The DOI matches its Crossref record; 11 of the 11 references it cites were found in a registry or an index.
Utility and appropriateness of the fatty liver inhibition of progression (FLIP) algorithm and steatosis, activity, and fibrosis (SAF) score in the evaluation of biopsies of nonalcoholic fatty liver disease
Open accessAbstract
Biopsy is still the gold standard for the diagnosis of nonalcoholic steatohepatitis but the definition may vary among pathologists, a drawback especially in evaluation of biopsies for clinical trials. We previously developed a scoring system (steatosis, activity, fibrosis [SAF]) allowing the use of an algorithm (fatty liver inhibition of progression [FLIP]) for the classification of liver injury in morbid obesity. The aim of this study was to determine whether the use of the SAF score and FLIP algorithm can decrease interobserver variations among pathologists. In a first session, pathologists categorized 40 liver biopsies of patients with nonalcoholic fatty liver disease (NAFLD) according to their own experience. In a second reading session, each pathologist reclassified the same slides by using the FLIP algorithm and SAF score, blinded to their first evaluation. The experiment was repeated with two different groups of pathologists at varying levels of training in liver pathology. The percentage of biopsy interpretation concordant with reference evaluation increased from 77% to 97% in Group 1 and from 42% to 75% in Group 2 after the use of the SAF score and FLIP algorithm. The strength of concordance in classification increased in Group 1 from moderate (κ = 0.54) to substantial (κ = 0.66) and from fair (κ = 0.35) to substantial (κ = 0.61) in Group 2 with application of the algorithm. With regard to the SAF score, concordance was substantial in Group 1 for steatosis (κ = 0.61), activity (κ = 0.75), and almost perfect for fibrosis (κ = 0.83 after pooling 1a, 1b, and 1c together into a single score F1). Similar trends were observed in Group 2 (κ = 0.54 for S, κ = 0.68 for A, and κ = 0.72 for F). Conclusion: The FLIP algorithm based on the SAF score should decrease interobserver variations among pathologists and are likely to be implemented in pathology practice. (Hepatology 2014;60:565–575)
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Statistical Methods for Rates and Proportions
Fleiss, J. L., Levin, B., & Paik, M. C. (2003) · Wiley Series in Probability and Statistics · doi:10.1002/0471445428 · Cited by 18,646
Weighted kappa: nominal scale agreement provision for scaled disagreement or partial credit
Cohen, J. (1968) · Psychological Bulletin · doi:10.1037/h0026256 · Cited by 8,736
Nonalcoholic fatty liver disease: a spectrum of clinical and pathological severity.
MATTEONI, C., YOUNOSSI, Z., GRAMLICH, T., BOPARAI, N., LIU, Y., & MCCULLOUGH, A. (1999) · Gastroenterology · doi:10.1016/s0016-5085(99)70506-8 · Cited by 3,345
Pioglitazone, Vitamin E, or Placebo for Nonalcoholic Steatohepatitis
Sanyal, A. J., Chalasani, N., Kowdley, K. V., McCullough, A., Diehl, A. M., Bass, N. M., Neuschwander-Tetri, B. A., Lavine, J. E., Tonascia, J., Unalp, A., et al. (2010) · New England Journal of Medicine · doi:10.1056/nejmoa0907929 · Cited by 3,327
Sampling Variability of Liver Biopsy in Nonalcoholic Fatty Liver Disease
Ratziu, V., Charlotte, F., Heurtier, A., Gombert, S., Giral, P., Bruckert, E., Grimaldi, A., Capron, F., & Poynard, T. (2005) · Gastroenterology · doi:10.1053/j.gastro.2005.03.084 · Cited by 2,106 · cited 1×
“However, liver biopsy is prone to limitations such as sampling error and observer variability.(29,30) The degree of interobserver variability is mainly determined by the accuracy of the definition of a pathological feature and its different semiquantitative grades and the applicability to common practice.”
BackgroundRisk of Cardiovascular Disease in Patients with Nonalcoholic Fatty Liver Disease
Targher, G., Day, C. P., & Bonora, E. (2010) · New England Journal of Medicine · doi:10.1056/nejmra0912063 · Cited by 1,907
A placebo-controlled trial of pioglitazone in subjects with nonalcoholic steatohepatitis
Belfort, R., Harrison, S. A., Brown, K., Darland, C., Finch, J., Hardies, J., Balas, B., Gastaldelli, A., Tio, F., Pulcini, J., et al. (2006) · New England Journal of Medicine · doi:10.1056/nejmoa060326 · Cited by 1,827
Aithal, G. P., Thomas, J. A., Kaye, P. V., Lawson, A., Ryder, S. D., Spendlove, I., Austin, A. S., Freeman, J. G., Morgan, L., & Webber, J. (2008) · Gastroenterology · doi:10.1053/j.gastro.2008.06.047 · Cited by 721
Angulo, P., Bugianesi, E., Bjornsson, E. S., Charatcharoenwitthaya, P., Mills, P. R., Barrera, F., Haflidadottir, S., Day, C. P., & George, J. (2013) · Gastroenterology · doi:10.1053/j.gastro.2013.06.057 · Cited by 502
Pathology of nonalcoholic fatty liver disease
Brunt, E. M. (2010) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2010.21 · Cited by 484
Cited by
Chalasani, N., Younossi, Z., Lavine, J. E., Charlton, M., Cusi, K., Rinella, M., Harrison, S. A., Brunt, E. M., & Sanyal, A. J. (2018) · Hepatology · doi:10.1002/hep.29367 · Cited by 7,239
EASL–EASD–EASO Clinical Practice Guidelines for the management of non-alcoholic fatty liver disease
(2016) · Journal of Hepatology · doi:10.1016/j.jhep.2015.11.004 · Cited by 4,836
Angulo, P., Kleiner, D. E., Dam-Larsen, S., Adams, L. A., Bjornsson, E. S., Charatcharoenwitthaya, P., Mills, P. R., Keach, J. C., Lafferty, H. D., Stahler, A., et al. (2015) · Gastroenterology · doi:10.1053/j.gastro.2015.04.043 · Cited by 2,987
Non-alcoholic fatty liver disease
Powell, E. E., Wong, V. W.-S., & Rinella, M. (2021) · The Lancet · doi:10.1016/s0140-6736(20)32511-3 · Cited by 2,789
Rinella, M. E., Neuschwander-Tetri, B. A., Siddiqui, M. S., Abdelmalek, M. F., Caldwell, S., Barb, D., Kleiner, D. E., & Loomba, R. (2023) · Hepatology · doi:10.1097/hep.0000000000000323 · Cited by 2,667
Taylor, R. S., Taylor, R. J., Bayliss, S., Hagström, H., Nasr, P., Schattenberg, J. M., Ishigami, M., Toyoda, H., Wai-Sun Wong, V., Peleg, N., et al. (2020) · Gastroenterology · doi:10.1053/j.gastro.2020.01.043 · Cited by 1,069
Hagström, H., Nasr, P., Ekstedt, M., Hammar, U., Stål, P., Hultcrantz, R., & Kechagias, S. (2017) · Journal of Hepatology · doi:10.1016/j.jhep.2017.07.027 · Cited by 1,067
A Randomized, Controlled Trial of the Pan-PPAR Agonist Lanifibranor in NASH
Francque, S. M., Bedossa, P., Ratziu, V., Anstee, Q. M., Bugianesi, E., Sanyal, A. J., Loomba, R., Harrison, S. A., Balabanska, R., Mateva, L., et al. (2021) · New England Journal of Medicine · doi:10.1056/nejmoa2036205 · Cited by 801
Liu, Y.-L., Reeves, H. L., Burt, A. D., Tiniakos, D., McPherson, S., Leathart, J. B. S., Allison, M. E. D., Alexander, G. J., Piguet, A.-C., Anty, R., et al. (2014) · Nature Communications · doi:10.1038/ncomms5309 · Cited by 623
Krenkel, O., Puengel, T., Govaere, O., Abdallah, A. T., Mossanen, J. C., Kohlhepp, M., Liepelt, A., Lefebvre, E., Luedde, T., Hellerbrand, C., et al. (2018) · Hepatology · doi:10.1002/hep.29544 · Cited by 557
A diet-induced animal model of non-alcoholic fatty liver disease and hepatocellular cancer
Asgharpour, A., Cazanave, S. C., Pacana, T., Seneshaw, M., Vincent, R., Banini, B. A., Kumar, D. P., Daita, K., Min, H.-K., Mirshahi, F., et al. (2016) · Journal of Hepatology · doi:10.1016/j.jhep.2016.05.005 · Cited by 538
Anstee, Q. M., Darlay, R., Cockell, S., Meroni, M., Govaere, O., Tiniakos, D., Burt, A. D., Bedossa, P., Palmer, J., Liu, Y.-L., et al. (2020) · Journal of Hepatology · doi:10.1016/j.jhep.2020.04.003 · Cited by 499
Self-citationPast, present and future perspectives in nonalcoholic fatty liver disease
Sanyal, A. J. (2019) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0144-8 · Cited by 522
Targeting mitochondria-located circrna scar alleviates nash via reducing mros output
Zhao, Q., Liu, J., Deng, H., Ma, R., Liao, J.-Y., Liang, H., Hu, J., Li, J., Guo, Z., Cai, J., et al. (2020) · Cell · doi:10.1016/j.cell.2020.08.009 · Cited by 469
Farrell, G., Schattenberg, J. M., Leclercq, I., Yeh, M. M., Goldin, R., Teoh, N., & Schuppan, D. (2019) · Hepatology · doi:10.1002/hep.30333 · Cited by 313
Kleiner, D. E., & Makhlouf, H. R. (2016) · Clinics in Liver Disease · doi:10.1016/j.cld.2015.10.011 · Cited by 303
Harrison, S. A., Gawrieh, S., Roberts, K., Lisanti, C. J., Schwope, R. B., Cebe, K. M., Paradis, V., Bedossa, P., Aldridge Whitehead, J. M., Labourdette, A., et al. (2021) · Journal of Hepatology · doi:10.1016/j.jhep.2021.02.034 · Cited by 293
Self-citationNon-alcoholic fatty liver disease: A patient guideline
Francque, S. M., Marchesini, G., Kautz, A., Walmsley, M., Dorner, R., Lazarus, J. V., Zelber-Sagi, S., Hallsworth, K., Busetto, L., Frühbeck, G., et al. (2021) · JHEP Reports · doi:10.1016/j.jhepr.2021.100322 · Cited by 264
Vacca, M., Kamzolas, I., Harder, L. M., Oakley, F., Trautwein, C., Hatting, M., Ross, T., Bernardo, B., Oldenburger, A., Hjuler, S. T., et al. (2024) · Nature Metabolism · doi:10.1038/s42255-024-01043-6 · Cited by 262
Self-citationNonalcoholic fatty liver disease in adults: current concepts in etiology, outcomes, and management
Marjot, T., Moolla, A., Cobbold, J. F., Hodson, L., & Tomlinson, J. W. (2020) · Endocrine Reviews · doi:10.1210/endrev/bnz009 · Cited by 228
Impact of non-invasive biomarkers on hepatology practice: past, present and future
Anstee, Q. M., Castera, L., & Loomba, R. (2022) · Journal of Hepatology · doi:10.1016/j.jhep.2022.03.026 · Cited by 224
Ratziu, V., de Guevara, L., Safadi, R., Poordad, F., Fuster, F., Flores-Figueroa, J., Arrese, M., Fracanzani, A. L., Ben Bashat, D., Lackner, K., et al. (2021) · Nature Medicine · doi:10.1038/s41591-021-01495-3 · Cited by 222
Vali, Y., Lee, J., Boursier, J., Petta, S., Wonders, K., Tiniakos, D., Bedossa, P., Geier, A., Francque, S., Allison, M., et al. (2023) · The Lancet Gastroenterology & Hepatology · doi:10.1016/s2468-1253(23)00017-1 · Cited by 224
Self-citationMicrobiome-derived ethanol in nonalcoholic fatty liver disease
Meijnikman, A. S., Davids, M., Herrema, H., Aydin, O., Tremaroli, V., Rios-Morales, M., Levels, H., Bruin, S., de Brauw, M., Verheij, J., et al. (2022) · Nature Medicine · doi:10.1038/s41591-022-02016-6 · Cited by 215
Younes, R., Govaere, O., Petta, S., Miele, L., Tiniakos, D., Burt, A., David, E., Vecchio, F. M., Maggioni, M., Cabibi, D., et al. (2022) · Gut · doi:10.1136/gutjnl-2020-322564 · Cited by 205
Boursier, J., Hagström, H., Ekstedt, M., Moreau, C., Bonacci, M., Cure, S., Ampuero, J., Nasr, P., Tallab, L., Canivet, C. M., et al. (2022) · Journal of Hepatology · doi:10.1016/j.jhep.2021.12.031 · Cited by 206
Younes, R., Caviglia, G. P., Govaere, O., Rosso, C., Armandi, A., Sanavia, T., Pennisi, G., Liguori, A., Francione, P., Gallego-Durán, R., et al. (2021) · Journal of Hepatology · doi:10.1016/j.jhep.2021.05.008 · Cited by 196
Mosca, A., Nobili, V., De Vito, R., Crudele, A., Scorletti, E., Villani, A., Alisi, A., & Byrne, C. D. (2017) · Journal of Hepatology · doi:10.1016/j.jhep.2016.12.025 · Cited by 161
Mechanisms of Insulin Resistance in Primary and Secondary Nonalcoholic Fatty Liver
Jelenik, T., Kaul, K., Séquaris, G., Flögel, U., Phielix, E., Kotzka, J., Knebel, B., Fahlbusch, P., Hörbelt, T., Lehr, S., et al. (2017) · Diabetes · doi:10.2337/db16-1147 · Cited by 154
Brunt, E. M., Kleiner, D. E., Wilson, L. A., Sanyal, A. J., Neuschwander‐Tetri, B. A., & for the Nonalcoholic Steatohepatitis Clinical Research Network (2019) · Hepatology · doi:10.1002/hep.30418 · Cited by 154
Forlano, R., Mullish, B. H., Giannakeas, N., Maurice, J. B., Angkathunyakul, N., Lloyd, J., Tzallas, A. T., Tsipouras, M., Yee, M., Thursz, M. R., et al. (2020) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2019.12.025 · Cited by 142
Performance of the PRO-C3 collagen neo-epitope biomarker in non-alcoholic fatty liver disease
Boyle, M., Tiniakos, D., Schattenberg, J. M., Ratziu, V., Bugianessi, E., Petta, S., Oliveira, C. P., Govaere, O., Younes, R., McPherson, S., et al. (2019) · JHEP Reports · doi:10.1016/j.jhepr.2019.06.004 · Cited by 140
Castera, L., Laouenan, C., Vallet-Pichard, A., Vidal-Trécan, T., Manchon, P., Paradis, V., Roulot, D., Gault, N., Boitard, C., Terris, B., et al. (2023) · Diabetes Care · doi:10.2337/dc22-2048 · Cited by 136
Hagström, H., Nasr, P., Ekstedt, M., Stål, P., Hultcrantz, R., & Kechagias, S. (2019) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2018.11.030 · Cited by 132
Naoumov, N. V., Brees, D., Loeffler, J., Chng, E., Ren, Y., Lopez, P., Tai, D., Lamle, S., & Sanyal, A. J. (2022) · Journal of Hepatology · doi:10.1016/j.jhep.2022.06.018 · Cited by 115
Hansen, C. D., Gram-Kampmann, E.-M., Hansen, J. K., Hugger, M. B., Madsen, B. S., Jensen, J. M., Olesen, S., Torp, N., Rasmussen, D. N., Kjærgaard, M., et al. (2023) · Annals of Internal Medicine · doi:10.7326/m22-1787 · Cited by 110
Lei, L., Bruneau, A., El Mourabit, H., Guégan, J., Folseraas, T., Lemoinne, S., Karlsen, T. H., Hoareau, B., Morichon, R., Gonzalez‐Sanchez, E., et al. (2022) · Hepatology · doi:10.1002/hep.32456 · Cited by 94
Persistence of severe liver fibrosis despite substantial weight loss with bariatric surgery
Pais, R., Aron‐Wisnewsky, J., Bedossa, P., Ponnaiah, M., Oppert, J., Siksik, J., Genser, L., Charlotte, F., Thabut, D., Clement, K., et al. (2022) · Hepatology · doi:10.1002/hep.32358 · Cited by 95
Non-alcoholic fatty liver disease alters expression of genes governing hepatic nitrogen conversion
Eriksen, P. L., Vilstrup, H., Rigbolt, K., Suppli, M. P., Sørensen, M., Heebøll, S., Veidal, S. S., Knop, F. K., & Thomsen, K. L. (2019) · Liver International · doi:10.1111/liv.14205 · Cited by 81
Puengel, T., Lefere, S., Hundertmark, J., Kohlhepp, M., Penners, C., Van de Velde, F., Lapauw, B., Hoorens, A., Devisscher, L., Geerts, A., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23126696 · Cited by 59
Iyer, J. S., Juyal, D., Le, Q., Shanis, Z., Pokkalla, H., Pouryahya, M., Pedawi, A., Stanford-Moore, S. A., Biddle-Snead, C., Carrasco-Zevallos, O., et al. (2024) · Nature Medicine · doi:10.1038/s41591-024-03172-7 · Cited by 54
Use of Artificial Intelligence as an Innovative Method for Liver Graft Macrosteatosis Assessment
Cesaretti, M., Brustia, R., Goumard, C., Cauchy, F., Poté, N., Dondero, F., Paugam‐Burtz, C., Durand, F., Paradis, V., Diaspro, A., et al. (2020) · Liver Transplantation · doi:10.1002/lt.25801 · Cited by 50
Canivet, C. M., Costentin, C., Irvine, K. M., Delamarre, A., Lannes, A., Sturm, N., Oberti, F., Patel, P. J., Decaens, T., Irles‐Depé, M., et al. (2023) · Hepatology · doi:10.1002/hep.32665 · Cited by 49
Akuta, N., Kawamura, Y., Fujiyama, S., Sezaki, H., Hosaka, T., Kobayashi, M., Kobayashi, M., Saitoh, S., Suzuki, F., Suzuki, Y., et al. (2020) · Internal Medicine · doi:10.2169/internalmedicine.4398-19 · Cited by 48
Chronic hepatitis B infection with concomitant hepatic steatosis: current evidence and opinion
Shi, Y.-W., Yang, R.-X., & Fan, J.-G. (2021) · World Journal of Gastroenterology · doi:10.3748/wjg.v27.i26.3971 · Cited by 47
Authors, & Collaborators: (2022) · Zeitschrift für Gastroenterologie · doi:10.1055/a-1880-2388 · Cited by 30
Patel, Y. A., Imperial, J. C., Muir, A. J., Anstee, Q. M., DeBrota, D., Dimick-Santos, L., Filozof, C., Mehta, R., Sanyal, A. J., Schabel, E., et al. (2017) · Gastroenterology · doi:10.1053/j.gastro.2017.07.024 · Cited by 25
Cazanave, S. C., Warren, A. D., Pacula, M., Touti, F., Zagorska, A., Gural, N., Huang, E. K., Sherman, S., Cheema, M., Ibarra, S., et al. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.abe8939 · Cited by 23
Metadata
- Authors
- Bedossa, P.
- Venue
- Hepatology
- Published
- 2014-08
- Volume
- 60
- Issue
- 2
- Pages
- 565-575
- ISSN
- 0270-9139 (ISSN-L)
- OpenAlex
- W2139654088
- Cited by
- 625
- References
- 11
- FWCI
- 24.27
- Type
- journal article
- Language
- en
- Open access
- bronze
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 ›
Are you an author, or do you see a problem with this page? Request a review
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.
