Performance characteristics of next-generation sequencing in clinical mutation detection of colorectal cancers

被引:47
作者
Haley, Lisa [1 ]
Tseng, Li-Hui [1 ,2 ]
Zheng, Gang [1 ]
Dudley, Jonathan [1 ,3 ]
Anderson, Derek A. [1 ]
Azad, Nilofer S. [4 ]
Gocke, Christopher D. [1 ,4 ]
Eshleman, James R. [1 ,4 ]
Lin, Ming-Tseh [1 ]
机构
[1] Johns Hopkins Univ, Sch Med, Dept Pathol, Johns Hopkins Hosp, Baltimore, MD 21287 USA
[2] Natl Taiwan Univ Hosp, Dept Med Genet, Taipei, Taiwan
[3] Massachusetts Gen Hosp, Dept Pathol, Boston, MA 02114 USA
[4] Johns Hopkins Univ, Sch Med, Johns Hopkins Hosp, Dept Oncol, Baltimore, MD 21287 USA
关键词
RAS MUTATIONS; ACQUIRED-RESISTANCE; KRAS MUTATIONS; PHASE-III; BRAF; CETUXIMAB; GENE; PANITUMUMAB; VALIDATION; CHALLENGES;
D O I
10.1038/modpathol.2015.86
中图分类号
R36 [病理学];
学科分类号
100104 ;
摘要
Activating mutations in downstream genes of the epidermal growth factor receptor (EGFR) pathway may cause anti-EGFR resistance in patients with colorectal cancers. We present performance characteristics of a next-generation sequencing assay designed to detect such mutations. In this retrospective quality assessment study, we analyzed mutation detected in the KRAS, NRAS, BRAF, and PIK3CA genes by a clinically validated next-generation sequencing assay in 310 colorectal cancer specimens. Tumor cellularity and mutant allele frequency were analyzed to identify tumor heterogeneity and mutant allele-specific imbalance. Next-generation sequencing showed precise measurement of mutant allele frequencies and detected 23% of mutations with 2-20% mutant allele frequencies. Of the KRAS mutations detected, 17% were outside of codons 12 and 13. Among PIK3CA mutations, 48% were outside of codons 542, 545, and 1047. The percentage of tumors with predicted resistance to anti-EGFR therapy increased from 40% when testing for only mutations in KRAS exon 2 to 47% when testing for KRAS exons 2-4, 48% when testing for KRAS and NRAS exons 2-4, 58% when including BRAF codon 600 mutations, and 59% when adding PIK3CA exon 20 mutations. Right-sided colorectal cancers carried a higher risk of predicted anti-EGFR resistance. A concomitant KRAS mutation was detected in 51% of PIK3CA, 23% of NRAS, and 33% of kinase-impaired BRAF-mutated tumors. Lower than expected mutant allele frequency indicated tumor heterogeneity, while higher than expected mutant allele frequency indicated mutant allele-specific imbalance. Two paired neuroendocrine carcinomas and adjacent adenomas showed identical KRAS mutations, but only PIK3CA mutations in neuroendocrine carcinomas. Next-generation sequencing is a robust tool for mutation detection in clinical laboratories. It demonstrates high analytic sensitivity and broad reportable range, and it provides simultaneous detection of concomitant mutations and a quantitative measurement of mutant allele frequencies to predict tumor heterogeneity and mutant allele-specific imbalance.
引用
收藏
页码:1390 / 1399
页数:10
相关论文
共 41 条
[1]   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].
Allegra, Carmen J. ;
Jessup, J. Milburn ;
Somerfield, Mark R. ;
Hamilton, Stanley R. ;
Hammond, Elizabeth H. ;
Hayes, Daniel F. ;
McAllister, Pamela K. ;
Morton, Roscoe F. ;
Schilsky, Richard L. .
JOURNAL OF CLINICAL ONCOLOGY, 2009, 27 (12) :2091-2096
[2]   Multisite Analytic Performance Studies of a Real-Time Polymerase Chain Reaction Assay for the Detection of BRAF V600E Mutations in Formalin-Fixed, Paraffin-Embedded Tissue Specimens of Malignant Melanoma [J].
Anderson, Steven ;
Bloom, Kenneth J. ;
Vallera, Dino U. ;
Rueschoff, Josef ;
Meldrum, Cliff ;
Schilling, Robert ;
Kovach, Barbara ;
Lee, Ju Ruey-Jiuan ;
Ochoa, Pam ;
Langland, Rachel ;
Halait, Harkanwal ;
Lawrence, H. Jeffrey ;
Dugan, Michael C. .
ARCHIVES OF PATHOLOGY & LABORATORY MEDICINE, 2012, 136 (11) :1385-1391
[3]  
Brule SY, 2013, J CLIN ONCOL, V31
[4]   PIK3CA in colorectal cancer [J].
Cathomas, Gieri .
FRONTIERS IN ONCOLOGY, 2014, 4
[5]   Lymph node metastases of melanoma: challenges for BRAF mutation detection [J].
Chen, Guoli ;
Dudley, Jonathan ;
Tseng, Li-Hui ;
Smith, Kirstin ;
Gurda, Grzegorz T. ;
Gocke, Christopher D. ;
Eshleman, James R. ;
Lin, Ming-Tseh .
HUMAN PATHOLOGY, 2015, 46 (01) :113-119
[6]   Clinical activity of FOLFIRI plus cetuximab according to extended gene mutation status by next-generation sequencing: findings from the CAPRI-GOIM trial [J].
Ciardiello, F. ;
Normanno, N. ;
Maiello, E. ;
Martinelli, E. ;
Troiani, T. ;
Pisconti, S. ;
Giuliani, F. ;
Barone, C. ;
Carteni, G. ;
Rachiglio, A. M. ;
Montesarchio, V. ;
Tonini, G. ;
Rizzi, D. ;
Cinieri, S. ;
Bordonaro, R. ;
Febbraro, A. ;
De Vita, F. ;
Orditura, M. ;
Fenizia, F. ;
Lambiase, M. ;
Rinaldi, A. ;
Tatangelo, F. ;
Botti, G. ;
Colucci, G. .
ANNALS OF ONCOLOGY, 2014, 25 (09) :1756-1761
[7]   Cetuximab monotherapy and cetuximab plus irinotecan in irinotecan-refractory metastatic colorectal cancer [J].
Cunningham, D ;
Humblet, Y ;
Siena, S ;
Khayat, D ;
Bleiberg, H ;
Santoro, A ;
Bets, D ;
Mueser, M ;
Harstrick, A ;
Verslype, C ;
Chau, I ;
Van Cutsem, E .
NEW ENGLAND JOURNAL OF MEDICINE, 2004, 351 (04) :337-345
[8]   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 [J].
De Roock, Wendy ;
Claes, Bart ;
Bernasconi, David ;
De Schutter, Jef ;
Biesmans, Bart ;
Fountzilas, George ;
Kalogeras, Konstantine T. ;
Kotoula, Vassiliki ;
Papamichael, Demetris ;
Laurent-Puig, Pierre ;
Penault-Llorca, Frederique ;
Rougier, Philippe ;
Vincenzi, Bruno ;
Santini, Daniele ;
Tonini, Giuseppe ;
Cappuzzo, Federico ;
Frattini, Milo ;
Molinari, Francesca ;
Saletti, Piercarlo ;
De Dosso, Sara ;
Martini, Miriam ;
Bardelli, Alberto ;
Siena, Salvatore ;
Sartore-Bianchi, Andrea ;
Tabernero, Josep ;
Macarulla, Teresa ;
Di Fiore, Frederic ;
Gangloff, Alice Oden ;
Ciardiello, Fortunato ;
Pfeiffer, Per ;
Qvortrup, Camilla ;
Hansen, Tine Plato ;
Van Cutsem, Eric ;
Piessevaux, Hubert ;
Lambrechts, Diether ;
Delorenzi, Mauro ;
Tejpar, Sabine .
LANCET ONCOLOGY, 2010, 11 (08) :753-762
[9]  
Deeb KK, 2013, J NATL COMPR CANC NE, V11, pS9
[10]   Wild-Type BRAF Is Required for Response to Panitumumab or Cetuximab in Metastatic Colorectal Cancer [J].
Di Nicolantonio, Federica ;
Martini, Miriam ;
Molinari, Francesca ;
Sartore-Bianchi, Andrea ;
Arena, Sabrina ;
Saletti, Piercarlo ;
De Dosso, Sara ;
Mazzucchelli, Luca ;
Frattini, Milo ;
Siena, Salvatore ;
Bardelli, Alberto .
JOURNAL OF CLINICAL ONCOLOGY, 2008, 26 (35) :5705-5712