A Fecal MicroRNA Signature by Small RNA Sequencing Accurately Distinguishes Colorectal Cancers: Results From a Multicenter Study.


Journal

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

Informations de publication

Date de publication:
09 2023
Historique:
received: 08 08 2022
revised: 18 04 2023
accepted: 24 05 2023
medline: 22 8 2023
pubmed: 2 6 2023
entrez: 1 6 2023
Statut: ppublish

Résumé

Fecal tests currently used for colorectal cancer (CRC) screening show limited accuracy in detecting early tumors or precancerous lesions. In this respect, we comprehensively evaluated stool microRNA (miRNA) profiles as biomarkers for noninvasive CRC diagnosis. A total of 1273 small RNA sequencing experiments were performed in multiple biospecimens. In a cross-sectional study, miRNA profiles were investigated in fecal samples from an Italian and a Czech cohort (155 CRCs, 87 adenomas, 96 other intestinal diseases, 141 colonoscopy-negative controls). A predictive miRNA signature for cancer detection was defined by a machine learning strategy and tested in additional fecal samples from 141 CRC patients and 80 healthy volunteers. miRNA profiles were compared with those of 132 tumors/adenomas paired with adjacent mucosa, 210 plasma extracellular vesicle samples, and 185 fecal immunochemical test leftover samples. Twenty-five miRNAs showed altered levels in the stool of CRC patients in both cohorts (adjusted P < .05). A 5-miRNA signature, including miR-149-3p, miR-607-5p, miR-1246, miR-4488, and miR-6777-5p, distinguished patients from control individuals (area under the curve [AUC], 0.86; 95% confidence interval [CI], 0.79-0.94) and was validated in an independent cohort (AUC, 0.96; 95% CI, 0.92-1.00). The signature classified control individuals from patients with low-/high-stage tumors and advanced adenomas (AUC, 0.82; 95% CI, 0.71-0.97). Tissue miRNA profiles mirrored those of stool samples, and fecal profiles of different gastrointestinal diseases highlighted miRNAs specifically dysregulated in CRC. miRNA profiles in fecal immunochemical test leftover samples showed good correlation with those of stool collected in preservative buffer, and their alterations could be detected in adenoma or CRC patients. Our comprehensive fecal miRNome analysis identified a signature accurately discriminating cancer aimed at improving noninvasive diagnosis and screening strategies.

Sections du résumé

BACKGROUND & AIMS
Fecal tests currently used for colorectal cancer (CRC) screening show limited accuracy in detecting early tumors or precancerous lesions. In this respect, we comprehensively evaluated stool microRNA (miRNA) profiles as biomarkers for noninvasive CRC diagnosis.
METHODS
A total of 1273 small RNA sequencing experiments were performed in multiple biospecimens. In a cross-sectional study, miRNA profiles were investigated in fecal samples from an Italian and a Czech cohort (155 CRCs, 87 adenomas, 96 other intestinal diseases, 141 colonoscopy-negative controls). A predictive miRNA signature for cancer detection was defined by a machine learning strategy and tested in additional fecal samples from 141 CRC patients and 80 healthy volunteers. miRNA profiles were compared with those of 132 tumors/adenomas paired with adjacent mucosa, 210 plasma extracellular vesicle samples, and 185 fecal immunochemical test leftover samples.
RESULTS
Twenty-five miRNAs showed altered levels in the stool of CRC patients in both cohorts (adjusted P < .05). A 5-miRNA signature, including miR-149-3p, miR-607-5p, miR-1246, miR-4488, and miR-6777-5p, distinguished patients from control individuals (area under the curve [AUC], 0.86; 95% confidence interval [CI], 0.79-0.94) and was validated in an independent cohort (AUC, 0.96; 95% CI, 0.92-1.00). The signature classified control individuals from patients with low-/high-stage tumors and advanced adenomas (AUC, 0.82; 95% CI, 0.71-0.97). Tissue miRNA profiles mirrored those of stool samples, and fecal profiles of different gastrointestinal diseases highlighted miRNAs specifically dysregulated in CRC. miRNA profiles in fecal immunochemical test leftover samples showed good correlation with those of stool collected in preservative buffer, and their alterations could be detected in adenoma or CRC patients.
CONCLUSIONS
Our comprehensive fecal miRNome analysis identified a signature accurately discriminating cancer aimed at improving noninvasive diagnosis and screening strategies.

Identifiants

pubmed: 37263306
pii: S0016-5085(23)00811-9
doi: 10.1053/j.gastro.2023.05.037
pii:
doi:

Substances chimiques

MicroRNAs 0
Biomarkers, Tumor 0
MIRN149 microRNA, human 0

Types de publication

Multicenter Study Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

582-599.e8

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.

Auteurs

Barbara Pardini (B)

Italian Institute for Genomic Medicine, Turin, Italy; Candiolo Cancer Institute, FPO-IRCCS, Turin, Italy. Electronic address: barbara.pardini@iigm.it.

Giulio Ferrero (G)

Department of Clinical and Biological Sciences, University of Turin, Turin, Italy; Department of Computer Science, University of Turin, Turin, Italy.

Sonia Tarallo (S)

Italian Institute for Genomic Medicine, Turin, Italy; Candiolo Cancer Institute, FPO-IRCCS, Turin, Italy.

Gaetano Gallo (G)

Department of Surgery, Sapienza University of Rome, Rome, Italy; Department of Colorectal Surgery, Clinica S. Rita, Vercelli, Italy.

Antonio Francavilla (A)

Italian Institute for Genomic Medicine, Turin, Italy.

Nicola Licheri (N)

Department of Computer Science, University of Turin, Turin, Italy.

Mario Trompetto (M)

Department of Colorectal Surgery, Clinica S. Rita, Vercelli, Italy.

Giuseppe Clerico (G)

Department of Colorectal Surgery, Clinica S. Rita, Vercelli, Italy.

Carlo Senore (C)

Epidemiology and Screening Unit-CPO, University Hospital Città della Salute e della Scienza, Turin, Italy.

Sergio Peyre (S)

LILT (Lega Italiana Lotta contro i Tumori), associazione provinciale di Biella, Biella, Italy.

Veronika Vymetalkova (V)

Department of Molecular Biology of Cancer, Institute of Experimental Medicine of the Czech Academy of Sciences, Prague, Czech Republic; Institute of Biology and Medical Genetics, 1st Medical Faculty, Charles University, Prague, Czech Republic; Biomedical Center, Faculty of Medicine in Pilsen, Charles University, Pilsen, Czech Republic.

Ludmila Vodickova (L)

Department of Molecular Biology of Cancer, Institute of Experimental Medicine of the Czech Academy of Sciences, Prague, Czech Republic; Institute of Biology and Medical Genetics, 1st Medical Faculty, Charles University, Prague, Czech Republic; Biomedical Center, Faculty of Medicine in Pilsen, Charles University, Pilsen, Czech Republic.

Vaclav Liska (V)

Biomedical Center, Faculty of Medicine in Pilsen, Charles University, Pilsen, Czech Republic; Department of Surgery, University Hospital and Faculty of Medicine in Pilsen, Charles University, Pilsen, Czech Republic.

Ondrej Vycital (O)

Biomedical Center, Faculty of Medicine in Pilsen, Charles University, Pilsen, Czech Republic; Department of Surgery, University Hospital and Faculty of Medicine in Pilsen, Charles University, Pilsen, Czech Republic.

Miroslav Levy (M)

Department of Surgery, First Faculty of Medicine, Charles University and Thomayer Hospital, Prague, Czech Republic.

Peter Macinga (P)

Department of Gastroenterology and Hepatology, Institute for Clinical and Experimental Medicine, Prague, Czech Republic.

Tomas Hucl (T)

Department of Gastroenterology and Hepatology, Institute for Clinical and Experimental Medicine, Prague, Czech Republic.

Eva Budinska (E)

RECETOX, Faculty of Science, Masaryk University, Brno, Czech Republic.

Pavel Vodicka (P)

Department of Molecular Biology of Cancer, Institute of Experimental Medicine of the Czech Academy of Sciences, Prague, Czech Republic; Institute of Biology and Medical Genetics, 1st Medical Faculty, Charles University, Prague, Czech Republic; Biomedical Center, Faculty of Medicine in Pilsen, Charles University, Pilsen, Czech Republic.

Francesca Cordero (F)

Department of Computer Science, University of Turin, Turin, Italy.

Alessio Naccarati (A)

Italian Institute for Genomic Medicine, Turin, Italy; Candiolo Cancer Institute, FPO-IRCCS, Turin, Italy. Electronic address: alessio.naccarati@iigm.it.

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