Metabolic dysfunction associated steatotic liver disease in lean patients. Diagnostic and treatment challenges
https://doi.org/10.31146/1682-8658-ecg-229-9-96-109
Abstract
About the Authors
E. E. ZabotinaRussian Federation
Yu. A. Khabarova
Russian Federation
N. Yu. Stukova
Russian Federation
References
1. European Association for the Study of the Liver (EASL); European Association for the Study of Diabetes (EASD); European Association for the Study of Obesity (EASO); European Association for the Study of the Liver (EASL). EASL-EASD-EASO Clinical Practice Guidelines on the management of metabolic dysfunction-associated steatotic liver disease (MASLD). J Hepatol. Published online June 5, 2024. doi: 10.1016/j.jhep.2024.04.031.
2. Ge X, Zheng L, Wang M, Du Y, Jiang J. Prevalence trends in non-alcoholic fatty liver disease at the global, regional and national levels, 1990-2017: a population-based observational study. BMJ Open. 2020 Aug 3;10(8): e036663. doi: 10.1136/bmjopen-2019-036663.
3. Wang, W., Ren, J., Zhou, W. et al. Lean non-alcoholic fatty liver disease (Lean-NAFLD) and the development of metabolic syndrome: a retrospective study. Sci Rep 12, 10977 (2022). doi: 10.1038/s41598-022-14701-0.
4. Long MT, Noureddin M, Lim JK. AGA Clinical Practice Update: Diagnosis and Management of Nonalcoholic Fatty Liver Disease in Lean Individuals: Expert Review. Gastroenterology. 2022;163(3):764-774.e1. doi: 10.1053/j.gastro.2022.06.023.
5. Sato-Espinoza K, Chotiprasidhi P, Huaman MR, Díaz-Ferrer J. Update in lean metabolic dysfunction-associated steatotic liver disease. World J Hepatol. 2024;16(3):452-464. doi: 10.4254/wjh.v16.i3.452.
6. Wang AY, Dhaliwal J, Mouzaki M. Lean non-alcoholic fatty liver disease. Clin Nutr. 2019;38(3):975-981. doi: 10.1016/j.clnu.2018.08.008.
7. Ding C, Chan Z, Magkos F. Lean, but not healthy: the ‘metabolically obese, normal-weight’ phenotype. Curr Opin Clin Nutr Metab Care. 2016 Nov;19(6):408-417. doi: 10.1097/MCO.0000000000000317.
8. Young S., Tariq R., Provenza J., Satapathy S.K., Faisal K., Choudhry A., Friedman S.L., Singal A.K. Prevalence and Profile of Nonalcoholic Fatty Liver Disease in Lean Adults: Systematic Review and Meta-Analysis. Hepatol Commun. 2020 May 21;4(7):953-972. doi: 10.1002/hep4.1519.
9. Younes R, Govaere O, Petta S, et al. Caucasian lean subjects with non-alcoholic fatty liver disease share long-term prognosis of non-lean: time for reappraisal of BMI-driven approach?. Gut. 2022;71(2):382-390. doi: 10.1136/gutjnl-2020-322564.
10. Rinella M.E., Lazarus J.V., Ratziu V., Francque S.M., Sanyal A.J.; Kanwal F., et al.; NAFLD Nomenclature consensus group. A multisociety Delphi consensus statement on new fatty liver disease nomenclature. Hepatology. 2023;78(6):1966-86. doi: 10.1097/ HEP.0000000000000520.
11. Raikhelson K.L., Maevskaya M.V., Zharkova M.S. et al. Steatotic Liver Disease: New Nomenclature and Its Localization in the Russian Federation.Russian Journal of Gastroenterology, Hepatology, Coloproctology. 2024;34(2):35-44. doi: 10.22416/1382-4376-2024-961.@@ Райхельсон К.Л., Маевская М.В., Жаркова М.С. и др. Жировая болезнь печени: новая номенклатура и ее адаптация в Российской Федерации. Российский журнал гастроэнтерологии, гепатологии, колопроктологии. 2024. doi: 10.22416/1382-4376-2024-961.
12. Perazzo H, Pacheco AG, Griep RH; Collaborators. Changing from NAFLD through MAFLD to MASLD: Similar prevalence and risk factors in a large Brazilian cohort. J Hepatol. 2024;80(2): e72-e74. doi: 10.1016/j.jhep.2023.08.025.
13. Hagström H, Vessby J, Ekstedt M, Shang Y. 99% of patients with NAFLD meet MASLD criteria and natural history is therefore identical. J Hepatol. 2024 Feb;80(2): e76-e77. doi: 10.1016/j.jhep.2023.08.026.
14. Ye Q., Zou B., Yeo Y.H. et al. Global prevalence, incidence, and outcomes of non-obese or lean non-alcoholic fatty liver disease: a systematic review and meta-analysis. Lancet Gastroenterol Hepatol. 2020;5(8):739-752. doi: 10.1016/S2468-1253(20)30077-7.
15. Tang A., Ng C.H., Phang P.H. et al.Comparative Burden of Metabolic Dysfunction in Lean NAFLD vs Non-lean NAFLD - A Systematic Review and Meta-analysis. Clin Gastroenterol Hepatol. 2023 Jul;21(7):1750-1760.e12. doi: 10.1016/j.cgh.2022.06.029.
16. Tatsumi Y., Nakao Y.M., Masuda I. et al. Risk for metabolic diseases in normal weight individuals with visceral fat accumulation: a cross-sectional study in Japan. BMJ Open. 2017;7(1): e013831. Published 2017 Jan 16. doi: 10.1136/bmjopen-2016-013831.
17. Kim D., Kim W.R. Nonobese Fatty Liver Disease. Clin Gastroenterol Hepatol. 2017 Apr;15(4):474-485. doi: 10.1016/j.cgh.2016.08.028.
18. Liu, C., Li, N., Sheng, D. et al. Increased visceral fat area to skeletal muscle mass ratio is positively associated with the risk of metabolic dysfunction-associated steatotic liver disease in a Chinese population. Lipids Health Dis 23, 104 (2024). doi: 10.1186/s12944-024-02100-5.
19. Chen M, Cao Y, Ji G, Zhang L. Lean nonalcoholic fatty liver disease and sarcopenia. Front Endocrinol (Lausanne). 2023 Jun 23;14:1217249. doi: 10.3389/fendo.2023.1217249.
20. Waist Circumference and Waist-Hip Ratio: Report of a WHO Expert Consultation. 2008. Available at: https://www.who.int/publications/i/item/9789241501491.
21. Lu, YC., Lin, Y.C., Yen, A.MF. et al. Dual-energy X-ray absorptiometry-assessed adipose tissues in metabolically unhealthy normal weight Asians. Sci Rep. 2019:9: 17698. doi: 10.1038/s41598-019-53557-9.
22. Kamel E., McNeill G., Han T. et al. Measurement of abdominal fat by magnetic resonance imaging, dual-energy X-ray absorptiometry and anthropometry in non-obese men and women.Int J Obes. 1999; 23:686-692. doi: 10.1038/sj.ijo.0800904.
23. Hu H.H., Nayak K.S., Goran M.I. Assessment of abdominal adipose tissue and organ fat content by magnetic resonance imaging. Obes Rev. 2011 May;12(5): e504-15. doi: 10.1111/j.1467-789X.2010.00824.x.
24. Tsygankova O.V., Badin A.R., Starichkov A.A., Lozhkina N.G. Non-alcoholic fatty liver disease: a disease of civilization or a syndrome of modern age? RMJ. Medical Review. 2018;(3):23-28. (in Russ.)@@ Цыганкова О.В., Бадин А.Р., Старичков А.А., Ложкина Н.Г. Неалкогольная жировая болезнь печени - болезнь цивилизации или синдром современности? // РМЖ. Медицинское обозрение. 2018. № 3. С. 23-28.
25. Jiang, Y., Wu, L., Zhu, X. et al. Advances in management of metabolic dysfunction-associated steatotic liver disease: from mechanisms to therapeutics. Lipids Health Dis. 2024;23:95. doi: 10.1186/s12944-024-02092-2.
26. Rinella M.E., Neuschwander-Tetri B.A., Siddiqui M.S. et al. AASLD Practice Guidance on the clinical assessment and management of nonalcoholic fatty liver disease. Hepatology. 2023 May 1;77(5):1797-1835. doi: 10.1097/HEP.0000000000000323.
27. Maevskaya M.V., Kotovskaya Y.V., Ivashkin V.T. et al. The National Consensus statement on the management of adult patients with non-alcoholic fatty liver disease and main comorbidities. Terapevticheskii arkhiv. 2022;94(2):216-253. (in Russ.) doi: 10.26442/00403660. 2022.02.201363.@@ Маевская М.В., Котовская Ю.В., Ивашкин В.Т. и др. Национальный Консенсус для врачей по ведению взрослых пациентов с неалкогольной жировой болезнью печени и ее основными коморбидными состояниями // Терапевтический архив. - 2022. - Т. 94. - № 2. - C. 216-253. doi: 10.26442/00403660.2022.02.201363.
28. Younes R., Bugianesi E. NASH in Lean Individuals. Semin Liver Dis. 2019;39(1):86-95. doi: 10.1055/s-0038-1677517.
29. Danpanichkul P., Suparan K., Kim D., Wijarnpreecha K. What Is New in Metabolic Dysfunction-Associated Steatotic Liver Disease in Lean Individuals: From Bench to Bedside. J Clin Med. 2024 Jan 3;13(1):278. doi: 10.3390/jcm13010278.
30. Anstee Q.M., Darlay R., Cockell S. et al. Genome-wide association study of non-alcoholic fatty liver and steatohepatitis in a histologically characterised cohort* J Hepatol. 2020;73(3):505-515. doi: 10.1016/j.jhep.2020.04.003.
31. Liu Y.L., Reeves H.L., Burt A.D. et al. TM6SF2 rs58542926 influences hepatic fibrosis progression in patients with non-alcoholic fatty liver disease. Nat Commun. 2014 Jun 30;5:4309. doi: 10.1038/ncomms5309.
32. Wu N., Li J., Zhang J. et al. Waist circumference mediates the association between rs1260326 in GCKR gene and the odds of lean NAFLD. Sci Rep. 2023;(13):6488. doi: 10.1038/s41598-023-33753-4.
33. Ebrahimi R., Shanaki M., Mohassel Azadi S., Bahiraee A., Radmard A.R., Poustchi H., Emamgholipour S. Low level of adiponectin predicts the development of Nonalcoholic fatty liver disease: is it irrespective to visceral adiposity index, visceral adipose tissue thickness and other obesity indices? Arch Physiol Biochem. 2022 Feb;128(1):24-31. doi: 10.1080/13813455.2019.1661496.
34. Muzurović E., Polyzos S.A., Mikhailidis D.P., Borozan S., Novosel D., Cmiljanić O., Kadić N., Mantzoros C.S. Non-alcoholic Fatty Liver Disease in Children. Curr Vasc Pharmacol. 2023;21(1):4-25. doi: 10.2174/1570161121666221118155136.
35. Straub LG, Scherer PE. Metabolic Messengers: Adiponectin. Nat Metab. 2019 Mar;1(3):334-339. doi: 10.1038/s42255-019-0041-z.
36. Lu C.W., Yang K.C., Chi Y.C., Wu T.Y., Chiang C.H., Chang H.H., Huang K.C., Yang W.S. Adiponectin-leptin ratio for the early detection of lean non-alcoholic fatty liver disease independent of insulin resistance. Ann Med. 2023 Dec;55(1):634-642. doi: 10.1080/07853890.2023.2179106.
37. Duarte S.M.B., Stefano J.T., Miele L. et al. Gut microbiome composition in lean patients with NASH is associated with liver damage independent of caloric intake: A prospective pilot study. Nutr Metab Cardiovasc Dis. 2018 Apr;28(4):369-384. doi: 10.1016/j.numecd.2017.10.014.
38. Chen F., Esmaili S., Rogers G.B. et al. Lean NAFLD: A Distinct Entity Shaped by Differential Metabolic Adaptation. Hepatology. 2020 Apr;71(4):1213-1227. doi: 10.1002/hep.30908.
39. Martínez-Domínguez S.J., García-Mateo S., Gargallo-Puyuelo C.J. et al. Inflammatory Bowel Disease Is an Independent Risk Factor for Metabolic Dysfunction-Associated Steatotic Liver Disease in Lean Individuals. Inflamm Bowel Dis. 2024 Aug 1;30(8):1274-1283. doi: 10.1093/ibd/izad175.
40. Alisi A., Panera N., Agostoni C., Nobili V.Intrauterine growth retardation and nonalcoholic Fatty liver disease in children.Int J Endocrinol. 2011;2011:269853. doi: 10.1155/2011/269853.
41. Nobili V., Alisi A., Panera N., Agostoni C. Low birth weight and catch-up-growth associated with metabolic syndrome: a ten year systematic review. Pediatr Endocrinol Rev. 2008 Dec;6(2):241-7. PMID: 19202511.
42. Meas T. Fetal origins of insulin resistance and the metabolic syndrome: a key role for adipose tissue? Diabetes Metab. 2010;36(1):11-20. doi: 10.1016/j.diabet.2009.09.001.
43. Kim D., Kim W.R. Nonobese Fatty Liver Disease. Clin Gastroenterol Hepatol. 2017 Apr;15(4):474-485. doi: 10.1016/j.cgh.2016.08.028.
44. Bowden Davies K.A., Sprung V.S., Norman J.A. et al. Physical Activity and Sedentary Time: Association with Metabolic Health and Liver Fat. Med Sci Sports Exerc. 2019;51(6):1169-1177. doi: 10.1249/MSS. 0000000000001901.
45. Abid A., Taha O., Nseir W., Farah R., Grosovski M., Assy N. Soft drink consumption is associated with fatty liver disease independent of metabolic syndrome. J Hepatol. 2009 Nov;51(5):918-24. doi: 10.1016/j.jhep.2009.05.033.
46. Alam S., Eslam M., Skm Hasan N. et al. Risk factors of nonalcoholic fatty liver disease in lean body mass population: A systematic review and meta-analysis. JGH Open. 2021;5(11):1236-1249. Published 2021 Oct 4. doi: 10.1002/jgh3.12658.
47. Chen M., Cao Y., Ji G., Zhang L. Lean nonalcoholic fatty liver disease and sarcopenia. Front Endocrinol (Lausanne). 2023 Jun 23;14:1217249. doi: 10.3389/fendo.2023.1217249.
48. Ekstedt M., Hagström H., Nasr P., Fredrikson M., Stål P., Kechagias S., Hultcrantz R. Fibrosis stage is the strongest predictor for disease-specific mortality in NAFLD after up to 33 years of follow-up. Hepatology. 2015 May;61(5):1547-54. doi: 10.1002/hep.27368.
49. Ng C.H., Lim W.H., Hui Lim G.E., Hao Tan D.J., Syn N., Muthiah M.D., Huang D.Q., Loomba R. Mortality Outcomes by Fibrosis Stage in Nonalcoholic Fatty Liver Disease: A Systematic Review and Meta-analysis. Clin Gastroenterol Hepatol. 2023 Apr;21(4):931-939.e5. doi: 10.1016/j.cgh.2022.04.014.
50. Fu C., Wai J.W., Nik Mustapha N.R. et al. Performance of Simple Fibrosis Scores in Nonobese Patients With Nonalcoholic Fatty Liver Disease. Clin Gastroenterol Hepatol. 2020 Nov;18(12):2843-2845.e2. doi: 10.1016/j.cgh.2019.09.027.
51. Berger D., Desai V., Janardhan S. Con: Liver Biopsy Remains the Gold Standard to Evaluate Fibrosis in Patients With Nonalcoholic Fatty Liver Disease. Clin Liver Dis (Hoboken). 2019;13(4):114-116. Published 2019 Apr 30. doi: 10.1002/cld.740.
52. Leung J.C., Loong T.C., Wei J.L. et al. Histological severity and clinical outcomes of nonalcoholic fatty liver disease in nonobese patients. Hepatology. 2017;65(1):54-64. doi: 10.1002/hep.28697.
53. Weinberg E.M., Trinh H.N., Firpi R.J. et al. Lean Americans With Nonalcoholic Fatty Liver Disease Have Lower Rates of Cirrhosis and Comorbid Diseases. Clin Gastroenterol Hepatol. 2021 May;19(5):996-1008.e6. doi: 10.1016/j.cgh.2020.06.066.
54. De A., Mehta M., Singh P., Bhagat N., Mitra S., Das A., Duseja A. Lean Indian patients with non-alcoholic fatty liver disease (NAFLD) have less metabolic risk factors but similar liver disease severity as non-lean patients with NAFLD.Int J Obes (Lond). 2023 Oct;47(10):986-992. doi: 10.1038/s41366-023-01346-w.
55. Wakabayashi S.I., Tamaki N., Kimura T., Umemura T., Kurosaki M., Izumi N. Natural history of lean and non-lean metabolic dysfunction-associated steatotic liver disease. J Gastroenterol. 2024 Jun;59(6):494-503. doi: 10.1007/s00535-024-02093-z.
56. De A., Bhagat N., Mehta M., Taneja S., Duseja A. Metabolic dysfunction-associated steatotic liver disease (MASLD) definition is better than MAFLD criteria for lean patients with NAFLD. J Hepatol. 2024 Feb;80(2): e61-e62. doi: 10.1016/j.jhep.2023.07.031.
57. Hagström H., Nasr P., Ekstedt M., Hammar U., Stål P., Hultcrantz R., Kechagias S. Risk for development of severe liver disease in lean patients with nonalcoholic fatty liver disease: A long-term follow-up study. Hepatol Commun. 2017 Nov 30;2(1):48-57. doi: 10.1002/hep4.1124.
58. Golabi P., Paik J.M., Kumar A. et al. Nonalcoholic fatty liver disease (NAFLD) and associated mortality in individuals with type 2 diabetes, pre-diabetes, metabolically unhealthy, and metabolically healthy individuals in the United States. Metabolism. 2023;146:155642. doi: 10.1016/j.metabol.2023.155642.
59. Dabbah S., Ben Yakov G., Kaufmann M.I., Cohen-Ezra O., Likhter M., Davidov Y., Ben Ari Z. Predictors of advanced liver fibrosis and the performance of fibrosis scores: lean compared to non-lean metabolic dysfunction-associated steatotic liver disease (MASLD) patients. Minerva Gastroenterol (Torino). 2024 Sep;70(3):322-331. doi: 10.23736/S2724-5985.23.03518-0.
60. Ahmed O.T., Gidener T., Mara K.C., Larson J.J., Therneau T.M., Allen A.M. Natural History of Nonalcoholic Fatty Liver Disease With Normal Body Mass Index: A Population-Based Study. Clin Gastroenterol Hepatol. 2022;20(6):1374-1381.e6. doi: 10.1016/j.cgh.2021.07.016.
61. Wijarnpreecha K., Li F., Lundin S.K. et al. Higher mortality among lean patients with non-alcoholic fatty liver disease despite fewer metabolic comorbidities. Aliment Pharmacol Ther. 2023;57(9):1014-1027. doi: 10.1111/apt.17424.
62. Ha J., Yim S.Y., Karagozian R. Mortality and Liver-Related Events in Lean Versus Non-Lean Nonalcoholic Fatty Liver Disease: A Systematic Review and Meta-analysis. Clin Gastroenterol Hepatol. 2023 Sep;21(10): 2496-2507.e5. doi: 10.1016/j.cgh.2022.11.019.
63. Chrysavgis L., Ztriva E., Protopapas A., Tziomalos K., Cholongitas E. Nonalcoholic fatty liver disease in lean subjects: Prognosis, outcomes and management. World J Gastroenterol. 2020 Nov 14;26(42):6514-6528. doi: 10.3748/wjg.v26.i42.6514.
64. Byrne C.D., Targher G. NAFLD: a multisystem disease. J Hepatol. 2015;62(1 Suppl): S47-S64. doi: 10.1016/j.jhep.2014.12.012.
65. Lee H., Lee Y.H., Kim S.U., Kim H.C. Metabolic Dysfunction-Associated Fatty Liver Disease and Incident Cardiovascular Disease Risk: A Nationwide Cohort Study. Clin Gastroenterol Hepatol. 2021 Oct;19(10):2138-2147.e10. doi: 10.1016/j.cgh.2020.12.022.
66. Feng R.N., Du S.S., Wang C. et al. Lean-non-alcoholic fatty liver disease increases risk for metabolic disorders in a normal weight Chinese population. World J Gastroenterol. 2014;20(47):17932-17940. doi: 10.3748/wjg.v20.i47.17932.
67. Golabi P., Paik J., Fukui N., Locklear C.T., de Avilla L., Younossi Z.M. Patients With Lean Nonalcoholic Fatty Liver Disease Are Metabolically Abnormal and Have a Higher Risk for Mortality. Clin Diabetes. 2019;37(1):65-72. doi: 10.2337/cd18-0026.
68. Fracanzani A.L., Petta S., Lombardi R. et al. Liver and Cardiovascular Damage in Patients With Lean Nonalcoholic Fatty Liver Disease, and Association With Visceral Obesity. Clin Gastroenterol Hepatol. 2017 Oct;15(10):1604-1611.e1. doi: 10.1016/j.cgh.2017.04.045.
69. Tang A., Ng C.H., Phang P.H. et al.Comparative Burden of Metabolic Dysfunction in Lean NAFLD vs Non-lean NAFLD - A Systematic Review and Meta-analysis. Clin Gastroenterol Hepatol. 2023 Jul;21(7):1750-1760.e12. doi: 10.1016/j.cgh.2022.06.029.
70. Weinberg E.M., Trinh H.N., Firpi R.J. et al. Lean Americans With Nonalcoholic Fatty Liver Disease Have Lower Rates of Cirrhosis and Comorbid Diseases. Clin Gastroenterol Hepatol. 2021 May;19(5):996-1008.e6. doi: 10.1016/j.cgh.2020.06.066.
71. Lim G.E.H., Tang A., Ng C.H. et al. An Observational Data Meta-analysis on the Differences in Prevalence and Risk Factors Between MAFLD vs NAFLD. Clin Gastroenterol Hepatol. 2023 Mar;21(3):619-629.e7. doi: 10.1016/j.cgh.2021.11.038.
72. Ishido S., Tamaki N., Takahashi Y. et al. Risk of cardiovascular disease in lean patients with nonalcoholic fatty liver disease. BMC Gastroenterol. 2023 Jun 17;23(1):211. doi: 10.1186/s12876-023-02848-7.
73. Ezeani C., Omaliko C., Al-Ajlouni Y.A., Njei B. Mortality, Hepatic Decompensation, and Cardiovascular- and Renal-Related Outcomes in Lean Versus Non-lean Patients Hospitalized With Metabolic Dysfunction-Associated Steatohepatitis (MASH). Cureus. 2024 May 24;16(5): e60968. doi: 10.7759/cureus.60968.
74. Zou B., Yeo Y.H., Nguyen V.H., Cheung R., Ingelsson E., Nguyen M.H. Prevalence, characteristics and mortality outcomes of obese, nonobese and lean NAFLD in the United States, 1999-2016. J Intern Med. 2020 Jul;288(1):139-151. doi: 10.1111/joim.13069.
75. Nso N., Mergen D., Ikram M. et al. Cardiovascular morbidity and mortality in lean vs. non-lean MASLD: A comprehensive meta-analysis. Curr Probl Cardiol. 2024 Jun;49(6):102569. doi: 10.1016/j.cpcardiol.2024.102569.
76. Younossi Z.M., Corey K.E., Lim J.K. AGA Clinical Practice Update on Lifestyle Modification Using Diet and Exercise to Achieve Weight Loss in the Management of Nonalcoholic Fatty Liver Disease: Expert Review. Gastroenterology. 2021 Feb;160(3):912-918. doi: 10.1053/j.gastro.2020.11.051.
77. Marchesini G., Petta S., Dalle Grave R. Diet, weight loss, and liver health in nonalcoholic fatty liver disease: Pathophysiology, evidence, and practice. Hepatology. 2016;63(6):2032-2043. doi: 10.1002/hep.28392.
78. Vilar-Gomez E., Martinez-Perez Y., Calzadilla-Bertot L. et al. Weight Loss Through Lifestyle Modification Significantly Reduces Features of Nonalcoholic Steatohepatitis. Gastroenterology. 2015 Aug;149(2):367-78.e5; quiz e14-5. doi: 10.1053/j.gastro.2015.04.005.
79. Wong V.W., Wong G.L., Chan R.S. et al. Beneficial effects of lifestyle intervention in non-obese patients with non-alcoholic fatty liver disease. J Hepatol. 2018 Dec;69(6):1349-1356. doi: 10.1016/j.jhep.2018.08.011.
80. Sinn D.H., Kang D., Cho S.J., Paik S.W., Guallar E., Cho J., Gwak G.Y. Weight change and resolution of fatty liver in normal weight individuals with nonalcoholic fatty liver disease. Eur J Gastroenterol Hepatol. 2021 Dec 1;33(1S Suppl 1): e529-e534. doi: 10.1097/MEG.0000000000002158.
81. Plauth M., Bernal W., Dasarathy S., Merli M., Plank L.D., Schütz T., Bischoff S.C. ESPEN guideline on clinical nutrition in liver disease. Clin Nutr. 2019 Apr;38(2):485-521. doi: 10.1016/j.clnu.2018.12.022.
82. Keating S.E., Hackett D.A., George J., Johnson N.A. Exercise and non-alcoholic fatty liver disease: a systematic review and meta-analysis. J Hepatol. 2012 Jul;57(1):157-66. doi: 10.1016/j.jhep.2012.02.023.
83. Parry S.A., Hodson L. Managing NAFLD in Type 2 Diabetes: The Effect of Lifestyle Interventions, a Narrative Review. Adv Ther. 2020 Apr;37(4):1381-1406. doi: 10.1007/s12325-020-01281-6.
84. Kaliora A.C., Gioxari A., Kalafati I.P., Diolintzi A., Kokkinos A., Dedoussis G.V. The Effectiveness of Mediterranean Diet in Nonalcoholic Fatty Liver Disease Clinical Course: An Intervention Study. J Med Food. 2019 Jul;22(7):729-740. doi: 10.1089/jmf.2018.0020.
85. Hassani Zadeh S., Mansoori A., Hosseinzadeh M. Relationship between dietary patterns and non-alcoholic fatty liver disease: A systematic review and meta-analysis. J Gastroenterol Hepatol. 2021 Jun;36(6):1470-1478. doi: 10.1111/jgh.15363.
86. Bagheri M., Nouri M., Homayounfar R., Akhlaghi M. Association between adherence to the Mediterranean diet with cardiometabolic risk factors: a cross-sectional study on PERSIAN cohort study in Fasa. Sci Rep. 2023 Sep 8;13(1):14870. doi: 10.1038/s41598-023-41935-3.
87. Zhang S., Gan S., Zhang Q. et al. Ultra-processed food consumption and the risk of non-alcoholic fatty liver disease in the Tianjin Chronic Low-grade Systemic Inflammation and Health Cohort Study.Int J Epidemiol. 2022 Feb 18;51(1):237-249. doi: 10.1093/ije/dyab174.
88. Zelber-Sagi S., Grinshpan L.S., Ivancovsky-Wajcman D., Goldenshluger A., Gepner Y. One size does not fit all; practical, personal tailoring of the diet to NAFLD patients. Liver Int. 2022 Aug;42(8):1731-1750. doi: 10.1111/liv.15335.
89. Ouyang X., Cirillo P., Sautin Y., McCall S., Bruchette J.L., Diehl A.M., Johnson R.J., Abdelmalek M.F. Fructose consumption as a risk factor for non-alcoholic fatty liver disease. J Hepatol. 2008 Jun;48(6):993-9. doi: 10.1016/j.jhep.2008.02.011.
90. Abdelbasset W.K., Tantawy S.A., Kamel D.M., Alqahtani B.A., Soliman G.S. A randomized controlled trial on the effectiveness of 8-week high-intensity interval exercise on intrahepatic triglycerides, visceral lipids, and health-related quality of life in diabetic obese patients with nonalcoholic fatty liver disease. Medicine (Baltimore). 2019 Mar;98(12): e14918. doi: 10.1097/MD.0000000000014918.
91. Kim D., Murag S., Cholankeril G., Cheung A., Harrison S.A., Younossi Z.M., Ahmed A. Physical Activity, Measured Objectively, Is Associated With Lower Mortality in Patients With Nonalcoholic Fatty Liver Disease. Clin Gastroenterol Hepatol. 2021 Jun;19(6):1240-1247.e5. doi: 10.1016/j.cgh.2020.07.023.
92. Chun H.S., Lee M., Lee H.A. et al. Association of Physical Activity With Risk of Liver Fibrosis, Sarcopenia, and Cardiovascular Disease in Nonalcoholic Fatty Liver Disease. Clin Gastroenterol Hepatol. 2023 Feb;21(2):358-369.e12. doi: 10.1016/j.cgh.2021.12.043.
93. Henry A., Paik J.M., Austin P. et al. Vigorous physical activity provides protection against all-cause deaths among adults patients with nonalcoholic fatty liver disease (NAFLD). Aliment Pharmacol Ther. 2023 Mar;57(6):709-722. doi: 10.1111/apt.17308.
94. Lowe D.A., Wu N., Rohdin-Bibby L. et al. Effects of Time-Restricted Eating on Weight Loss and Other Metabolic Parameters in Women and Men With Overweight and Obesity: The TREAT Randomized Clinical Trial. JAMA Intern Med. 2020 Nov 1;180(11):1491-1499. doi: 10.1001/jamainternmed.2020.4153.
95. Chun H.S., Lee M., Lee H.A. et al. Association of Physical Activity With Risk of Liver Fibrosis, Sarcopenia, and Cardiovascular Disease in Nonalcoholic Fatty Liver Disease. Clin Gastroenterol Hepatol. 2023 Feb;21(2):358-369.e12. doi: 10.1016/j.cgh.2021.12.043.
96. Åberg F., Puukka P., Salomaa V. et al. Risks of Light and Moderate Alcohol Use in Fatty Liver Disease: Follow-Up of Population Cohorts. Hepatology. 2020 Mar;71(3):835-848. doi: 10.1002/hep.30864.
97. Jarvis H., O’Keefe H,. Craig D., Stow D., Hanratty B., Anstee Q.M. Does moderate alcohol consumption accelerate the progression of liver disease in NAFLD? A systematic review and narrative synthesis. BMJ Open. 2022 Jan 4;12(1): e049767. doi: 10.1136/bmjopen-2021-049767.
98. Parmar M.P., Kaur M., Bhavanam S. et al. A Systematic Review of the Effects of Smoking on the Cardiovascular System and General Health. Cureus. 2023 Apr 24;15(4): e38073. doi: 10.7759/cureus.38073.
99. Marti-Aguado D., Clemente-Sanchez A., Bataller R. Cigarette smoking and liver diseases. J Hepatol. 2022 Jul;77(1):191-205. doi: 10.1016/j.jhep.2022.01.016.
100. Harrison S.A., Bedossa P., Guy C.D. et al. A Phase 3, Randomized, Controlled Trial of Resmetirom in NASH with Liver Fibrosis. N Engl J Med. 2024;390(6):497-509. doi: 10.1056/NEJMoa2309000.
101. Sanyal A.J., Chalasani N., Kowdley K.V. et al. Pioglitazone, vitamin E, or placebo for nonalcoholic steatohepatitis. N Engl J Med. 2010;362:1675-1685. 76.
102. Cusi K., Orsak B., Bril F. et al. Long-term pioglitazone treatment for patients with nonalcoholic steatohepatitis and prediabetes or type 2 diabetes mellitus: a randomized trial. Ann Intern Med. 2016;165:305-315.
103. Miller E.R. 3rd., Pastor-Barriuso R., Dalal D. et al. Metaanalysis: high-dosage vitamin E supplementation may increase all-cause mortality. Ann Intern Med. 2005;142(1):37-46. doi: 10.7326/0003-4819-142-1-200501040-00110.
104. Abner E.L., Schmitt F.A., Mendiondo M.S. et al. Vitamin E and allcause mortality: a meta-analysis. Curr Aging Sci. 2011;4(2):158-70. doi: 10.2174/1874609811104020158.
105. Huang J., Weinstein S.J., Yu K., Männistö S., Albanes D. Relationship Between Serum Alpha-Tocopherol and Overall and Cause-Specific Mortality. Circ Res. 2019;125(1):29-40. doi: 10.1161/CIRCRESAHA.119.314944.
106. Belfort R., Harrison S.A., Brown K. et al. A placebo-controlled trial of pioglitazone in subjects with nonalcoholic steatohepatitis. N Engl J Med. 2006;355(22):2297-2307. doi: 10.1056/NEJMoa060326.
107. Bril F., Biernacki D.M., Kalavalapalli S. et al. Role of Vitamin E for Nonalcoholic Steatohepatitis in Patients With Type 2 Diabetes: A Randomized Controlled Trial. Diabetes Care. 2019 Aug;42(8):1481-1488. doi: 10.2337/dc19-0167.
108. Tang H., Shi W., Fu S. et al. Pioglitazone and bladder cancer risk: a systematic review and meta-analysis. Cancer Med. 2018;7(4):1070-1080. doi: 10.1002/cam4.1354.
109. Viscoli C.M., Inzucchi S.E., Young L.H., Insogna K.L., Conwit R., Furie K.L., Gorman M., Kelly M.A., Lovejoy A.M., Kernan W.N.; IRIS Trial Investigators. Pioglitazone and Risk for Bone Fracture: Safety Data From a Randomized Clinical Trial. J Clin Endocrinol Metab. 2017 Mar 1;102(3):914-922. doi: 10.1210/jc.2016-3237.
110. Bellentani S. Immunomodulating and anti-apoptotic action of ursodeoxycholic acid: where are we and where should we go?. Eur J Gastroenterol Hepatol. 2005;17(2):137-140. doi: 10.1097/00042737-200502000-00001.
111. Lindor K.D., Kowdley K.V., Heathcote E.J. et al. Ursodeoxycholic acid for treatment of nonalcoholic steatohepatitis: results of a randomized trial. Hepatology. 2004;39(3):770-778. doi: 10.1002/hep.20092.
112. Leuschner U.F., Lindenthal B., Herrmann G. et al. High-dose ursodeoxycholic acid therapy for nonalcoholic steatohepatitis: a double-blind, randomized, placebo-controlled trial. Hepatology. 2010;52(2):472-479. doi: 10.1002/hep.23727.
113. Nadinskaia M., Maevskaya M., Ivashkin V., Kodzoeva Kh., Pirogova I. et al. Ursodeoxycholic acid as a means of preventing atherosclerosis, steatosis and liver fibrosis in patients with nonalcoholic fatty liver disease. World J Gastroenterol. 2021;27(10):959-75. doi: 10.3748/wjg.v27.i10.959.
114. Zhang W., Tang Y., Huang J., Hu H. Efficacy of ursodeoxycholic acid in nonalcoholic fatty liver disease: An updated meta-analysis of randomized controlled trials. Asia Pac J Clin Nutr. 2020;29(4):696-705. doi: 10.6133/apjcn.202012_29(4).0004.
115. Reardon J., Hussaini T., Alsahafi M., Azalgara V.M., Erb S.R., Partovi N., Yoshida E.M. Ursodeoxycholic Acid in Treatment of Non-cholestatic Liver Diseases: A Systematic Review. J Clin Transl Hepatol. 2016 Sep 28;4(3):192-205. doi: 10.14218/JCTH.2016.00023.
116. Brown E., Heerspink H.J.L., Cuthbertson D.J., Wilding J.P.H. SGLT2 inhibitors and GLP-1 receptor agonists: established and emerging indications. Lancet. 2021;398(10296):262-276. doi: 10.1016/S0140-6736(21)00536-5.
117. Newsome P.N., Buchholtz K., Cusi K. et al. A Placebo-Controlled Trial of Subcutaneous Semaglutide in Nonalcoholic Steatohepatitis. N Engl J Med. 2021;384(12):1113-1124. doi: 10.1056/NEJMoa2028395.
118. Latva-Rasku A., Honka M.J., Kullberg J. et al. The SGLT2 Inhibitor Dapagliflozin Reduces Liver Fat but Does Not Affect Tissue Insulin Sensitivity: A Randomized, Double-Blind, Placebo-Controlled Study With 8-Week Treatment in Type 2 Diabetes Patients. Diabetes Care. 2019;42(5):931-937. doi: 10.2337/dc18-1569.
119. Harrison S.A., Manghi F.P., Smith W.B. et al. Licogliflozin for nonalcoholic steatohepatitis: a randomized, double-blind, placebo-controlled, phase 2a study. Nat Med. 2022;28(7):1432-1438. doi: 10.1038/s41591-022-01861-9.
120. Saponaro F., Sestito S., Runfola M., Rapposelli S., Chiellini G. Selective Thyroid Hormone Receptor-Beta (TRβ) Agonists: New Perspectives for the Treatment of Metabolic and Neurodegenerative Disorders. Front Med (Lausanne). 2020;7:331. Published 2020 Jul 9. doi: 10.3389/fmed.2020.00331.
Review
For citations:
Zabotina E.E., Khabarova Yu.A., Stukova N.Yu. Metabolic dysfunction associated steatotic liver disease in lean patients. Diagnostic and treatment challenges. Experimental and Clinical Gastroenterology. 2024;(9):96-109. (In Russ.) https://doi.org/10.31146/1682-8658-ecg-229-9-96-109