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Diagnostic accuracy of non-invasive tests for advanced fibrosis in patients with NAFLD: an individual patient data meta-analysis |
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Gut. 2022 May;71(5):1006-1019. doi: 10.1136/gutjnl-2021-324243.Epub 2021 May 17.
Ferenc Emil Mózes 1, Jenny A Lee 2, Emmanuel Anandraj Selvaraj 1 3 4, Arjun Narayan Ajmer Jayaswal 1, Michael Trauner 5, Jerome Boursier 6 7, Céline Fournier 8, Katharina Staufer 5 9 10, Rudolf E Stauber 11, Elisabetta Bugianesi 12, Ramy Younes 13, Silvia Gaia 12, Monica Lup?or-Platon 14, Salvatore Petta 15, Toshihide Shima 16, Takeshi Okanoue 16, Sanjiv Mahadeva 17, Wah-Kheong Chan 17, Peter J Eddowes 18 19, Gideon M Hirschfield 20, Philip Noel Newsome 18 21 22, Vincent Wai-Sun Wong 23, Victor de Ledinghen 24 25, Jiangao Fan 26, Feng Shen 26, Jeremy F Cobbold 3 4, Yoshio Sumida 27, Akira Okajima 28, Jörn M Schattenberg 29, Christian Labenz 29, Won Kim 30, Myoung Seok Lee 31, Johannes Wiegand 32, Thomas Karlas 32, Yusuf Yilmaz 33 34, Guruprasad Padur Aithal 19 35, Naaventhan Palaniyappan 19 35, Christophe Cassinotto 36, Sandeep Aggarwal 37, Harshit Garg 37, Geraldine J Ooi 38, Atsushi Nakajima 39, Masato Yoneda 39, Marianne Ziol 40, Nathalie Barget 41, Andreas Geier 42, Theresa Tuthill 43, M Julia Brosnan 43, Quentin Mark Anstee 44, Stefan Neubauer 1, Stephen A Harrison 1, Patrick M Bossuyt 2, Michael Pavlides 45 3 4, LITMUS Investigators
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Author information
Collaborators:
LITMUS Investigators:
Quentin Anstee, Ann Daly, Katherine Johnson, Olivier Govaere, Simon Cockell, Dina Tiniakos, Pierre Bedossa, Fiona Oakley, Heather Cordell, Chris Day, Kristy Wonders, Patrick Bossuyt, Hadi Zafarmand, Yasaman Vali, Jenny Lee, Vlad Ratziu, Karine Clement, Raluca Pais, Detlef Schuppan, Jörn Schattenberg, Detlef Schuppan, Jörn Schattenberg, Toni Vidal-Puig, Michele Vacca, Sergio Rodrigues-Cuenca, Mike Allison, Ioannis Kamzolas, Evangelia Petsalaki, Matej Oresic, Tuulia Hyötyläinen, Aiden McGlinchey, Jose M Mato, Oscar Millet, Jean-François Dufour, Annalisa Berzigotti, Michael Pavlides, Stephen Harrison, Stefan Neubauer, Jeremy Cobbold, Ferenc Mozes, Salma Akhtar, Rajarshi Banerjee, Matt Kelly, Elizabeth Shumbayawonda, Andrea Dennis, Charlotte Erpicum, Micheala Graham, Manuel Romero-Gómez, Emilio Gómez-González, Javier Ampuero, Javier Castell, Rocío Gallego-Durán, Isabel Fernández, Rocío Montero-Vallejo, Morten Karsdal, Elisabeth Erhardtsen, Daniel Rasmussen, Diana Julie Leeming, Mette Juul Fisker, Antonia Sinisi, Kishwar Musa, Fay Betsou, Estelle Sandt, Manuela Tonini, Elisabetta Bugianesi, Chiara Rosso, Angelo Armandi, Fabio Marra, Amalia Gastaldelli, Gianluca Svegliati, Jérôme Boursier, Sven Francque, Luisa Vonghia, Mattias Ekstedt, Stergios Kechagias, Hannele Yki-Jarvinen, Kimmo Porthan, Saskia van Mil, George Papatheodoridis, Helena Cortez-Pinto, Luca Valenti, Salvatore Petta, Luca Miele, Andreas Geier, Christian Trautwein, Guru Aithal, Paul Hockings, Philip Newsome, David Wenn, Cecília Maria Rodrigues, Pierre Chaumat, Rémy Hanf, Aldo Trylesinski, Pablo Ortiz, Kevin Duffin, Julia Brosnan, Theresa Tuthill, Euan McLeod, Judith Ertle, Ramy Younes, Rachel Ostroff, Leigh Alexander, Mette Skalshøi Kjær, Lars Friis Mikkelsen, Maria-Magdalena Balp, Clifford Brass, Lori Jennings, Miljen Martic, Juergen Loeffler, Guido Hanauer, Sudha Shankar, Céline Fournier, Kay Pepin, Richard Ehman, Joel Myers, Gideon Ho, Richard Torstenson, Rob Myers, Lynda Doward
Affiliations
- 1Cardiovascular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, UK.
- 2Department of Epidemiology and Data Science, Amsterdam UMC, University of Amsterdam, Amsterdam, The Netherlands.
- 3Translational Gastroenterology Unit, University of Oxford, Oxford, Oxfordshire, UK.
- 4NIHR Oxford Biomedical Research Centre, Oxford University Hospitals NHS Foundation Trust and the University of Oxford, Oxford, UK.
- 5Division of Gastroenterology and Hepatology, Department of Medicine III, Medical University of Vienna, Vienna, Austria.
- 6Laboratoire HIFIH, UPRES EA 3859, SFR ICAT 4208, Universite d'Angers, Angers, Pays de la Loire, France.
- 7Service d'Hepato-Gastroenterologie et Oncologie Digestive, Centre Hospitalier Universitaire d'Angers, Angers, Pays de la Loire, France.
- 8Echosens SA, Paris, Île-de-France, France.
- 9Department of Visceral Surgery and Medicine, Inselspital University Hospital Bern, Bern, Switzerland.
- 10Department of Surgery, Division of Transplantation, Medical University of Vienna, Vienna, Austria.
- 11Department of Internal Medicine, Medical University of Graz, Graz, Austria.
- 12Medical Sciences, University of Turin, Torino, Italy.
- 13Boehringer Ingelheim International GmbH, Ingelheim, Rheinland-Pfalz, Germany.
- 14Department of Ultrasonography, University of Medicine and Pharmacy, Regional Institute of Gastroenterology and Hepatology "Prof. Dr. Octavian Fodor", Cluj Napoca, Romania.
- 15Section of Gastroenterology and Hepatology, PROMISE, Palermo, Italy.
- 16Hepatology Center, Saiseikai Suita Hospital, Suita, Osaka, Japan.
- 17Faculty of Medicine, Department of Medicine, University of Malaya, Kuala Lumpur, Wilayah Persekutuan, Malaysia.
- 18NIHR Biomedical Research Centre, University of Birmingham, Birmingham, UK.
- 19NIHR Nottingham Biomedical Research Centre, University of Nottingham, Nottingham, Nottinghamshire, UK.
- 20Toronto Centre for Liver Disease, University Health Network, Toronto, Ontario, Canada.
- 21Centre for Liver and Gastrointestinal Research, Institute of Immunology and Immunotherapy, University of Birmingham, Birmingham, UK.
- 22Liver Unit, University Hospitals Birmingham NHS Foundation Trust, Birmingham, UK.
- 23Department of Medicine and Therapeutics, Chinese University of Hong Kong, Hong Kong, Hong Kong.
- 24Centre d'Investigation de la Fibrose Hépatique, Hopital Haut-Leveque, Pessac, France.
- 25INSERM1053, Universite de Bordeaux, Talence, Aquitaine, France.
- 26Department of Gastroenterology, Xinhua Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
- 27Department of Internal Medicine, Aichi Medical University, Nagakute, Aichi, Japan.
- 28Department of Gastroenterology, Koseikai Takeda Hospital, Kyoto, Japan.
- 29Department of Internal Medicine I, University Medical Centre of the Johannes Gutenberg-University Mainz, Mainz, Rhineland-Palatinate, Germany.
- 30Department of Gastroenterology and Hepatology, Department of Internal Medicine, Seoul National University College of Medicine, Seoul Metropolitan Government Boramae Medical Center, Seoul, South Korea.
- 31Department of Radiology, Seoul National University Seoul Metropolitan Government Boramae Medical Center, Dongjak-gu, Seoul, The Republic of Korea.
- 32Department of Medicine II, Leipzig University Medical Center, Leipzig, Sachsen, Germany.
- 33Department of Gastroenterology, Marmara University School of Medicine, Istanbul, Turkey.
- 34Institute of Gastroenterology, Marmara University, Istanbul, Turkey.
- 35Nottingham Digestive Diseases Centre, School of Medicine, University of Nottingham, Nottingham, UK.
- 36Diagnostic and Interventional Radiology, University Hospital Centre Montpellier, Montpellier, Languedoc-Roussillon, France.
- 37Department of Surgical Disciplines, AIIMS, New Delhi, Delhi, India.
- 38Department of Surgery, Monash University, Prahran, Victoria, Australia.
- 39Department of Gastroenterology and Hepatology, Yokohama City University, Yokohama, Kanagawa, Japan.
- 40Service d'Anatomie Pathologique et Centre de Ressources Biologiques, Hopital Jean Verdier, Paris, France.
- 41Centre de Ressources Biologiques, Hopitaux Universitaires Paris-Seine-Saint-Denis, Bondy, Île-de-France, France.
- 42Division of Hepatology, University Hospital Wurzburg, Wurzburg, Bayern, Germany.
- 43Internal Medicine Research Unit, Pfizer Inc, Cambridge, Massachusetts, USA.
- 44Translational and Clinical Research Institute, Faculty of Medicine, Newcastle University, Newcastle upon Tyne, Tyne and Wear, UK.
- 45Cardiovascular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, UK michael.pavlides@cardiov.ox.ac.uk.
Abstract
Objective: Liver biopsy is still needed for fibrosis staging in many patients with non-alcoholic fatty liver disease. The aims of this study were to evaluate the individual diagnostic performance of liver stiffness measurement by vibration controlled transient elastography (LSM-VCTE), Fibrosis-4 Index (FIB-4) and NAFLD (non-alcoholic fatty liver disease) Fibrosis Score (NFS) and to derive diagnostic strategies that could reduce the need for liver biopsies.
Design: Individual patient data meta-analysis of studies evaluating LSM-VCTE against liver histology was conducted. FIB-4 and NFS were computed where possible. Sensitivity, specificity and area under the receiver operating curve (AUROC) were calculated. Biomarkers were assessed individually and in sequential combinations.
Results: Data were included from 37 primary studies (n=5735; 45% women; median age: 54 years; median body mass index: 30 kg/m2; 33% had type 2 diabetes; 30% had advanced fibrosis). AUROCs of individual LSM-VCTE, FIB-4 and NFS for advanced fibrosis were 0.85, 0.76 and 0.73. Sequential combination of FIB-4 cut-offs (<1.3; ≥2.67) followed by LSM-VCTE cut-offs (<8.0; ≥10.0 kPa) to rule-in or rule-out advanced fibrosis had sensitivity and specificity (95% CI) of 66% (63-68) and 86% (84-87) with 33% needing a biopsy to establish a final diagnosis. FIB-4 cut-offs (<1.3; ≥3.48) followed by LSM cut-offs (<8.0; ≥20.0 kPa) to rule out advanced fibrosis or rule in cirrhosis had a sensitivity of 38% (37-39) and specificity of 90% (89-91) with 19% needing biopsy.
Conclusion: Sequential combinations of markers with a lower cut-off to rule-out advanced fibrosis and a higher cut-off to rule-in cirrhosis can reduce the need for liver biopsies.
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