Cited by 320Colorectal Cancer Treatments and StudiesGenetic factors in colorectal cancerColorectal Cancer Surgical Treatments

The DOI matches its Crossref record; 319 of the 319 references it cites were found in a registry or an index.

Biomarker-guided therapy for colorectal cancer: strength in complexity

Open access
Sveen, Anita, Kopetz, Scott, Lothe, Ragnhild A.·2020·Nature Reviews Clinical Oncology

Abstract

The number of molecularly stratified treatment options available to patients with colorectal cancer (CRC) is increasing, with a parallel rise in the use of biomarkers to guide prognostication and treatment decision-making. The increase in both the number of biomarkers and their use has resulted in a progressively complex situation, evident both from the extensive interactions between biomarkers and from their sometimes complex associations with patient prognosis and treatment benefit. Current and emerging biomarkers also reflect the genomic complexity of CRC, and include a wide range of aberrations such as point mutations, amplifications, fusions and hypermutator phenotypes, in addition to global gene expression subtypes. In this Review, we provide an overview of current and emerging clinically relevant biomarkers and their role in the management of patients with CRC, illustrating the intricacies of biomarker interactions and the growing treatment opportunities created by the availability of comprehensive molecular profiling.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41571-019-0241-1

Cites

319 of 319 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Show all 319 references

Research works printed but not linked: 44

  1. Diaz, L. A. et al. Pembrolizumab therapy for microsatellite instability high (MSI-H) colorectal cancer (CRC) and non-CRC. J. Clin. Oncol. 35, (3071 (2017).
  2. Kopetz, S. et al. Randomized trial of irinotecan and cetuximab with or without vemurafenib in BRAF-mutant metastatic colorectal cancer (SWOG 1406). J. Clin. Oncol. 35, 520 (2017). Meeting abstract describing initial data from a prospective randomized trial indicating prolonged PFS in patients with BRAF V600E-mutated and RAS wild-type metastatic CRCs by addition of vemurafenib to the combination of irinotecan plus cetuximab. · DOI
  3. Siena, S. et al. Rechallenge with EGFR inhibitors in patients with metastatic colorectal cancer: effect on outcomes [abstract P-320]. Ann. Oncol. 28 (Suppl. 3), mdx261.317 (2017).
  4. Sinicrope, F. et al. Overall survival result and outcomes by KRAS, BRAF, and DNA mismatch repair in relation to primary tumor site in colon cancers from a randomized trial of adjuvant chemotherapy: NCCTG (Alliance) N0147. J. Clin. Oncol. 32, 3525–3525 (2014). · DOI
  5. Willis, J. et al. Impact of microsatellite instability (MSI) on tumor clonal evolution in metastatic colorectal cancer (mCRC). J. Clin. Oncol. 36, 616 (2018). · DOI
  6. Heinemann, V. et al. Somatic DNA mutations, tumor mutational burden (TMB), and MSI status: association with efficacy in patients (pts) with metastatic colorectal cancer (mCRC) of FIRE-3 (AIO KRK-0306). J. Clin. Oncol. 36, 3591 (2018). · DOI
  7. Margonis, G. A. et al. Microsatellite instability in resectable colorectal liver metastasis: an international multi-institutional analysis. J. Clin. Oncol. 36, 220 (2018). · DOI
  8. Price, T. J. et al. Outcomes for metastatic colorectal cancer (mCRC) based on microsatellite instability. J. Clin. Oncol. 36, 759 (2018). · DOI
  9. Venook, A. P. et al. Impact of primary (1°) tumor location on overall survival (OS) and progression-free survival (PFS) in patients (pts) with metastatic colorectal cancer (mCRC): analysis of CALGB/SWOG 80405 (Alliance). J. Clin. Oncol. 34, 3504–3504 (2016). · DOI
  10. Diaz, L. A. et al. Phase 3, open-label, randomized study of first-line pembrolizumab (pembro) versus investigator-choice chemotherapy for mismatch repair-deficient (dMMR) or microsatellite instability-high (MSI-H) metastatic colorectal carcinoma (mCRC): KEYNOTE-177. J. Clin. Oncol. 35 (Suppl. 4), TPS3618 (2017). · DOI · Paper page
  11. Lenz, H. J. J. et al. Durable clinical benefit with nivolumab (NIVO) plus low-dose ipilimumab (IPI) as first-line therapy in microsatellite instability-high/mismatch repair deficient (MSI-H/dMMR) metastatic colorectal cancer (mCRC) [abstract LBA18_PR]. Ann. Oncol. 29, mdy424.019 (2018).
  12. Chalabi, M. et al. Neoadjuvant ipilimumab plus nivolumab in early stage colon cancer [abstract LBA37_PR]. Ann. Oncol. 29, mdy424.047 (2018).
  13. Chen, E. X. et al. The CCTG CO.26 trial: a phase II randomized study of durvalumab plustremelimumab and best supportive care (BSC) versus BSC alone in patients with advanced colorectal carcinoma (CRC) refractory to standard therapies. J. Clin. Oncol. 35, (TPS3621 (2017).
  14. Galon, J. et al. MSI status plus immunoscore to select metastatic colorectal cancer patients for immunotherapies [abstract 12P]. Ann. Oncol. 29, mdy493.011 (2018). · DOI
  15. Stintzing, S. et al. Mutations within the EGFR signaling pathway: influence on efficacy in FIRE-3 — a randomized phase III study of FOLFIRI plus cetuximab or bevacizumab as first-line treatment for wild-type (WT) KRAS (exon 2) metastatic colorectal cancer (mCRC) patients. J. Clin. Oncol. 32, 445 (2014). · DOI
  16. Peeters, M. et al. Updated analysis of KRAS/NRAS and BRAF mutations in study 20050181 of panitumumab (pmab) plus FOLFIRI for second-line treatment (tx) of metastatic colorectal cancer (mCRC). J. Clin. Oncol. 32, 3568 (2014). · DOI
  17. Van Cutsem, E. et al. Updated results of the MEK inhibitor trametinib (T), BRAF inhibitor dabrafenib (D), and anti-EGFR antibody panitumumab (P) in patients (pts) with BRAF V600E mutated (BRAFm) metastatic colorectal cancer (mCRC) [abstract LBA-07]. Ann. Oncol. 26, iv119 (2015). · DOI
  18. Tabernero, J. et al. Phase 2 results: encorafenib (enco) and cetuximab (cetux) with or without alpelisib (alp) in patients with advanced BRAF-mutant colorectal cancer (BRAFm CRC). J. Clin. Oncol. 34, 3544 (2016). · DOI
  19. Van Cutsem, E. et al. BEACON CRC study safety lead-in: assessment of the BRAF inhibitor encorafenib + MEK inhibitor binimetinib + anti-epidermal growth factor receptor antibody cetuximab for BRAF V600E metastatic colorectal cancer [abstract O-027]. Ann. Oncol. 29, mdy149.026 (2018). · DOI
  20. Schirripa, M. et al. Clinico-pathological and molecular characterisation of BRAF mutant metastatic colorectal cancer (mCRC): are all mutations created equal? J. Clin. Oncol. 36, 3590 (2018). · DOI
  21. Clark, J. W., Niedzwiecki, D., Hollis, D. & Mayer, R. Phase-II trial of 5-fluororuacil (5-FU), leucovorin (LV), oxaliplatin (Ox), and trastuzumab (T) for patients with metastatic colorectal cancer (CRC) refractory to initial therapy. Onkologie 26, (46 (2003).
  22. Gluck, W. L. et al. Prolonged response of widely metastatic HER2-positive colon cancer to trastuzumab therapy. Colorectal Cancer 6, 57–61 (2017). · DOI
  23. Haslem, D. S., Ji, H. P., Ford, J. M. & Nadauld, L. D. Precision oncology strategy in trastuzumab-resistant human epidermal growth factor receptor 2-positive colon cancer: case report of durable response to ado-trastuzumab emtansine. JCO Precis. Oncol. https://doi.org/10.1200/PO.16.00055 (2017). · DOI
  24. Siena, S. et al. HER2 amplification as a ‘molecular bait’ for trastuzumab-emtansine (T-DM1) precision chemotherapy to overcome anti-HER2 resistance in HER2 positive metastatic colorectal cancer: the HERACLES-RESCUE trial. J. Clin. Oncol. 34 (Suppl. 4), TPS774 (2017).
  25. Yoshino, T. et al. Updated results of phase I study of trastuzumab deruxtecan (DS-8201a) in HER2-expressing advanced colorectal cancer [abstract 563P]. Ann. Oncol. 29, mdy281.109 (2018). · DOI · Paper page
  26. Madison, R. et al. Kinase fusions in colorectal cancers: a unique biologic subset [abstract 457PD]. Ann. Oncol. 29, viii152 (2018). · DOI
  27. Demetri, G. D. et al. Efficacy and safety of entrectinib in patients with NTRK fusion-positive (NTRK-fp) tumors: pooled analysis of STARTRK-2, STARTRK-1 and ALKA-372-001 [abstract LBA17]. Ann. Oncol. 29, mdy424.017 (2018).
  28. Shaw, A. T. et al. Avelumab (anti-PD-L1) in combination with crizotinib or lorlatinib in patients with previously treated advanced NSCLC: phase 1b results from JAVELIN Lung 101. J. Clin. Oncol. 36, 9008 (2018). · DOI
  29. Janku, F. et al. Phase I study of WNT974, a first-in-class Porcupine inhibitor, in advanced solid tumors. Mol. Cancer Ther. 14, C45 (2015). · DOI
  30. Rodon, J. et al. Biomarker analyses from a phase I study of WNT974, a first-in-class Porcupine inhibitor, in patients (pts) with advanced solid tumors. Cancer Res. 78, CT175 (2018). · DOI
  31. Sinicrope, F. A. et al. Association of DNA mismatch repair and mutations in BRAF and KRAS with survival after recurrence in stage III colon cancers: a secondary analysis of 2 randomized clinical trials. JAMA Oncol. 3, 472–480 (2017). · DOI
  32. Wang, Y. et al. Distinct impacts of KRAS, NRAS and BRAF mutations on survival of patients with metastatic colorectal cancer. J. Clin. Oncol. 36, 3513 (2018). · DOI
  33. Brudvik, K. W. et al. RAS mutation clinical risk score to predict survival after resection of colorectal liver metastases. Ann. Surg. 269, 120–126 (2019). · DOI
  34. Marisa, L. et al. Clinical utility of colon cancer molecular subtypes: validation of two main colorectal molecular classifications on the PETACC-8 phase III trial cohort. J. Clin. Oncol. 35, 3509 (2017). · DOI
  35. Yamaguchi, S. et al. A validation study of stratification by the 55-gene classifier for assessing recurrence risk in stage II colon cancer: the 55 STAR study (UMIN23879). J. Clin. Oncol. 36, 3526 (2018). · DOI
  36. Laurent-Puig, P. et al. Colon cancer molecular subtype intratumoral heterogeneity and its prognostic impact: an extensive molecular analysis of the PETACC-8 [abstract 60PD]. Ann. Oncol. 29, mdy269.058 (2018).
  37. Fontana, E., Eason, K., Cervantes, A., Salazar, R. & Sadanandam, A. Context matters — consensus molecular subtypes of colorectal cancer as biomarkers for clinical trials. Ann. Oncol. 30, 520–527 (2019). · DOI
  38. Song, N. et al. Clinical outcome from oxaliplatin treatment in stage II/III colon cancer according to intrinsic subtypes: secondary analysis of NSABP C-07/NRG Oncology randomized clinical trial. JAMA Oncol. 2, 1162–1169 (2016). · DOI
  39. Teufel, M. et al. Molecular subtypes and outcomes in regorafenib-treated patients with metastatic colorectal cancer (mCRC) enrolled in the CORRECT trial. J. Clin. Oncol. 33, 3558 (2015). · DOI · Paper page
  40. Grothey, A. et al. Fluoropyrimidine (FP) + bevacizumab (BEV) + atezolizumab vs FP/BEV in BRAFwt metastatic colorectal cancer (mCRC): findings from Cohort 2 of MODUL — a multicentre, randomized trial of biomarker-driven maintenance treatment following first-line induction therapy [abstract LBA19]. Ann. Oncol. 29, mdy424.020 (2018). · DOI
  41. Kopetz, S. et al. M7824 (MSB0011359C), a bifunctional fusion protein targeting PD-L1 and TGF-β, in patients with heavily pretreated CRC: preliminary results from a phase I trial. J. Clin. Oncol. 36, 764 (2018). · DOI
  42. Bendell, J. C. et al. A phase Ib study of safety and clinical activity of atezolizumab (A) and cobimetinib (C) in patients (pts) with metastatic colorectal cancer (mCRC). J. Clin. Oncol. 36, 560 (2018). · DOI
  43. Sorich, M. J. et al. Extended RAS mutations and anti-EGFR monoclonal antibody survival benefit in metastatic colorectal cancer: a meta-analysis of randomized, controlled trials. Ann. Oncol. 26, 13–21 (2015). · DOI
  44. Hochster, H. S. et al. Efficacy and safety of atezolizumab (atezo) and bevacizumab (bev) in a phase Ib study of microsatellite instability (MSI)-high metastatic colorectal cancer (mCRC). J. Clin. Oncol. 35, 673–673 (2017). · DOI · Paper page

Cited by

Sorted by citations

Metadata

Authors
Sveen, A., Kopetz, S., & Lothe, R. A.
Affiliations
  • Oslo University Hospital (NO)
  • The University of Texas MD Anderson Cancer Center (US)
Corresponding author
Sveen, Anita
Venue
Nature Reviews Clinical Oncology
Published
2019-07-09
Volume
17
Issue
1
Pages
11-32
ISSN
  • 1759-4774 (ISSN-L)
  • 1759-4782
OpenAlex
W2957125530
Cited by
320
References
319
Citations by year
2026: 16 · 2025: 39 · 2024: 55 · 2023: 44 · 2022: 57 · 2021: 65 · 2020: 40 · 2019: 4
FWCI
3.96
Type
journal article
Language
en
Open access
Locations
  • Nature Reviews Clinical Oncology (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institutes of Health (KL2TR000370)
  • National Cancer Institute (R01CA184843, P50CA221707, R01CA218230, R01CA187238, P30CA016672)
  • National Center for Advancing Translational Sciences
Topics
  • Health Sciences › Medicine › Oncology › Colorectal Cancer Treatments and Studies
  • Health Sciences › Medicine › Pathology and Forensic Medicine › Genetic factors in colorectal cancer
  • Health Sciences › Medicine › Oncology › Colorectal Cancer Surgical Treatments
Keywords
colorectal cancer, biomarkers, biomarker interaction, molecular stratification, targeted therapy, prognostic factors, molecular profiling, gene expression subtypes, hypermutator phenotype, gene amplification, gene fusion, point mutations, treatment decision-making
MeSH terms
Clinical Trials as Topic, Humans, Prognosis, Biomarkers, Tumor, Colorectal Neoplasms, Precision Medicine, Molecular Targeted Therapy, Molecular Medicine

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review