Serum coding and non‐coding RNAs as biomarkers of NAFLD and fibrosis severity
Background & Aims In patients with non‐alcoholic fatty liver disease (NAFLD), liver biopsy is the gold standard to detect non‐alcoholic steatohepatitis (NASH) and stage liver fibrosis. We aimed to identify differentially expressed mRNAs and non‐coding RNAs in serum samples of biopsy‐diagnosed mi...
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| Published in: | Liver international Vol. 39; no. 9; pp. 1742 - 1754 |
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| Main Authors: | , , , , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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United States
Wiley Subscription Services, Inc
01.09.2019
John Wiley and Sons Inc |
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| ISSN: | 1478-3223, 1478-3231, 1478-3231 |
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| Abstract | Background & Aims
In patients with non‐alcoholic fatty liver disease (NAFLD), liver biopsy is the gold standard to detect non‐alcoholic steatohepatitis (NASH) and stage liver fibrosis. We aimed to identify differentially expressed mRNAs and non‐coding RNAs in serum samples of biopsy‐diagnosed mild and severe NAFLD patients with respect to controls and to each other.
Methods
We first performed a whole transcriptome analysis through microarray (n = 12: four Control: CTRL; four mild NAFLD: NAS ≤ 4 F0; four severe NAFLD NAS ≥ 5 F3), followed by validation of selected transcripts through real‐time PCRs in an independent internal cohort of 88 subjects (63 NAFLD, 25 CTRL) and in an external cohort of 50 NAFLD patients. A similar analysis was also performed on liver biopsies and HepG2 cells exposed to oleate:palmitate or only palmitate (cellular model of NAFL/NASH) at intracellular/extracellular levels. Transcript correlation with histological/clinical data was also analysed.
Results
We identified several differentially expressed coding/non‐coding RNAs in each group of the study cohort. We validated the up‐regulation of UBE2V1, BNIP3L mRNAs, RP11‐128N14.5 lncRNA, TGFB2/TGFB2‐OT1 coding/lncRNA in patients with NAS ≥ 5 (vs NAS ≤ 4) and the up‐regulation of HBA2 mRNA, TGFB2/TGFB2‐OT1 coding/lncRNA in patients with Fibrosis stages = 3‐4 (vs F = 0‐2). In in vitro models: UBE2V1, RP11‐128N14.5 and TGFB2/TGFB2‐OT1 had an increasing expression trend ranging from CTRL to oleate:palmitate or only palmitate‐treated cells both at intracellular and extracellular level, while BNIP3L was up‐regulated only at extracellular level. UBE2V1, RP11‐128N14.5, TGFB2/TGFB2‐OT1 and HBA2 up‐regulation was also observed at histological level. UBE2V1, RP11‐128N14.5, BNIP3L and TGFB2/TGFB2‐OT1 correlated with histological/biochemical data. Combinations of TGFB2/TGFB2‐OT1 + Fibrosis Index based on the four factors (FIB‐4) showed an Area Under the Curve (AUC) of 0.891 (P = 3.00E‐06) or TGFB2/TGFB2‐OT1 + Fibroscan (AUC = 0.892, P = 2.00E‐06) improved the detection of F = 3‐4 with respect to F = 0‐2 fibrosis stages.
Conclusions
We identified specific serum coding/non‐coding RNA profiles in severe and mild NAFLD patients that possibly mirror the molecular mechanisms underlying NAFLD progression towards NASH/fibrosis. TGFB2/TGFB2‐OT1 detection improves FIB‐4/Fibroscan diagnostic performance for advanced fibrosis discrimination. |
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| AbstractList | Background & AimsIn patients with non‐alcoholic fatty liver disease (NAFLD), liver biopsy is the gold standard to detect non‐alcoholic steatohepatitis (NASH) and stage liver fibrosis. We aimed to identify differentially expressed mRNAs and non‐coding RNAs in serum samples of biopsy‐diagnosed mild and severe NAFLD patients with respect to controls and to each other.MethodsWe first performed a whole transcriptome analysis through microarray (n = 12: four Control: CTRL; four mild NAFLD: NAS ≤ 4 F0; four severe NAFLD NAS ≥ 5 F3), followed by validation of selected transcripts through real‐time PCRs in an independent internal cohort of 88 subjects (63 NAFLD, 25 CTRL) and in an external cohort of 50 NAFLD patients. A similar analysis was also performed on liver biopsies and HepG2 cells exposed to oleate:palmitate or only palmitate (cellular model of NAFL/NASH) at intracellular/extracellular levels. Transcript correlation with histological/clinical data was also analysed.ResultsWe identified several differentially expressed coding/non‐coding RNAs in each group of the study cohort. We validated the up‐regulation of UBE2V1, BNIP3L mRNAs, RP11‐128N14.5 lncRNA, TGFB2/TGFB2‐OT1 coding/lncRNA in patients with NAS ≥ 5 (vs NAS ≤ 4) and the up‐regulation of HBA2 mRNA, TGFB2/TGFB2‐OT1 coding/lncRNA in patients with Fibrosis stages = 3‐4 (vs F = 0‐2). In in vitro models: UBE2V1, RP11‐128N14.5 and TGFB2/TGFB2‐OT1 had an increasing expression trend ranging from CTRL to oleate:palmitate or only palmitate‐treated cells both at intracellular and extracellular level, while BNIP3L was up‐regulated only at extracellular level. UBE2V1, RP11‐128N14.5, TGFB2/TGFB2‐OT1 and HBA2 up‐regulation was also observed at histological level. UBE2V1, RP11‐128N14.5, BNIP3L and TGFB2/TGFB2‐OT1 correlated with histological/biochemical data. Combinations of TGFB2/TGFB2‐OT1 + Fibrosis Index based on the four factors (FIB‐4) showed an Area Under the Curve (AUC) of 0.891 (P = 3.00E‐06) or TGFB2/TGFB2‐OT1 + Fibroscan (AUC = 0.892, P = 2.00E‐06) improved the detection of F = 3‐4 with respect to F = 0‐2 fibrosis stages.ConclusionsWe identified specific serum coding/non‐coding RNA profiles in severe and mild NAFLD patients that possibly mirror the molecular mechanisms underlying NAFLD progression towards NASH/fibrosis. TGFB2/TGFB2‐OT1 detection improves FIB‐4/Fibroscan diagnostic performance for advanced fibrosis discrimination. In patients with non-alcoholic fatty liver disease (NAFLD), liver biopsy is the gold standard to detect non-alcoholic steatohepatitis (NASH) and stage liver fibrosis. We aimed to identify differentially expressed mRNAs and non-coding RNAs in serum samples of biopsy-diagnosed mild and severe NAFLD patients with respect to controls and to each other.BACKGROUND & AIMSIn patients with non-alcoholic fatty liver disease (NAFLD), liver biopsy is the gold standard to detect non-alcoholic steatohepatitis (NASH) and stage liver fibrosis. We aimed to identify differentially expressed mRNAs and non-coding RNAs in serum samples of biopsy-diagnosed mild and severe NAFLD patients with respect to controls and to each other.We first performed a whole transcriptome analysis through microarray (n = 12: four Control: CTRL; four mild NAFLD: NAS ≤ 4 F0; four severe NAFLD NAS ≥ 5 F3), followed by validation of selected transcripts through real-time PCRs in an independent internal cohort of 88 subjects (63 NAFLD, 25 CTRL) and in an external cohort of 50 NAFLD patients. A similar analysis was also performed on liver biopsies and HepG2 cells exposed to oleate:palmitate or only palmitate (cellular model of NAFL/NASH) at intracellular/extracellular levels. Transcript correlation with histological/clinical data was also analysed.METHODSWe first performed a whole transcriptome analysis through microarray (n = 12: four Control: CTRL; four mild NAFLD: NAS ≤ 4 F0; four severe NAFLD NAS ≥ 5 F3), followed by validation of selected transcripts through real-time PCRs in an independent internal cohort of 88 subjects (63 NAFLD, 25 CTRL) and in an external cohort of 50 NAFLD patients. A similar analysis was also performed on liver biopsies and HepG2 cells exposed to oleate:palmitate or only palmitate (cellular model of NAFL/NASH) at intracellular/extracellular levels. Transcript correlation with histological/clinical data was also analysed.We identified several differentially expressed coding/non-coding RNAs in each group of the study cohort. We validated the up-regulation of UBE2V1, BNIP3L mRNAs, RP11-128N14.5 lncRNA, TGFB2/TGFB2-OT1 coding/lncRNA in patients with NAS ≥ 5 (vs NAS ≤ 4) and the up-regulation of HBA2 mRNA, TGFB2/TGFB2-OT1 coding/lncRNA in patients with Fibrosis stages = 3-4 (vs F = 0-2). In in vitro models: UBE2V1, RP11-128N14.5 and TGFB2/TGFB2-OT1 had an increasing expression trend ranging from CTRL to oleate:palmitate or only palmitate-treated cells both at intracellular and extracellular level, while BNIP3L was up-regulated only at extracellular level. UBE2V1, RP11-128N14.5, TGFB2/TGFB2-OT1 and HBA2 up-regulation was also observed at histological level. UBE2V1, RP11-128N14.5, BNIP3L and TGFB2/TGFB2-OT1 correlated with histological/biochemical data. Combinations of TGFB2/TGFB2-OT1 + Fibrosis Index based on the four factors (FIB-4) showed an Area Under the Curve (AUC) of 0.891 (P = 3.00E-06) or TGFB2/TGFB2-OT1 + Fibroscan (AUC = 0.892, P = 2.00E-06) improved the detection of F = 3-4 with respect to F = 0-2 fibrosis stages.RESULTSWe identified several differentially expressed coding/non-coding RNAs in each group of the study cohort. We validated the up-regulation of UBE2V1, BNIP3L mRNAs, RP11-128N14.5 lncRNA, TGFB2/TGFB2-OT1 coding/lncRNA in patients with NAS ≥ 5 (vs NAS ≤ 4) and the up-regulation of HBA2 mRNA, TGFB2/TGFB2-OT1 coding/lncRNA in patients with Fibrosis stages = 3-4 (vs F = 0-2). In in vitro models: UBE2V1, RP11-128N14.5 and TGFB2/TGFB2-OT1 had an increasing expression trend ranging from CTRL to oleate:palmitate or only palmitate-treated cells both at intracellular and extracellular level, while BNIP3L was up-regulated only at extracellular level. UBE2V1, RP11-128N14.5, TGFB2/TGFB2-OT1 and HBA2 up-regulation was also observed at histological level. UBE2V1, RP11-128N14.5, BNIP3L and TGFB2/TGFB2-OT1 correlated with histological/biochemical data. Combinations of TGFB2/TGFB2-OT1 + Fibrosis Index based on the four factors (FIB-4) showed an Area Under the Curve (AUC) of 0.891 (P = 3.00E-06) or TGFB2/TGFB2-OT1 + Fibroscan (AUC = 0.892, P = 2.00E-06) improved the detection of F = 3-4 with respect to F = 0-2 fibrosis stages.We identified specific serum coding/non-coding RNA profiles in severe and mild NAFLD patients that possibly mirror the molecular mechanisms underlying NAFLD progression towards NASH/fibrosis. TGFB2/TGFB2-OT1 detection improves FIB-4/Fibroscan diagnostic performance for advanced fibrosis discrimination.CONCLUSIONSWe identified specific serum coding/non-coding RNA profiles in severe and mild NAFLD patients that possibly mirror the molecular mechanisms underlying NAFLD progression towards NASH/fibrosis. TGFB2/TGFB2-OT1 detection improves FIB-4/Fibroscan diagnostic performance for advanced fibrosis discrimination. In patients with non-alcoholic fatty liver disease (NAFLD), liver biopsy is the gold standard to detect non-alcoholic steatohepatitis (NASH) and stage liver fibrosis. We aimed to identify differentially expressed mRNAs and non-coding RNAs in serum samples of biopsy-diagnosed mild and severe NAFLD patients with respect to controls and to each other. We first performed a whole transcriptome analysis through microarray (n = 12: four Control: CTRL; four mild NAFLD: NAS ≤ 4 F0; four severe NAFLD NAS ≥ 5 F3), followed by validation of selected transcripts through real-time PCRs in an independent internal cohort of 88 subjects (63 NAFLD, 25 CTRL) and in an external cohort of 50 NAFLD patients. A similar analysis was also performed on liver biopsies and HepG2 cells exposed to oleate:palmitate or only palmitate (cellular model of NAFL/NASH) at intracellular/extracellular levels. Transcript correlation with histological/clinical data was also analysed. We identified several differentially expressed coding/non-coding RNAs in each group of the study cohort. We validated the up-regulation of UBE2V1, BNIP3L mRNAs, RP11-128N14.5 lncRNA, TGFB2/TGFB2-OT1 coding/lncRNA in patients with NAS ≥ 5 (vs NAS ≤ 4) and the up-regulation of HBA2 mRNA, TGFB2/TGFB2-OT1 coding/lncRNA in patients with Fibrosis stages = 3-4 (vs F = 0-2). In in vitro models: UBE2V1, RP11-128N14.5 and TGFB2/TGFB2-OT1 had an increasing expression trend ranging from CTRL to oleate:palmitate or only palmitate-treated cells both at intracellular and extracellular level, while BNIP3L was up-regulated only at extracellular level. UBE2V1, RP11-128N14.5, TGFB2/TGFB2-OT1 and HBA2 up-regulation was also observed at histological level. UBE2V1, RP11-128N14.5, BNIP3L and TGFB2/TGFB2-OT1 correlated with histological/biochemical data. Combinations of TGFB2/TGFB2-OT1 + Fibrosis Index based on the four factors (FIB-4) showed an Area Under the Curve (AUC) of 0.891 (P = 3.00E-06) or TGFB2/TGFB2-OT1 + Fibroscan (AUC = 0.892, P = 2.00E-06) improved the detection of F = 3-4 with respect to F = 0-2 fibrosis stages. We identified specific serum coding/non-coding RNA profiles in severe and mild NAFLD patients that possibly mirror the molecular mechanisms underlying NAFLD progression towards NASH/fibrosis. TGFB2/TGFB2-OT1 detection improves FIB-4/Fibroscan diagnostic performance for advanced fibrosis discrimination. Background & Aims In patients with non‐alcoholic fatty liver disease (NAFLD), liver biopsy is the gold standard to detect non‐alcoholic steatohepatitis (NASH) and stage liver fibrosis. We aimed to identify differentially expressed mRNAs and non‐coding RNAs in serum samples of biopsy‐diagnosed mild and severe NAFLD patients with respect to controls and to each other. Methods We first performed a whole transcriptome analysis through microarray (n = 12: four Control: CTRL; four mild NAFLD: NAS ≤ 4 F0; four severe NAFLD NAS ≥ 5 F3), followed by validation of selected transcripts through real‐time PCRs in an independent internal cohort of 88 subjects (63 NAFLD, 25 CTRL) and in an external cohort of 50 NAFLD patients. A similar analysis was also performed on liver biopsies and HepG2 cells exposed to oleate:palmitate or only palmitate (cellular model of NAFL/NASH) at intracellular/extracellular levels. Transcript correlation with histological/clinical data was also analysed. Results We identified several differentially expressed coding/non‐coding RNAs in each group of the study cohort. We validated the up‐regulation of UBE2V1, BNIP3L mRNAs, RP11‐128N14.5 lncRNA, TGFB2/TGFB2‐OT1 coding/lncRNA in patients with NAS ≥ 5 (vs NAS ≤ 4) and the up‐regulation of HBA2 mRNA, TGFB2/TGFB2‐OT1 coding/lncRNA in patients with Fibrosis stages = 3‐4 (vs F = 0‐2). In in vitro models: UBE2V1, RP11‐128N14.5 and TGFB2/TGFB2‐OT1 had an increasing expression trend ranging from CTRL to oleate:palmitate or only palmitate‐treated cells both at intracellular and extracellular level, while BNIP3L was up‐regulated only at extracellular level. UBE2V1, RP11‐128N14.5, TGFB2/TGFB2‐OT1 and HBA2 up‐regulation was also observed at histological level. UBE2V1, RP11‐128N14.5, BNIP3L and TGFB2/TGFB2‐OT1 correlated with histological/biochemical data. Combinations of TGFB2/TGFB2‐OT1 + Fibrosis Index based on the four factors (FIB‐4) showed an Area Under the Curve (AUC) of 0.891 (P = 3.00E‐06) or TGFB2/TGFB2‐OT1 + Fibroscan (AUC = 0.892, P = 2.00E‐06) improved the detection of F = 3‐4 with respect to F = 0‐2 fibrosis stages. Conclusions We identified specific serum coding/non‐coding RNA profiles in severe and mild NAFLD patients that possibly mirror the molecular mechanisms underlying NAFLD progression towards NASH/fibrosis. TGFB2/TGFB2‐OT1 detection improves FIB‐4/Fibroscan diagnostic performance for advanced fibrosis discrimination. |
| Author | Purrello, Francesco Urbano, Francesca Di Mauro, Stefania Pipitone, Rosaria M. Fracanzani, Anna Petta, Salvatore Dongiovanni, Paola Privitera, Graziella Rabuazzo, Agata M. Ragusa, Marco Purrello, Michele Grimaudo, Stefania Scamporrino, Alessandra Craxì, Antonio Di Pino, Antonino Valenti, Luca Di Martino, Maria T. Filippello, Agnese Piro, Salvatore Scicali, Roberto Scionti, Francesca |
| AuthorAffiliation | 5 Department of Experimental and Clinical Medicine Magna Graecia University Catanzaro Italy 1 Department of Clinical and Experimental Medicine, Internal Medicine, Garibaldi‐Nesima Hospital University of Catania Catania Italy 4 Oasi Research Institute - IRCCS Troina 94018 Italy 6 Translational Medicine University of Milan, Fondazione IRCCS Ca' Granda Pad Marangoni Milan Italy 3 Department of BioMedical Sciences and BioTechnology Section of Biology and Genetics Giovanni Sichel, Unit of Molecular, Genome and Complex Systems BioMedicine Catania Italy 2 Section of Gastroenterology, Di.Bi.M.I.S University of Palermo Palermo Italy 7 Department of Pathophysiology and Transplantation, Section of Internal Medicine University of Milan, Fondazione Ca' Granda IRCCS Ospedale Maggiore Policlinico Milan Italy |
| AuthorAffiliation_xml | – name: 1 Department of Clinical and Experimental Medicine, Internal Medicine, Garibaldi‐Nesima Hospital University of Catania Catania Italy – name: 2 Section of Gastroenterology, Di.Bi.M.I.S University of Palermo Palermo Italy – name: 4 Oasi Research Institute - IRCCS Troina 94018 Italy – name: 6 Translational Medicine University of Milan, Fondazione IRCCS Ca' Granda Pad Marangoni Milan Italy – name: 7 Department of Pathophysiology and Transplantation, Section of Internal Medicine University of Milan, Fondazione Ca' Granda IRCCS Ospedale Maggiore Policlinico Milan Italy – name: 3 Department of BioMedical Sciences and BioTechnology Section of Biology and Genetics Giovanni Sichel, Unit of Molecular, Genome and Complex Systems BioMedicine Catania Italy – name: 5 Department of Experimental and Clinical Medicine Magna Graecia University Catanzaro Italy |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31169972$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | 2019 The Authors. Published by John Wiley & Sons Ltd 2019 The Authors. Liver International Published by John Wiley & Sons Ltd. 2019 John Wiley & Sons A/S |
| Copyright_xml | – notice: 2019 The Authors. Published by John Wiley & Sons Ltd – notice: 2019 The Authors. Liver International Published by John Wiley & Sons Ltd. – notice: 2019 John Wiley & Sons A/S |
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| Keywords | RNAs NAFLD liquid-biopsy fibrosis NASH |
| Language | English |
| License | Attribution 2019 The Authors. Liver International Published by John Wiley & Sons Ltd. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. |
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| Notes | Funding information This study was funded by 2016/2018 Department Research Plan of University of Catania, Department of Clinical and Experimental Medicine (project #A) and by 2016/2018 Department Research Plan of University of Catania, Department of Biomedical and Biotechnological Sciences (2nd line of intervention). Handling Editor: Frank Tacke ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Handling Editor: Frank Tacke Stefania Di Mauro and Alessandra Scamporrino authors contributed equally to this manuscript. |
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| References | 2017; 7 2015; 14 2017; 1 2017; 49 2015; 50 2007; 165 2017; 65 2015; 11 2004; 45 2017; 23 2019; 17 2016; 2016 2018; 41 2011; 6 2015; 7 2014; 60 2001; 47 2016; 79 2016; 283 2015; 67 2018; 19 2018; 18 2016; 6 2009; 58 2002; 48 2016; 7 2013; 37 2013; 33 2007; 170 2015; 61 2018; 115 2008; 27 2015; 21 2016; 432 2014; 59 2008; 117 2008; 412 2018; 50 2012; 6 2014; 9 2016; 26 2009; 1792 2007; 46 2010; 51 2016; 151 e_1_2_19_28_1 e_1_2_19_29_1 e_1_2_19_26_1 e_1_2_19_49_1 e_1_2_19_27_1 e_1_2_19_48_1 e_1_2_19_20_1 e_1_2_19_43_1 e_1_2_19_21_1 e_1_2_19_42_1 Tesfay M (e_1_2_19_3_1) 2018; 115 e_1_2_19_41_1 e_1_2_19_40_1 e_1_2_19_24_1 e_1_2_19_47_1 e_1_2_19_25_1 e_1_2_19_22_1 e_1_2_19_45_1 Tu L (e_1_2_19_46_1) 2018; 41 Arita T (e_1_2_19_15_1) 2013; 33 e_1_2_19_23_1 e_1_2_19_44_1 e_1_2_19_9_1 e_1_2_19_8_1 e_1_2_19_7_1 e_1_2_19_6_1 e_1_2_19_5_1 e_1_2_19_4_1 e_1_2_19_2_1 Hasselmann DO (e_1_2_19_14_1) 2001; 47 e_1_2_19_16_1 e_1_2_19_39_1 e_1_2_19_18_1 e_1_2_19_37_1 e_1_2_19_17_1 e_1_2_19_38_1 e_1_2_19_19_1 e_1_2_19_31_1 e_1_2_19_32_1 e_1_2_19_10_1 e_1_2_19_30_1 e_1_2_19_12_1 e_1_2_19_35_1 e_1_2_19_11_1 e_1_2_19_36_1 e_1_2_19_33_1 e_1_2_19_13_1 e_1_2_19_34_1 |
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| Snippet | Background & Aims
In patients with non‐alcoholic fatty liver disease (NAFLD), liver biopsy is the gold standard to detect non‐alcoholic steatohepatitis (NASH)... In patients with non-alcoholic fatty liver disease (NAFLD), liver biopsy is the gold standard to detect non-alcoholic steatohepatitis (NASH) and stage liver... Background & AimsIn patients with non‐alcoholic fatty liver disease (NAFLD), liver biopsy is the gold standard to detect non‐alcoholic steatohepatitis (NASH)... |
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| SubjectTerms | Adult Biomarkers Biomarkers - blood Biopsy Cohort Studies Control Diagnostic systems Disease Progression DNA microarrays Extracellular levels Fatty liver Female Fibrosis Gene expression Gene Expression Profiling Hepatocytes Humans Intracellular liquid‐biopsy Liver Liver - enzymology Liver - pathology Liver Cirrhosis - blood Liver Cirrhosis - diagnosis Liver Cirrhosis - pathology Liver diseases Male Metabolic Liver Disease Middle Aged Molecular modelling NAFLD NASH Non-alcoholic Fatty Liver Disease - blood Non-alcoholic Fatty Liver Disease - diagnosis Non-alcoholic Fatty Liver Disease - pathology Palmitic acid Predictive Value of Tests RNA, Untranslated - blood RNAs ROC Curve Severity of Illness Index Transcription |
| Title | Serum coding and non‐coding RNAs as biomarkers of NAFLD and fibrosis severity |
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