Have a personal or library account? Click to login
KRAS, NRAS, BRAF, HER2 and microsatellite instability in metastatic colorectal cancer – practical implications for the clinician Cover

KRAS, NRAS, BRAF, HER2 and microsatellite instability in metastatic colorectal cancer – practical implications for the clinician

Open Access
|Sep 2019

References

  1. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics. CA Cancer J Clin 2002; 2005: 74-108. doi: 10.3322/canjclin.55.2.74
  2. Moghimi-Dehkordi B, Safaee A. An overview of colorectal cancer survival rates and prognosis in Asia. World J Gastrointest Oncol 2012; 4: 71-5. doi: 10.4251/wjgo.v4.i4.71
  3. Wolpin BM, Mayer RJ. Systemic treatment of colorectal cancer. Gastroenterology 2008; 134: 1296-310. doi: 10.1053/j.gastro.2008.02.098
  4. Kelly H, Goldberg RM. Systemic therapy for metastatic colorectal cancer: current options, current evidence. J Clin Oncol 2005; 23: 4553-60. doi: 10.1200/JCO.2005.17.749
  5. Bos JL, Fearon ER, Hamilton SR, Verlaan-de Vries M, van Boom JH, van der Eb AJ, et al. Prevalence of RAS mutations in human colorectal cancers. Nature 1987; 327: 293-7. doi: 10.1038/327293a0
  6. Finkelstein SD, Sayegh R, Christensen S, Swalsky PA. Genotypic classification of colorectal adenocarcinoma. Cancer 1993; 71: 3827-38. 10.1002/1097-0142(19930615)71:12<3827::aid-cncr2820711207>3.0.co;2-n
  7. Boughdady IS, Kinsella AR, Haboubi NY, Schofield PF. K-ras gene mutations in adenomas and carcinomas of the colon. Surg Oncol 1992; 1: 275-82. doi: 10.1016/0960-7404(92)90087-2
  8. Heinemann V, Stintzing S, Kirchner T, Boeck S, Jung A. Clinical relevance of EGFR- and KRAS-status in colorectal cancer patients treated with monoclonal antibodies directed against the EGFR. Cancer Treat Rev 2009; 35: 262-71. doi: 10.1016/j.ctrv.2008.11.005
  9. Gong J, Cho M, Sy M, Salgia R, Fakih M. Molecular profiling of metastatic colorectal tumors using next-generation sequencing: a single-institution experience. Oncotarget 2017; 8: 42198-213. doi: 10.18632/oncotarget.15030
  10. Ibrahim T, Saer-Ghorra C, Trak-Smayra V, Nadiri S, Yazbeck C, Baz M, et al. Molecular characteristics of colorectal cancer in a Middle Eastern population in a single institution. Ann Saudi Med 2018; 38: 251-9. doi: 10.5144/0256-4947.2018.251
  11. Abubaker J, Bavi P, Al-Haqawi W, Sultana M, Al-Harbi S, Al-Sanea N, et al. Prognostic significance of alterations in KRAS isoforms KRAS-4A/4B and KRAS mutations in colorectal carcinoma. J Pathol 2009; 219: 435-45. doi: 10.1002/path.2625
  12. Zahrani A, Kandil M, Badar T, Abdelsalam M, Al-Faiar A, Ismail A. Clinico-pathological study of K-ras mutations in colorectal tumors in Saudi Arabia. Tumori 2014; 100: 75-9. doi: 10.1700/1430.15819
  13. Murtaza B, Bibi A, Rashid M, Khan Y, Chaudri M, Shakoori A. Spectrum of KRAS mutations in Pakistani colorectal cancer patients. Braz J Med Biol Res 2014; 47: 35-41. doi: 10.1590/1414-431X20133046
  14. Segal G, Liebermann N, Klang S, Siegelmann-Daniel N, Beit-Or A, Klien B, et al. Identification of KRAS mutations in colorectal cancer patients in Israel. Harefuah 2011; 150: 447-50.
  15. Marchoudi N, Joutei HAH, Jouali F, Fekkak J, Rhaissi H. Distribution of KRAS and BRAF mutations in Moroccan patients with advanced colorectal cancer. Pathol Biol 2013; 61: 273-6. doi: 10.1016/j.patbio.2013.05.004
  16. Chaiyapan W, Duangpakdee P, Boonpipattanapong T, Kanngern S, Sangkhatthat S. Somatic mutations of K-RAS and BRAF in Thai colorectal cancer and their prognostic value. Asian Pac J Cancer Prev 2013; 14: 329-32. doi: 10.7314/apjcp.2013.14.1.329
  17. Kafatos G, Niepel D, Lowe K, Jenkins-Anderson S, Westhead H, Garawin T, et al. RAS mutation prevalence among patients with metastatic colorectal cancer : a meta-analysis of real-world data. Biomark Med 2017; 11: 751-60. doi: 10.2217/bmm-2016-0358
  18. Kwak MS, Cha JM, Cho YH, Kim SH, Yoon JY, Jeon JW, et al. Clinical predictors for KRAS codon 13 mutations in patients with colorectal cancer. J Clin Gastroenterol 2018; 52: 431-6. doi: 10.1097/MCG.0000000000000809
  19. Dobre M, Dinu DE, Panaitescu E, Birla RE, Iosif CI, Boeriu M, et al. KRAS gene mutations – prognostic factor in colorectal cancer? Rom J Morphol Embryol 2015; 56(2 Suppl): 671-8. PMID: 26429158
  20. Van Cutsem, Köhne CH, Hitre E, Zaluski J, Chang Chien CR, Makhson A, et al. Cetuximab and chemotherapy as initial treatment for metastatic colorectal cancer. N Engl J Med 2009; 360: 1408-17. doi: 10.1056/NEJMoa0805019
  21. 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: 1535-46. doi: 10.1093/annonc/mdq632
  22. Pentheroudakis G, Kotoula V, De Roock W, Kouvatseas G, Papakostas P, Makatsoris T, et al. Biomarkers of benefit from cetuximab-based therapy in metastatic colorectal cancer: interaction of EGFR ligand expression with RAS/ RAF, PIK3CA genotypes. BMC Cancer 2013; 13: 49. doi: 10.1186/1471-2407-13-49
  23. Mao C, Yang ZY, Hu XF, Chen Q, Tang JL. PIK3CA exon 20 mutations as a potential biomarker for resistance to anti- EGFR monoclonal antibodies in KRAS wild-type metastatic colorectal cancer: a systematic review and meta-analysis. Ann Oncol 2012; 23: 1518-25. doi: 10.1093/annonc/mdr464
  24. Brulé SY, Jonker DJ, Karapetis CS, O’Callaghan CJ, Moore MJ, Wong R, et al. Location of colon cancer (right-sided versus left-sided) as a prognostic factor and a predictor of benefit from cetuximab in NCIC CO.17. Eur J Cancer 2015; 51: 1405-14. doi: 10.1016/j.ejca.2015.03.015
  25. Petrelli F, Tomasello G, Borgonov K, Ghidini M, Turati L, Dallera P, et al. Prognostic survival associated with left-sided vs right-sided colon cancer. A systematic review and meta-analysis. JAMA Oncol 2016; 3: 211-19. doi: 10.1001/jamaoncol.2016.4227
  26. Tejpar S, Celik I, Schlichting M, Sartorius U, Bokemeyer C, Van Cutsem E. Association of KRAS G13D tumor mutations with outcome in patients with metastatic colorectal cancer treated with first-line chemotherapy with or without cetuximab. J Clin Oncol 2012; 30: 3570-7. doi: 10.1200/ JCO.2012.42.2592
  27. Chen J, Ye Y, Sun H, Shi G. Association between KRAS codon 13 mutations and clinical response to anti-EGFR treatment in patients with metastatic colorectal cancer: results from a meta-analysis. Cancer Chemother Pharmacol 2013; 71: 265-72. doi: 10.1007/s00280-012-2005-9
  28. Peeters M, Douillard JY, Van Cutsem E, Siena S, Zhang K, Williams R, et al. Mutant KRAS codon 12 and 13 alleles in patients with metastatic colorectal cancer: assessment as prognostic and predictive biomarkers of response to panitumumab. J Clin Oncol 2013; 31: 759-65. doi: 10.1200/ JCO.2012.45.1492
  29. Andreyev HJ, Norman AR, Cunningham D, Oates JR, Clarke PA. Kirsten Ras mutations in patients with colorectal cancer: the multicenter ‘‘RASCAL” study. J Natl Cancer Inst 1998; 90: 675-84. doi: 10.1093/jnci/90.9.675
  30. Roth AD, Tejpar S, Delorenzi M, Yan P, Fiocca R, Klingbiel D, et al. Prognostic role of KRAS and BRAF in stage II and III resected colon cancer: results of the translational study onthe PETACC-3, EORTC 40993, SAKK 60-00 trial. J Clin Oncol 2010; 28: 466-74. doi: 10.1200/JCO.2009.23.3452
  31. Ogino S, Meyerhardt JA, Irahara N, Niedzwiecki D, Hollis D, Saltz LB, et al. KRAS mutation in stage III colon cancer and clinical outcome following intergroup trial CALGB 89803. Clin Cancer Res 2009; 15: 7322-9. doi: 10.1158/1078-0432.CCR-09-1570
  32. Karapetis CS, Khambata-Ford S, Jonker DJ, O’Callaghan CJ, Tu D, Tebbutt NC, et al. K-ras mutations and benefit from cetuximab in advanced colorectal cancer. N Engl J Med 2008; 359: 1757-65. doi: 10.1056/NEJMoa0804385
  33. De Roock W, Claes B, Bernasconi D, De Schutter J, Biesmans B, Fountzilas G, et al. Effects of KRAS, BRAF, NRAS, and PIK3CA mutations on the efficacy of cetuximab plus chemotherapy in chemotherapy-refractory metastatic colorectal cancer: a retrospective consortium analysis. Lancet Oncol 2010; 11: 753-62. doi: 10.1016/S1470-2045(10)70130-3
  34. Schiripa M, Cremolini C, Loupakis F, Morvillo M, Bergamo F, Zoratto F, et al. Role of NRAS mutations as prognostic and predictive markers in metastatic colorectal cancer. Int J Cancer 2015; 136: 83-90. doi: 10.1002/ijc.28955
  35. Au HJ, Karapetis CS, O’Callaghan CJ, Tu D, Moore MJ, Zalcberg JR, et al. Health-related quality of life in patients with advanced colorectal cancer treated with cetuximab: Overall and KRAS-specific results of the NCIC CTG and AGITG CO.17 Trial. J Clin Oncol 2009; 27: 1822-8. doi: 10.1200/ JCO.2008.19.6048
  36. Matallanas D, Birtwistle M, Romano D, Zebisch A, Rauch J, von Kriegsheim A, et al. Raf family kinases: old dogs have learned new tricks. Genes Cancer 2011; 2: 232-60. doi: 10.1177/1947601911407323
  37. Wan PT, Garnett MJ, Roe SM, Lee S, Niculescu-Duvaz D, Good VM, et al. Mechanism of activation of the RAF- ERK signaling pathway by oncogenic mutations of B-RAF. Cell 2004; 116: 855-67. doi: 10.1016/s0092-8674(04)00215-6
  38. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, et al. Mutations of the BRAF gene in human cancer. Nature 2002; 417: 949-54. doi: 10.1038/ nature00766
  39. Maughan TS, Adams RA, Smith CG, Meade AM, Seymour MT, Wilson RH, et al. Addition of cetuximab to oxaliplatin-based first-line combination chemotherapy for treatment of advanced colorectal cancer: results of the randomised phase 3 MRC COIN trial. Lancet 2011; 377: 2103-14. doi: 10.1016/S0140-6736(11)60613-2
  40. Souglakos J, Philips J, Wang R, Marwah S, Silver M, Tzardi M, et al. Prognostic and predictive value of common mutations for treatment response and survival in patients with metastatic colorectal cancer. Br J Cancer 2009; 101: 465-72. doi: 10.1038/sj.bjc.6605164
  41. Richman SD, Seymour MT, Chambers P, Elliott F, Daly CL, Meade AM, et al. KRAS and BRAF mutations in advanced colorectal cancer are associated with poor prognosis but do not preclude benefit from oxaliplatin or irinotecan: results from theMRC FOCUS trial. J Clin Oncol 2009; 27: 5931-7. doi: 10.1200/JCO.2009.22.4295
  42. Tran B, Kopetz S, Tie J, Gibbs P, Jiang ZQ, Lieu CH, et al. Impact of BRAF mutation and microsatellite instability on the pattern of metastatic spread and prognosis in metastatic colorectal cancer. Cancer 2011; 117: 4623-32. doi: 10.1002/cncr.26086
  43. Yokota T, Ura T, Shibata N, Takahari D, Shitara K, Nomura M, et al. BRAF mutation is a powerful prognostic factor in advanced and recurrent colorectal cancer. Br J Cancer 2011; 104: 856-62. doi: 10.1038/bjc.2011.19
  44. Tie J, Gibbs P, Lipton L, Christie M, Jorissen RN, Burgess AW, et al. Optimizing targeted therapeutic develop- ment: analysis of a colorectal cancer patient population with the BRAF(V600E) mutation. Int J Cancer 2011; 128: 207584. doi: 10.1002/ijc.25555
  45. Li HT, Lu YY, An YX, Wang X, Zhao QC. KRAS, BRAF and PIK3CA mutations in human colorectal cancer: relationship with metastatic colorectal cancer. Oncol Rep 2011; 25: 1691-97. doi: 10.3892/or.2011.1217
  46. Hsieh LL, Er TK, Chen CC, Hsieh JS, Chang JG, Liu TC. Characteristics and prevalence of KRAS, BRAF, and PIK3CA mutations in colorectal cancer by high-resolution melting analysis in Taiwanese population. Clin Chim Acta 2012; 413: 1605-11. doi: 10.1016/j.cca.2012.04.029
  47. Shen Y, Wang J, Han X, Yang H, Wang S, Lin D et al. Effectors of epidermal growth factor receptor pathway: the genetic profiling of KRAS, BRAF, PIK3CA, NRAS mutations in colorectal cancer characteristics and personalized medicine. PLoS One 2013; 8: e81628. doi: 10.1371/journal.pone.0081628
  48. Lo L, Price T, Young J, Townsend A. BRAF mutation in colorectal cancer. [cited 10 Feb 2019]. Available at: https://www.intechopen.com/books/colorectal-cancer-from-pathogenesis-to-treatment/braf-mutation-in-colorectal-cancer doi: 10.5772/62226
  49. Kambara T, Simms LA, Whitehall VL, Spring KJ, Wynter CV, Walsh MD, et al. BRAF mutation is associated with DNA methylation in serrated polyps and cancers of the colorectum. Gut 2004; 53: 1137-44. doi: 10.1136/gut.2003.037671
  50. Tran B, Kopetz S, Tie J, Gibbs P, Jiang ZQ, Lieu CH, et al. Impact of BRAF mutation and microsatellite instability on the pattern of metastatic spread and prognosis in metastatic colorectal cancer. Cancer 2011; 117: 4623-32. doi: 10.1002/cncr.26086
  51. Chen D, Huang JF, Liu K, Zhang LQ, Yang Z, Chuai ZR, et al. BRAF V600E mutation and its association with clinicopathological features of colorectal cancer: a systematic review and meta-analysis. PLoS One 2014; 2014; 9: e90607. doi: 10.1371/journal.pone.0090607
  52. Ogino S, Nosho K, Kirkner GJ, Shima K, Irahara N, Kure S, et al. PIK3CA mutation is associated with poor prognosis among patients with curatively resected colon cancer. J Clin Oncol 2009; 27: 1477-84. doi: 10.1200/ JCO.2008.18.654
  53. Zarkavelis G, Boussiosa S, Papadakia A, Katsanos KH, Christodoulou DK, Pentheroudakis G. Current and future biomarkers in colorectal cancer. Ann Gastroenterol 2017; 30: 613-21. doi: 10.20524/aog.2017.0191
  54. Imai K, Yamamoto H. Carcinogenesis and microsatellite instability: the interrelation- ship between genetics and epigenetics. Carcinogenesis 2008; 29: 673-80. doi: 10.1093/carcin/bgm228
  55. Jensen LH, Lindebjerg J, Byriel L, Kolvraa S, Crüger DG. Strategy in clinical practice for classification of unselected colorectal tumours based on mismatch repair deficiency. Colorectal Dis 2008; 10: 490-7. doi: 10.1111/j.1463-1318.2007.01378.x
  56. Rahner N, Friedrichs N, Steinke V, Aretz S, Friedl W, Buettner R, et al. Coexisting somatic promoter hypermethylation and pathogenic MLH1 germline mutation in Lynch syndrome. J Pathol 2008; 214: 10-16. doi: 10.1002/path.2263
  57. Domingo E, Laiho P, Ollikainen M, Pinto L, Wang A, French J, et al. BRAF screening as a low-cost effective strategy for simplifying HNPCC genetic testing. J Med Genet 2004; 41: 664-8. doi: 10.1136/jmg.2004.020651
  58. Cremolini C, Loupakis F, Antoniotti C, Lupi C, Sensi E, Lonardi S, et al. FOLFOXIRI plus bevacizumab versus FOLFIRI plus bevacizumab as first-line treatment of patients with metastatic colorectal cancer: updated overall survival and molecular subgroup analyses of the open-label, phase 3 TRIBE study. Lancet Oncol 2015; 16: 1306-15. doi: 10.1016/S1470-2045(15)00122-9
  59. Sanz- Garcia E, Argiles G, Elez E, Tabernero J. BRAF mutant colorectal cancer: prognosis, treatment, and new perspectives. Ann Oncol 2017; 28: 2648-57. doi: 10.1093/annonc/mdx401
  60. Renaud S, Romain B, Falcoz PE, Olland A, Santelmo N, Brigand C, et al. KRAS and BRAF mutations are prognostic biomarkers in patients undergoing lung metastasectomy of colorectal cancer. Br J Cancer 2015; 112: 720-8. doi: 10.1038/bjc.2014.499
  61. Bokemeyer C, Van Cutsem E, Rougier P, Ciardiello F, Heeger S, Schlichting, et al. Addition of cetuximab to chemotherapy as first-line treatment for KRAS wild-type metastatic colorectal cancer: pooled analysis of the CRYSTAL and OPUS randomised clinical trials. Eur J Cancer 2012; 48: 1466-75. doi: 10.1016/j.ejca.2012.02.057
  62. 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: 1023-34. doi: 10.1056/NEJMoa1305275
  63. Seymour MT, Brown SR, Middleton G, Maughan T, Richman S, Gwyther S, et al. Panitumumab and irinotecan versus irinotecan alone for patients with KRAS wild-type, fluorouracil-resistant advanced colorectal cancer (PICCOLO): a prospectively stratified randomised trial. Lancet Oncol 2013; 14: 749-59. doi: 10.1016/S1470-2045(13)70163-3
  64. Karapetis CS, Jonker D, Daneshmand M, Hanson JE, O’Callaghan CJ, Marginean C, et al. PIK3CA, BRAF, and PTEN status and benefit from cetuximab in the treatment of advanced colorectal cancer—results from NCIC CTG/AGITG CO.17. Clin Cancer Res 2014; 20: 744-53. doi: 10.1158/1078-0432.CCR-13-0606
  65. 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: 107-16. doi: 10.1093/annonc/mdt523
  66. Pietrantonio F, Petrelli F, Coinu A, Di Bartolomeo M, Borgonovo K, Maggi C, et al. Predictive role of BRAF mutations in patients with advanced colorectal cancer receiving cetuximab and panitumumab: a meta-analysis. Eur J Cancer 2015; 51: 587-94. doi: 10.1016/j.ejca.2015.01.054
  67. Rowland A, Dias MM, Wiese MD, Kichenadasse G, McKinnon RA, Karapetis CS, et al. Meta-analysis of BRAF mutation as a predictive biomarker of benefit from anti-EGFR monoclonal antibody therapy for RAS wild-type metastatic colorectal cancer. Br J Cancer 2015; 112: 1888-94. doi: 10.1038/ bjc.2015.173
  68. Yuan ZX, Wang XY, Qin QY, Chen DF, Zhong QH, Wang L, et al. The prognostic role of BRAF mutation in metastatic colorectal cancer receiving anti-EGFR monoclonal antibodies: a meta-analysis. PLoS One 2013; 8: e65995. doi: 10.1371/journal.pone
  69. Loupakis F, Cremolini C, Salvatore L, Masi G, Sensi E, Schirripa M, et al. FOLFOXIRI plus bevacizumab as first-line treatment in BRAF mutant metastatic colorectal cancer. Eur J Cancer 2014; 50: 57-63. doi: 10.1016/j.ejca
  70. Van Cutsem E, Huijberts S, Grothey A, Yaeger R, Cuyle PJ, Elez E, et al. BEACON CRC study safety lead-in (SLI) in patients with BRAF V600E metastatic colorectal cancer: Binimetinib, Encorafenib and Cetuximab Triplet Therapy for patients with BRAF V600E-mutant metastatic colorectal cancer: safety lead-in results from the phase III BEACON colorectal cancer study. J Clin Oncol 2019: 37: 1460-9. doi: 10.1200/JCO.18.02459
  71. Schuell B, Gruenberger T, Scheithauer W, Zielinski Ch, Wrba F. HER 2/neu protein expression in colorectal cancer. BMC Cancer 2006; 6: 123. doi: 10.1186/1471-2407-6-123
  72. Siena S, Sartore-Bianchi A, Marsoni S, Hurwitz HI, McCall SJ, Penault-Llorca F, et al. Targeting the human epidermal growth factor receptor 2 ( HER2) oncogene in colorectal cancer. Ann Oncol 2018; 29: 1108-19. doi: 10.1093/ annonc/mdy100
  73. Seo AN, Kwak Y, Kim DW, Kang SB, Choe G, Kim WH, et al. Her2 status in colorectal cancer: its clinical significance and the relationship between HER2 gene amplification and expression. PLoS One 2014; 9: e98528. doi: 10.1371/journal.pone
  74. Ingold Heppner B, Behrens HM, Balschun K, Haag J, Krüger S, Becker T, et al. HER2/neu testing in primary colorectal carcinoma. Br J Cancer 2014; 111: 1977-84. doi: 10.1038/bjc.2014.483
  75. Missiaglia E, Jacobs B, D’Ario G, Di Narzo AF, Soneson C, Budinska E, et al. Distal and proximal colon cancers differ in terms of molecular, pathological, and clinical features. Ann Oncol 2014; 25: 1995-2001. doi: 10.1093/annonc/ mdu275
  76. Nam SK, Yun S, Koh J, Kwak Y, Seo AN, Park KU, et al. BRAF, PIK3CA, and HER2 oncogenic alterations according to KRAS mutation status in advanced colorectal cancers with distant metastasis. PLoS One 2016; 11: e0151865. doi: 10.1371/journal.pone
  77. Bertotti A, Migliardi G, Galimi F, Sassi F, Torti D, Isella C, et al. A molecularly annotated platform of patient-derived xenografts (“Xenopatient”) identifies HER2 as an effective therapeutic target in cetuximab-resistant colorectal cancer. Cancer Discovery 2011; 1: 508-23. doi: 10.1158/2159-8290
  78. Yonesaka K, Zejnullahu K, Okamoto I, Satoh T, Cappuzzo F, Souglakos J, et al. Activation of ERBB2 signaling causes resistance to the EGFR-directed therapeutic antibody cetuximab. Sci Transl Med 2011; 3: 99ra86. doi: 10.1126/ scitranslmed.3002442
  79. Martin V, Landi L, Molinari F, Fountzilas G, Geva R, Riva A, et al. HER2 gene copy number status may influence clinical efficacy to anti-EGFR monoclonal antibodies in metastatic colorectal cancer patients. Br J Cancer 2013; 108: 668-75. doi: 10.1038/bjc.2013
  80. Osako T, Miyahara M, Uchino S, Inomata M, Kitano S, Kobayashi M. Immunohistochemical study of c-erbB-2 protein in colorectal cancer and the correlation with patient survival. Oncology 1998; 55: 548-55. doi: 10.1159/000011911
  81. Kapitanovic S, Radosevic S, Kapitanovic M, Andelinovic S, Ferencic Z, Tavassoli M, et al. The expression of p185(HER-2/neu) correlates with the stage of disease and survival in colorectal cancer. Gastroenterology 1997; 112: 1103-13. doi: 10.1016/S0016-5085(97)70120-3
  82. Li C, Liu DR, Ye LY, Huang LN, Jaiswai S, Li XW, et al. HER-2 overexpression and survival in colorectal cancer: a meta-analysis. J Zhejiang Univ Sci B 2014; 15: 582-9. doi: 10.1631/jzus.B1300258
  83. Zhang L. Immunohistochemistry versus microsatellite instability testing for screening colorectal cancer patients at risk for hereditary nonpolyposis colorectal cancer syndrome. Part II. The utility of microsatellite instability testing. J Mol Diagn 2008; 10: 301-7. doi: 10.2353/jmoldx.2008.080062
  84. Ward R, Meagher A, Tomlinson I, O’Connor T, Norrie M, Wu R, et al. Microsatellite instability and the clinicopathological features of sporadic colorectal cancer. Gut 2001; 48: 821-9. doi: 10.1136/gut.48.6.821
  85. Tiwari AK, Roy HK, Lynch HT. Lynch syndrome in the 21st century: clinical perspectives. QJM 2016; 109: 151-8. doi: 10.1093/qjmed/hcv137
  86. Ashktorab H, Ahuja S, Kannan L, Lior X, Ellis NA, Xicola RM, et al. A meta-analysis of MSI frequency and race in colorectal cancer. Oncotarget 2016; 7: 34546-57. doi: 10.18632/oncotarget.8945
  87. Overman MJ, Lonardi S, Wong KYM, Lenz HJ, Gelsomino F, Aglietta M, et al. Durable clinical benefit with nivolumab plus ipilimumab in DNA mismatch repair-deficient/microsatellite instability-high metastatic colorectal cancer. J Clin Oncol 2018; 36: 773-9. doi: 10.1200/JCO.2017.76.9901
  88. Fujiyoshi K, Yamamoto G, Takenoya T, Takahashi A, Arai Y, Yamada M, et al. Metastatic pattern of stage IV colorectal cancer with high-frequency micro-satellite instability as a prognostic factor. Anticancer Res 2017; 37: 239-47. doi: 10.21873/anticanres.11313
  89. Kawakami H, Zaanan A, Sinicrope FA. MSI testing and its role in management of colorectal cancer. Curr Treat Options Oncol 2015; 16: 30. doi: 10.1007/s11864-015-0348-2
DOI: https://doi.org/10.2478/raon-2019-0033 | Journal eISSN: 1581-3207 | Journal ISSN: 1318-2099
Language: English
Page range: 265 - 274
Submitted on: Feb 16, 2019
|
Accepted on: Jun 24, 2019
|
Published on: Sep 24, 2019
In partnership with: Paradigm Publishing Services
Publication frequency: 4 issues per year

© 2019 Vlad-Adrian Afrăsânie, Mihai Vasile Marinca, Teodora Alexa-Stratulat, Bogdan Gafton, Marius Păduraru, Anca Maria Adavidoaiei, Lucian Miron, Cristina Rusu, published by Association of Radiology and Oncology
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.