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

B. Pardini, G. Ferrero, S. Tarallo, G. Gallo, A. Francavilla, N. Licheri, M. Trompetto, G. Clerico, C. Senore, S. Peyre, V. Vymetalkova, L. Vodickova, V. Liska, O. Vycital, M. Levy, P. Macinga, T. Hucl, E. Budinska, P. Vodicka, F. Cordero, A. Naccarati

. 2023 ; 165 (3) : 582-599.e8. [pub] 20230530

Jazyk angličtina Země Spojené státy americké

Typ dokumentu multicentrická studie, časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/bmc23016424

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.

Citace poskytuje Crossref.org

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$a Pardini, Barbara $u Italian Institute for Genomic Medicine, Turin, Italy; Candiolo Cancer Institute, FPO-IRCCS, Turin, Italy. Electronic address: barbara.pardini@iigm.it
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$a 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.
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$a Ferrero, Giulio $u Department of Clinical and Biological Sciences, University of Turin, Turin, Italy; Department of Computer Science, University of Turin, Turin, Italy
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$a Tarallo, Sonia $u Italian Institute for Genomic Medicine, Turin, Italy; Candiolo Cancer Institute, FPO-IRCCS, Turin, Italy
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$a Gallo, Gaetano $u Department of Surgery, Sapienza University of Rome, Rome, Italy; Department of Colorectal Surgery, Clinica S. Rita, Vercelli, Italy
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$a Francavilla, Antonio $u Italian Institute for Genomic Medicine, Turin, Italy
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$a Licheri, Nicola $u Department of Computer Science, University of Turin, Turin, Italy
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$a Trompetto, Mario $u Department of Colorectal Surgery, Clinica S. Rita, Vercelli, Italy
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$a Clerico, Giuseppe $u Department of Colorectal Surgery, Clinica S. Rita, Vercelli, Italy
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$a Senore, Carlo $u Epidemiology and Screening Unit-CPO, University Hospital Città della Salute e della Scienza, Turin, Italy
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$a Peyre, Sergio $u LILT (Lega Italiana Lotta contro i Tumori), associazione provinciale di Biella, Biella, Italy
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$a Vymetalkova, Veronika $u Department of Molecular Biology of Cancer, Institute of Experimental Medicine of the Czech Academy of Sciences, Prague, Czech Republic; Institute of Biology and Medical Genetics, 1st Medical Faculty, Charles University, Prague, Czech Republic; Biomedical Center, Faculty of Medicine in Pilsen, Charles University, Pilsen, Czech Republic
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$a Vodickova, Ludmila $u Department of Molecular Biology of Cancer, Institute of Experimental Medicine of the Czech Academy of Sciences, Prague, Czech Republic; Institute of Biology and Medical Genetics, 1st Medical Faculty, Charles University, Prague, Czech Republic; Biomedical Center, Faculty of Medicine in Pilsen, Charles University, Pilsen, Czech Republic
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$a Liska, Vaclav $u Biomedical Center, Faculty of Medicine in Pilsen, Charles University, Pilsen, Czech Republic; Department of Surgery, University Hospital and Faculty of Medicine in Pilsen, Charles University, Pilsen, Czech Republic
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$a Vycital, Ondrej $u Biomedical Center, Faculty of Medicine in Pilsen, Charles University, Pilsen, Czech Republic; Department of Surgery, University Hospital and Faculty of Medicine in Pilsen, Charles University, Pilsen, Czech Republic
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$a Levy, Miroslav $u Department of Surgery, First Faculty of Medicine, Charles University and Thomayer Hospital, Prague, Czech Republic
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$a Macinga, Peter $u Department of Gastroenterology and Hepatology, Institute for Clinical and Experimental Medicine, Prague, Czech Republic
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$a Hucl, Tomas $u Department of Gastroenterology and Hepatology, Institute for Clinical and Experimental Medicine, Prague, Czech Republic
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$a Budinska, Eva $u RECETOX, Faculty of Science, Masaryk University, Brno, Czech Republic
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$a Vodicka, Pavel $u Department of Molecular Biology of Cancer, Institute of Experimental Medicine of the Czech Academy of Sciences, Prague, Czech Republic; Institute of Biology and Medical Genetics, 1st Medical Faculty, Charles University, Prague, Czech Republic; Biomedical Center, Faculty of Medicine in Pilsen, Charles University, Pilsen, Czech Republic
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$a Cordero, Francesca $u Department of Computer Science, University of Turin, Turin, Italy
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$a Naccarati, Alessio $u Italian Institute for Genomic Medicine, Turin, Italy; Candiolo Cancer Institute, FPO-IRCCS, Turin, Italy. Electronic address: alessio.naccarati@iigm.it
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