A Liquid Biopsy Assay for Noninvasive Identification of Lymph Node Metastases in T1 Colorectal Cancer.


Journal

Gastroenterology
ISSN: 1528-0012
Titre abrégé: Gastroenterology
Pays: United States
ID NLM: 0374630

Informations de publication

Date de publication:
07 2021
Historique:
received: 04 09 2020
revised: 02 03 2021
accepted: 22 03 2021
pubmed: 6 4 2021
medline: 26 10 2021
entrez: 5 4 2021
Statut: ppublish

Résumé

We recently reported use of tissue-based transcriptomic biomarkers (microRNA [miRNA] or messenger RNA [mRNA]) for identification of lymph node metastasis (LNM) in patients with invasive submucosal colorectal cancers (T1 CRC). In this study, we translated our tissue-based biomarkers into a blood-based liquid biopsy assay for noninvasive detection of LNM in patients with high-risk T1 CRC. We analyzed 330 specimens from patients with high-risk T1 CRC, which included 188 serum samples from 2 clinical cohorts-a training cohort (N = 46) and a validation cohort (N = 142)-and matched formalin-fixed paraffin-embedded samples (N = 142). We performed quantitative reverse-transcription polymerase chain reaction, followed by logistic regression analysis, to develop an integrated transcriptomic panel and establish a risk-stratification model combined with clinical risk factors. We used comprehensive expression profiling of a training cohort of LNM-positive and LMN-negative serum specimens to identify an optimized transcriptomic panel of 4 miRNAs (miR-181b, miR-193b, miR-195, and miR-411) and 5 mRNAs (AMT, forkhead box A1 [FOXA1], polymeric immunoglobulin receptor [PIGR], matrix metalloproteinase 1 [MMP1], and matrix metalloproteinase 9 [MMP9]), which robustly identified patients with LNM (area under the curve [AUC], 0.86; 95% confidence interval [CI], 0.72-0.94). We validated panel performance in an independent validation cohort (AUC, 0.82; 95% CI, 0.74-0.88). Our risk-stratification model was more accurate than the panel and an independent predictor for identification of LNM (AUC, 0.90; univariate: odds ratio [OR], 37.17; 95% CI, 4.48-308.35; P < .001; multivariate: OR, 17.28; 95% CI, 1.82-164.07; P = .013). The model limited potential overtreatment to only 18% of all patients, which is dramatically superior to pathologic features that are currently used (92%). A novel risk-stratification model for noninvasive identification of T1 CRC has the potential to avoid unnecessary operations for patients classified as high-risk by conventional risk-classification criteria.

Sections du résumé

BACKGROUND & AIMS
We recently reported use of tissue-based transcriptomic biomarkers (microRNA [miRNA] or messenger RNA [mRNA]) for identification of lymph node metastasis (LNM) in patients with invasive submucosal colorectal cancers (T1 CRC). In this study, we translated our tissue-based biomarkers into a blood-based liquid biopsy assay for noninvasive detection of LNM in patients with high-risk T1 CRC.
METHODS
We analyzed 330 specimens from patients with high-risk T1 CRC, which included 188 serum samples from 2 clinical cohorts-a training cohort (N = 46) and a validation cohort (N = 142)-and matched formalin-fixed paraffin-embedded samples (N = 142). We performed quantitative reverse-transcription polymerase chain reaction, followed by logistic regression analysis, to develop an integrated transcriptomic panel and establish a risk-stratification model combined with clinical risk factors.
RESULTS
We used comprehensive expression profiling of a training cohort of LNM-positive and LMN-negative serum specimens to identify an optimized transcriptomic panel of 4 miRNAs (miR-181b, miR-193b, miR-195, and miR-411) and 5 mRNAs (AMT, forkhead box A1 [FOXA1], polymeric immunoglobulin receptor [PIGR], matrix metalloproteinase 1 [MMP1], and matrix metalloproteinase 9 [MMP9]), which robustly identified patients with LNM (area under the curve [AUC], 0.86; 95% confidence interval [CI], 0.72-0.94). We validated panel performance in an independent validation cohort (AUC, 0.82; 95% CI, 0.74-0.88). Our risk-stratification model was more accurate than the panel and an independent predictor for identification of LNM (AUC, 0.90; univariate: odds ratio [OR], 37.17; 95% CI, 4.48-308.35; P < .001; multivariate: OR, 17.28; 95% CI, 1.82-164.07; P = .013). The model limited potential overtreatment to only 18% of all patients, which is dramatically superior to pathologic features that are currently used (92%).
CONCLUSIONS
A novel risk-stratification model for noninvasive identification of T1 CRC has the potential to avoid unnecessary operations for patients classified as high-risk by conventional risk-classification criteria.

Identifiants

pubmed: 33819484
pii: S0016-5085(21)00589-8
doi: 10.1053/j.gastro.2021.03.062
pmc: PMC10360659
mid: NIHMS1913336
pii:
doi:

Substances chimiques

Biomarkers, Tumor 0
FOXA1 protein, human 0
Hepatocyte Nuclear Factor 3-alpha 0
MicroRNAs 0
RNA, Messenger 0
Receptors, Polymeric Immunoglobulin 0
MMP9 protein, human EC 3.4.24.35
Matrix Metalloproteinase 9 EC 3.4.24.35
MMP1 protein, human EC 3.4.24.7
Matrix Metalloproteinase 1 EC 3.4.24.7

Types de publication

Journal Article Research Support, N.I.H., Extramural Validation Study

Langues

eng

Sous-ensembles de citation

IM

Pagination

151-162.e1

Subventions

Organisme : NCI NIH HHS
ID : R01 CA202797
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA184792
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA181572
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA072851
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA227602
Pays : United States

Commentaires et corrections

Type : CommentIn
Type : CommentIn

Informations de copyright

Copyright © 2021 AGA Institute. Published by Elsevier Inc. All rights reserved.

Références

Sci Rep. 2019 Jun 6;9(1):8342
pubmed: 31171832
Int J Cancer. 2010 Jul 1;127(1):118-26
pubmed: 19876917
Can J Surg. 2018 Feb;61(1):19-27
pubmed: 29368673
Dis Colon Rectum. 2009 Mar;52(3):438-45
pubmed: 19333043
Dis Colon Rectum. 2002 Feb;45(2):200-6
pubmed: 11852333
Endoscopy. 2013 Sep;45(9):718-24
pubmed: 23918621
Endoscopy. 2012 Jun;44(6):590-5
pubmed: 22638780
Gastroenterology. 2018 Mar;154(4):844-848.e7
pubmed: 29199088
J Natl Cancer Inst. 2013 Jun 19;105(12):849-59
pubmed: 23704278
Endoscopy. 2015 Sep;47(9):829-54
pubmed: 26317585
Surg Endosc. 2016 Oct;30(10):4405-15
pubmed: 26895892
Mod Pathol. 2010 Aug;23(8):1068-72
pubmed: 20473277
Gut. 2018 Feb;67(2):284-290
pubmed: 27811313
World J Surg. 2012 Feb;36(2):424-30
pubmed: 22187130
Ann Surg. 2014 Apr;259(4):735-43
pubmed: 23982750
Int J Clin Oncol. 2015 Apr;20(2):207-39
pubmed: 25782566
Am J Clin Pathol. 2019 Sep 9;152(4):463-470
pubmed: 31263894
Gut. 2020 Jun;69(6):977-980
pubmed: 31822579
J Gastroenterol. 2017 Nov;52(11):1169-1179
pubmed: 28194526
JAMA. 2005 Jun 1;293(21):2609-17
pubmed: 15928282
Exp Mol Pathol. 2016 Feb;100(1):125-31
pubmed: 26681654
J Gastrointest Surg. 2004 Dec;8(8):1032-9; discussion 1039-40
pubmed: 15585391
Gut. 2017 Apr;66(4):654-665
pubmed: 26701878
Surgery. 2016 Mar;159(3):713-20
pubmed: 26477474
Dis Colon Rectum. 2003 Oct;46(10 Suppl):S89-93
pubmed: 14530664
Ann Surg. 2012 Sep;256(3):544-51
pubmed: 22868372
Gastroenterology. 2004 Aug;127(2):385-94
pubmed: 15300569
Gastroenterology. 2019 Jun;156(8):2338-2341.e3
pubmed: 30797795
Clin Gastroenterol Hepatol. 2014 Apr;12(4):662-8.e1-2
pubmed: 23872238
Oncol Rep. 2000 Jul-Aug;7(4):783-8
pubmed: 10854544
Gastroenterology. 2013 Mar;144(3):551-9; quiz e14
pubmed: 23232297
Hepatogastroenterology. 2008 Jul-Aug;55(85):1293-7
pubmed: 18795675
J Clin Pathol. 2007 Aug;60(8):912-5
pubmed: 16997919
Ann Surg Treat Res. 2017 Nov;93(5):266-271
pubmed: 29184880
Dig Endosc. 2015 May;27(4):417-434
pubmed: 25652022
J Gastroenterol Hepatol. 2012 Jun;27(6):1057-62
pubmed: 22142484
Medicine (Baltimore). 2016 Sep;95(37):e4373
pubmed: 27631203
Cell Res. 2008 Oct;18(10):997-1006
pubmed: 18766170
Gut. 2009 Oct;58(10):1375-81
pubmed: 19201770
Clin Gastroenterol Hepatol. 2006 Dec;4(12):1522-7
pubmed: 16979956
Methods. 2001 Dec;25(4):402-8
pubmed: 11846609
Hepatogastroenterology. 2004 Jul-Aug;51(58):998-1000
pubmed: 15239233
Mod Pathol. 2020 Dec;33(12):2626-2636
pubmed: 32581367
Ann Oncol. 2016 Oct;27(10):1879-86
pubmed: 27502702
Clin Cancer Res. 2007 Nov 15;13(22 Pt 2):6885s-9s
pubmed: 18006794

Auteurs

Yuma Wada (Y)

Center for Gastrointestinal Research, Baylor Scott & White Research Institute and Charles A. Sammons Cancer Center, Baylor University Medical Center, Dallas, Texas; Department of Surgery, Tokushima University, Tokushima, Japan; Department of Molecular Diagnostics and Experimental Therapeutics, Beckman Research Institute of City of Hope Comprehensive Cancer Center, Duarte, California.

Mitsuo Shimada (M)

Department of Surgery, Tokushima University, Tokushima, Japan.

Tatsuro Murano (T)

Department of Gastroenterology and Endoscopy, National Cancer Center Hospital East, Chiba, Japan.

Hiroyuki Takamaru (H)

Endoscopy Division, National Cancer Center Hospital, Tokyo, Japan.

Yuji Morine (Y)

Department of Surgery, Tokushima University, Tokushima, Japan.

Tetsuya Ikemoto (T)

Department of Surgery, Tokushima University, Tokushima, Japan.

Yu Saito (Y)

Department of Surgery, Tokushima University, Tokushima, Japan.

Francesc Balaguer (F)

Gastroenterology Department, Hospital Clinic de Barcelona, Barcelona, Spain; Department of Gastroenterology, Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), University of Barcelona, Barcelona, Spain.

Luis Bujanda (L)

Gastroenterology Department, Instituto Biodonostia, Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), Universidad del País Vasco (UPV)/Euskal Herriko Unibertsitatea (EHU), San Sebastián, Spain.

Maria Pellise (M)

Gastroenterology Department, Hospital Clinic de Barcelona, Barcelona, Spain; Department of Gastroenterology, Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), University of Barcelona, Barcelona, Spain.

Ken Kato (K)

Department of Gastrointestinal Medical Oncology, National Cancer Center Hospital, Tokyo, Japan; Clinical Research Support Office, Clinical Research Coordinating Section, Biobank Translational Research Support Section, National Cancer Center Hospital, Tokyo, Japan.

Yutaka Saito (Y)

Endoscopy Division, National Cancer Center Hospital, Tokyo, Japan.

Hiroaki Ikematsu (H)

Department of Gastroenterology and Endoscopy, National Cancer Center Hospital East, Chiba, Japan.

Ajay Goel (A)

Center for Gastrointestinal Research, Baylor Scott & White Research Institute and Charles A. Sammons Cancer Center, Baylor University Medical Center, Dallas, Texas; Department of Molecular Diagnostics and Experimental Therapeutics, Beckman Research Institute of City of Hope Comprehensive Cancer Center, Duarte, California. Electronic address: ajgoel@coh.org.

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