignancies
- Keywords
- metastatic colorectal cancer, KRAS wild-type, cetuximab, bevacizumab, first-line chemotherapy, mFOLFOX6, FOLFIRI, oxaliplatin, irinotecan, monoclonal antibodies, overall survival, progression-free survival, anti-EGFR therapy, anti-VEGF therapy, community oncology
- MeSH terms
- Bevacizumab, Cetuximab, Adult, Aged, Aged, 80 and over, Antineoplastic Agents, Antineoplastic Combined Chemotherapy Protocols, Camptothecin, Canada, Leucovorin, Female, Fluorouracil, Humans, Male, Middle Aged, Organoplatinum Compounds, Genes, ras, United States, Colorectal Neoplasms, Treatment Outcome, Disease-Free Survival, Angiogenesis Inhibitors, Kaplan-Meier Estimate
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