Tumor cellularity as a quality assurance measure for accurate clinical detection of braf mutations in melanoma

Molecular Diagnosis and Therapy

Volumn 18, Issue 4, 2014, Pages 409-418

  Dudley, Jonathan C ^a   Gurda, Grzegorz T ^a   Tseng, Li Hui ^a,b   Anderson, Derek A ^a   Chen, Guoli ^a   Taube, Janis M ^a   Gocke, Christopher D ^a   Eshleman, James R ^a   Lin, Ming Tseh ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE;

GENETICS; HUMAN; MELANOMA; MUTATION; NUCLEOTIDE SEQUENCE; SKIN NEOPLASMS;

DNA MUTATIONAL ANALYSIS; HUMANS; MELANOMA; MUTATION; PROTO-ONCOGENE PROTEINS B-RAF; SKIN NEOPLASMS;

EID: 84905686054     PISSN: 11771062     EISSN: 11792000     Source Type: Journal    
DOI: 10.1007/s40291-014-0091-6     Document Type: Article

References (57)

1. 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(6892):949-54. (Pubitemid 34716871)
2. Kong Y, Kumar SM, Xu X. Molecular pathogenesis of sporadic melanoma and melanoma-initiating cells. Arch Pathol Lab Med. 2010;134(12):1740-9.
3. Roring M, Brummer T. Aberrant B-Raf signaling in human cancer: 10 years from bench to bedside. Crit Rev Oncog. 2012;17(1):97-121.
4. Amanuel B, Grieu F, Kular J, Millward M, Iacopetta B. Incidence of BRAF p.Val600Glu and p.Val600Lys mutations in a consecutive series of 183 metastatic melanoma patients from a high incidence region. Pathology. 2012;44(4):357-9.
5. Curtin JA, Fridlyand J, Kageshita T, Patel HN, Busam KJ, Kutzner H, et al. Distinct sets of genetic alterations in melanoma. N Engl J Med. 2005;353(20):2135-47. (Pubitemid 41653105)
6. Long GV, Menzies AM, Nagrial AM, Haydu LE, Hamilton AL, Mann GJ, et al. Prognostic and clinicopathologic associations of oncogenic BRAF in metastatic melanoma. J Clin Oncol. 2011;29(10):1239-46.
7. Ellerhorst JA, Greene VR, Ekmekcioglu S, Warneke CL, Johnson MM, Cooke CP, et al. Clinical correlates of NRAS and BRAF mutations in primary human melanoma. Clin Cancer Res. 2011;17(2):229-35.
8. Ugurel S, Thirumaran RK, Bloethner S, Gast A, Sucker A, Mueller-Berghaus J, et al. B-RAF and N-RAS mutations are preserved during short time in vitro propagation and differentially impact prognosis. PLoS One. 2007;2(2):e236.
9. Greaves WO, Verma S, Patel KP, Davies MA, Barkoh BA, Galbincea JM, et al. Frequency and spectrum of BRAF mutations in a retrospective, single-institution study of 1112 cases of melanoma. J Mol Diagn. 2013;15(2):220-6.
10. Menzies AM, Haydu LE, Visintin L, Carlino MS, Howle JR, Thompson JF, et al. Distinguishing clinicopathologic features of patients with V600E and V600K BRAF-mutant metastatic melanoma. Clin Cancer Res. 2012;18(12):3242-9.
11. Rubinstein JC, Sznol M, Pavlick AC, Ariyan S, Cheng E, Bacchiocchi A, et al. Incidence of the V600K mutation amongmelanoma patients with BRAF mutations, and potential therapeutic response to the specific BRAF inhibitor PLX4032. J Transl Med. 2010;8:67.
12. Bollag G, Hirth P, Tsai J, Zhang J, Ibrahim PN, Cho H, et al. Clinical efficacy of a RAF inhibitor needs broad target blockade in BRAF-mutant melanoma. Nature. 2010;467(7315):596-9.
13. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J, et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med. 2011;364(26):2507-16.
14. Klein O, Clements A, Menzies AM, O'Toole S, Kefford RF, Long GV. BRAF inhibitor activity in V600R metastatic melanoma. Eur J Cancer. 2013;49(5):1073-9.
15. McArthur G, Hauschild A, Robert C, Larkin J, Haanen JB, Ribas A, et al. Efficacy of vemurafenib in BRAFV600K mutation-positive melanoma disease: results from phase 3 clinical study BRIM3. Pigment Cell Melanoma Res. 2012;25(6):871.
16. Sosman JA, Kim KB, Schuchter L, Gonzalez R, Pavlick AC, Weber JS, et al. Survival in BRAF V600-mutant advanced melanoma treated with vemurafenib. N Engl J Med. 2012;366(8):707-14.
17. Ascierto PA, Minor D, Ribas A, Lebbe C, O'Hagan A, Arya N, et al. Phase II trial (BREAK-2) of the BRAF inhibitor dabrafenib (GSK2118436) in patients with metastatic melanoma. J Clin Oncol. 2013;31(26):3205-11.
18. Falchook GS, Lewis KD, Infante JR, Gordon MS, Vogelzang NJ, DeMarini DJ, et al. Activity of the oral MEK inhibitor trametinib in patients with advanced melanoma: a phase 1 dose-escalation trial. Lancet Oncol. 2012;13(8):782-9.
19. Falchook GS, Long GV, Kurzrock R, Kim KB, Arkenau TH, Brown MP, et al. Dabrafenib in patients with melanoma, untreated brain metastases, and other solid tumours: a phase 1 dose-escalation trial. Lancet. 2012;379(9829):1893-901.
20. Flaherty KT, Robert C, Hersey P, Nathan P, Garbe C, Milhem M, et al. Improved survival with MEK inhibition in BRAF-mutated melanoma. N Engl J Med. 2012;367(2):107-14.
21. Hauschild A, Grob JJ, Demidov LV, Jouary T, Gutzmer R, Millward M, et al. Dabrafenib in BRAF-mutated metastatic melanoma: a multicentre, open-label, phase 3 randomised controlled trial. Lancet. 2012;380(9839):358-65.
22. Anderson S, Bloom KJ, Vallera DU, Rueschoff J, Meldrum C, Schilling R, et al. Multisite analytic performance studies of a realtime polymerase chain reaction assay for the detection of BRAF V600E mutations in formalin-fixed, paraffin-embedded tissue specimens of malignant melanoma. Arch Pathol Lab Med. 2012;136(11):1385-91.
23. Halait H, Demartin K, Shah S, Soviero S, Langland R, Cheng S, et al. Analytical performance of a real-time PCR-based assay for V600 mutations in the BRAF gene, used as the companion diagnostic test for the novel BRAF inhibitor vemurafenib in metastatic melanoma. Diagn Mol Pathol. 2012;21(1):1-8.
24. Qu K, Pan Q, Zhang X, Rodriguez L, Zhang K, Li H, et al. Detection of BRAF V600 mutations in metastatic melanoma: comparison of the Cobas 4800 and Sanger sequencing assays. J Mol Diagn. 2013;15(6):790-5.
25. Fadhil W, Ibrahem S, Seth R, Ilyas M. Quick-multiplex-consensus (QMC)-PCR followed by high-resolution melting: a simple and robust method for mutation detection in formalin-fixed paraffin-embedded tissue. J Clin Pathol. 2010;63(2):134-40.
26. Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthur GA, Sosman JA, et al. Inhibition of mutated, activated BRAF in metastatic melanoma. N Engl J Med. 2010;363(9):809-19.
27. Kotoula V, Charalambous E, Biesmans B, Malousi A, Vrettou E, Fountzilas G, et al. Targeted KRAS mutation assessment on patient tumor histologic material in real time diagnostics. PLoS One. 2009;4(11):e7746.
28. Tan YH, Liu Y, Eu KW, Ang PW, Li WQ, Salto-Tellez M, et al. Detection of BRAF V600E mutation by pyrosequencing. Pathology. 2008;40(3):295-8. (Pubitemid 351563933)
29. Lin MT, Tseng LH, Rich RG, Hafez MJ, Harada S, Murphy KM, et al. Delta-PCR, a simple method to detect translocations and insertion/deletion mutations. J Mol Diagn. 2011;13(1):85-92.
30. Chen G, Olson MT, O'Neill A, Norris A, Beierl K, Harada S, et al. A virtual pyrogram generator to resolve complex pyrosequencing results. J Mol Diagn. 2012;14(2):149-59.
31. Tsiatis AC, Norris-Kirby A, Rich RG, Hafez MJ, Gocke CD, Eshleman JR, et al. Comparison of Sanger sequencing, pyrosequencing, and melting curve analysis for the detection of KRAS mutations: diagnostic and clinical implications. J Mol Diagn. 2010;12(4):425-32.
32. Olson MT, Harrington C, Beierl K, Chen G, Thiess M, O'Neill A, Taube J, Zeiger MA, Lin MT, Eshleman JR. BRAF pyrosequencing analysis aided by a lookup table. Am J Clin Pathol. 2014 (in press)
33. Lin MT, Tseng LH, Beierl K, Hsieh A, Thiess M, Chase N, et al. Tandem duplication PCR: an ultrasensitive assay for the detection of internal tandem duplications of the FLT3 gene. Diagn Mol Pathol. 2013;22(3):149-55.
34. Harada S, Henderson LB, Eshleman JR, Gocke CD, Burger P, Griffin CA, et al. Genomic changes in gliomas detected using single nucleotide polymorphism array in formalin-fixed, paraffin-embedded tissue: superior results compared with microsatellite analysis. J Mol Diagn. 2011;13(5):541-8.
35. Colomba E, Helias-Rodzewicz Z, Von Deimling A, Marin C, Terrones N, Pechaud D, et al. Detection of BRAF p. V600E mutations in melanomas: comparison of four methods argues for sequential use of immunohistochemistry and pyrosequencing. J Mol Diagn. 2013;15(1):94-100.
36. Ihle MA, Fassunke J, Konig K, Grunewald I, Schlaak M, Kreuzberg N, et al. Comparison of high resolution melting analysis, pyrosequencing, next generation sequencing and immunohistochemistry to conventional Sanger sequencing for the detection of p. V600E and non-p.V600E BRAF mutations. BMC Cancer. 2014;14(1):13.
37. Mullins FM, Dietz L, Lay M, Zehnder JL, Ford J, Chun N, et al. Identification of an intronic single nucleotide polymorphism leading to allele dropout during validation of a CDH1 sequencing assay: implications for designing polymerase chain reactionbased assays. Genet Med. 2007;9(11):752-60. (Pubitemid 350129410)
38. Schwartz KM, Pike-Buchanan LL, Muralidharan K, Redman JB, Wilson JA, Jarvis M, et al. Identification of cystic fibrosis variants by polymerase chain reaction/oligonucleotide ligation assay. J Mol Diagn. 2009;11(3):211-5.
39. Ward KJ, Ellard S, Yajnik CS, Frayling TM, Hattersley AT, Venigalla PN, et al. Allelic drop-out may occur with a primer binding site polymorphism for the commonly used RFLP assay for the -1131T>C polymorphism of the Apolipoprotein AV gene. Lipids Health Dis. 2006;5:11.
40. Lade-Keller J, Romer KM, Guldberg P, Riber-Hansen R, Hansen LL, Steiniche T, et al. Evaluation of BRAF mutation testing methodologies in formalin-fixed, paraffin-embedded cutaneous melanomas. J Mol Diagn. 2013;15(1):70-80.
41. Magnin S, Viel E, Baraquin A, Valmary-Degano S, Kantelip B, Pretet JL, et al. A multiplex SNaPshot assay as a rapid method for detecting KRAS and BRAF mutations in advanced colorectal cancers. J Mol Diagn. 2011;13(5):485-92.
42. McCourt CM, McArt DG, Mills K, Catherwood MA, Maxwell P, Waugh DJ, et al. Validation of next generation sequencing technologies in comparison to current diagnostic gold standards for BRAF, EGFR and KRAS mutational analysis. PLoS One. 2013;8(7):e69604.
43. Rechsteiner M, von Teichman A, Ruschoff JH, Fankhauser N, Pestalozzi B, Schraml P, et al. KRAS, BRAF, and TP53 deep sequencing for colorectal carcinoma patient diagnostics. J Mol Diagn. 2013;15(3):299-311.
44. Szankasi P, Reading NS, Vaughn CP, Prchal JT, Bahler DW, Kelley TW. A quantitative allele-specific PCR test for the BRAF V600E mutation using a single heterozygous control plasmid for quantitation: a model for qPCR testing without standard curves. J Mol Diagn. 2013;15(2):248-54.
45. Tuononen K, Maki-Nevala S, Sarhadi VK, Wirtanen A, Ronty M, Salmenkivi K, et al. Comparison of targeted next-generation sequencing (NGS) and real-time PCR in the detection of EGFR, KRAS, and BRAF mutations on formalin-fixed, paraffin-embedded tumor material of non-small cell lung carcinoma-superiority of NGS. Genes Chromosomes Cancer. 2013;52(5):503-11.
46. Busam KJ, Hedvat C, Pulitzer M, von Deimling A, Jungbluth AA. Immunohistochemical analysis of BRAF(V600E) expression of primary and metastatic melanoma and comparison with mutation status and melanocyte differentiation antigens of metastatic lesions. Am J Surg Pathol. 2013;37(3):413-20.
47. Long GV, Wilmott JS, Capper D, Preusser M, Zhang YE, Thompson JF, et al. Immunohistochemistry is highly sensitive and specific for the detection of V600E BRAF mutation in melanoma. Am J Surg Pathol. 2013;37(1):61-5.
48. Routhier CA, Mochel MC, Lynch K, Dias-Santagata D, Louis DN, Hoang MP. Comparison of 2 monoclonal antibodies for immunohistochemical detection of BRAF V600E mutation in malignant melanoma, pulmonary carcinoma, gastrointestinal carcinoma, thyroid carcinoma, and gliomas. Hum Pathol. 2013;44(11):2563-70.
49. Marin C, Beauchet A, Capper D, Zimmermann U, Julie C, Ilie M, et al. Detection of BRAF p. V600E mutations in melanoma by immunohistochemistry has a good interobserver reproducibility. Arch Pathol Lab Med. 2014;138(1):71-5.
50. Hoorens A, Jouret-Mourin A, Sempoux C, Demetter P, De Hertogh G, Teugels E. Accurate KRAS mutation testing for EGFR-targeted therapy in colorectal cancer: emphasis on the key role and responsibility of pathologists. Acta Gastroenterol Belg. 2010;73(4):497-503.
51. van Krieken JH, Jung A, Kirchner T, Carneiro F, Seruca R, Bosman FT, et al. KRAS mutation testing for predicting response to anti-EGFR therapy for colorectal carcinoma: proposal for an European quality assurance program. Virchows Arch. 2008;453(5):417-31.
52. Bellon E, Ligtenberg MJ, Tejpar S, Cox K, de Hertogh G, de Stricker K, et al. External quality assessment for KRAS testing is needed: setup of a European program and report of the first joined regional quality assessment rounds. Oncologist. 2011;16(4):467-78.
53. Smits AJ, Kummer JA, de Bruin PC, Bol M, van den Tweel JG, Seldenrijk KA, et al. The estimation of tumor cell percentage for molecular testing by pathologists is not accurate. Mod Pathol. 2014;27(2):168-74.
54. Viray H, Li K, Long TA, Vasalos P, Bridge JA, Jennings LJ, et al. A prospective, multi-institutional diagnostic trial to determine pathologist accuracy in estimation of percentage of malignant cells. Arch Pathol Lab Med. 2013;137(11):1545-9.
55. Boissiere-Michot F, Lopez-Crapez E, Frugier H, Berthe ML, Ho-Pun-Cheung A, Assenat E, et al. KRAS genotyping in rectal adenocarcinoma specimens with low tumor cellularity after neoadjuvant treatment. Mod Pathol. 2012;25(5):731-9.
56. Ondrejka SL, Schaeffer DF, Jakubowski MA, Owen DA, Bronner MP. Does neoadjuvant therapy alter KRAS and/or MSI results in rectal adenocarcinoma testing? Am J Surg Pathol. 2011;35(9):1327-30.
57. Viray H, Coulter M, Li K, Lane K, Madan A, Mitchell K, et al. Automated objective determination of percentage of malignant nuclei for mutation testing. Appl Immunohistochem Mol Morphol (Epub 24 Oct 2013).