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Cited by 214Liver Disease Diagnosis and TreatmentLiver Disease and TransplantationLiver Diseases and Immunity

The DOI matches its Crossref record; 27 of the 28 references it cites were found in a registry or an index.

Performance of non-invasive tests and histology for the prediction of clinical outcomes in patients with non-alcoholic fatty liver disease: an individual participant data meta-analysis

Open access
Mózes, Ferenc E, Lee, Jenny A, Vali, Yasaman, Alzoubi, Osama, Staufer, Katharina, Trauner, Michael, Paternostro, Rafael, Stauber, Rudolf E, Holleboom, Adriaan G, van Dijk, Anne-Marieke, Mak, Anne Linde, Boursier, Jérôme, de Saint Loup, Marc, Shima, Toshihide, Bugianesi, Elisabetta, Gaia, Silvia, Armandi, Angelo, Shalimar, Lupșor-Platon, Monica, Wong, Vincent Wai-Sun, Li, Guanlin, Wong, Grace Lai-Hung, Cobbold, Jeremy, Karlas, Thomas, Wiegand, Johannes, Sebastiani, Giada, Tsochatzis, Emmanuel, Liguori, Antonio, Yoneda, Masato, Nakajima, Atsushi, Hagström, Hannes, Akbari, Camilla, Hirooka, Masashi, Chan, Wah-Kheong, Mahadeva, Sanjiv, Rajaram, Ruveena, Zheng, Ming-Hua, George, Jacob, Eslam, Mohammed, Petta, Salvatore, Pennisi, Grazia, Viganò, Mauro, Ridolfo, Sofia, Aithal, Guruprasad Padur, Palaniyappan, Naaventhan, Lee, Dae Ho, Ekstedt, Mattias, Nasr, Patrik, Cassinotto, Christophe, de Lédinghen, Victor, Berzigotti, Annalisa, Mendoza, Yuly P, Noureddin, Mazen, Truong, Emily, Fournier-Poizat, Céline, Geier, Andreas, Martic, Miljen, Tuthill, Theresa, Anstee, Quentin M, Harrison, Stephen A, Bossuyt, Patrick M, Pavlides, Michael, Anstee, Quentin M, Daly, Ann K, Govaere, Olivier, Cockell, Simon, Tiniakos, Dina, Bedossa, Pierre, Burt, Alastair, Oakley, Fiona, Cordell, Heather J, Day, Christopher P, Wonders, Kristy, Missier, Paolo, McTeer, Matthew, Vale, Luke, Oluboyede, Yemi, Breckons, Matt, Bossuyt, Patrick M, Zafarmand, Hadi, Vali, Yasaman, Lee, Jenny, Nieuwdorp, Max, Holleboom, Adriaan G, Verheij, Joanne, Ratziu, Vlad, Clément, Karine, Patino-Navarrete, Rafael, Pais, Raluca, Paradis, Valerie, Schuppan, Detlef, Schattenberg, Jörn M, Surabattula, Rambabu, Myneni, Sudha, Straub, Beate K, Vidal-Puig, Toni, Vacca, Michele, Rodrigues-Cuenca, Sergio, Allison, Mike, Kamzolas, Ioannis, Petsalaki, Evangelia, Campbell, Mark, Lelliott, Chris J, Davies, Susan, Orešič, Matej, Hyötyläinen, Tuulia, McGlinchey, Aiden, Mato, Jose M, Millet, Óscar, Dufour, Jean-François, Berzigotti, Annalisa, Masoodi, Mojgan, Pavlides, Michael, Harrison, Stephen, Neubauer, Stefan, Cobbold, Jeremy, Mozes, Ferenc, Akhtar, Salma, Olodo-Atitebi, Seliat, Banerjee, Rajarshi, Kelly, Matt, Shumbayawonda, Elizabeth, Dennis, Andrea, Andersson, Anneli, Wigley, Ioan, Romero-Gómez, Manuel, Gómez-González, Emilio, Ampuero, Javier, Castell, Javier, Gallego-Durán, Rocío, Fernández, Isabel, Montero-Vallejo, Rocío, Karsdal, Morten, Rasmussen, Daniel Guldager Kring, Leeming, Diana Julie, Sinisi, Antonia, Musa, Kishwar, Sandt, Estelle, Tonini, Manuela, Bugianesi, Elisabetta, Rosso, Chiara, Armandi, Angelo, Marra, Fabio, Gastaldelli, Amalia, Svegliati, Gianluca, Boursier, Jérôme, Francque, Sven, Vonghia, Luisa, Driessen, Ann, Ekstedt, Mattias, Kechagias, Stergios, Yki-Järvinen, Hannele, Porthan, Kimmo, Arola, Johanna, van Mil, Saskia, Papatheodoridis, George, Cortez-Pinto, Helena, Rodrigues, Cecilia M P, Valenti, Luca, Pelusi, Serena, Petta, Salvatore, Pennisi, Grazia, Miele, Luca, Geier, Andreas, Trautwein, Christian, Reißing, Johanna, Aithal, Guruprasad P, Francis, Susan, Palaniyappan, Naaventhan, Bradley, Christopher, Hockings, Paul, Schneider, Moritz, Newsome, Philip, Hübscher, Stefan, Wenn, David, Rosenquist, Christian, Trylesinski, Aldo, Mayo, Rebeca, Alonso, Cristina, Duffin, Kevin, Perfield, James W, Chen, Yu, Yunis, Carla, Tuthill, Theresa, Harrington, Magdalena Alicia, Miller, Melissa, Chen, Yan, McLeod, Euan James, Ross, Trenton, Bernardo, Barbara, Schölch, Corinna, Ertle, Judith, Younes, Ramy, Oldenburger, Anouk, Coxson, Harvey, Ostroff, Rachel, Alexander, Leigh, Biegel, Hannah, Kjær, Mette Skalshøi, Harder, Lea Mørch, Davidsen, Peter, Ellegaard, Jens, Balp, Maria-Magdalena, Brass, Clifford, Jennings, Lori, Martic, Miljen, Löffler, Jürgen, Applegate, Douglas, Shankar, Sudha, Torstenson, Richard, Lindén, Daniel, Fournier-Poizat, Céline, Llorca, Anne, Kalutkiewicz, Michael, Pepin, Kay, Ehman, Richard, Horan, Gerald, Ho, Gideon, Tai, Dean, Chng, Elaine, Patterson, Scott D, Billin, Andrew, Doward, Lynda, Twiss, James, Thakker, Paresh, Derdak, Zoltan, Landgren, Henrik, Lackner, Carolin, Gouw, Annette, Hytiroglou, Prodromos·2023·The Lancet Gastroenterology & Hepatology
DOI 10.1016/s2468-1253(23)00141-3
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Abstract

BACKGROUND: Histologically assessed liver fibrosis stage has prognostic significance in patients with non-alcoholic fatty liver disease (NAFLD) and is accepted as a surrogate endpoint in clinical trials for non-cirrhotic NAFLD. Our aim was to compare the prognostic performance of non-invasive tests with liver histology in patients with NAFLD. METHODS: This was an individual participant data meta-analysis of the prognostic performance of histologically assessed fibrosis stage (F0-4), liver stiffness measured by vibration-controlled transient elastography (LSM-VCTE), fibrosis-4 index (FIB-4), and NAFLD fibrosis score (NFS) in patients with NAFLD. The literature was searched for a previously published systematic review on the diagnostic accuracy of imaging and simple non-invasive tests and updated to Jan 12, 2022 for this study. Studies were identified through PubMed/MEDLINE, EMBASE, and CENTRAL, and authors were contacted for individual participant data, including outcome data, with a minimum of 12 months of follow-up. The primary outcome was a composite endpoint of all-cause mortality, hepatocellular carcinoma, liver transplantation, or cirrhosis complications (ie, ascites, variceal bleeding, hepatic encephalopathy, or progression to a MELD score ≥15). We calculated aggregated survival curves for trichotomised groups and compared them using stratified log-rank tests (histology: F0-2 vs F3 vs F4; LSM: <10 vs 10 to <20 vs ≥20 kPa; FIB-4: <1·3 vs 1·3 to ≤2·67 vs >2·67; NFS: <-1·455 vs -1·455 to ≤0·676 vs >0·676), calculated areas under the time-dependent receiver operating characteristic curves (tAUC), and performed Cox proportional-hazards regression to adjust for confounding. This study was registered with PROSPERO, CRD42022312226. FINDINGS: Of 65 eligible studies, we included data on 2518 patients with biopsy-proven NAFLD from 25 studies (1126 [44·7%] were female, median age was 54 years [IQR 44-63), and 1161 [46·1%] had type 2 diabetes). After a median follow-up of 57 months [IQR 33-91], the composite endpoint was observed in 145 (5·8%) patients. Stratified log-rank tests showed significant differences between the trichotomised patient groups (p<0·0001 for all comparisons). The tAUC at 5 years were 0·72 (95% CI 0·62-0·81) for histology, 0·76 (0·70-0·83) for LSM-VCTE, 0·74 (0·64-0·82) for FIB-4, and 0·70 (0·63-0·80) for NFS. All index tests were significant predictors of the primary outcome after adjustment for confounders in the Cox regression. INTERPRETATION: Simple non-invasive tests performed as well as histologically assessed fibrosis in predicting clinical outcomes in patients with NAFLD and could be considered as alternatives to liver biopsy in some cases. FUNDING: Innovative Medicines Initiative 2.

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Authors
Mózes, F. E., Lee, J. A., Vali, Y., Alzoubi, O., Staufer, K., Trauner, M., Paternostro, R., Stauber, R. E., Holleboom, A. G., van Dijk, A.-M., Mak, A. L., Boursier, J., de Saint Loup, M., Shima, T., Bugianesi, E., Gaia, S., Armandi, A., Shalimar, Lupșor-Platon, M., Wong, V. W.-S., Li, G., Wong, G. L.-H., Cobbold, J., Karlas, T., Wiegand, J., Sebastiani, G., Tsochatzis, E., Liguori, A., Yoneda, M., Nakajima, A., Hagström, H., Akbari, C., Hirooka, M., Chan, W.-K., Mahadeva, S., Rajaram, R., Zheng, M.-H., George, J., Eslam, M., Petta, S., Pennisi, G., Viganò, M., Ridolfo, S., Aithal, G. P., Palaniyappan, N., Lee, D. H., Ekstedt, M., Nasr, P., Cassinotto, C., de Lédinghen, V., Berzigotti, A., Mendoza, Y. P., Noureddin, M., Truong, E., Fournier-Poizat, C., Geier, A., Martic, M., Tuthill, T., Anstee, Q. M., Harrison, S. A., Bossuyt, P. M., Pavlides, M., Anstee, Q. M., Daly, A. K., Govaere, O., Cockell, S., Tiniakos, D., Bedossa, P., Burt, A., Oakley, F., Cordell, H. J., Day, C. P., Wonders, K., Missier, P., McTeer, M., Vale, L., Oluboyede, Y., Breckons, M., Bossuyt, P. M., Zafarmand, H., Vali, Y., Lee, J., Nieuwdorp, M., Holleboom, A. G., Verheij, J., Ratziu, V., Clément, K., Patino-Navarrete, R., Pais, R., Paradis, V., Schuppan, D., Schattenberg, J. M., Surabattula, R., Myneni, S., Straub, B. K., Vidal-Puig, T., Vacca, M., Rodrigues-Cuenca, S., Allison, M., Kamzolas, I., Petsalaki, E., Campbell, M., Lelliott, C. J., Davies, S., Orešič, M., Hyötyläinen, T., McGlinchey, A., Mato, J. M., Millet, Ó., Dufour, J.-F., Berzigotti, A., Masoodi, M., Pavlides, M., Harrison, S., Neubauer, S., Cobbold, J., Mozes, F., Akhtar, S., Olodo-Atitebi, S., Banerjee, R., Kelly, M., Shumbayawonda, E., Dennis, A., Andersson, A., Wigley, I., Romero-Gómez, M., Gómez-González, E., Ampuero, J., Castell, J., Gallego-Durán, R., Fernández, I., Montero-Vallejo, R., Karsdal, M., Rasmussen, D. G. K., Leeming, D. J., Sinisi, A., Musa, K., Sandt, E., Tonini, M., Bugianesi, E., Rosso, C., Armandi, A., Marra, F., Gastaldelli, A., Svegliati, G., Boursier, J., Francque, S., Vonghia, L., Driessen, A., Ekstedt, M., Kechagias, S., Yki-Järvinen, H., Porthan, K., Arola, J., van Mil, S., Papatheodoridis, G., Cortez-Pinto, H., Rodrigues, C. M. P., Valenti, L., Pelusi, S., Petta, S., Pennisi, G., Miele, L., Geier, A., Trautwein, C., Reißing, J., Aithal, G. P., Francis, S., Palaniyappan, N., Bradley, C., Hockings, P., Schneider, M., Newsome, P., Hübscher, S., Wenn, D., Rosenquist, C., Trylesinski, A., Mayo, R., Alonso, C., Duffin, K., Perfield, J. W., Chen, Y., Yunis, C., Tuthill, T., Harrington, M. A., Miller, M., Chen, Y., McLeod, E. J., Ross, T., Bernardo, B., Schölch, C., Ertle, J., Younes, R., Oldenburger, A., Coxson, H., Ostroff, R., Alexander, L., Biegel, H., Kjær, M. S., Harder, L. M., Davidsen, P., Ellegaard, J., Balp, M.-M., Brass, C., Jennings, L., Martic, M., Löffler, J., Applegate, D., Shankar, S., Torstenson, R., Lindén, D., Fournier-Poizat, C., Llorca, A., Kalutkiewicz, M., Pepin, K., Ehman, R., Horan, G., Ho, G., Tai, D., Chng, E., Patterson, S. D., Billin, A., Doward, L., Twiss, J., Thakker, P., Derdak, Z., Landgren, H., Lackner, C., Gouw, A., & Hytiroglou, P.
Affiliations
  • University of Jordan (JO)
  • Medical University of Vienna (AT)
  • Medical University of Graz (AT)
  • Amsterdam University Medical Centers (NL)
  • Chinese University of Hong Kong (HK)
  • University Hospital Leipzig (DE)
  • Royal Free London NHS Foundation Trust (GB)
  • Università Cattolica del Sacro Cuore (IT)
  • Karolinska University Hospital (SE)
  • Karolinska Institutet (SE)
  • McGill University Health Centre (CA)
  • University of Malaya (MY)
  • First Affiliated Hospital of Wenzhou Medical University (CN)
  • The University of Sydney (AU)
  • Ehime University (JP)
  • University of Milan (IT)
  • Gachon University (KR)
  • Linköping University (SE)
  • Houston Methodist (US)
  • Cedars-Sinai Medical Center (US)
  • Inserm (FR)
  • University of Bern (CH)
  • Amsterdam Public Health (NL)
  • National Health Service (GB)
  • University of Oxford (GB)
  • Universitätsklinikum Würzburg (DE)
  • University of Turin (IT)
  • Centre Hospitalier Universitaire d'Angers (FR)
  • University of Nottingham (GB)
  • Pfizer (United States) (US)
  • Novartis Institutes for BioMedical Research (CH)
  • Echosens (France) (FR)
Corresponding author
  • Straub, Beate K
  • Ostroff, Rachel
ORCID
Venue
The Lancet Gastroenterology & Hepatology
Publisher
Elsevier BV
Published
2023-08
Volume
8
Issue
8
Pages
704-713
ISSN
  • 2468-1156 (ISSN-L)
  • 2468-1253
DOI
10.1016/s2468-1253(23)00141-3
OpenAlex
W4379467566
Cited by
214
References
28
Citations by year
2026: 52 · 2025: 62 · 2024: 78 · 2023: 22
FWCI
8.33
Type
journal article
Language
en
Open access
Licence
Locations
  • The Lancet. Gastroenterology & hepatology (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion, other-oa)
  • DiVA (Linkoping University) (submittedVersion, other-oa)
  • HAL (submittedVersion, cc-by)
  • Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) (submittedVersion, other-oa)
  • Nova Science Publishers (Nova Science Publishers, Inc.) (submittedVersion, other-oa)
  • Institutional Research Information System University of Turin (University of Turin) (submittedVersion, other-oa)
  • Lirias (submittedVersion, cc-by)
  • Repository@Nottingham (University of Nottingham) (submittedVersion, cc-by)
  • PubliCatt (Università Cattolica del Sacro Cuore) (submittedVersion, cc-by-nc-nd)
  • Pure Amsterdam UMC (submittedVersion, cc-by)
  • University of Birmingham Research Portal (University of Birmingham) (submittedVersion, cc-by)
  • Utrecht University Repository (Utrecht University) (submittedVersion, cc-by)
Funders
  • Royal Society (221805/Z/20/Z)
  • Wellcome Trust
  • Ministry of Health and Welfare
  • European Federation of Pharmaceutical Industries and Associations
  • Korea Health Industry Development Institute (HI14C1135)
  • IMI
  • Innovative Medicines Initiative (777377)
  • Fonds de Recherche du Québec - Santé (296306)
  • NIHR Newcastle Biomedical Research Centre
  • National Institute for Health and Care Research
Topics
  • Health Sciences › Medicine › Hepatology › Liver Disease Diagnosis and Treatment
  • Health Sciences › Medicine › Hepatology › Liver Disease and Transplantation
  • Health Sciences › Medicine › Hepatology › Liver Diseases and Immunity
Keywords
non-alcoholic fatty liver disease, liver fibrosis, noninvasive fibrosis assessment, vibration-controlled transient elastography, liver stiffness, FIB-4, NAFLD fibrosis score, liver histopathology, prognostic performance, all-cause mortality, hepatocellular carcinoma, liver cirrhosis, liver transplantation, cirrhosis complications, MELD score, surrogate endpoints
MeSH terms
Diabetes Mellitus, Type 2, Esophageal and Gastric Varices, Female, Fibrosis, Gastrointestinal Hemorrhage, Humans, Liver Cirrhosis, Male, Middle Aged, Non-alcoholic Fatty Liver Disease

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