Candidate biomarkers for the diagnosis and prognosis of drug‐induced liver injury: An international collaborative effort
Current blood biomarkers are suboptimal in detecting drug‐induced liver injury (DILI) and predicting its outcome. We sought to characterize the natural variabilty and performance characteristics of 14 promising DILI biomarker candidates. Serum or plasma from multiple cohorts of healthy volunteers (n...
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| Published in: | Hepatology (Baltimore, Md.) Vol. 69; no. 2; pp. 760 - 773 |
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| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
United States
Wiley Subscription Services, Inc
01-02-2019
Wiley-Blackwell |
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| Abstract | Current blood biomarkers are suboptimal in detecting drug‐induced liver injury (DILI) and predicting its outcome. We sought to characterize the natural variabilty and performance characteristics of 14 promising DILI biomarker candidates. Serum or plasma from multiple cohorts of healthy volunteers (n = 192 and n = 81), subjects who safely took potentially hepatotoxic drugs without adverse effects (n = 55 and n = 92) and DILI patients (n = 98, n = 28, and n = 143) were assayed for microRNA‐122 (miR‐122), glutamate dehydrogenase (GLDH), total cytokeratin 18 (K18), caspase cleaved K18, glutathione S‐transferase α, alpha‐fetoprotein, arginase‐1, osteopontin (OPN), sorbitol dehydrogenase, fatty acid binding protein, cadherin‐5, macrophage colony‐stimulating factor receptor (MCSFR), paraoxonase 1 (normalized to prothrombin protein), and leukocyte cell‐derived chemotaxin‐2. Most candidate biomarkers were significantly altered in DILI cases compared with healthy volunteers. GLDH correlated more closely with gold standard alanine aminotransferase than miR‐122, and there was a surprisingly wide inter‐ and intra‐individual variability of miR‐122 levels among healthy volunteers. Serum K18, OPN, and MCSFR levels were most strongly associated with liver‐related death or transplantation within 6 months of DILI onset. Prediction of prognosis among DILI patients using the Model for End‐Stage Liver Disease was improved by incorporation of K18 and MCSFR levels. Conclusion: GLDH appears to be more useful than miR‐122 in identifying DILI patients, and K18, OPN, and MCSFR are promising candidates for prediction of prognosis during an acute DILI event. Serial assessment of these biomarkers in large prospective studies will help further delineate their role in DILI diagnosis and management. |
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| AbstractList | Current blood biomarkers are suboptimal in detecting drug‐induced liver injury (DILI) and predicting its outcome. We sought to characterize the natural variabilty and performance characteristics of 14 promising DILI biomarker candidates. Serum or plasma from multiple cohorts of healthy volunteers (n = 192 and n = 81), subjects who safely took potentially hepatotoxic drugs without adverse effects (n = 55 and n = 92) and DILI patients (n = 98, n = 28, and n = 143) were assayed for microRNA‐122 (miR‐122), glutamate dehydrogenase (GLDH), total cytokeratin 18 (K18), caspase cleaved K18, glutathione S ‐transferase α, alpha‐fetoprotein, arginase‐1, osteopontin (OPN), sorbitol dehydrogenase, fatty acid binding protein, cadherin‐5, macrophage colony‐stimulating factor receptor (MCSFR), paraoxonase 1 (normalized to prothrombin protein), and leukocyte cell‐derived chemotaxin‐2. Most candidate biomarkers were significantly altered in DILI cases compared with healthy volunteers. GLDH correlated more closely with gold standard alanine aminotransferase than miR‐122, and there was a surprisingly wide inter‐ and intra‐individual variability of miR‐122 levels among healthy volunteers. Serum K18, OPN, and MCSFR levels were most strongly associated with liver‐related death or transplantation within 6 months of DILI onset. Prediction of prognosis among DILI patients using the Model for End‐Stage Liver Disease was improved by incorporation of K18 and MCSFR levels. Conclusion : GLDH appears to be more useful than miR‐122 in identifying DILI patients, and K18, OPN, and MCSFR are promising candidates for prediction of prognosis during an acute DILI event. Serial assessment of these biomarkers in large prospective studies will help further delineate their role in DILI diagnosis and management. Current blood biomarkers are suboptimal in detecting drug-induced liver injury (DILI) and predicting its outcome. We sought to characterize the natural variabilty and performance characteristics of fourteen promising DILI biomarker candidates. Serum or plasma from multiple cohorts of healthy volunteers (n=192 and =81), subjects who safely took potentially hepatotoxic drugs without adverse effects (n=55 and =92) and DILI patients (n=98, =28, and =143) were assayed for microRNA-122 (miR-122), glutamate dehydrogenase (GLDH), total keratin 18 (K18), caspase cleaved K18 (ccK18), glutathione S-transferase alpha (GSTα), alpha fetoprotein (AFP), arginase-1 (ARG1), osteopontin (OPN), sorbitol dehydrogenase (SDH), fatty acid binding protein (FABP1), cadherin-5 (CDH5), macrophage colony stimulating factor receptor (MCSFR), paraoxonase 1 (PON1, normalized to prothrombin protein), and leucocyte cell-derived chemotaxin-2 (LECT2). Most candidate biomarkers were significantly altered in DILI cases compared to healthy volunteers. GLDH correlated more closely with gold standard alanine aminotransferase (ALT) than miR-122 and there was a surprisingly wide inter- and intra-individual variability of miR-122 levels among the healthy volunteers. Serum K18, OPN, and MCSFR levels were most strongly associated with liver-related death or transplant within 6 months of DILI-onset. Prediction of prognosis among DILI patients using Model for End-stage Liver Disease (MELD) was improved by incorporation of K18 and MCSFR levels. Conclusion : GLDH appears to be more useful than miR-122 in identifying DILI patients. K18, OPN and MCSFR are promising candidates for prediction of prognosis during an acute DILI event. Serial assessment of these biomarkers in large prospective studies will help further delineate their role in DILI diagnosis and management. |
| Author | Sauer, John‐Michael Poynard, Thierry Fontana, Robert J. Marcinak, John Chalasani, Naga Wolenski, Francis Bonkovsky, Herbert L. Kirby, Simon Kullak‐Ublick, Gerd A. Kirby, Patrick Schuppe‐Koistinen, Ina Hackman, Frances Goepfert, Jens C. Arber, Nadir King, Nicholas M. P. van Bömmel, Florian Ormarsdottir, Sif Andrade, Raul J. Watkins, Paul B. Schomaker, Shelli J. Church, Rachel J. Aubrecht, Jiri Merz, Michael |
| AuthorAffiliation | 9 Natural and Medical Sciences Institute, Reutlingen, Germany 2 Division of Pharmacotherapy and Experimental Therapeutics, UNC Eshelman School of Pharmacy, Chapel Hill, North Carolina 3 Department of Clinical Pharmacology and Toxicology, University Hospital Zurich, University of Zurich, Switzerland 1 Institute for Drug Safety Sciences, University of North Carolina at Chapel Hill, Research Triangle Park, NC 21 Department of Hepatology, Groupe Hospitalier Pitié Salpêtrière, University Pierre et Marie Curie, INSERM UMR 938, Paris, France 20 Section of Hepatology, Clinic of Gastroenterology and Hepatology, University Hospital Leipzig, Leipzig, Germany 5 Drug Safety R&D, Pfizer Inc,. Groton, CT 17 Tel Aviv Sourasky Medical Center, Tel Aviv University, Israel 8 University of Michigan, Ann Arbor, MI 7 School of Medicine, Indiana University, Indianapolis, IN 18 Discovery and Investigative Safety, Novartis Institutes for Biomedical Research, Basel, Switzerland 19 Unidad de Gestión Clínica de Aparato Diges |
| AuthorAffiliation_xml | – name: 6 Wake Forest University School of Medicine, Winston-Salem, NC – name: 5 Drug Safety R&D, Pfizer Inc,. Groton, CT – name: 14 Global Patient Safety, AstraZeneca R&D, Gothenburg, Sweden – name: 7 School of Medicine, Indiana University, Indianapolis, IN – name: 16 Science for Life Laboratory, Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden – name: 1 Institute for Drug Safety Sciences, University of North Carolina at Chapel Hill, Research Triangle Park, NC – name: 4 Mechanistic Safety, Novartis Global Drug Development, Basel, Switzerland – name: 18 Discovery and Investigative Safety, Novartis Institutes for Biomedical Research, Basel, Switzerland – name: 20 Section of Hepatology, Clinic of Gastroenterology and Hepatology, University Hospital Leipzig, Leipzig, Germany – name: 2 Division of Pharmacotherapy and Experimental Therapeutics, UNC Eshelman School of Pharmacy, Chapel Hill, North Carolina – name: 3 Department of Clinical Pharmacology and Toxicology, University Hospital Zurich, University of Zurich, Switzerland – name: 10 Pfizer Inc., New York, USA – name: 11 Predictive Safety Testing Consortium, Tucson AZ, USA – name: 21 Department of Hepatology, Groupe Hospitalier Pitié Salpêtrière, University Pierre et Marie Curie, INSERM UMR 938, Paris, France – name: 9 Natural and Medical Sciences Institute, Reutlingen, Germany – name: 17 Tel Aviv Sourasky Medical Center, Tel Aviv University, Israel – name: 12 Takeda Pharmaceuticals, Deerfield, IL – name: 8 University of Michigan, Ann Arbor, MI – name: 19 Unidad de Gestión Clínica de Aparato Digestivo, Instituto de Investigación Biomédica de Málaga-IBIMA, Hospital Universitario Virgen de la Victoria, Universidad de Málaga, Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Málaga, Spain |
| Author_xml | – sequence: 1 givenname: Rachel J. surname: Church fullname: Church, Rachel J. email: rchurch@unc.edu organization: University of North Carolina Eshelman School of Pharmacy – sequence: 2 givenname: Gerd A. surname: Kullak‐Ublick fullname: Kullak‐Ublick, Gerd A. organization: Novartis Global Drug Development – sequence: 3 givenname: Jiri surname: Aubrecht fullname: Aubrecht, Jiri organization: Pfizer Inc – sequence: 4 givenname: Herbert L. surname: Bonkovsky fullname: Bonkovsky, Herbert L. organization: Wake Forest University School of Medicine – sequence: 5 givenname: Naga surname: Chalasani fullname: Chalasani, Naga organization: Indiana University – sequence: 6 givenname: Robert J. surname: Fontana fullname: Fontana, Robert J. organization: University of Michigan – sequence: 7 givenname: Jens C. surname: Goepfert fullname: Goepfert, Jens C. organization: Natural and Medical Sciences Institute – sequence: 8 givenname: Frances surname: Hackman fullname: Hackman, Frances organization: Pfizer Inc – sequence: 9 givenname: Nicholas M. P. surname: King fullname: King, Nicholas M. P. organization: Predictive Safety Testing Consortium – sequence: 10 givenname: Simon surname: Kirby fullname: Kirby, Simon organization: Pfizer Inc – sequence: 11 givenname: Patrick surname: Kirby fullname: Kirby, Patrick organization: Takeda Pharmaceuticals – sequence: 12 givenname: John surname: Marcinak fullname: Marcinak, John organization: Takeda Pharmaceuticals – sequence: 13 givenname: Sif surname: Ormarsdottir fullname: Ormarsdottir, Sif organization: AstraZeneca R&D – sequence: 14 givenname: Shelli J. surname: Schomaker fullname: Schomaker, Shelli J. organization: Pfizer Inc – sequence: 15 givenname: Ina surname: Schuppe‐Koistinen fullname: Schuppe‐Koistinen, Ina organization: Karolinska Institute – sequence: 16 givenname: Francis surname: Wolenski fullname: Wolenski, Francis organization: Takeda Pharmaceuticals – sequence: 17 givenname: Nadir surname: Arber fullname: Arber, Nadir organization: Tel Aviv University – sequence: 18 givenname: Michael surname: Merz fullname: Merz, Michael organization: Novartis Institutes for Biomedical Research – sequence: 19 givenname: John‐Michael surname: Sauer fullname: Sauer, John‐Michael organization: Predictive Safety Testing Consortium – sequence: 20 givenname: Raul J. surname: Andrade fullname: Andrade, Raul J. organization: Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd) – sequence: 21 givenname: Florian surname: van Bömmel fullname: van Bömmel, Florian organization: University Hospital Leipzig – sequence: 22 givenname: Thierry surname: Poynard fullname: Poynard, Thierry organization: University Pierre et Marie Curie, INSERM UMR 938 – sequence: 23 givenname: Paul B. surname: Watkins fullname: Watkins, Paul B. organization: University of North Carolina Eshelman School of Pharmacy |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29357190$$D View this record in MEDLINE/PubMed https://hal.sorbonne-universite.fr/hal-03974879$$DView record in HAL http://kipublications.ki.se/Default.aspx?queryparsed=id:140189261$$DView record from Swedish Publication Index |
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| ContentType | Journal Article |
| Copyright | 2018 by the American Association for the Study of Liver Diseases. 2019 by the American Association for the Study of Liver Diseases. Distributed under a Creative Commons Attribution 4.0 International License |
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| Language | English |
| License | 2018 by the American Association for the Study of Liver Diseases. Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0 |
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| Notes | Potential conflicts of interest: Dr. Kullak‐Ublick received compensation from Novartis. Dr. Ormarsdottir consults for Pfizer and AstraZeneca. Dr. Poynard consults and owns stock in BioPredictive. Dr. Bonkovsky consults and received grants from Alnylam and Mitsubishi‐Tanabe. He received grants from Gilead. Dr. Marcinak is employed by Takeda. Dr. van Boemmel consults, is on the speakers' bureau and received grants from Gilead, Roche and AbbVie. He is on the speakers' bureau for Siemens. Dr. Wolenski is employed by Takeda. Dr. Aubrecht is employed by Pfizer. He owns stock in PFE. Dr. Sauer owns stock in Amgen and Telsa. Dr. Fontana consults for Alnylam. He received grants from Bristol‐Myers Squibb, Gilead and AbbVie. These authors share senior authorship. is supported by the National Institute of Diabetes and Digestive and Kidney Diseases as a Cooperative Agreement (U01s) under grants U01‐DK065176 (Duke University), U01‐DK065201 (University of North Carolina), U01‐DK065184 (University of Michigan), U01‐DK065211 (Indiana University), U01DK065193 (University of Connecticut), U01‐DK065238 (University of California, San Francisco/California Pacific Medical Center), U01‐DK083023 (University of Texas Southwestern), U01‐DK083027 (Thomas Jefferson Hospital/University of Pennsylvania), U01‐DK082992 (Mayo Clinic), U01‐DK083020 (University of Southern California), and U01‐DK100928 (Illinois Critical Access Hospital Network). Additional funding is provided by Clinical and Translational Science Awards grants UL1 RR025761 (Indiana University), UL1 RR025747 (University of North Carolina), UL1 RR024986 (University of Michigan), and UL1 TR001420 (Wake Forest University). The Safer and Faster Evidence‐Based Translation Consortium received support from the Innovative Medicines Initiative Joint Undertaking under grant agreement #115003, the resources of which comprise financial contributions from the European Union's Seventh Framework Programme (FP7/2007‐2013) and European Federation of Pharmaceutical Industries and Associations companies. Additional support was received from the National Institute for Health Research Nottingham Digestive Diseases Biomedical Research Unit at the Nottingham University Hospitals National Health Service Trust and the University of Nottingham. The Drug‐Induced Liver Injury Network www.dilin.org These authors share first authorship. Current affiliation: Department of Gastroenterology and Hepatology, University Hospital, Iceland Authors share first authorship Authors share senior authorship Current Affiliation: Sanofi, Framingham, MA |
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| PublicationDate | February 2019 |
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| PublicationTitle | Hepatology (Baltimore, Md.) |
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hep29802-bib-0003-20241017 article-title: Muscular exercise can cause highly pathological liver function tests in healthy men publication-title: Br J Clin Pharmacol doi: 10.1111/j.1365-2125.2007.03001.x – volume: 60 start-page: 1336 year: 2014 ident: hep29802-bib-0030-20241017 article-title: Serum mitochondrial biomarkers and damage‐associated molecular patterns are higher in acetaminophen overdose patients with poor outcome publication-title: Hepatology doi: 10.1002/hep.27265 – volume: 122 start-page: 1574 year: 2012 ident: hep29802-bib-0029-20241017 article-title: The mechanism underlying acetaminophen‐induced hepatotoxicity in humans and mice involves mitochondrial damage and nuclear DNA fragmentation publication-title: J Clin Invest doi: 10.1172/JCI59755 – volume: 124 start-page: 71 year: 2003 ident: hep29802-bib-0005-20241017 article-title: Determinants of the association of overweight with elevated serum alanine aminotransferase activity in the United States publication-title: Gastroenterology doi: 10.1053/gast.2003.50004 – volume: 89 start-page: 806 year: 2011 ident: hep29802-bib-0006-20241017 article-title: Case definition and phenotype standardization in drug‐induced liver injury publication-title: Clin Pharmacol Ther doi: 10.1038/clpt.2011.58 – volume: 56 start-page: 1070 year: 2012 ident: hep29802-bib-0015-20241017 article-title: Molecular forms of HMGB1 and keratin‐18 as mechanistic biomarkers for mode of cell death and prognosis during clinical acetaminophen hepatotoxicity publication-title: J Hepatol doi: 10.1016/j.jhep.2011.12.019 – volume: 37 start-page: 132 year: 2017 ident: hep29802-bib-0020-20241017 article-title: Elevated levels of circulating CDH5 and FABP1 in association with human drug‐induced liver injury publication-title: Liver Int doi: 10.1111/liv.13174 – volume: 127 start-page: e132 year: 2011 ident: hep29802-bib-0021-20241017 article-title: Serum transaminase levels in boys with Duchenne and Becker muscular dystrophy publication-title: Pediatrics doi: 10.1542/peds.2010-0929 – volume: 14 start-page: 572 year: 2009 ident: hep29802-bib-0035-20241017 article-title: A systems biology approach to understanding elevated serum alanine transaminase levels in a clinical trial with ximelagatran publication-title: Biomarkers doi: 10.3109/13547500903261354 – volume: 53 start-page: 639 year: 2010 ident: hep29802-bib-0037-20241017 article-title: Cytokeratin 18‐based modification of the MELD score improves prediction of spontaneous survival after acute liver injury publication-title: J Hepatol doi: 10.1016/j.jhep.2010.04.029 – volume: 137 start-page: 947 year: 2002 ident: hep29802-bib-0001-20241017 article-title: Results of a prospective study of acute liver failure at 17 tertiary care centers in the United States publication-title: Ann Intern Med doi: 10.7326/0003-4819-137-12-200212170-00007 – volume: 92 start-page: 332 year: 2012 ident: hep29802-bib-0008-20241017 article-title: Alanine aminotransferase: a clinical and regulatory tool for detecting liver injury‐past, present, and future publication-title: Clin Pharmacol Ther doi: 10.1038/clpt.2012.108 – volume: 132 start-page: 276 year: 2013 ident: hep29802-bib-0018-20241017 article-title: Assessment of emerging biomarkers of liver injury in human subjects publication-title: Toxicol Sci doi: 10.1093/toxsci/kft009 – volume: 66 start-page: 24A year: 2017 ident: hep29802-bib-0041-20241017 article-title: Candidate liver safety biomarkers provide prognostic and mechanistic insights in patients with drug‐induced liver injury publication-title: Hepatology |
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| Snippet | Current blood biomarkers are suboptimal in detecting drug‐induced liver injury (DILI) and predicting its outcome. We sought to characterize the natural... Current blood biomarkers are suboptimal in detecting drug-induced liver injury (DILI) and predicting its outcome. We sought to characterize the natural... |
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| SubjectTerms | Adult Alanine Alanine transaminase Arginase Biomarkers Biomarkers - blood Cadherins Case-Control Studies Caspase Chemical and Drug Induced Liver Injury - blood Chemical and Drug Induced Liver Injury - diagnosis Chemical and Drug Induced Liver Injury - etiology Cytokeratin Dehydrogenases Diagnosis Fatty acid-binding protein Female Glutamate dehydrogenase Glutathione Hepatology Humans Immunosuppressive agents Life Sciences Liver Liver diseases Liver transplantation Macrophages Male Medicin och hälsovetenskap Middle Aged miRNA Osteopontin Paraoxonase Paraoxonase 1 Prognosis Prothrombin Sorbitol |
| Title | Candidate biomarkers for the diagnosis and prognosis of drug‐induced liver injury: An international collaborative effort |
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