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
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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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All these tests were significant predictors of the primary outcome of overall mortality and liver-related outcomes.
“All these tests were signi fi cant predictors of the primary outcome (overall mortality and liver-related outcomes). 187”
From EASL-EASD-EASO Clinical Practice Guidelines on the management of metabolic dysfunction-associated steatotic liver disease (MASLD). (2024) · cites this paper as [187]
A recent individual participant data meta-analysis including 2,518 participants with median follow-up of 57 months showed time-dependent AUCs at 5 years of 0.72 for histology, 0.76 for LSM-VCTE, 0.74 for FIB-4, and 0.70 for NFS.
“A recent individual participant data meta-analysis including 2,518 participants, with a median follow-up of 57 months, showed that time-dependent AUCs at 5 years were 0.72 for histology, 0.76 for LSM-VCTE, 0.74 for FIB-4, and 0.70 for NFS.”
From EASL-EASD-EASO Clinical Practice Guidelines on the management of metabolic dysfunction-associated steatotic liver disease (MASLD). (2024) · cites this paper as [187]
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MAFLD in adults: non-invasive tests for diagnosis and monitoring of MAFLD
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Self-citationThe Impact of Metabolic Health and Obesity on Liver Transplant Candidates and Recipients
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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
- Alzoubi, Osama
- Staufer, Katharina
- Trauner, Michael
- Paternostro, Rafael
- Stauber, Rudolf E
- Mak, Anne Linde
- Shima, Toshihide
- Gaia, Silvia
- Wong, Vincent Wai-Sun
- Li, Guanlin
- Wong, Grace Lai-Hung
- Karlas, Thomas
- Wiegand, Johannes
- Sebastiani, Giada
- Tsochatzis, Emmanuel
- Liguori, Antonio
- Yoneda, Masato
- Nakajima, Atsushi
- Hagström, Hannes
- Hirooka, Masashi
- Chan, Wah-Kheong
- Mahadeva, Sanjiv
- Rajaram, Ruveena
- Zheng, Ming-Hua
- George, Jacob
- Eslam, Mohammed
- Viganò, Mauro
- Ridolfo, Sofia
- Lee, Dae Ho
- Nasr, Patrik
- Cassinotto, Christophe
- Mendoza, Yuly P
- Noureddin, Mazen
- Truong, Emily
- Daly, Ann K
- Govaere, Olivier
- Cockell, Simon
- Tiniakos, Dina
- Burt, Alastair
- Oakley, Fiona
- Cordell, Heather J
- Day, Christopher P
- Wonders, Kristy
- McTeer, Matthew
- Vale, Luke
- Oluboyede, Yemi
- Nieuwdorp, Max
- Verheij, Joanne
- Ratziu, Vlad
- Clément, Karine
- Pais, Raluca
- Schattenberg, Jörn M
- Surabattula, Rambabu
- Straub, Beate K
- Kamzolas, Ioannis
- Petsalaki, Evangelia
- Lelliott, Chris J
- Davies, Susan
- Orešič, Matej
- Hyötyläinen, Tuulia
- Millet, Óscar
- Dufour, Jean-François
- Masoodi, Mojgan
- Neubauer, Stefan
- Banerjee, Rajarshi
- Kelly, Matt
- Shumbayawonda, Elizabeth
- Dennis, Andrea
- Andersson, Anneli
- Gómez-González, Emilio
- Ampuero, Javier
- Karsdal, Morten
- Rasmussen, Daniel Guldager Kring
- Rosso, Chiara
- Marra, Fabio
- Gastaldelli, Amalia
- Francque, Sven
- Vonghia, Luisa
- Driessen, Ann
- Kechagias, Stergios
- Porthan, Kimmo
- Arola, Johanna
- Papatheodoridis, George
- Valenti, Luca
- Pelusi, Serena
- Miele, Luca
- Trautwein, Christian
- Reißing, Johanna
- Francis, Susan
- Bradley, Christopher
- Hockings, Paul
- Newsome, Philip
- Hübscher, Stefan
- Rosenquist, Christian
- Mayo, Rebeca
- Alonso, Cristina
- Duffin, Kevin
- Perfield, James W
- Chen, Yu
- Yunis, Carla
- Miller, Melissa
- Chen, Yan
- Bernardo, Barbara
- Ertle, Judith
- Younes, Ramy
- Oldenburger, Anouk
- Coxson, Harvey
- Ostroff, Rachel
- Alexander, Leigh
- Biegel, Hannah
- Kjær, Mette Skalshøi
- Harder, Lea Mørch
- Davidsen, Peter
- Balp, Maria-Magdalena
- Jennings, Lori
- Löffler, Jürgen
- Shankar, Sudha
- Lindén, Daniel
- Pepin, Kay
- Ehman, Richard
- Ho, Gideon
- Tai, Dean
- Chng, Elaine
- Patterson, Scott D
- Billin, Andrew
- Doward, Lynda
- Thakker, Paresh
- Lackner, Carolin
- Gouw, Annette
- Hytiroglou, Prodromos
- 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
- 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
- hybrid
- doi.org
- 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 › Epidemiology › 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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