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Метаболически ассоциированная стеатотическая болезнь печени у пациентов с предиабетом и сахарным диабетом 2-го типа - Журнал Терапевтический архив №8 Вопросы лечения 2025
Метаболически ассоциированная стеатотическая болезнь печени у пациентов с предиабетом и сахарным диабетом 2-го типа
Сасунова А.Н., Гончаров А.А., Морозов С.В., Пилипенко В.И., Исаков В.А. Метаболически ассоциированная стеатотическая болезнь печени у пациентов с предиабетом и сахарным диабетом 2-го типа. Терапевтический архив. 2025;97(8):689–695. DOI: 10.26442/00403660.2025.08.203339
© ООО «КОНСИЛИУМ МЕДИКУМ», 2025 г.
© ООО «КОНСИЛИУМ МЕДИКУМ», 2025 г.
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Аннотация
Цель. Выявить распространенность различных степеней стеатоза и стадий фиброза печени (ФбП) при метаболически ассоциированной стеатотической болезни печени (МАСБП) в связи с наличием нарушений углеводного обмена, таких как предиабет и сахарный диабет 2-го типа (СД 2).
Материалы и методы. Проведен ретроспективный анализ базы данных, включающей 4101 пациента. Степени стеатоза и стадии ФбП оценивали с помощью вибрационно-контролируемой транзиторной эластографии печени с оценкой контролируемого параметра угасания ультразвукового сигнала. В зависимости от наличия и типа нарушений углеводного обмена пациенты с МАCБП распределены в группы: без предиабета и СД 2 (группа 1), с предиабетом (группа 2) и с СД 2 (группа 3).
Результаты. Доля пациентов с тяжелым стеатозом (степени S3) оказалась ниже в группе 1 (61,9%), в то время как между группами 2 и 3 различий по этому показателю не выявлено (74,3% против 76,7%; p=0,5). Доля пациентов с умеренным или тяжелым ФбП (стадии F2–F4) ниже в группе 1 (24,1%), с достоверными отличиями также между группами 2 и 3 (34,0% против 45,4%; p=0,004). Метаболически ассоциированный стеатогепатит выявлен у сопоставимого числа пациентов в группах 2 и 3 (33,9% против 35,4%; p=0,7), но в группе 1 частота его выявления ниже (26,7% против 33,9% и 35,4%; p=0,02 и p<0,001 соответственно).
Заключение. Нарушения углеводного обмена тесно связаны с прогрессирующим стеатозом и ФбП у пациентов с МАCБП. При этом нет отличий в тяжести стеатоза печени в группах больных МАСБП с предиабетом и СД 2, однако при СД 2 распространенность выраженного/тяжелого ФбП наибольшая среди всех исследованных групп пациентов.
Ключевые слова: метаболически ассоциированная стеатотическая болезнь печени, сахарный диабет 2-го типа, нарушение толерантности к глюкозе, нарушение гликемии натощак, фиброз печени, стеатоз печени
Materials and methods. Retrospective database search (4101 records) was performed. Vibration-controlled transient liver elastography with controlled attenuation parameter module was used for the assessment of liver steatosis and fibrosis. Based on the presence of carbohydrate metabolism disorders, subjects with MASLD were allocated to one of the following groups: MASLD without prediabetes or DM (group 1), MASLD with prediabetes (group 2) and MASLD with DM (group 3).
Results. Proportion of patients with severe liver steatosis (S3) was lowest in the group 1 (61.9%), while no difference was found between groups 2 and 3 (74.3% vs 76.7%; p=0.5). Moderate-to-severe liver fibrosis (stages F2–F4) was less widespread in the group 1 (24.1%); significant difference by this parameter was also revealed between groups 2 and 3 (34.0% vs 45.4%; p=0.004). Proportion of patients with metabolic dysfunction-associated steatohepatitis was similar in groups 2 and 3 (33.9% vs 35.4%; p=0.7), but was lower in the group 1 (26.7% vs 33.9% and 35.4%; p=0.02 and p<0.001, respectively).
Conclusion. Carbohydrate metabolism disorders are closely associated with progressive steatosis and liver fibrosis in patients with MASLD. No differences in the severity of liver steatosis was found between groups with prediabetes and T2DM, however, in T2DM, the prevalence of advanced/severe liver fibrosis was highest among all studied groups.
Keywords: metabolic dysfunction-associated steatotic liver disease, diabetes mellitus, impaired glucose tolerance, impaired fasting glucose, liver fibrosis, liver steatosis
Материалы и методы. Проведен ретроспективный анализ базы данных, включающей 4101 пациента. Степени стеатоза и стадии ФбП оценивали с помощью вибрационно-контролируемой транзиторной эластографии печени с оценкой контролируемого параметра угасания ультразвукового сигнала. В зависимости от наличия и типа нарушений углеводного обмена пациенты с МАCБП распределены в группы: без предиабета и СД 2 (группа 1), с предиабетом (группа 2) и с СД 2 (группа 3).
Результаты. Доля пациентов с тяжелым стеатозом (степени S3) оказалась ниже в группе 1 (61,9%), в то время как между группами 2 и 3 различий по этому показателю не выявлено (74,3% против 76,7%; p=0,5). Доля пациентов с умеренным или тяжелым ФбП (стадии F2–F4) ниже в группе 1 (24,1%), с достоверными отличиями также между группами 2 и 3 (34,0% против 45,4%; p=0,004). Метаболически ассоциированный стеатогепатит выявлен у сопоставимого числа пациентов в группах 2 и 3 (33,9% против 35,4%; p=0,7), но в группе 1 частота его выявления ниже (26,7% против 33,9% и 35,4%; p=0,02 и p<0,001 соответственно).
Заключение. Нарушения углеводного обмена тесно связаны с прогрессирующим стеатозом и ФбП у пациентов с МАCБП. При этом нет отличий в тяжести стеатоза печени в группах больных МАСБП с предиабетом и СД 2, однако при СД 2 распространенность выраженного/тяжелого ФбП наибольшая среди всех исследованных групп пациентов.
Ключевые слова: метаболически ассоциированная стеатотическая болезнь печени, сахарный диабет 2-го типа, нарушение толерантности к глюкозе, нарушение гликемии натощак, фиброз печени, стеатоз печени
________________________________________________
Materials and methods. Retrospective database search (4101 records) was performed. Vibration-controlled transient liver elastography with controlled attenuation parameter module was used for the assessment of liver steatosis and fibrosis. Based on the presence of carbohydrate metabolism disorders, subjects with MASLD were allocated to one of the following groups: MASLD without prediabetes or DM (group 1), MASLD with prediabetes (group 2) and MASLD with DM (group 3).
Results. Proportion of patients with severe liver steatosis (S3) was lowest in the group 1 (61.9%), while no difference was found between groups 2 and 3 (74.3% vs 76.7%; p=0.5). Moderate-to-severe liver fibrosis (stages F2–F4) was less widespread in the group 1 (24.1%); significant difference by this parameter was also revealed between groups 2 and 3 (34.0% vs 45.4%; p=0.004). Proportion of patients with metabolic dysfunction-associated steatohepatitis was similar in groups 2 and 3 (33.9% vs 35.4%; p=0.7), but was lower in the group 1 (26.7% vs 33.9% and 35.4%; p=0.02 and p<0.001, respectively).
Conclusion. Carbohydrate metabolism disorders are closely associated with progressive steatosis and liver fibrosis in patients with MASLD. No differences in the severity of liver steatosis was found between groups with prediabetes and T2DM, however, in T2DM, the prevalence of advanced/severe liver fibrosis was highest among all studied groups.
Keywords: metabolic dysfunction-associated steatotic liver disease, diabetes mellitus, impaired glucose tolerance, impaired fasting glucose, liver fibrosis, liver steatosis
Полный текст
Список литературы
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2. Maldonado-Rojas ADC, Zuarth-Vázquez JM, Uribe M, et al. Insulin resistance and Metabolic dysfunction-associated steatotic liver disease (MASLD): Pathways of action of hypoglycemic agents. Ann Hepatol. 2024;29(2):101182. DOI:10.1016/j.aohep.2023.101182
3. Williamson RM, Price JF, Glancy S, et al. Prevalence of and risk factors for hepatic steatosis and non-alcoholic Fatty liver disease in people with type 2 diabetes: the Edinburgh Type 2 Diabetes Study. Diabetes Care. 2011;34(5):1139-44. DOI:10.2337/dc10-2229
4. Ametov AS, Amikishieva KA, Gurieva IV. Management of patients with metabolic-associated fatty liver disease: an endocrinologist's view. Endokrinologiia: novosti, mneniia, obuchenie. 2024;13(2):35-46 (in Russian). DOI:10.33029/2304-9529-2024-13-2-35-46
5. Qi X, Li J, Caussy C, et al. Epidemiology, screening, and co-management of type 2 diabetes mellitus and metabolic dysfunction-associated steatotic liver disease. Hepatology. 2024. DOI:10.1097/HEP.0000000000000913
6. Godoy-Matos AF, Valério CM, Silva Júnior WS, et al. 2024 UPDATE: the Brazilian Diabetes Society position on the management of metabolic dysfunction-associated steatotic liver disease (MASLD) in people with prediabetes or type 2 diabetes. Diabetol Metab Syndr. 2024;16(1):23. DOI:10.1186/s13098-024-01259-2
7. Younossi ZM, Kalligeros M, Henry L. Epidemiology of metabolic dysfunction-associated steatotic liver disease. Clin Mol Hepatol. 2025;31(Suppl):S32-50. DOI:10.3350/cmh.2024.0431
8. Rooney MR, Fang M, Ogurtsova K, et al. Global Prevalence of Prediabetes. Diabetes Care. 2023;46(7):1388-94. DOI:10.2337/dc22-2376
9. Saeedi P, Petersohn I, Salpea P, et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: Results from the International Diabetes Federation Diabetes Atlas, 9th edition. Diabetes Res Clin Pract. 2019;157:107843. DOI:10.1016/j.diabres.2019.107843
10. Yuan F, Fang D, Xu H, et al. One-hour post-load glucose is associated with biopsy-proven metabolic dysfunction-associated steatotic liver disease in obese individuals. Diabetes Metab. 2025;51(1):101588. DOI:10.1016/j.diabet.2024.101588
11. Han E, Lee BW, Kang ES, et al. Mortality in metabolic dysfunction-associated steatotic liver disease: A nationwide population-based cohort study. Metabolism. 2024;152:155789. DOI:10.1016/j.metabol.2024.155789
12. Mezzacappa C. Co-occurring MASLD and Diabetes Is Associated With Increased Incidence of Cardiovascular Events and Mortality. Gastroenterology. 2024;167(4):812-3. DOI:10.1053/j.gastro.2024.04.021
13. Matsubayashi Y, Fujihara K, Khin L, et al. Association of changes in the type 2 diabetes and MASLD/related SLD status with risk of developing cardiovascular disease. Diabetes Obes Metab. 2025;27(4):2035-43. DOI:10.1111/dom.16196
14. Dedov II, Shestakova MV, Mayorov AYu. Diabetes mellitus type 2 in adults. Diabetes mellitus. 2020;23(2S):4-102 (in Russian). DOI:10.14341/DM12507
15. Sasunova AN, Goncharov AA, Gapparova KM, Isakov VA. The relationship between diabetes mellitus and non-alcoholic fatty liver disease: a clinical and instrumental paired study. Terapevticheskii Arkhiv (Ter. Arkh.). 2024;96(8):764-70 (in Russian). DOI:10.26442/00403660.2024.08.202810
16. Karlas T, Petroff D, Sasso M, et al. Individual patient data meta-analysis of controlled attenuation parameter (CAP) technology for assessing steatosis. J Hepatol. 2017;66(5):1022-30. DOI:10.1016/j.jhep.2016.12.022
17. Tsochatzis EA, Gurusamy KS, Ntaoula S, et al. Elastography for the diagnosis of severity of fibrosis in chronic liver disease: a meta-analysis of diagnostic accuracy. J Hepatol. 2011;54(4):650-9. DOI:10.1016/j.jhep.2010.07.033
18. Dedov II, Shestakova MV, Maiorov AIu. Algoritmy spetsializirovannoi meditsinskoi pomoshchi bolnym sakharnym diabetom. Moscow, 2023. Iss. 11 (in Russian). DOI:10.14341/DM13042
19. Chan KE, Ong EYH, Chung CH, et al. Longitudinal Outcomes Associated With Metabolic Dysfunction-Associated Steatotic Liver Disease: A Meta-analysis of 129 Studies. Clin Gastroenterol Hepatol. 2024;22(3):488-98.e14. DOI:10.1016/j.cgh.2023.09.018
20. Cuthbertson DJ, Koskinen J, Brown E, et al. Fatty liver index predicts incident risk of prediabetes, type 2 diabetes and non-alcoholic fatty liver disease (NAFLD). Ann Med. 2021;53(1):1256-64. DOI:10.1080/07853890.2021.1956685
21. Parry SA, Hodson L. Managing NAFLD in Type 2 Diabetes: The Effect of Lifestyle Interventions, a Narrative Review. Adv Ther. 2020;37(4):1381-406. DOI:10.1007/s12325-020-01281-6
22. Shao J, Zhou M, Xie X, Lan Sh . Association between fatty liver disease and risk of microvascular complications in Type-2 diabetes mellitus: A systematic review and meta-analysis. Pak J Med Sci. 2025;41(3):902-9. DOI:10.12669/pjms.41.3.11362
23. Adams LA, Harmsen S, St Sauver JL, et al. Nonalcoholic fatty liver disease increases risk of death among patients with diabetes: a community-based cohort study. Am J Gastroenterol. 2010;105(7):1567-73. DOI:10.1038/ajg.2010.18
24. Kim KS, Hong S, Han K, Park CY. Association of non-alcoholic fatty liver disease with cardiovascular disease and all cause death in patients with type 2 diabetes mellitus: nationwide population based study. BMJ. 2024;384:e076388. DOI:10.1136/bmj-2023-076388
25. Ebert T, Widman L, Stenvinkel P, Hagström H. Increased risk for microvascular outcomes in NAFLD-A nationwide, population-based cohort study. J Intern Med. 2023;294(2):216-27. DOI:10.1111/joim.13673
26. Song QR, Liu SL, Bi YG, et al. Non-alcoholic Fatty Liver Disease Is Associated With Cardiovascular Outcomes in Subjects With Prediabetes and Diabetes: A Prospective Community-Based Cohort Study. Front Cardiovasc Med. 2022;9:889597. DOI:10.3389/fcvm.2022.889597
27. Choi W, Park M, Park S, et al. Combined impact of prediabetes and hepatic steatosis on cardiometabolic outcomes in young adults. Cardiovasc Diabetol. 2024;23(1):422. DOI:10.1186/s12933-024-02516-4
28. Arias-Fernández M, Fresneda S, Abbate M, et al. Fatty Liver Disease in Patients with Prediabetes and Overweight or Obesity. Metabolites. 2023;13(4):531. DOI:10.3390/metabo13040531
29. Ng CH, Chan KE, Chin YH, et al. The effect of diabetes and prediabetes on the prevalence, complications and mortality in nonalcoholic fatty liver disease. Clin Mol Hepatol. 2022;28(3):565-74. DOI:10.3350/cmh.2022.0096
30. Alfadda AA, Alqutub AN, Sherbeeni SM, et al. Predictors of liver fibrosis progression in cohort of type 2 diabetes mellitus patients with MASLD. J Diabetes Complications. 2025;39(2):108910. DOI:10.1016/j.jdiacomp.2024.108910
31. Huang DQ, Noureddin N, Ajmera V, et al. Type 2 diabetes, hepatic decompensation, and hepatocellular carcinoma in patients with non-alcoholic fatty liver disease: an individual participant-level data meta-analysis. Lancet Gastroenterol Hepatol. 2023;8(9):829-36. DOI:10.1016/S2468-1253(23)00157-7
32. Martínez-Sánchez FD, Corredor-Nassar MJ, Feria-Agudelo SM. Factors Associated With Advanced Liver Fibrosis in a Population With Type 2 Diabetes: A Multicentric Study in Mexico City. J Clin Exp Hepatol. 2025;15(4):102536. DOI:10.1016/j.jceh.2025.102536
33. Isaacs SD, Farrelly FV, Brennan PN. Role of anti-diabetic medications in the management of MASLD. Frontline Gastroenterology. 2025;16(3):239-49. DOI:10.1136/flgastro-2024-102856
34. Musso G, Cassader M, Paschetta E, et al. Thiazolidinediones and Advanced Liver Fibrosis in Nonalcoholic Steatohepatitis: A Meta-analysis. JAMA Intern Med. 2017;177(5):633-40. DOI:10.1001/jamainternmed.2016.9607
35. Guo W, Tian W, Lin L, Xu X. Liraglutide or insulin glargine treatments improves hepatic fat in obese patients with type 2 diabetes and nonalcoholic fatty liver disease in twenty-six weeks: A randomized placebo-controlled trial. Diabetes Res Clin Pract. 2020;170:108487. DOI:10.1016/j.diabres.2020.108487
36. Flint A, Andersen G, Hockings P, et al. Randomised clinical trial: semaglutide versus placebo reduced liver steatosis but not liver stiffness in subjects with non-alcoholic fatty liver disease assessed by magnetic resonance imaging. Aliment Pharmacol Ther. 2021;54(9):1150-61. DOI:10.1111/apt.16608
37. Passos PRC, Filho VOC, Noronha MM, et al. Influence of glucagon-like peptide-1 receptor agonists on hepatic events in type 2 diabetes: a systematic review and meta-analysis. J Gastroenterol Hepatol. 2025;40(1):67-77. DOI:10.1111/jgh.16752
38. Wei Q, Xu X, Guo L, et al. Effect of SGLT2 Inhibitors on Type 2 Diabetes Mellitus With Non-Alcoholic Fatty Liver Disease: A Meta-Analysis of Randomized Controlled Trials. Front Endocrinol (Lausanne). 2021;12:635556. DOI:10.3389/fendo.2021.635556
39. Jin Z, Yuan Y, Zheng C, et al. Effects of sodium-glucose co-transporter 2 inhibitors on liver fibrosis in non-alcoholic fatty liver disease patients with type 2 diabetes mellitus: An updated meta-analysis of randomized controlled trials. J Diabetes Complications. 2023;37(8):108558. DOI:10.1016/j.jdiacomp.2023.108558
40. Mantovani A, Petracca G, Beatrice G, et al. Non-alcoholic fatty liver disease and risk of incident diabetes mellitus: an updated meta-analysis of 501 022 adult individuals. Gut. 2021;70(5):962-9. DOI:10.1136/gutjnl-2020-322572
2. Maldonado-Rojas ADC, Zuarth-Vázquez JM, Uribe M, et al. Insulin resistance and Metabolic dysfunction-associated steatotic liver disease (MASLD): Pathways of action of hypoglycemic agents. Ann Hepatol. 2024;29(2):101182. DOI:10.1016/j.aohep.2023.101182
3. Williamson RM, Price JF, Glancy S, et al. Prevalence of and risk factors for hepatic steatosis and non-alcoholic Fatty liver disease in people with type 2 diabetes: the Edinburgh Type 2 Diabetes Study. Diabetes Care. 2011;34(5):1139-44. DOI:10.2337/dc10-2229
4. Аметов А.С., Амикишиева К.А., Гурьева И.В. Ведение пациентов с метаболически ассоциированной жировой болезнью печени: взгляд эндокринолога. Эндокринология: новости, мнения, обучение. 2024;13(2):35-46 [Ametov AS, Amikishieva KA, Gurieva IV. Management of patients with metabolic-associated fatty liver disease: an endocrinologist's view. Endokrinologiia: novosti, mneniia, obuchenie. 2024;13(2):35-46 (in Russian)]. DOI:10.33029/2304-9529-2024-13-2-35-46
5. Qi X, Li J, Caussy C, et al. Epidemiology, screening, and co-management of type 2 diabetes mellitus and metabolic dysfunction-associated steatotic liver disease. Hepatology. 2024. DOI:10.1097/HEP.0000000000000913
6. Godoy-Matos AF, Valério CM, Silva Júnior WS, et al. 2024 UPDATE: the Brazilian Diabetes Society position on the management of metabolic dysfunction-associated steatotic liver disease (MASLD) in people with prediabetes or type 2 diabetes. Diabetol Metab Syndr. 2024;16(1):23. DOI:10.1186/s13098-024-01259-2
7. Younossi ZM, Kalligeros M, Henry L. Epidemiology of metabolic dysfunction-associated steatotic liver disease. Clin Mol Hepatol. 2025;31(Suppl):S32-50. DOI:10.3350/cmh.2024.0431
8. Rooney MR, Fang M, Ogurtsova K, et al. Global Prevalence of Prediabetes. Diabetes Care. 2023;46(7):1388-94. DOI:10.2337/dc22-2376
9. Saeedi P, Petersohn I, Salpea P, et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: Results from the International Diabetes Federation Diabetes Atlas, 9th edition. Diabetes Res Clin Pract. 2019;157:107843. DOI:10.1016/j.diabres.2019.107843
10. Yuan F, Fang D, Xu H, et al. One-hour post-load glucose is associated with biopsy-proven metabolic dysfunction-associated steatotic liver disease in obese individuals. Diabetes Metab. 2025;51(1):101588. DOI:10.1016/j.diabet.2024.101588
11. Han E, Lee BW, Kang ES, et al. Mortality in metabolic dysfunction-associated steatotic liver disease: A nationwide population-based cohort study. Metabolism. 2024;152:155789. DOI:10.1016/j.metabol.2024.155789
12. Mezzacappa C. Co-occurring MASLD and Diabetes Is Associated With Increased Incidence of Cardiovascular Events and Mortality. Gastroenterology. 2024;167(4):812-3. DOI:10.1053/j.gastro.2024.04.021
13. Matsubayashi Y, Fujihara K, Khin L, et al. Association of changes in the type 2 diabetes and MASLD/related SLD status with risk of developing cardiovascular disease. Diabetes Obes Metab. 2025;27(4):2035-43. DOI:10.1111/dom.16196
14. Дедов И.И., Шестакова М.В., Майоров А.Ю., и др. Сахарный диабет 2 типа у взрослых. Сахарный диабет. 2020;23(2S):4-102 [Dedov II, Shestakova MV, Mayorov AYu. Diabetes mellitus type 2 in adults. Diabetes mellitus. 2020;23(2S):4-102 (in Russian)]. DOI:10.14341/DM12507
15. Сасунова А.Н., Гончаров А.А., Гаппарова К.М., Исаков В.А. Взаимосвязь сахарного диабета и неалкогольной жировой болезни печени: клинико-инструментальное парное исследование. Терапевтический архив. 2024;96(8):764-70 [Sasunova AN, Goncharov AA, Gapparova KM, Isakov VA. The relationship between diabetes mellitus and non-alcoholic fatty liver disease: a clinical and instrumental paired study. Terapevticheskii Arkhiv (Ter. Arkh.). 2024;96(8):764-70 (in Russian)]. DOI:10.26442/00403660.2024.08.202810
16. Karlas T, Petroff D, Sasso M, et al. Individual patient data meta-analysis of controlled attenuation parameter (CAP) technology for assessing steatosis. J Hepatol. 2017;66(5):1022-30. DOI:10.1016/j.jhep.2016.12.022
17. Tsochatzis EA, Gurusamy KS, Ntaoula S, et al. Elastography for the diagnosis of severity of fibrosis in chronic liver disease: a meta-analysis of diagnostic accuracy. J Hepatol. 2011;54(4):650-9. DOI:10.1016/j.jhep.2010.07.033
18. Дедов И.И., Шестакова М.В., Майоров А.Ю. Алгоритмы специализированной медицинской помощи больным сахарным диабетом. М., 2023. 11-й выпуск [Dedov II, Shestakova MV, Maiorov AIu. Algoritmy spetsializirovannoi meditsinskoi pomoshchi bolnym sakharnym diabetom. Moscow, 2023. Iss. 11 (in Russian)]. DOI:10.14341/DM13042
19. Chan KE, Ong EYH, Chung CH, et al. Longitudinal Outcomes Associated With Metabolic Dysfunction-Associated Steatotic Liver Disease: A Meta-analysis of 129 Studies. Clin Gastroenterol Hepatol. 2024;22(3):488-98.e14. DOI:10.1016/j.cgh.2023.09.018
20. Cuthbertson DJ, Koskinen J, Brown E, et al. Fatty liver index predicts incident risk of prediabetes, type 2 diabetes and non-alcoholic fatty liver disease (NAFLD). Ann Med. 2021;53(1):1256-64. DOI:10.1080/07853890.2021.1956685
21. Parry SA, Hodson L. Managing NAFLD in Type 2 Diabetes: The Effect of Lifestyle Interventions, a Narrative Review. Adv Ther. 2020;37(4):1381-406. DOI:10.1007/s12325-020-01281-6
22. Shao J, Zhou M, Xie X, Lan Sh . Association between fatty liver disease and risk of microvascular complications in Type-2 diabetes mellitus: A systematic review and meta-analysis. Pak J Med Sci. 2025;41(3):902-9. DOI:10.12669/pjms.41.3.11362
23. Adams LA, Harmsen S, St Sauver JL, et al. Nonalcoholic fatty liver disease increases risk of death among patients with diabetes: a community-based cohort study. Am J Gastroenterol. 2010;105(7):1567-73. DOI:10.1038/ajg.2010.18
24. Kim KS, Hong S, Han K, Park CY. Association of non-alcoholic fatty liver disease with cardiovascular disease and all cause death in patients with type 2 diabetes mellitus: nationwide population based study. BMJ. 2024;384:e076388. DOI:10.1136/bmj-2023-076388
25. Ebert T, Widman L, Stenvinkel P, Hagström H. Increased risk for microvascular outcomes in NAFLD-A nationwide, population-based cohort study. J Intern Med. 2023;294(2):216-27. DOI:10.1111/joim.13673
26. Song QR, Liu SL, Bi YG, et al. Non-alcoholic Fatty Liver Disease Is Associated With Cardiovascular Outcomes in Subjects With Prediabetes and Diabetes: A Prospective Community-Based Cohort Study. Front Cardiovasc Med. 2022;9:889597. DOI:10.3389/fcvm.2022.889597
27. Choi W, Park M, Park S, et al. Combined impact of prediabetes and hepatic steatosis on cardiometabolic outcomes in young adults. Cardiovasc Diabetol. 2024;23(1):422. DOI:10.1186/s12933-024-02516-4
28. Arias-Fernández M, Fresneda S, Abbate M, et al. Fatty Liver Disease in Patients with Prediabetes and Overweight or Obesity. Metabolites. 2023;13(4):531. DOI:10.3390/metabo13040531
29. Ng CH, Chan KE, Chin YH, et al. The effect of diabetes and prediabetes on the prevalence, complications and mortality in nonalcoholic fatty liver disease. Clin Mol Hepatol. 2022;28(3):565-74. DOI:10.3350/cmh.2022.0096
30. Alfadda AA, Alqutub AN, Sherbeeni SM, et al. Predictors of liver fibrosis progression in cohort of type 2 diabetes mellitus patients with MASLD. J Diabetes Complications. 2025;39(2):108910. DOI:10.1016/j.jdiacomp.2024.108910
31. Huang DQ, Noureddin N, Ajmera V, et al. Type 2 diabetes, hepatic decompensation, and hepatocellular carcinoma in patients with non-alcoholic fatty liver disease: an individual participant-level data meta-analysis. Lancet Gastroenterol Hepatol. 2023;8(9):829-36. DOI:10.1016/S2468-1253(23)00157-7
32. Martínez-Sánchez FD, Corredor-Nassar MJ, Feria-Agudelo SM. Factors Associated With Advanced Liver Fibrosis in a Population With Type 2 Diabetes: A Multicentric Study in Mexico City. J Clin Exp Hepatol. 2025;15(4):102536. DOI:10.1016/j.jceh.2025.102536
33. Isaacs SD, Farrelly FV, Brennan PN. Role of anti-diabetic medications in the management of MASLD. Frontline Gastroenterology. 2025;16(3):239-49. DOI:10.1136/flgastro-2024-102856
34. Musso G, Cassader M, Paschetta E, et al. Thiazolidinediones and Advanced Liver Fibrosis in Nonalcoholic Steatohepatitis: A Meta-analysis. JAMA Intern Med. 2017;177(5):633-40. DOI:10.1001/jamainternmed.2016.9607
35. Guo W, Tian W, Lin L, Xu X. Liraglutide or insulin glargine treatments improves hepatic fat in obese patients with type 2 diabetes and nonalcoholic fatty liver disease in twenty-six weeks: A randomized placebo-controlled trial. Diabetes Res Clin Pract. 2020;170:108487. DOI:10.1016/j.diabres.2020.108487
36. Flint A, Andersen G, Hockings P, et al. Randomised clinical trial: semaglutide versus placebo reduced liver steatosis but not liver stiffness in subjects with non-alcoholic fatty liver disease assessed by magnetic resonance imaging. Aliment Pharmacol Ther. 2021;54(9):1150-61. DOI:10.1111/apt.16608
37. Passos PRC, Filho VOC, Noronha MM, et al. Influence of glucagon-like peptide-1 receptor agonists on hepatic events in type 2 diabetes: a systematic review and meta-analysis. J Gastroenterol Hepatol. 2025;40(1):67-77. DOI:10.1111/jgh.16752
38. Wei Q, Xu X, Guo L, et al. Effect of SGLT2 Inhibitors on Type 2 Diabetes Mellitus With Non-Alcoholic Fatty Liver Disease: A Meta-Analysis of Randomized Controlled Trials. Front Endocrinol (Lausanne). 2021;12:635556. DOI:10.3389/fendo.2021.635556
39. Jin Z, Yuan Y, Zheng C, et al. Effects of sodium-glucose co-transporter 2 inhibitors on liver fibrosis in non-alcoholic fatty liver disease patients with type 2 diabetes mellitus: An updated meta-analysis of randomized controlled trials. J Diabetes Complications. 2023;37(8):108558. DOI:10.1016/j.jdiacomp.2023.108558
40. Mantovani A, Petracca G, Beatrice G, et al. Non-alcoholic fatty liver disease and risk of incident diabetes mellitus: an updated meta-analysis of 501 022 adult individuals. Gut. 2021;70(5):962-9. DOI:10.1136/gutjnl-2020-322572
________________________________________________
2. Maldonado-Rojas ADC, Zuarth-Vázquez JM, Uribe M, et al. Insulin resistance and Metabolic dysfunction-associated steatotic liver disease (MASLD): Pathways of action of hypoglycemic agents. Ann Hepatol. 2024;29(2):101182. DOI:10.1016/j.aohep.2023.101182
3. Williamson RM, Price JF, Glancy S, et al. Prevalence of and risk factors for hepatic steatosis and non-alcoholic Fatty liver disease in people with type 2 diabetes: the Edinburgh Type 2 Diabetes Study. Diabetes Care. 2011;34(5):1139-44. DOI:10.2337/dc10-2229
4. Ametov AS, Amikishieva KA, Gurieva IV. Management of patients with metabolic-associated fatty liver disease: an endocrinologist's view. Endokrinologiia: novosti, mneniia, obuchenie. 2024;13(2):35-46 (in Russian). DOI:10.33029/2304-9529-2024-13-2-35-46
5. Qi X, Li J, Caussy C, et al. Epidemiology, screening, and co-management of type 2 diabetes mellitus and metabolic dysfunction-associated steatotic liver disease. Hepatology. 2024. DOI:10.1097/HEP.0000000000000913
6. Godoy-Matos AF, Valério CM, Silva Júnior WS, et al. 2024 UPDATE: the Brazilian Diabetes Society position on the management of metabolic dysfunction-associated steatotic liver disease (MASLD) in people with prediabetes or type 2 diabetes. Diabetol Metab Syndr. 2024;16(1):23. DOI:10.1186/s13098-024-01259-2
7. Younossi ZM, Kalligeros M, Henry L. Epidemiology of metabolic dysfunction-associated steatotic liver disease. Clin Mol Hepatol. 2025;31(Suppl):S32-50. DOI:10.3350/cmh.2024.0431
8. Rooney MR, Fang M, Ogurtsova K, et al. Global Prevalence of Prediabetes. Diabetes Care. 2023;46(7):1388-94. DOI:10.2337/dc22-2376
9. Saeedi P, Petersohn I, Salpea P, et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: Results from the International Diabetes Federation Diabetes Atlas, 9th edition. Diabetes Res Clin Pract. 2019;157:107843. DOI:10.1016/j.diabres.2019.107843
10. Yuan F, Fang D, Xu H, et al. One-hour post-load glucose is associated with biopsy-proven metabolic dysfunction-associated steatotic liver disease in obese individuals. Diabetes Metab. 2025;51(1):101588. DOI:10.1016/j.diabet.2024.101588
11. Han E, Lee BW, Kang ES, et al. Mortality in metabolic dysfunction-associated steatotic liver disease: A nationwide population-based cohort study. Metabolism. 2024;152:155789. DOI:10.1016/j.metabol.2024.155789
12. Mezzacappa C. Co-occurring MASLD and Diabetes Is Associated With Increased Incidence of Cardiovascular Events and Mortality. Gastroenterology. 2024;167(4):812-3. DOI:10.1053/j.gastro.2024.04.021
13. Matsubayashi Y, Fujihara K, Khin L, et al. Association of changes in the type 2 diabetes and MASLD/related SLD status with risk of developing cardiovascular disease. Diabetes Obes Metab. 2025;27(4):2035-43. DOI:10.1111/dom.16196
14. Dedov II, Shestakova MV, Mayorov AYu. Diabetes mellitus type 2 in adults. Diabetes mellitus. 2020;23(2S):4-102 (in Russian). DOI:10.14341/DM12507
15. Sasunova AN, Goncharov AA, Gapparova KM, Isakov VA. The relationship between diabetes mellitus and non-alcoholic fatty liver disease: a clinical and instrumental paired study. Terapevticheskii Arkhiv (Ter. Arkh.). 2024;96(8):764-70 (in Russian). DOI:10.26442/00403660.2024.08.202810
16. Karlas T, Petroff D, Sasso M, et al. Individual patient data meta-analysis of controlled attenuation parameter (CAP) technology for assessing steatosis. J Hepatol. 2017;66(5):1022-30. DOI:10.1016/j.jhep.2016.12.022
17. Tsochatzis EA, Gurusamy KS, Ntaoula S, et al. Elastography for the diagnosis of severity of fibrosis in chronic liver disease: a meta-analysis of diagnostic accuracy. J Hepatol. 2011;54(4):650-9. DOI:10.1016/j.jhep.2010.07.033
18. Dedov II, Shestakova MV, Maiorov AIu. Algoritmy spetsializirovannoi meditsinskoi pomoshchi bolnym sakharnym diabetom. Moscow, 2023. Iss. 11 (in Russian). DOI:10.14341/DM13042
19. Chan KE, Ong EYH, Chung CH, et al. Longitudinal Outcomes Associated With Metabolic Dysfunction-Associated Steatotic Liver Disease: A Meta-analysis of 129 Studies. Clin Gastroenterol Hepatol. 2024;22(3):488-98.e14. DOI:10.1016/j.cgh.2023.09.018
20. Cuthbertson DJ, Koskinen J, Brown E, et al. Fatty liver index predicts incident risk of prediabetes, type 2 diabetes and non-alcoholic fatty liver disease (NAFLD). Ann Med. 2021;53(1):1256-64. DOI:10.1080/07853890.2021.1956685
21. Parry SA, Hodson L. Managing NAFLD in Type 2 Diabetes: The Effect of Lifestyle Interventions, a Narrative Review. Adv Ther. 2020;37(4):1381-406. DOI:10.1007/s12325-020-01281-6
22. Shao J, Zhou M, Xie X, Lan Sh . Association between fatty liver disease and risk of microvascular complications in Type-2 diabetes mellitus: A systematic review and meta-analysis. Pak J Med Sci. 2025;41(3):902-9. DOI:10.12669/pjms.41.3.11362
23. Adams LA, Harmsen S, St Sauver JL, et al. Nonalcoholic fatty liver disease increases risk of death among patients with diabetes: a community-based cohort study. Am J Gastroenterol. 2010;105(7):1567-73. DOI:10.1038/ajg.2010.18
24. Kim KS, Hong S, Han K, Park CY. Association of non-alcoholic fatty liver disease with cardiovascular disease and all cause death in patients with type 2 diabetes mellitus: nationwide population based study. BMJ. 2024;384:e076388. DOI:10.1136/bmj-2023-076388
25. Ebert T, Widman L, Stenvinkel P, Hagström H. Increased risk for microvascular outcomes in NAFLD-A nationwide, population-based cohort study. J Intern Med. 2023;294(2):216-27. DOI:10.1111/joim.13673
26. Song QR, Liu SL, Bi YG, et al. Non-alcoholic Fatty Liver Disease Is Associated With Cardiovascular Outcomes in Subjects With Prediabetes and Diabetes: A Prospective Community-Based Cohort Study. Front Cardiovasc Med. 2022;9:889597. DOI:10.3389/fcvm.2022.889597
27. Choi W, Park M, Park S, et al. Combined impact of prediabetes and hepatic steatosis on cardiometabolic outcomes in young adults. Cardiovasc Diabetol. 2024;23(1):422. DOI:10.1186/s12933-024-02516-4
28. Arias-Fernández M, Fresneda S, Abbate M, et al. Fatty Liver Disease in Patients with Prediabetes and Overweight or Obesity. Metabolites. 2023;13(4):531. DOI:10.3390/metabo13040531
29. Ng CH, Chan KE, Chin YH, et al. The effect of diabetes and prediabetes on the prevalence, complications and mortality in nonalcoholic fatty liver disease. Clin Mol Hepatol. 2022;28(3):565-74. DOI:10.3350/cmh.2022.0096
30. Alfadda AA, Alqutub AN, Sherbeeni SM, et al. Predictors of liver fibrosis progression in cohort of type 2 diabetes mellitus patients with MASLD. J Diabetes Complications. 2025;39(2):108910. DOI:10.1016/j.jdiacomp.2024.108910
31. Huang DQ, Noureddin N, Ajmera V, et al. Type 2 diabetes, hepatic decompensation, and hepatocellular carcinoma in patients with non-alcoholic fatty liver disease: an individual participant-level data meta-analysis. Lancet Gastroenterol Hepatol. 2023;8(9):829-36. DOI:10.1016/S2468-1253(23)00157-7
32. Martínez-Sánchez FD, Corredor-Nassar MJ, Feria-Agudelo SM. Factors Associated With Advanced Liver Fibrosis in a Population With Type 2 Diabetes: A Multicentric Study in Mexico City. J Clin Exp Hepatol. 2025;15(4):102536. DOI:10.1016/j.jceh.2025.102536
33. Isaacs SD, Farrelly FV, Brennan PN. Role of anti-diabetic medications in the management of MASLD. Frontline Gastroenterology. 2025;16(3):239-49. DOI:10.1136/flgastro-2024-102856
34. Musso G, Cassader M, Paschetta E, et al. Thiazolidinediones and Advanced Liver Fibrosis in Nonalcoholic Steatohepatitis: A Meta-analysis. JAMA Intern Med. 2017;177(5):633-40. DOI:10.1001/jamainternmed.2016.9607
35. Guo W, Tian W, Lin L, Xu X. Liraglutide or insulin glargine treatments improves hepatic fat in obese patients with type 2 diabetes and nonalcoholic fatty liver disease in twenty-six weeks: A randomized placebo-controlled trial. Diabetes Res Clin Pract. 2020;170:108487. DOI:10.1016/j.diabres.2020.108487
36. Flint A, Andersen G, Hockings P, et al. Randomised clinical trial: semaglutide versus placebo reduced liver steatosis but not liver stiffness in subjects with non-alcoholic fatty liver disease assessed by magnetic resonance imaging. Aliment Pharmacol Ther. 2021;54(9):1150-61. DOI:10.1111/apt.16608
37. Passos PRC, Filho VOC, Noronha MM, et al. Influence of glucagon-like peptide-1 receptor agonists on hepatic events in type 2 diabetes: a systematic review and meta-analysis. J Gastroenterol Hepatol. 2025;40(1):67-77. DOI:10.1111/jgh.16752
38. Wei Q, Xu X, Guo L, et al. Effect of SGLT2 Inhibitors on Type 2 Diabetes Mellitus With Non-Alcoholic Fatty Liver Disease: A Meta-Analysis of Randomized Controlled Trials. Front Endocrinol (Lausanne). 2021;12:635556. DOI:10.3389/fendo.2021.635556
39. Jin Z, Yuan Y, Zheng C, et al. Effects of sodium-glucose co-transporter 2 inhibitors on liver fibrosis in non-alcoholic fatty liver disease patients with type 2 diabetes mellitus: An updated meta-analysis of randomized controlled trials. J Diabetes Complications. 2023;37(8):108558. DOI:10.1016/j.jdiacomp.2023.108558
40. Mantovani A, Petracca G, Beatrice G, et al. Non-alcoholic fatty liver disease and risk of incident diabetes mellitus: an updated meta-analysis of 501 022 adult individuals. Gut. 2021;70(5):962-9. DOI:10.1136/gutjnl-2020-322572
Авторы
А.Н. Сасунова1, А.А. Гончаров1, С.В. Морозов*1,2, В.И. Пилипенко1, В.А. Исаков1
1ФГБУН «Федеральный исследовательский центр питания, биотехнологии и безопасности пищи», Москва, Россия;
2ФГБОУ ДПО «Российская медицинская академия непрерывного профессионального образования» Минздрава России, Москва, Россия
*morosoffsv@mail.ru
1Federal Research Centre of Nutrition, Biotechnology and Food Safety, Moscow, Russia;
2Russian Medical Academy of Continuous Professional Education, Moscow, Russia
*morosoffsv@mail.ru
1ФГБУН «Федеральный исследовательский центр питания, биотехнологии и безопасности пищи», Москва, Россия;
2ФГБОУ ДПО «Российская медицинская академия непрерывного профессионального образования» Минздрава России, Москва, Россия
*morosoffsv@mail.ru
________________________________________________
1Federal Research Centre of Nutrition, Biotechnology and Food Safety, Moscow, Russia;
2Russian Medical Academy of Continuous Professional Education, Moscow, Russia
*morosoffsv@mail.ru
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