Panitumumab in metastatic colorectal cancer: The importance of tumour RAS status

Drugs

Volumn 75, Issue 7, 2015, Pages 731-748

  Peeters, Marc ^a   Karthaus, Meinolf ^b   Rivera, Fernando ^c   Terwey, Jan Henrik ^d   Douillard, Jean Yves ^e  

^a ANTWERP UNIVERSITY HOSPITAL   (Belgium)

^b Klinikum Neuperlach   (Germany)

^c HOSPITAL UNIVERSITARIO MARQUÉS DE VALDECILLA   (Spain)

^d AMGEN INC   (United States)

^e CENTRE RENÉ GAUDUCHEAU   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; MONOCLONAL ANTIBODY; PANITUMUMAB; RAS PROTEIN; TUMOR MARKER;

COLORECTAL NEOPLASMS; HUMAN; METABOLISM; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PROSPECTIVE STUDY; RANDOMIZED CONTROLLED TRIAL (TOPIC); RETROSPECTIVE STUDY;

ANTIBODIES, MONOCLONAL; BIOMARKERS, TUMOR; CLINICAL TRIALS, PHASE II AS TOPIC; CLINICAL TRIALS, PHASE III AS TOPIC; COLORECTAL NEOPLASMS; HUMANS; PROSPECTIVE STUDIES; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RAS PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RETROSPECTIVE STUDIES;

EID: 84937763357     PISSN: 00126667     EISSN: 11791950     Source Type: Journal    
DOI: 10.1007/s40265-015-0386-x     Document Type: Article

References (72)

1. Heinemann V, Douillard JY, Ducreux M, Peeters M. Targeted therapy in metastatic colorectal cancer - an example of personalised medicine in action. Cancer Treat Rev. 2013;39(6):592-601.
2. Pritchard CC, Grady WM. Colorectal cancer molecular biology moves into clinical practice. Gut. 2011;60(1):116-29.
3. Siddiqui AD, Piperdi B. KRAS mutation in colon cancer: a marker of resistance to EGFR-I therapy. Ann Surg Oncol. 2010;17(4):1168-76.
4. Benvenuti S, Sartore-Bianchi A, Di Nicolantonio F, Zanon C, Moroni M, Veronese S, et al. Oncogenic activation of the RAS/RAF signaling pathway impairs the response of metastatic colorectal cancers to anti-epidermal growth factor receptor antibody therapies. Cancer Res. 2007;67(6):2643-8.
5. Di Fiore F, Blanchard F, Charbonnier F, Le Pessot F, Lamy A, Galais MP, et al. Clinical relevance of KRAS mutation detection in metastatic colorectal cancer treated by cetuximab plus chemotherapy. Br J Cancer. 2007;96(8):1166-9.
6. Freeman DJ, Juan T, Reiner M, Hecht JR, Meropol NJ, Berlin J, et al. Association of K-ras mutational status and clinical outcomes in patients with metastatic colorectal cancer receiving panitumumab alone. Clin Colorectal Cancer. 2008;7(3):184-90.
7. ®: NCCN Guidelines™ Version 1.2008 Colon Cancer. http://www.nccn.org/. Accessed 7 Apr 2015.
8. Allegra CJ, Jessup JM, Somerfield MR, Hamilton SR, Hammond EH, Hayes DF, et al. American Society of Clinical Oncology provisional clinical opinion: testing for KRAS gene mutations in patients with metastatic colorectal carcinoma to predict response to anti-epidermal growth factor receptor monoclonal antibody therapy. J Clin Oncol. 2009;27(12):2091-6.
9. ®: NCCN Guidelines™ Version 1.2014 Colon Cancer. http://www.nccn.org/. Accessed 7 Apr 2015.
10. Douillard JY, Siena S, Cassidy J, Tabernero J, Burkes R, Barugel M, et al. Randomized, phase III trial of panitumumab with infusional fluorouracil, leucovorin, and oxaliplatin (FOLFOX4) versus FOLFOX4 alone as first-line treatment in patients with previously untreated metastatic colorectal cancer: the PRIME study. J Clin Oncol. 2010;28(31):4697-705.
11. Peeters M, Price TJ, Cervantes A, Sobrero AF, Ducreux M, Hotko Y, et al. Randomized phase III study of panitumumab with fluorouracil, leucovorin, and irinotecan (FOLFIRI) compared with FOLFIRI alone as second-line treatment in patients with metastatic colorectal cancer. J Clin Oncol. 2010;28(31):4706-13.
12. Douillard JY, Oliner KS, Siena S, Tabernero J, Burkes R, Barugel M, et al. Panitumumab-FOLFOX4 treatment and RAS mutations in colorectal cancer. N Engl J Med. 2013;369(11):1023-34.
13. Amado RG, Wolf M, Peeters M, Van Cutsem E, Siena S, Freeman DJ, et al. Wild-type KRAS is required for panitumumab efficacy in patients with metastatic colorectal cancer. J Clin Oncol. 2008;26(10):1626-34.
14. Peeters M, Oliner KS, Price TJ, Cervantes A, Sobrero AF, Ducreux M, et al. Updated analysis of KRAS/NRAS and BRAF mutations in study 20050181 of panitumumab (pmab) + FOLFIRI for 2nd-line treatment (tx) of metastatic colorectal cancer (mCRC). J Clin Oncol 2014;32(Suppl.). Abstract 3568.
15. Peeters M, Oliner K, Parker A, Siena S, Van Cutsem E, Huang J, et al. Massively parallel tumor multigene sequencing to evaluate response to panitumumab in a randomized phase 3 study of metastatic colorectal cancer. Clin Cancer Res. 2013;19(7):1902-12.
16. Patterson SD, Cohen N, Karnoub M, Truter SL, Emison E, Khambata-Ford S, et al. Prospective-retrospective biomarker analysis for regulatory consideration: white paper from the industry pharmacogenomics working group. Pharmacogenomics. 2011;12(7):939-51.
17. Wang SJ, Cohen N, Katz DA, Ruano G, Shaw PM, Spear B. Retrospective validation of genomic biomarkers - what are the questions, challenges and strategies for developing useful relationships to clinical outcomes - workshop summary. Pharmacogenomics J. 2006;6(2):82-8.
18. European Medicines Agency: committee for medicinal products for human use (CHMP) summary of opinion (post authorisation) for Vectibix (panitumumab). 2013. http://www.ema.europa.eu/docs/en-GB/document-library/Summary-of-opinion/human/000741/WC500144827.pdf. Accessed 7 Apr 2015.
19. Karnoub AE, Weinberg RA. Ras oncogenes: split personalities. Nat Rev Mol Cell Biol. 2008;9(7):517-31.
20. Janakiraman M, Vakiani E, Zeng Z, Pratilas CA, Taylor BS, Chitale D, et al. Genomic and biological characterization of exon 4 KRAS mutations in human cancer. Cancer Res. 2010;70(14):5901-11.
21. Fernández-Medarde A, Santos E. Ras in cancer and developmental diseases. Genes Cancer. 2011;2(3):344-58.
22. Bokemeyer C, Köhne CH, Ciardiello F, Lenz HJ, Heinemann V, Klinkhardt U, et al. Treatment outcome according to tumor RAS mutation status in OPUS study patients with metastatic colorectal cancer (mCRC) randomized to FOLFOX4 with/without cetuximab. J Clin Oncol 2014;32(Suppl.). Abstract 3505.
23. Van Cutsem E, Lenz HJ, Köhne CH, Heinemann V, Tejpar S, Melezinek I, et al. Fluorouracil, leucovorin, and irinotecan plus cetuximab treatment and RAS mutations in colorectal cancer. J Clin Oncol. 2015;33(7):692-700.
24. European Medicines Agency: Vectibix® (panitumumab) prescribing information. 2013. http://www.ema.europa.eu/docs/en-GB/document-library/EPAR---Product-Information/human/000741/WC500047710.pdf. Accessed 7 Apr 2015.
25. European Medicines Agency: Erbitux® (cetuximab) prescribing information. 2013. http://www.ema.europa.eu/docs/en-GB/document-library/EPAR---Product-Information/human/000558/WC500029119.pdf. Accessed 7 Apr 2015.
26. Douillard JY, Siena S, Cassidy J, Tabernero J, Burkes R, Barugel M, et al. Final results from PRIME: randomized phase III study of panitumumab with FOLFOX4 for first-line treatment of metastatic colorectal cancer. Ann Oncol. 2014;25(7):1346-55.
27. Chiappa A, Makuuchi M, Lygidakis NJ, Zbar AP, Chong G, Bertani E, et al. The management of colorectal liver metastases: expanding the role of hepatic resection in the age of multimodal therapy. Crit Rev Oncol Hematol. 2009;72(1):65-75.
28. Douillard JY, Siena S, Peeters M, Koukakis R, Terwey JH, Tabernero J. Impact of early tumour shrinkage and resection on outcomes in patients with wild-type RAS metastatic colorectal cancer. Eur J Cancer. 2015. (in press).
29. Rivera F, Karthaus M, Hecht JR, Fasola G, Canon JL, Koukakis R, et al. First-line treatment with modified FOLFOX6 (mFOLFOX6) + panitumumab (pmab) or bevacizumab (bev) in wild-type (WT) RAS metastatic colorectal carcinoma (mCRC): tumor response outcomes beyond RECIST. In: Gastrointestinal cancers symposium 2015, San Francisco. Abstract 660.
30. Peeters M, Price T, Cervantes A, Sobrero A, Ducreux M, André T, et al. Tumour shrinkage and response outcomes during second-line panitumumab (pmab) + FOLFIRI vs FOLFIRI treatment. Ann Oncol 2014;25(Suppl. 4). Abstract 7739.
31. Schwartzberg LS, Rivera F, Karthaus M, Fasola G, Canon JL, Hecht JR, et al. PEAK: A randomized, multicenter phase II study of panitumumab plus modified fluorouracil, leucovorin, and oxaliplatin (mFOLFOX6) or bevacizumab plus mFOLFOX6 in patients with previously untreated, unresectable, wild-type KRAS exon 2 metastatic colorectal cancer. J Clin Oncol. 2014;32(21):2240-7.
32. Schwartzberg LS, Rivera F, Karthaus M, Fasola G, Canon JL, Yu H, et al. Analysis of KRAS/NRAS mutations in PEAK: a randomized phase II study of FOLFOX6 plus panitumumab (pmab) or bevacizumab (bev) as first-line treatment (tx) for wild-type (WT) KRAS (exon 2) metastatic colorectal cancer (mCRC). J Clin Oncol 2013;31(Suppl.). Abstract 3631.
33. Abad A, Massuti B, Grávalos C, Escudero P, Guillén-Ponce C, Manzano JL, et al, On behalf of the Spanish Cooperative Group for the Treatment of Digestive Tumors (TTD). Phase II trial of panitumumab plus FOLFOX4 or FOLFIRI in subjects with KRAS wild-type colorectal cancer and liver-limited disease: the PLANET study. J Clin Oncol 2014;32(Suppl.). Abstract 3560.
34. Köhne CH, Hofheinz R, Mineur L, Letocha H, Greil R, Thaler J, et al. First-line panitumumab plus irinotecan/5-fluorouracil/leucovorin treatment in patients with metastatic colorectal cancer. J Cancer Res Clin Oncol. 2012;138(1):65-72.
35. Karthaus M, Hofheinz R, Mineur L, Greil R, Thaler J, Fernebro E, et al. Impact of tumour RAS/BRAF status on efficacy of first-line panitumumab + FOLFIRI in patients (pts) with metastatic colorectal cancer (mCRC). Ann Oncol 2014;25(Suppl. 4). Abstract 5672.
36. Peeters M, Price TJ, Cervantes A, Sobrero AF, Ducreux M, Hotko Y, et al. Final results from a randomized phase 3 study of FOLFIRI ± panitumumab for second-line treatment of metastatic colorectal cancer. Ann Oncol. 2014;25(1):107-16.
37. Peeters M, Price T, Cervantes A, Sobrero A, Ducreux M, André T, et al. Impact of baseline covariates and prior therapy on the efficacy of second-line panitumumab (pmab) + FOLFIRI vs FOLFIRI treatment. Ann Oncol 2014;25(Suppl. 4). Abstract 7798.
38. Hecht JR, Cohn AL, Dakhil SR, Saleh MN, Piperdi B, Cline-Burkhardt VJM, et al. SPIRITT (study 20060141): a randomized phase II study of FOLFIRI with either panitumumab (pmab) or bevacizumab (bev) as second-line treatment (tx) in patients (pts) with wild-type (WT) KRAS metastatic colorectal cancer (mCRC). J Clin Oncol 2013;31(Suppl. 4). Abstract 454.
39. Van Cutsem E, Peeters M, Siena S, Humblet Y, Hendlisz A, Neyns B, et al. Open-label phase III trial of panitumumab plus best supportive care compared with best supportive care alone in patients with chemotherapy-refractory metastatic colorectal cancer. J Clin Oncol. 2007;25(13):1658-64.
40. Van Cutsem E, Siena S, Humblet Y, Canon JL, Maurel J, Bajetta E, et al. An open-label, single-arm study assessing safety and efficacy of panitumumab in patients with metastatic colorectal cancer refractory to standard chemotherapy. Ann Oncol. 2008;19(1):92-8.
41. Price TJ, Peeters M, Kim TW, Li J, Cascinu S, Ruff P, et al. Panitumumab versus cetuximab in patients with chemotherapy-refractory wild-type KRAS exon 2 metastatic colorectal cancer (ASPECCT): a randomised, multicentre, open-label, non-inferiority phase 3 study. Lancet Oncol. 2014;15(6):569-79.
42. Patterson SD, Peeters M, Siena S, Van Cutsem E, Humblet Y, Van Laethem JL, et al. Comprehensive analysis of KRAS and NRAS mutations as predictive biomarkers for single agent panitumumab (pmab) response in a randomized, phase III metastatic colorectal cancer (mCRC) study (20020408). J Clin Oncol 31(Suppl.). Abstract 3617.
43. Bokemeyer C, Bondarenko I, Hartmann JT, de Braud F, Schuch G, Zubel A, et al. Efficacy according to biomarker status of cetuximab plus FOLFOX-4 as first-line treatment for metastatic colorectal cancer: the OPUS study. Ann Oncol. 2011;22(7):1535-46.
44. Lacouture ME. Mechanisms of cutaneous toxicities to EGFR inhibitors. Nat Rev Cancer. 2006;6(10):803-12.
45. Lacouture ME, Mitchell EP, Piperdi B, Pillai MV, Shearer H, Iannotti N, et al. Skin toxicity evaluation protocol with panitumumab (STEPP), a phase II, open-label, randomized trial evaluating the impact of a pre-emptive skin treatment regimen on skin toxicities and quality of life in patients with metastatic colorectal cancer. J Clin Oncol. 2010;28(8):1351-7.
46. Heinemann V, von Weikersthal LF, Decker T, Kiani A, Vehling-Kaiser U, Al-Batran SE, et al. FOLFIRI plus cetuximab versus FOLFIRI plus bevacizumab as first-line treatment for patients with metastatic colorectal cancer (FIRE-3): a randomised, open-label, phase 3 trial. Lancet Oncol. 2014;15(10):1065-75.
47. Heinemann V, Modest DP, Fischer von Weikersthal L, Decker T, Kiani A, Vehling-Kaiser U, et al. Independent radiological evaluation of objective response, early tumour shrinkage, and depth of response in FIRE-3 (AIO KRK-0306). Ann Oncol. 2014;25(Suppl. 2):ii117 (Abstract O-0030).
48. Venook AP, Niedzwiecki D, Lenz HJ, Innocenti F, Mahoney MR, O'Neil BH, et al. CALGB/SWOG 80405: Phase III trial of irinotecan/5-FU/leucovorin (FOLFIRI) or oxaliplatin/5-FU/leucovorin (mFOLFOX6) with bevacizumab (BV) or cetuximab (CET) for patients (pts) with KRAS wild-type (wt) untreated metastatic adenocarcinoma of the rectum or colon (MCRC). J Clin Oncol 2014;32(Suppl.):5S. (Abstract LBA3).
49. Lenz H, Niedzwiecki D, Innocenti F, Blanke C, Mahoney MR, O'Neil BH, et al. CALGB/SWOG 80405: Phase III trial of irinotecan/5-FU/leucovorin (FOLFIRI) or oxaliplatin/5-FU/leucovorin (mFOLFOX6) with bevacizumab (BV) or cetuximab (CET) for patients (pts) with expanded ras analyses untreated metastatic adenocarcinoma of the colon or rectum (mCRC). Ann Oncol 25(Suppl. 2). Abstract 501O.
50. Peeters M, Douillard JY, Siena S, Price T, Tabernero J, Sidhu R, et al. Impact of post-progression anti-vascular endothelial growth factor-containing therapy on survival in patients with metastatic colorectal cancer: data from the PRIME study. Eur J Cancer. 2013;49(Suppl. 4):S18 (Abstract MC13-0024).
51. van Krieken H, Tol J. Setting future standards for KRAS testing in colorectal cancer. Pharmacogenomics. 2009;10(1):1-3.
52. European Society of Pathology: colon external quality assessment scheme 2014. http://kras.eqascheme.org/. Accessed 7 Apr 2015.
53. van Krieken JH, Siebers AG, Normanno N. European consensus conference for external quality assessment in molecular pathology. Ann Oncol. 2013;24(8):1958-63.
54. Shankaran V, Bentrem DJ, Mulcahy MF, Bennett CL, Benson A, III. Economic implications of KRAS testing in metastatic colorectal cancer (mCRC). In: Gastrointestinal cancers symposium 2009, San Francisco. Abstract 298.
55. Mancl EE, Kolesar JM, Vermeulen LC. Clinical and economic value of screening for Kras mutations as predictors of response to epidermal growth factor receptor inhibitors. Am J Health Syst Pharm. 2009;66(23):2105-12.
56. Vijayaraghavan A, Efrusy MB, Goke B, Kirchner T, Santas CC, Goldberg RM. Cost-effectiveness of KRAS testing in metastatic colorectal cancer patients in the United States and Germany. Int J Cancer. 2012;131(2):438-45.
57. Gallagher J, BBC News. Cancer cost 'crisis' warning from oncologists. 2011. http://www.bbc.co.uk/news/health-15032862. Accessed 7 Apr 2015.
58. Königsberg R, Hulla W, Klimpfinger M, Reiner-Concin A, Steininger T, Buchler W, et al. Clinical and economic aspects of KRAS mutational status as predictor for epidermal growth factor receptor inhibitor therapy in metastatic colorectal cancer patients. Oncology. 2011;81(5-6):359-64.
59. Blank PR, Moch H, Szucs TD, Schwenkglenks M. KRAS and BRAF mutation analysis in metastatic colorectal cancer: a cost-effectiveness analysis from a Swiss perspective. Clin Cancer Res. 2011;17(19):6338-46.
60. De Roock W, De Vriendt V, Normanno N, Ciardiello F, Tejpar S. KRAS, BRAF, PIK3CA, and PTEN mutations: implications for targeted therapies in metastatic colorectal cancer. Lancet Oncol. 2011;12(6):594-603.
61. Sartore-Bianchi A, Martini M, Molinari F, Veronese S, Nichelatti M, Artale S, et al. PIK3CA mutations in colorectal cancer are associated with clinical resistance to EGFR-targeted monoclonal antibodies. Cancer Res. 2009;69(5):1851-7.
62. Sood A, McClain D, Maitra R, Basu-Mallick A, Seetharam R, Kaubisch A, et al. PTEN gene expression and mutations in the PIK3CA gene as predictors of clinical benefit to anti-epidermal growth factor receptor antibody therapy in patients with KRAS wild-type metastatic colorectal cancer. Clin Colorectal Cancer. 2012;11(2):143-50.
63. Mao C, Liao RY, Chen Q. Loss of PTEN expression predicts resistance to EGFR-targeted monoclonal antibodies in patients with metastatic colorectal cancer. Br J Cancer. 2010;102(5):940.
64. Razis E, Briasoulis E, Vrettou E, Skarlos DV, Papamichael D, Kostopoulos I, et al. Potential value of PTEN in predicting cetuximab response in colorectal cancer: an exploratory study. BMC Cancer. 2008;8:234.
65. Khambata-Ford S, Garrett CR, Meropol NJ, Basik M, Harbison CT, Wu S, et al. Expression of epiregulin and amphiregulin and K-ras mutation status predict disease control in metastatic colorectal cancer patients treated with cetuximab. J Clin Oncol. 2007;25(22):3230-7.
66. Jacobs B, De Roock W, Piessevaux H, Van Oirbeek R, Biesmans B, De Schutter J, et al. Amphiregulin and epiregulin mRNA expression in primary tumors predicts outcome in metastatic colorectal cancer treated with cetuximab. J Clin Oncol. 2009;27(30):5068-74.
67. Baker JB, Dutta D, Watson D, Maddala T, Munneke BM, Shak S, et al. Tumour gene expression predicts response to cetuximab in patients with KRAS wild-type metastatic colorectal cancer. Br J Cancer. 2011;104(3):488-95.
68. Taniguchi K, Uchida J, Nishino K, Kumagai T, Okuyama T, Okami J, et al. Quantitative detection of EGFR mutations in circulating tumor DNA derived from lung adenocarcinomas. Clin Cancer Res. 2011;17(24):7808-15.
69. Higgins MJ, Jelovac D, Barnathan E, Blair B, Slater S, Powers P, et al. Detection of tumor PIK3CA status in metastatic breast cancer using peripheral blood. Clin Cancer Res. 2012;18(12):3462-9.
70. Misale S, Yaeger R, Hobor S, Scala E, Janakiraman M, Liska D, et al. Emergence of KRAS mutations and acquired resistance to anti-EGFR therapy in colorectal cancer. Nature. 2012;486(7404):532-6.
71. Diaz LA Jr, Williams RT, Wu J, Kinde I, Hecht JR, Berlin J, et al. The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers. Nature. 2012;486(7404):537-40.
72. Newhall K, Price T, Peeters M, Kim TW, Li J, Cascinu S, et al. Frequency of S492R mutations in the epidermal growth factor receptor: analysis of plasma DNA from metastatic colorectal cancer patients treated with panitumumab or cetuximab monotherapy; 16th World Congress on Gastrointestinal Cancer 2014. Ann Oncol 25(Suppl. 2): ii109. (Abstract O-0011).