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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 accessAbstract
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 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]
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“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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Metadata
- 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 › 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
About these checks
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