Efficacy and safety of chronomodulated irinotecan, oxaliplatin, 5-fluorouracil and leucovorin combination as first- or second-line treatment against metastatic colorectal cancer: Results from the International EORTC 05011 Trial.

FOLFIRINOX chemotherapy chronotherapy circadian colorectal cancer

Journal

International journal of cancer
ISSN: 1097-0215
Titre abrégé: Int J Cancer
Pays: United States
ID NLM: 0042124

Informations de publication

Date de publication:
15 May 2021
Historique:
revised: 20 10 2020
received: 22 07 2020
accepted: 11 11 2020
medline: 4 12 2020
pubmed: 4 12 2020
entrez: 3 12 2020
Statut: ppublish

Résumé

The triplet combination of irinotecan, oxaliplatin and fluorouracil is an active frontline regimen in metastatic colorectal cancer, but scarce data exist on its use as salvage treatment. We aimed at assessing its safety and efficacy profiles with its circadian-based administration (chronoIFLO5) as either first- or second-line treatment, within the time-finding EORTC 05011 trial. Five-day chronoIFLO5 was administered every 3 weeks in patients with PS 0, 1 or 2. It consisted of chronomodulated irinotecan (180 mg/sqm), oxaliplatin (80 mg/sqm) and fluorouracil-leucovorin (2800 and 1200 mg/sqm, respectively). For our study, toxicity and antitumour activity were evaluated separately in first- and second-line settings. Primary endpoints included Grade 3-4 toxicity rates, best objective response rate (ORR), progression-free survival (PFS) and overall survival (OS). One-hundred forty-nine and 44 patients were treated in first-line and second-line settings, respectively, with a total of 1138 cycles with median relative dose intensities of about 90%. Demographics were comparable in the two groups. Thirty-six (24.7%) and 10 (22.2%) patients experienced at least one episode of severe toxicity in first line and second line, respectively. Frontline chronoIFLO5 yielded an ORR of 62.3% [95% CI: 54.2-70.4] and resulted in median PFS and OS of 8.7 months [7.5-9.9] and 19.9 months [15.4-24.5]. Corresponding figures in second line were 37.5% [22.5-52.5], 6.7 months [4.8-8.9] and 16.3 months [11.8-20.8]. International and prospective evaluation revealed the favourable safety and efficacy profiles of chronoIFLO5, both as frontline and as salvage treatment against metastatic colorectal cancer. In particular, encouraging activity in second line was observed, with limited haematological toxicity.

Identifiants

pubmed: 33270911
doi: 10.1002/ijc.33422
pmc: PMC8048520
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

2512-2521

Subventions

Organisme : ARTBC International
ID : ad hoc

Informations de copyright

© 2020 The Authors. International Journal of Cancer published by John Wiley & Sons Ltd on behalf of UICC.

Références

Ferlay J, Colombet M, Soerjomataram I, et al. Cancer incidence and mortality patterns in Europe: estimates for 40 countries and 25 major cancers in 2018. Eur J Cancer. 2018;103:356-387.
Dekker E, Tanis PJ, Vleugels JLA, Kasi PM, Wallace MB. Colorectal cancer. Lancet. 2019;394:1467-1480.
Adam R, Kitano Y. Multidisciplinary approach of liver metastases from colorectal cancer. Ann Gastroenterol Surg. 2019;3:50-56.
Loupakis F, Cremolini C, Masi G, et al. Initial therapy with FOLFOXIRI and bevacizumab for metastatic colorectal cancer. N Engl J Med. 2014;371:1609-1618.
Gruenberger T, Bridgewater J, Chau I, et al. Bevacizumab plus mFOLFOX-6 or FOLFOXIRI in patients with initially unresectable liver metastases from colorectal cancer: the OLIVIA multinational randomised phase II trial. Ann Oncol. 2015;26:702-708.
Deyme L, Barbolosi D, Gattacceca F. Population pharmacokinetics of FOLFIRINOX: a review of studies and parameters. Cancer Chemother Pharmacol. 2019;83:27-42.
Dallmann R, Okyar A, Levi F. Dosing-time makes the poison: circadian regulation and pharmacotherapy. Trends Mol Med. 2016;22:430-445.
Innominato PF, Roche VP, Palesh OG, Ulusakarya A, Spiegel D, Levi FA. The circadian timing system in clinical oncology. Ann Med. 2014;46:191-207.
Ruben MD, Smith DF, FitzGerald GA, Hogenesch JB. Dosing time matters. Science. 2019;365:547-549.
Garufi C, Torsello A, Tumolo S, et al. Cetuximab plus chronomodulated irinotecan, 5-fluorouracil, leucovorin and oxaliplatin as neoadjuvant chemotherapy in colorectal liver metastases: POCHER trial. Br J Cancer. 2010;103:1542-1547.
Gholam D, Giacchetti S, Brezault-Bonnet C, et al. Chronomodulated irinotecan, oxaliplatin, and leucovorin-modulated 5-fluorouracil as ambulatory salvage therapy in patients with irinotecan- and oxaliplatin-resistant metastatic colorectal cancer. Oncologist. 2006;11:1072-1080.
Garufi C, Bria E, Vanni B, Zappala AM, Sperduti I, Terzoli E. A phase II study of irinotecan plus chronomodulated oxaliplatin, 5-fluorouracil and folinic acid in advanced colorectal cancer patients. Br J Cancer. 2003;89:1870-1875.
Lévi F, Karaboué A, Gorden L, et al. Cetuximab and circadian chronomodulated chemotherapy as salvage treatment for metastatic colorectal cancer (mCRC): safety, efficacy and improved secondary surgical resectability. Cancer Chemother Pharmacol. 2011;67:339-348.
Innominato PF, Ballesta A, Huang Q, et al. Sex-dependent least toxic timing of irinotecan combined with chronomodulated chemotherapy for metastatic colorectal cancer: randomized multicenter EORTC 05011 trial. Cancer Med. 2020;9:4148-4159.
Rickham PP. Human experimentation. Code of ethics of the World Medical Association. Br Med J. 1964;2(5402):177.
Hill RJW, Innominato PF, Lévi F, Ballesta A. Optimizing circadian drug infusion schedules towards personalized cancer chronotherapy. PLoS Comput Biol. 2020;16:e1007218.
Souglakos J, Androulakis N, Syrigos K, et al. FOLFOXIRI (folinic acid, 5-fluorouracil, oxaliplatin and irinotecan) vs FOLFIRI (folinic acid, 5-fluorouracil and irinotecan) as first-line treatment in metastatic colorectal cancer (MCC): a multicentre randomised phase III trial from the Hellenic Oncology Research Group (HORG). Br J Cancer. 2006;94:798-805.
Falcone A, Ricci S, Brunetti I, et al. Phase III trial of infusional fluorouracil, leucovorin, oxaliplatin, and irinotecan (FOLFOXIRI) compared with infusional fluorouracil, leucovorin, and irinotecan (FOLFIRI) as first-line treatment for metastatic colorectal cancer: the Gruppo Oncologico Nord Ovest. J Clin Oncol. 2007;25:1670-1676.
Ychou M, Viret F, Kramar A, et al. Tritherapy with fluorouracil/leucovorin, irinotecan and oxaliplatin (FOLFIRINOX): a phase II study in colorectal cancer patients with non-resectable liver metastases. Cancer Chemother Pharmacol. 2008;62:195-201.
Martinez J, Martin C, Chacon M, et al. Irinotecan, oxaliplatin plus bolus 5-fluorouracil and low dose folinic acid every 2 weeks: a feasibility study in metastatic colorectal cancer patients. Am J Clin Oncol. 2006;29:45-51.
Calvo E, Cortés J, Rodríguez J, et al. Irinotecan, oxaliplatin, and 5-fluorouracil/leucovorin combination chemotherapy in advanced colorectal carcinoma: a phase II study. Clin Colorectal Cancer. 2002;2:104-110.
Comella P, Casaretti R, De Rosa V, et al. Oxaliplatin plus irinotecan and leucovorin-modulated 5-fluorouracil triplet regimen every other week: a dose-finding study in patients with advanced gastrointestinal malignancies. Ann Oncol. 2002;13:1874-1881.
McWilliams RR, Goetz MP, Morlan BW, et al. Phase II trial of oxaliplatin/irinotecan/5-fluorouracil/leucovorin for metastatic colorectal cancer. Clin Colorectal Cancer. 2007;6:516-521.
Price TJ, Tang M, Gibbs P, et al. Targeted therapy for metastatic colorectal cancer. Expert Rev Anticancer Ther. 2018;18:991-1006.
Stathopoulos GP, Rigatos SK, Stathopoulos JG, Xynotroulas JP, Dimou E. Efficacy and tolerability of oxaliplatin plus irinotecan 5-fluouracil and leucovorin regimen in advanced stage colorectal cancer patients pretreated with irinotecan 5-fluouracil and leucovorin. Am J Clin Oncol. 2005;28:565-569.
Fernandes GDS, Braghiroli MI, Artioli M, et al. Combination of irinotecan, oxaliplatin and 5-fluorouracil as a rechallenge regimen for heavily pretreated metastatic colorectal cancer patients. J Gastrointest Cancer. 2018;49:470-475.
Montagnani F, Chiriatti A, Turrisi G, Francini G, Fiorentini G. A systematic review of FOLFOXIRI chemotherapy for the first-line treatment of metastatic colorectal cancer: improved efficacy at the cost of increased toxicity. Colorectal Dis. 2011;13:846-852.
Tournigand C, André T, Achille E, et al. FOLFIRI followed by FOLFOX6 or the reverse sequence in advanced colorectal cancer: a randomized GERCOR study. J Clin Oncol. 2004;22:229-237.
Galvano A, Incorvaia L, Badalamenti G, et al. How to deal with second line dilemma in metastatic colorectal cancer? A systematic review and meta-analysis. Cancers (Basel). 2019;11(8):1189. https://doi.org/10.3390/cancers11081189.
Kim SY, Kim TW. Current challenges in the implementation of precision oncology for the management of metastatic colorectal cancer. ESMO Open. 2020;5:e000634. https://doi.org/10.1136/esmoopen-2019-000634.
Cremolini C, Antoniotti C, Rossini D, et al. Upfront FOLFOXIRI plus bevacizumab and reintroduction after progression versus mFOLFOX6 plus bevacizumab followed by FOLFIRI plus bevacizumab in the treatment of patients with metastatic colorectal cancer (TRIBE2): a multicentre, open-label, phase 3, randomised, controlled trial. Lancet Oncol. 2020;21:497-507.
Assenat E, Desseigne F, Thezenas S, et al. Cetuximab plus FOLFIRINOX (ERBIRINOX) as first-line treatment for unresectable metastatic colorectal cancer: a phase II trial. Oncologist. 2011;16:1557-1564.
Chaix M, Vincent J, Lorgis V, Ghiringhelli F. FOLFIRINOX bevacizumab is a promising therapy for chemorefractory metastatic colorectal cancer. Oncology. 2014;87:148-158.
Adam R, Yi B, Innominato PF, et al. Resection of colorectal liver metastases after second-line chemotherapy: is it worthwhile? A LiverMetSurvey analysis of 6415 patients. Eur J Cancer. 2017;78:7-15.
Giacchetti S, Bjarnason G, Garufi C, et al. Phase III trial comparing 4-day chronomodulated therapy versus 2-day conventional delivery of fluorouracil, leucovorin, and oxaliplatin as first-line chemotherapy of metastatic colorectal cancer: the European Organisation for Research and Treatment of Cancer Chronotherapy Group. J Clin Oncol. 2006;24:3562-3569.
Conroy T, Desseigne F, Ychou M, et al. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N Engl J Med. 2011;364:1817-1825.
Tong H, Fan Z, Liu B, Lu T. The benefits of modified FOLFIRINOX for advanced pancreatic cancer and its induced adverse events: a systematic review and meta-analysis. Sci Rep. 2018;8:8666.
Sharma MR, Joshi SS, Karrison TG, et al. A UGT1A1 genotype-guided dosing study of modified FOLFIRINOX in previously untreated patients with advanced gastrointestinal malignancies. Cancer. 2019;125:1629-1636.
Innominato P, Komarzynski S, Karaboue A, et al. Home-based e-health platform for multidimensional telemonitoring of symptoms, body weight, sleep, and circadian activity: relevance for chronomodulated administration of irinotecan, fluorouracil-leucovorin, and oxaliplatin at home-results from a pilot study. JCO Clin Cancer Inform. 2018;2:1-15.
Alexander JL, Wilson ID, Teare J, Marchesi JR, Nicholson JK, Kinross JM. Gut microbiota modulation of chemotherapy efficacy and toxicity. Nat Rev Gastroenterol Hepatol. 2017;14:356-365.

Auteurs

Pasquale F Innominato (PF)

North Wales Cancer Centre, Ysbyty Gwynedd, Betsi Cadwaladr University Health Board, Bangor, UK.
Cancer Chronotherapy Team, Cancer Research Centre, Division of Biomedical Sciences, Warwick Medical School, Coventry, UK.
UPR "Chronotherapy, Cancers and Transplantation", Faculty of Medicine, Paris-Saclay University, Villejuif, France.

Abdoulaye Karaboué (A)

UPR "Chronotherapy, Cancers and Transplantation", Faculty of Medicine, Paris-Saclay University, Villejuif, France.
Medical Oncology Unit, GHI Le Raincy-Montfermeil, Montfermeil, France.

Christian Focan (C)

Department of Oncology, CHC-MontLegia, Groupe Santé CHC-Liège, Liège, Belgium.

Philippe Chollet (P)

Clinical and Translational Research Division, Jean Perrin Comprehensive Cancer Centre, Clermont-Ferrand, France.

Sylvie Giacchetti (S)

UPR "Chronotherapy, Cancers and Transplantation", Faculty of Medicine, Paris-Saclay University, Villejuif, France.
Department of Oncology, Saint Louis Hospital, Public Hospitals of Paris (AP-HP), Paris, France.

Mohamed Bouchahda (M)

UPR "Chronotherapy, Cancers and Transplantation", Faculty of Medicine, Paris-Saclay University, Villejuif, France.
Medical Oncology Unit, Clinique du Mousseau, Evry, France.
Medical Oncology Unit, Clinique Saint Jean L'Ermitage, Melun, France.
Chronotherapy Unit, Department of Medical Oncology, Paul Brousse Hospital, Public Hospitals of Paris (AP-HP), Villejuif, France.

Ayhan Ulusakarya (A)

UPR "Chronotherapy, Cancers and Transplantation", Faculty of Medicine, Paris-Saclay University, Villejuif, France.
Chronotherapy Unit, Department of Medical Oncology, Paul Brousse Hospital, Public Hospitals of Paris (AP-HP), Villejuif, France.

Angela Torsello (A)

Division of Medical Oncology, San Giovanni- Addolorata Hospital, Rome, Italy.

René Adam (R)

UPR "Chronotherapy, Cancers and Transplantation", Faculty of Medicine, Paris-Saclay University, Villejuif, France.
Hepatobiliary Centre, Paul Brousse Hospital, Public Hospitals of Paris (AP-HP), Villejuif, France.

Francis A Lévi (FA)

Cancer Chronotherapy Team, Cancer Research Centre, Division of Biomedical Sciences, Warwick Medical School, Coventry, UK.
UPR "Chronotherapy, Cancers and Transplantation", Faculty of Medicine, Paris-Saclay University, Villejuif, France.
Hepatobiliary Centre, Paul Brousse Hospital, Public Hospitals of Paris (AP-HP), Villejuif, France.

Carlo Garufi (C)

Division of Medical Oncology, San Camillo Forlanini Hospital, Rome, Italy.

Classifications MeSH