Accuracy of a sequential algorithm based on FIB-4 and ELF to identify high-risk advanced liver fibrosis at the primary care level.

Advanced liver fibrosis Chronic liver disease ELF FIB-4 NASH Type 2 diabetes

Journal

Internal and emergency medicine
ISSN: 1970-9366
Titre abrégé: Intern Emerg Med
Pays: Italy
ID NLM: 101263418

Informations de publication

Date de publication:
11 Nov 2023
Historique:
received: 02 12 2022
accepted: 21 06 2023
medline: 12 11 2023
pubmed: 12 11 2023
entrez: 11 11 2023
Statut: aheadofprint

Résumé

Non-alcoholic fatty liver disease (NAFLD) is the leading cause of chronic liver disease, and liver fibrosis is the strongest predictor of morbimortality. We aimed to assess the performance of a sequential algorithm encompassing the Fibrosis 4 (FIB-4) and Enhanced Liver Fibrosis (ELF) scores for identifying patients at risk of advanced fibrosis. This cross-sectional study included one hospital-based cohort with biopsy-proven NAFLD (n = 140) and two primary care cohorts from different clinical settings: Type 2 Diabetes (T2D) follow-up (n = 141) and chronic liver disease (CLD) initial study (n = 138). Logistic regression analysis was performed to assess liver fibrosis diagnosis models based on FIB-4 and ELF biomarkers. The sequential algorithm retrieved the following accuracy parameters in predicting stages F3-4 in the biopsy-confirmed cohort: sensitivity (85%), specificity (73%), negative predictive value (79%) and positive predictive value (81%). In both T2D and CLD cohorts, a total of 28% of patients were classified as stages F3-4. Furthermore, of all F3-4 classified patients in the T2D cohort, 80% had a diagnosis of liver disease and 44% were referred to secondary care. Likewise, of all F3-4 classified patients in the CLD cohort, 71% had a diagnosis of liver disease and 44% were referred to secondary care. These results suggest the potential utility of this algorithm as a liver fibrosis stratifying tool in primary care, where updating referral protocols to detect high-risk F3-4 is needed. FIB-4 and ELF sequential measurement is an efficient strategy to prioritize patients with high risk of F3-4 in populations with metabolic risk factors.

Identifiants

pubmed: 37952070
doi: 10.1007/s11739-023-03441-2
pii: 10.1007/s11739-023-03441-2
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023. The Author(s).

Références

Karlsen TH, Sheron N, Zelber-Sagi S, Carrieri P, Dusheiko G, Bugianesi E et al (2022) The EASL–lancet liver commission: protecting the next generation of Europeans against liver disease complications and premature mortality. Lancet 399:61–116. https://doi.org/10.1016/S0140-6736(21)01701-3
doi: 10.1016/S0140-6736(21)01701-3 pubmed: 34863359
Blanco-Grau A, Gabriel-Medina P, Rodriguez-Algarra F, Villena Y, Lopez-Martínez R, Augustín S et al (2021) Assessing liver fibrosis using the fib4 index in the community setting. Diagnostics 11:2236. https://doi.org/10.3390/diagnostics11122236
doi: 10.3390/diagnostics11122236 pubmed: 34943471 pmcid: 8700445
Cotter TG, Nonalcoholic RM, Disease FL (2020) The state of the disease (2020). Gastroenterology 158:1851–1864. https://doi.org/10.1053/j.gastro.2020.01.052
doi: 10.1053/j.gastro.2020.01.052 pubmed: 32061595
Younossi ZM, Koenig AB, Abdelatif D, Fazel Y, Henry L, Wymer M (2016) Global epidemiology of nonalcoholic fatty liver disease—meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology 64:73–84. https://doi.org/10.1002/hep.28431
doi: 10.1002/hep.28431 pubmed: 26707365
Younossi Z, Anstee QM, Marietti M, Hardy T, Henry L, Eslam M et al (2018) Global burden of NAFLD and NASH: trends, predictions, risk factors and prevention. Nat Rev Gastroenterol Hepatol 15:11–20. https://doi.org/10.1038/nrgastro.2017.109
doi: 10.1038/nrgastro.2017.109 pubmed: 28930295
Chalasani N, Younossi Z, Lavine JE, Charlton M, Cusi K, Rinella M et al (2018) The diagnosis and management of nonalcoholic fatty liver disease: practice guidance from the American association for the study of liver diseases. Hepatology 67:328–357. https://doi.org/10.1002/hep.29367
doi: 10.1002/hep.29367 pubmed: 28714183
Mazzolini G, Sowa JP, Atorrasagasti C, Kücükoglu Ö, Syn WK, Canbay A (2020) Significance of simple steatosis: an update on the clinical and molecular evidence. Cells 9:1–19. https://doi.org/10.3390/cells9112458
doi: 10.3390/cells9112458
Sanyal AJ, Van Natta ML, Clark J, Neuschwander-Tetri BA, Diehl A, Dasarathy S et al (2021) Prospective study of outcomes in adults with nonalcoholic fatty liver disease. N Engl J Med 385:1559–1569. https://doi.org/10.1056/NEJMoa2029349
doi: 10.1056/NEJMoa2029349 pubmed: 34670043 pmcid: 8881985
Angulo P, Kleiner DE, Dam-Larsen S, Adams LA, Bjornsson ES, Charatcharoenwitthaya P et al (2015) Liver fibrosis, but no other histologic features, is associated with long-term outcomes of patients with nonalcoholic fatty liver disease. Gastroenterology 149:389-397.e10. https://doi.org/10.1053/j.gastro.2015.04.043
doi: 10.1053/j.gastro.2015.04.043 pubmed: 25935633
Dulai PS, Singh S, Patel J, Soni M, Prokop LJ, Younossi Z et al (2017) Increased risk of mortality by fibrosis stage in nonalcoholic fatty liver disease: Systematic review and meta-analysis. Hepatology 65:1557–1565. https://doi.org/10.1002/hep.29085
doi: 10.1002/hep.29085 pubmed: 28130788
Estes C, Anstee QM, Arias-Loste MT, Bantel H, Bellentani S, Caballeria J et al (2018) Modeling NAFLD disease burden in China, France, Germany, Italy, Japan, Spain, United Kingdom, and United States for the period 2016–2030. J Hepatol 69:896–904. https://doi.org/10.1016/j.jhep.2018.05.036
doi: 10.1016/j.jhep.2018.05.036 pubmed: 29886156
Younossi Z (2019) Non-alcoholic fatty liver disease – a global public health perspective. J Hepatol 70:531–544. https://doi.org/10.1016/j.jhep.2018.10.033
doi: 10.1016/j.jhep.2018.10.033 pubmed: 30414863
Younossi ZM, Golabi P, de Avila L, Paik JM, Srishord M, Fukui N et al (2019) The global epidemiology of NAFLD and NASH in patients with type 2 diabetes: a systematic review and meta-analysis. J Hepatol 71:793–801. https://doi.org/10.1016/j.jhep.2019.06.021
doi: 10.1016/j.jhep.2019.06.021 pubmed: 31279902
Perrault J, McGill DB, Ott BJ, Taylor WF (1978) Liver biopsy: complications in 1000 inpatients and outpatients. Gastroenterology 74:103–106. https://doi.org/10.1016/0016-5085(78)90364-5
doi: 10.1016/0016-5085(78)90364-5 pubmed: 618417
Wai CT, Greenson JK, Fontana RJ, Kalbfleisch JD, Marrero JA, Conjeevaram HS et al (2003) A simple noninvasive index can predict both significant fibrosis and cirrhosis in patients with chronic hepatitis C. Hepatology 38:518–526. https://doi.org/10.1053/jhep.2003.50346
doi: 10.1053/jhep.2003.50346 pubmed: 12883497
Rossi E, Adams LA, Bulsara M, Jeffrey GP (2007) Assessing liver fibrosis with serum marker models. Clin Biochem Rev 28:3–10. https://doi.org/10.1053/jhep.2003.50346
doi: 10.1053/jhep.2003.50346 pubmed: 17603636 pmcid: 1904421
Gorowska-Kowolik K, Chobot A, Kwiecien J (2017) 13C methacetin breath test for assessment of microsomal liver function: methodology and clinical application. Gastroenterol Res Pract 2017:7397840. https://doi.org/10.1155/2017/7397840
doi: 10.1155/2017/7397840 pubmed: 28757868 pmcid: 5516731
da Silva Junior RG, de Miranda MLQ, de Araújo Caldeira Brant PE et al (2021) Acoustic radiation force impulse elastography and liver fibrosis risk scores in severe obesity. Arch Endocrinol Metab 65:730–738. https://doi.org/10.20945/2359-3997000000397
doi: 10.20945/2359-3997000000397 pubmed: 34762779
Reiter R, Wetzel M, Hamesch K et al (2018) Comparison of non-invasive assessment of liver fibrosis in patients with alpha1-antitrypsin deficiency using magnetic resonance elastography (MRE), acoustic radiation force impulse (ARFI) quantification, and 2D-shear wave elastography (2D-SWE). PLoS One 13:e0196486. https://doi.org/10.1371/journal.pone.0196486
doi: 10.1371/journal.pone.0196486 pubmed: 29698472 pmcid: 5919507
Hanquinet S, Rougemont AL, Courvoisier D et al (2013) Acoustic radiation force impulse (ARFI) elastography for the noninvasive diagnosis of liver fibrosis in children. Pediatr Radiol 43:545–551. https://doi.org/10.1007/s00247-012-2595-8
doi: 10.1007/s00247-012-2595-8 pubmed: 23271404
Serra-Burriel M, Graupera I, Torán P, Thiele M, Roulot D, Wai-Sun Wong V et al (2019) Transient elastography for screening of liver fibrosis: cost-effectiveness analysis from six prospective cohorts in Europe and Asia. J Hepatol 71:1141–1151. https://doi.org/10.1016/j.jhep.2019.08.019
doi: 10.1016/j.jhep.2019.08.019 pubmed: 31470067
Carrion JA, Puigvehí M, Coll S, Garcia-Retortillo M, Cañete N, Fernández R et al (2015) Applicability and accuracy improvement of transient elastography using the M and XL probes by experienced operators. J Viral Hepat 22:297–306. https://doi.org/10.1111/jvh.12296
doi: 10.1111/jvh.12296 pubmed: 25164560
Castera L, Friedrich-Rust M, Loomba R (2019) Noninvasive assessment of liver disease in patients with nonalcoholic fatty liver disease. Gastroenterology 156:1264-1281.e4. https://doi.org/10.1053/j.gastro.2018.12.036
doi: 10.1053/j.gastro.2018.12.036 pubmed: 30660725
Wong VWS, Adams LA, de Lédinghen V, Wong GLH, Sookoian S (2018) Noninvasive biomarkers in NAFLD and NASH—current progress and future promise. Nat Rev Gastroenterol Hepatol 15:461–478. https://doi.org/10.1038/s41575-018-0014-9
doi: 10.1038/s41575-018-0014-9 pubmed: 29844588
Sterling RK, Lissen E, Clumeck N, Sola R, Correa MC, Montaner J et al (2006) Development of a simple noninvasive index to predict significant fibrosis in patients with HIV/HCV coinfection. Hepatology 43:1317–1325. https://doi.org/10.1002/hep.21178
doi: 10.1002/hep.21178 pubmed: 16729309
Wang L, Wang M, Zhao W, Shi Y, Sun Y, Wu X et al (2015) Key points of 2015 EASL-ALEH clinical practice guidelines: non invasive tests for evaluation of liver severity and prognosis. Zhonghua Gan Zang Bing Za Zhi 23:488–492
pubmed: 26629574
Berzigotti A, Tsochatzis E, Boursier J, Castera L, Cazzagon N, Friedrich-Rust M et al (2021) EASL Clinical Practice Guidelines on non-invasive tests for evaluation of liver disease severity and prognosis – 2021 update. J Hepatol 75:659–689. https://doi.org/10.1016/j.jhep.2021.05.025
doi: 10.1016/j.jhep.2021.05.025
Boursier J, Hagström H, Ekstedt M, Moreau C, Bonacci M, Cure S et al (2022) Non-invasive tests accurately stratify patients with NAFLD based on their risk of liver-related events. J Hepatol 76:1013–1020. https://doi.org/10.1016/j.jhep.2021.12.031
doi: 10.1016/j.jhep.2021.12.031 pubmed: 35063601
Wong GLH, Chan HLY, Choi PCL, Chan AWH, Yu Z, Lai JWY et al (2014) Non-invasive algorithm of enhanced liver fibrosis and liver stiffness measurement with transient elastography for advanced liver fibrosis in chronic hepatitis B. Aliment Pharmacol Ther 39:197–208. https://doi.org/10.1111/apt.12559
doi: 10.1111/apt.12559 pubmed: 24261924
Fernandes FF, Ferraz ML, Andrade LE, Dellavance A, Terra C, Pereira G et al (2015) Enhanced liver fibrosis panel as a predictor of liver fibrosis in chronic hepatitis C patients. J Clin Gastroenterol 49:235–241. https://doi.org/10.1097/MCG.0000000000000128
doi: 10.1097/MCG.0000000000000128 pubmed: 24714186
Guillaume M, Moal V, Delabaudiere C, Zuberbuhler F, Robic MA, Lannes A et al (2019) Direct comparison of the specialised blood fibrosis tests FibroMeterV2G and Enhanced Liver Fibrosis score in patients with non-alcoholic fatty liver disease from tertiary care centres. Aliment Pharmacol Ther 50:1214–1222. https://doi.org/10.1111/apt.15529
doi: 10.1111/apt.15529 pubmed: 31617224
Mansour D, Grapes A, Herscovitz M, Cassidy P, Vernazza J, Broad A et al (2021) Embedding assessment of liver fibrosis into routine diabetic review in primary care. JHEP Reports 3:100293. https://doi.org/10.1016/j.jhepr.2021.100293
doi: 10.1016/j.jhepr.2021.100293 pubmed: 34179738 pmcid: 8213901
Boursier J, Tsochatzis EA (2021) Case-finding strategies in non-alcoholic fatty liver disease. JHEP Rep 3:100219. https://doi.org/10.1016/j.jhepr.2020.100219
doi: 10.1016/j.jhepr.2020.100219 pubmed: 33659890
Tsochatzis EA, Newsome PN (2018) Non-alcoholic fatty liver disease and the interface between primary and secondary care. Lancet Gastroenterol Hepatol 3:509–517. https://doi.org/10.1016/S2468-1253(18)30077-3
doi: 10.1016/S2468-1253(18)30077-3 pubmed: 29893235
Srivastava A, Jong S, Gola A, Gailer R, Morgan S, Sennett K et al (2019) Cost-comparison analysis of FIB-4, ELF and fibroscan in community pathways for non-alcoholic fatty liver disease. BMC Gastroenterol 19:122. https://doi.org/10.1186/s12876-019-1039-4
doi: 10.1186/s12876-019-1039-4 pubmed: 31296161 pmcid: 6624894
Vilar-Gomez E, Chalasani N (2018) Non-invasive assessment of non-alcoholic fatty liver disease: clinical prediction rules and blood-based biomarkers. J Hepatol 68:305–315. https://doi.org/10.1016/j.jhep.2017.11.013
doi: 10.1016/j.jhep.2017.11.013 pubmed: 29154965
Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW et al (2005) Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41:1313–1321. https://doi.org/10.1002/hep.20701
doi: 10.1002/hep.20701 pubmed: 15915461
Ferraioli G, Soares Monteiro LB (2019) Ultrasound-based techniques for the diagnosis of liver steatosis. World J Gastroenterol 25(40):6053–6062. https://doi.org/10.3748/wjg.v25.i40.6053
doi: 10.3748/wjg.v25.i40.6053 pubmed: 31686762 pmcid: 6824276
Castera L, Yuen Chan HL, Arrese M et al (2015) EASL-ALEH Clinical Practice Guidelines: non-invasive tests for evaluation of liver disease severity and prognosis. J Hepatol 63(1):237–264. https://doi.org/10.1016/j.jhep.2015.04.006
doi: 10.1016/j.jhep.2015.04.006
Eddowes PJ, Sasso M, Allison M et al (2019) Accuracy of fibroscan controlled attenuation parameter and liver stiffness measurement in assessing steatosis and fibrosis in patients with nonalcoholic fatty liver disease. Gastroenterology 156(6):1717–1730. https://doi.org/10.1053/j.gastro.2019.01.042
doi: 10.1053/j.gastro.2019.01.042 pubmed: 30689971
American Diabetes Association (2021) 2. Classification and diagnosis of diabetes: standards of medical care in diabetes-2021. Diabetes Care 44:S15–S33. https://doi.org/10.2337/dc21-S002
doi: 10.2337/dc21-S002
Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419. https://doi.org/10.1007/BF00280883
doi: 10.1007/BF00280883 pubmed: 3899825
Shashaj B, Luciano R, Contoli B, Morino GS, Spreghini MR, Rustico C et al (2016) Reference ranges of HOMA-IR in normal-weight and obese young Caucasians. Acta Diabetol 53:251–260. https://doi.org/10.1007/s00592-015-0782-4
doi: 10.1007/s00592-015-0782-4 pubmed: 26070771
Wong VWS, Vergniol J, Wong GLH, Foucher J, Chan HLY, Le Bail B et al (2010) Diagnosis of fibrosis and cirrhosis using liver stiffness measurement in nonalcoholic fatty liver disease. Hepatology 51:454–462. https://doi.org/10.1002/hep.23312
doi: 10.1002/hep.23312 pubmed: 20101745
Singh S, Allen AM, Wang Z, Prokop LJ, Murad MH, Loomba R (2015) Fibrosis progression in nonalcoholic fatty liver vs nonalcoholic steatohepatitis: a systematic review and meta-analysis of paired-biopsy studies. Clin Gastroenterol Hepatol 13:643-e40. https://doi.org/10.1016/j.cgh.2014.04.014
doi: 10.1016/j.cgh.2014.04.014 pubmed: 24768810
Guha IN, Parkes J, Roderick P, Chattopadhyay D, Cross R, Harris S et al (2008) Noninvasive markers of fibrosis in nonalcoholic fatty liver disease: validating the European liver fibrosis panel and exploring simple markers. Hepatology 47:455–460. https://doi.org/10.1002/hep.21984
doi: 10.1002/hep.21984 pubmed: 18038452
Dongiovanni P, Petta S, Maglio C, Fracanzani AL, Pipitone R, Mozzi E et al (2015) Transmembrane 6 superfamily member 2 gene variant disentangles nonalcoholic steatohepatitis from cardiovascular disease. Hepatology 61:506–514. https://doi.org/10.1002/hep.27490
doi: 10.1002/hep.27490 pubmed: 25251399
Lonardo A, Nascimbeni F, Mantovani A, Targher G (2018) Hypertension, diabetes, atherosclerosis and NASH: cause or consequence? J Hepatol 68(2):335–352. https://doi.org/10.1016/j.jhep.2017.09.021
doi: 10.1016/j.jhep.2017.09.021 pubmed: 29122390
Lomonaco R, Leiva EG, Bril F, Shrestha S, Mansour L, Budd J et al (2021) Advanced liver fibrosis is common in patients with type 2 diabetes followed in the outpatient setting: the need for systematic screening. Diabetes Care 44:399–406. https://doi.org/10.2337/dc20-1997
doi: 10.2337/dc20-1997 pubmed: 33355256 pmcid: 7818321
Sorrentino P, Terracciano L, D’Angelo S, Ferbo U, Bracigliano A, Vecchione R (2010) Predicting fibrosis worsening in obese patients with NASH through parenchymal fibronectin, HOMA-IR, and hypertension. Am J Gastroenterol 105:336–344. https://doi.org/10.1038/ajg.2009.587
doi: 10.1038/ajg.2009.587 pubmed: 19861959
Chatterjee A, Basu A, Das K, Singh P, Mondal D, Bhattacharya B et al (2020) Hepatic transcriptome signature correlated with HOMA-IR explains early nonalcoholic fatty liver disease pathogenesis. Ann Hepatol 19:472–481. https://doi.org/10.1016/j.aohep.2020.06.009
doi: 10.1016/j.aohep.2020.06.009 pubmed: 32682086
Dongiovanni P, Stender S, Pietrelli A, Mancina RM, Cespiati A, Petta S et al (2018) Causal relationship of hepatic fat with liver damage and insulin resistance in nonalcoholic fatty liver. J Intern Med 283:356–370. https://doi.org/10.1111/joim.12719
doi: 10.1111/joim.12719 pubmed: 29280273
Gabriel-Medina P, Ferrer-Costa R, Rodriguez-Frias F, Ciudin A, Augustin S, Rivera-Esteban J, Pericàs JM, Selva DM (2022) Influence of Type 2 diabetes in the association of PNPLA3 rs738409 and TM6SF2 rs58542926 polymorphisms in NASH advanced liver fibrosis. Biomedicines 10:1015. https://doi.org/10.3390/biomedicines10051015
doi: 10.3390/biomedicines10051015 pubmed: 35625751 pmcid: 9139123
Friedman SL, Neuschwander-Tetri BA, Rinella M, Sanyal AJ (2018) Mechanisms of NAFLD development and therapeutic strategies. Nat Med 24:908–922. https://doi.org/10.1038/s41591-018-0104-9
doi: 10.1038/s41591-018-0104-9 pubmed: 29967350 pmcid: 6553468
Myers RP, Crotty P, Pomier-Layrargues G, Ma M, Urbanski SJ, Elkashab M (2010) Prevalence, risk factors and causes of discordance in fibrosis staging by transient elastographyand liver biopsy. Liver Int 30:1471–1480. https://doi.org/10.1111/j.1478-3231.2010.02331.x
doi: 10.1111/j.1478-3231.2010.02331.x pubmed: 20807336
Kleiner DE, Bedossa P (2015) Liver histology and clinical trials for nonalcoholic steatohepatitis-perspectives from 2 pathologists. Gastroenterology 149:1305–1308. https://doi.org/10.1053/j.gastro.2015.09.015
doi: 10.1053/j.gastro.2015.09.015 pubmed: 26409177
Angulo P, Bugianesi E, Bjornsson ES, Charatcharoenwitthaya P, Mills PR, Barrera F et al (2013) Simple noninvasive systems predict long-term outcomes of patients with nonalcoholic fatty liver disease. Gastroenterology 145:782–9.e4. https://doi.org/10.1053/j.gastro.2013.06.057
doi: 10.1053/j.gastro.2013.06.057 pubmed: 23860502
Shah AG, Lydecker A, Murray K, Tetri BN, Contos MJ, Sanyal AJ, NASH Clinical Research Network (2009) Use of the fib4 index for non-invasive evaluation of fibrosis in nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 7:1104–1112. https://doi.org/10.1016/j.cgh.2009.05.033
doi: 10.1016/j.cgh.2009.05.033 pubmed: 19523535 pmcid: 3079239
Nobili V, Parkes J, Bottazzo G, Marcellini M, Cross R, Newman D (2009) Performance of ELF serum markers in predicting fibrosis stage in pediatric non-alcoholic fatty liver disease. Gastroenterology 136:160–167. https://doi.org/10.1053/j.gastro.2008.09.013
doi: 10.1053/j.gastro.2008.09.013 pubmed: 18992746
López IC, Aroca FG, Bernal MDF, Mompeán JAL, Bernal ÁB, Martínez AMH et al (2017) Utility of the ELF test for detecting steatohepatitis in morbid obese patients with suspicion of nonalcoholic fatty liver disease. Obes Surg 27:2347–2353. https://doi.org/10.1007/s11695-017-2606-9
doi: 10.1007/s11695-017-2606-9 pubmed: 28229316
Lichtinghagen R, Pietsch D, Bantel H, Manns MP, Brand K, Bahr MJ (2013) The enhanced liver fibrosis (ELF) score: normal values, influence factors and proposed cut-off values. J Hepatol 59:236–242. https://doi.org/10.1016/j.jhep.2013.03.016
doi: 10.1016/j.jhep.2013.03.016 pubmed: 23523583
Day J, Patel P, Parkes J, Rosenberg W (2019) Derivation and performance of standardized enhanced liver fibrosis (ELF) test thresholds for the detection and prognosis of liver fibrosis. J Appl Lab Med 3:815–826. https://doi.org/10.1373/jalm.2018.027359
doi: 10.1373/jalm.2018.027359 pubmed: 31639756
Parkes J, Roderick P, Harris S, Day C, Mutimer D, Collier J et al (2010) Enhanced liver fibrosis test can predict clinical outcomes in patients with chronic liver disease. Gut 59:1245–1251. https://doi.org/10.1136/gut.2009.203166
doi: 10.1136/gut.2009.203166 pubmed: 20675693
Soto M, Sampietro-Colom L, Lasalvia L, Mira A, Jiménez W, Navasa M (2017) Cost-effectiveness of enhanced liver fibrosis test to assess liver fibrosis in chronic hepatitis C virus and alcoholic liver disease patients. World J Gastroenterol 23:3163–3173. https://doi.org/10.3748/wjg.v23.i17.3163
doi: 10.3748/wjg.v23.i17.3163 pubmed: 28533673 pmcid: 5423053
Honda Y, Yoneda M, Imajo K, Nakajima A (2020) Elastography techniques for the assessment of liver fibrosis in non-alcoholic fatty liver disease. Int J Mol Sci 21:4039. https://doi.org/10.3390/ijms21114039
doi: 10.3390/ijms21114039 pubmed: 32516937 pmcid: 7313067
Kjaergaard M, Lindvig KP, Thorhauge KH et al (2023) Using the ELF test, FIB-4 and NAFLD fibrosis score to screen the population for liver disease. J Hepatol S0168–8278(23):00225–8. https://doi.org/10.1016/j.jhep.2023.04.002
doi: 10.1016/j.jhep.2023.04.002
Younossi ZM, Loomba R, Anstee QM, Rinella ME, Bugianesi E, Marchesini G et al (2018) Diagnostic modalities for nonalcoholic fatty liver disease, nonalcoholic steatohepatitis, and associated fibrosis. Hepatology 68:349–360. https://doi.org/10.1002/hep.29721
doi: 10.1002/hep.29721 pubmed: 29222917
Morling JR, Fallowfield JA, Guha IN, Nee LD, Glancy S, Williamson RM et al (2014) Using non-invasive biomarkers to identify hepatic fibrosis in people with type 2 diabetes mellitus: the Edinburgh type 2 diabetes study. J Hepatol 60:384–391. https://doi.org/10.1016/j.jhep.2013.10.017
doi: 10.1016/j.jhep.2013.10.017 pubmed: 24512822
Thiagarajan P, Chalmers J, Guha IN, James MW (2020) Detecting chronic liver disease: Are liver function tests the solution? Br J Hosp Med 81:1–8. https://doi.org/10.12968/hmed.2019.0308
doi: 10.12968/hmed.2019.0308
Romero-Gómez M, Aller R, Ampuero J et al (2022) AEEH consensus about detection and referral of hidden prevalent liver diseases. Gastroenterol Hepatol S0210–5705(22):00137–6. https://doi.org/10.1016/j.gastrohep.2022.04.001
doi: 10.1016/j.gastrohep.2022.04.001
Marchesini G, Day CP, Dufour JF, Canbay A, Nobili V, Ratziu V et al (2016) EASL-EASD-EASO clinical practice guidelines for the management of non-alcoholic fatty liver disease. J Hepatol 64:1388–1402. https://doi.org/10.1016/j.jhep.2015.11.004
doi: 10.1016/j.jhep.2015.11.004
Bazick J, Donithan M, Neuschwander-Tetri BA, Kleiner D, Brunt EM, Wilson L (2015) Clinical model for NASH and advanced fibrosis in adult patients with diabetes and NAFLD: guidelines for referral in NAFLD. Diabetes Care 38:1347–1355. https://doi.org/10.2337/dc14-1239
doi: 10.2337/dc14-1239 pubmed: 25887357 pmcid: 4477334
Rojano-Toimil A, Rivera-Esteban J, Manzano-Nuñez R, Bañares J, Selva DM, Gabriel-Medina P (2022) When sugar reaches the liver: phenotypes of patients with diabetes and NAFLD. J Clin Med 11:3286. https://doi.org/10.3390/jcm11123286
doi: 10.3390/jcm11123286 pubmed: 35743358 pmcid: 9225139

Auteurs

Pablo Gabriel-Medina (P)

Clinical Biochemistry Department, Vall d'Hebron University Hospital, 08035, Barcelona, Spain. pablo.gabriel@vallhebron.cat.
Biochemistry and Molecular Biology Department, Universitat Autònoma de Barcelona (UAB), 08193, Barcelona, Spain. pablo.gabriel@vallhebron.cat.
Clinical Biochemistry Research Team, Vall d'Hebron Institut de Recerca (VHIR), 08035, Barcelona, Spain. pablo.gabriel@vallhebron.cat.

Roser Ferrer-Costa (R)

Clinical Biochemistry Department, Vall d'Hebron University Hospital, 08035, Barcelona, Spain. roser.ferrer@vallhebron.cat.
Clinical Biochemistry Research Team, Vall d'Hebron Institut de Recerca (VHIR), 08035, Barcelona, Spain. roser.ferrer@vallhebron.cat.

Andreea Ciudin (A)

Endocrinology and Nutrition Department, Vall d'Hebron University Hospital, 08035, Barcelona, Spain.
Diabetes and Metabolism Department, Vall d'Hebron Institut de Recerca (VHIR), Universitat Autònoma de Barcelona (UAB), 08035, Barcelona, Spain.
Centro de Investigación Biomédica en Red de Diabetes y Enfermedades Metabólicas Asociadas (CIBERDEM), 28029, Madrid, Spain.

Salvador Augustin (S)

Liver Unit, Internal Medicine Department, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron University Hospital, 08035, Barcelona, Spain.
Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), 28029, Madrid, Spain.

Jesus Rivera-Esteban (J)

Biochemistry and Molecular Biology Department, Universitat Autònoma de Barcelona (UAB), 08193, Barcelona, Spain.
Liver Unit, Internal Medicine Department, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron University Hospital, 08035, Barcelona, Spain.

J M Pericàs (JM)

Liver Unit, Internal Medicine Department, Vall d'Hebron Institut de Recerca (VHIR), Vall d'Hebron University Hospital, 08035, Barcelona, Spain.
Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), 28029, Madrid, Spain.

D M Selva (DM)

Diabetes and Metabolism Department, Vall d'Hebron Institut de Recerca (VHIR), Universitat Autònoma de Barcelona (UAB), 08035, Barcelona, Spain.
Centro de Investigación Biomédica en Red de Diabetes y Enfermedades Metabólicas Asociadas (CIBERDEM), 28029, Madrid, Spain.

Francisco Rodriguez-Frias (F)

Clinical Biochemistry Department, Vall d'Hebron University Hospital, 08035, Barcelona, Spain.
Biochemistry and Molecular Biology Department, Universitat Autònoma de Barcelona (UAB), 08193, Barcelona, Spain.
Clinical Biochemistry Research Team, Vall d'Hebron Institut de Recerca (VHIR), 08035, Barcelona, Spain.
Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), 28029, Madrid, Spain.

Classifications MeSH