Взгляд клинициста на преимущества и противоречия новой номенклатуры стеатозной болезни печени

Павлов Ч.С., Теплюк Д.А., Лазебник Л.Б., Аметов А.С., Пашкова Е.Ю., Сороколетов С.М., Успенский Ю.П., Туркина С.В., Пономаренко Е.В., Маслаков А.С. Взгляд клинициста на преимущества и противоречия новой номенклатуры стеатозной болезни печени. Терапевтический архив. 2024;96(4):429–435.
DOI: 10.26442/00403660.2024.04.202747

© ООО «КОНСИЛИУМ МЕДИКУМ», 2024 г.

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Pavlov ChS, Teplyuk DA, Lazebnik LB, Ametov AS, Pashkova EYu, Sorokoletov SM, Uspenskiy YuP, Turkina SV, Ponomarenko EV, Maslakov AS. The clinician's view on the advantages and contradictions of the new nomenclature of steatotic liver disease: A review. Terapevticheskii Arkhiv (Ter. Arkh.). 2024;96(4):429–435.
DOI: 10.26442/00403660.2024.04.202747

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Аннотация

В сентябре 2023 г. после активной дискуссии с экспертами рабочая группа Европейской ассоциации по изучению болезней печени сформулировала предложения по изменению номенклатуры неалкогольной (метаболически-ассоциированной) жировой болезни печени. Цели пересмотра сформулированы как повышение осведомленности медицинских работников и пациентов о причинах и патогенезе заболевания, его течении, лечении и прогнозе. Сформулированы недостатки и противоречия классификации, которая применяется сегодня, такие как: стигматизация, связанная с акцентом на единственном этиологическом факторе заболевания, рассмотрением наиболее существенного фактора прогноза пациентов – кардиометаболического – и недооценкой других факторов прогрессирования заболевания, отсутствие понимания диагностической точности и места применения неинвазивных исследований, невозможность четкой формулировки критериев включения пациентов в клинические исследования и как итог – отсутствие новых, эффективных лекарственных препаратов. Термины «неалкогольная» и «жировая» решено рассматривать как потерявшие свою актуальность, в связи с чем в качестве альтернативы предложено использовать термин «стеатозная болезнь печени (steatotic liver disease – SLD)». Термины «неалкогольная жировая болезнь печени (non-alcoholic fatty liver disease – NAFLD)» или «метаболически-ассоциированная жировая болезнь печени (metabolic associated fatty liver disease – MAFLD)» заменили следующим: «ассоциированная с метаболической дисфункцией стеатозная болезнь печени (metabolic dysfunction-associated steatotic liver disease – MASLD)». При ее сочетании с существенным приемом алкоголя формулируется диагноз из двух составляющих: метаболическая дисфункция (metabolic dysfunction – Met) и алкогольная болезнь печени (alcoholic liver disease – ALD) – MetALD. Основополагающим моментом в патогенезе MASLD считается наличие кардиометаболического фактора. Потребление алкоголя усугубляет воздействие кардиометаболического фактора и увеличивает риск декомпенсации поражения печени. Термин «неалкогольный стеатогепатит (nonalcoholic steatohepatitis – NASH)» заменен на «стеатогепатит, ассоциированный с метаболической дисфункцией (metabolic dysfunction-associated steatohepatitis – MASH)». Принятие новой номенклатуры должно способствовать улучшению понимания патогенеза поражения печени и исходов болезни, а также внести вклад в улучшение качества диагностики и лечения.

Ключевые слова: ассоциированная с метаболической дисфункцией стеатозная болезнь печени, стеатозная болезнь печени, неалкогольная жировая болезнь печени, метаболически-ассоциированная жировая болезнь печени, стеатогепатит, стеатоз

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In September 2023, the European Association for the Study of the Liver (EASL) updated the disease nomenclature for non-alcoholic (metabolically associated) fatty liver disease. The goals of the revision were to increase awareness among health care professionals, civil society and patients about the disease, its course, treatment and outcomes; combating stigma; focusing on the initial etiological factor, including the main (cardiometabolic) risk of disease progression; improved diagnosis based on disease biomarkers; positive impact on the potency to search for new drugs; the ability to provide personalized medical care. The terms “non-alcoholic” and “fatty” were considered stigmatizing, and therefore, it was proposed to use the term steatotic liver disease (SLD) as the name of this nosology. The terms non-alcoholic fatty liver disease (NAFLD) or metabolic associated fatty liver disease (MAFLD) have been replaced by the term metabolic dysfunction-associated steatotic liver disease (MASLD). In the case of being combined with an alcohol factor, a diagnosis in which metabolic dysfunction is combined with alcoholic liver disease is referred to as MetALD. The fundamental principle in the diagnosis of MASLD is the presence of at least one of the cardiometabolic risk factors. Alcohol consumption interacts with cardiometabolic risk factors and increases the risk of SLD decompensation. The term nonalcoholic steatohepatitis (NASH), according to the new nomenclature, has been replaced by the term metabolic dysfunction-associated steatohepatitis (MASH). The adoption of the new nomenclature should help to increase awareness about the disease, its course and outcomes, as well as improve the quality of diagnosis and treatment.

Keywords: metabolic dysfunction-associated steatotic liver disease, steatotic liver disease, non-alcoholic fatty liver disease, metabolic associated fatty liver disease, steatohepatitis, steatosis, non-alcoholic fatty liver disease

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Список литературы

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18. Rao G, Peng X, Li X, et al. Unmasking the enigma of lipid metabolism in metabolic dysfunction-associated steatotic liver disease: from mechanism to the clinic. Front Med (Lausanne). 2023;10:1294267. DOI:10.3389/fmed.2023.1294267
19. Lim S, Kim J-W, Targher G. Links between metabolic syndrome and metabolic dysfunction-associated fatty liver disease. Trends Endocrinol Metab. 2021;32(7):500-14. DOI:10.1016/j.tem.2021.04.008
20. Buzzetti E, Pinzani M, Tsochatzis E. The multiple-hit pathogenesis of non-alcoholic fatty liver disease (NAFLD). Metabolism. 2016;65(8):1038-48. DOI:10.1016/j.metabol.2015.12.012
21. Ratziu V, Bellentani S, Cortez-Pinto H, et al. A position statement on NAFLD/NASH based on the EASL 2009 special conference. J Hepatol. 2010;53(2):372-84. DOI:10.1016/j.jhep.2010.04.008
22. Hutchison A, Tavaglione F, Romeo S, Charlton M. Endocrine aspects of metabolic dysfunction-associated steatotic liver disease (MASLD): Beyond insulin resistance. J Hepatol. 2023;79(6):1524-41. DOI:10.1016/j.jhep.2023.08.030
23. Shin S, Kim J, Lee J, et al. Mitochondrial quality control: its role in metabolic dysfunction-associated steatotic liver disease (MASLD). J Obes Metab Syndr. 2023;32(4):289-302. DOI:10.7570/jomes23054
24. Venkatesan N, Doskey L, Malhi H. The role of endoplasmic reticulum in lipotoxicity during metabolic dysfunction-associated steatotic liver disease (MASLD) pathogenesis. Am J Pathol. 2023;193(12):1887-99. DOI:10.1016/j.ajpath.2023.08.007
25. Vesković M, Šutulović N, Hrnčić D, et al. The interconnection between hepatic insulin resistance and metabolic dysfunction-associated steatotic liver disease – the transition from an adipocentric to liver-centric approach. Curr Issues Mol Biol. 2023;45(11):9084-102. DOI:10.3390/cimb45110570
26. Zhu B, Wei Y, Zhang M, et al. Metabolic dysfunction-associated steatotic liver disease: ferroptosis related mechanisms and potential drugs. Front Pharmacol. 2023;14:1286449. DOI:10.3389/fphar.2023.1286449
27. Ziamanesh F, Mohammadi M, Ebrahimpour S, et al. Unraveling the link between insulin resistance and non-alcoholic fatty liver disease (or metabolic dysfunction-associated steatotic liver disease): A narrative review. J Diabetes Metab Disord. 2023;22(2):1083-94. DOI:10.1007/s40200-023-01293-3
28. Bellentani S, Tiribelli C. Is it time to change NAFLD and NASH nomenclature? Lancet Gastroenterol Hepatol. 2017;2(8):547-8. DOI:10.1016/S2468-1253(17)30146-2
29. Loria P, Lonardo A, Carulli N. Should nonalcoholic fatty liver disease be renamed? Dig Dis. 2005;23(1):72-82. DOI:10.1159/000084728
30. Eslam M, Newsome PN, Sarin SK, et al. A new definition for metabolic dysfunction-associated fatty liver disease: an international expert consensus statement. J Hepatol. 2020;73(1):202-9. DOI:10.1016/j.jhep.2020.03.039
31. Цуканов В.В., Васютин А.В., Тонких Ю.Л. Новые аспекты неалкогольной жировой болезни печени. Доктор.Ру. 2021;20(4):33-9 [Cukanov VV, Vasyutin AV, Tonkih YL. New aspects of non-alcoholic fatty liver disease. Doktor.Ru. 2021;20(4):33-9 (in Russian)]. DOI:10.31550/1727-2378-2021-20-4-33-39
32. De A, Bhagat N, Mehta M, et al. Metabolic dysfunction-associated steatotic liver disease (MASLD) definition is better than MAFLD criteria for lean patients with NAFLD. J Hepatol. 2024;80(2):e61-2. DOI:10.1016/j.jhep.2023.07.031
33. Rinella M, Lazarus J, Ratziu V, et al. A multisociety Delphi consensus statement on new fatty liver disease nomenclature. Hepatology. 2023;78(6):1966-86. DOI:10.1097/HEP.0000000000000520
34. EASL SLD Summit 2023. EASL-The Home of Hepatology. Available at: https://easl.eu/event/easl-sld-summit-2023/abstract-bursaries/ Accessed: 19.12.2023.
35. EASL Congress 2023. EASL-The Home of Hepatology. Available at: https://easl.eu/event/easl-congress-2023/ Accessed: 19.12.2023.
36. AASLD. New MASLD Nomenclature. Available at: https://www.aasld.org/new-masld-nomenclature. Accessed: 19.12.2023.
37. Ciardullo S, Carbone M, Invernizzi P, Perseghin G. Exploring the landscape of steatotic liver disease in the general US population. Liver Int. 2023;43(11):2425-33. DOI:10.1111/liv.15695
38. Li M, Xie W. Are there all-cause mortality differences between metabolic dysfunction-associated steatotic liver disease subtypes? J Hepatol. 2023:S0168-8278(23)04989-9. DOI:10.1016/j.jhep.2023.07.012

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1. Non-alcoholic fatty liver disease in adults. Clinical recommendations. 2022 (in Russian). Available at: https://cr.minzdrav.gov.ru/recomend/748_1 Accessed: 19.12.2023.
2. Backer S, Khanna D. The Lasting Effects of COVID-19 on the Progression of Metabolic Dysfunction-Associated Steatotic Liver Disease (MASLD). Cureus. 2023;15(9):45231. DOI:10.7759/cureus.45231
3. Chan W-K, Chuah K-H, Rajaram B, et al. Metabolic dysfunction-associated steatotic liver disease (MASLD): A state-of-the-art review. J Obes Metab Syndr. 2023;32(3):197-213. DOI:10.7570/jomes23052
4. Eskridge W, Cryer D, Gastaldelli A, Malhi H. Metabolic dysfunction-associated steatotic liver disease and metabolic dysfunction-associated steatohepatitis: The patient and physician perspective. J Clin Med. 2023;12(19):6216. DOI:10.3390/jcm12196216
5. Lai J, Luo L, Feng X, et al. Alterations in circulating bile acids in metabolic dysfunction-associated steatotic liver disease: A systematic review and meta-analysis. Biomolecules. 2023;13(9):1356. DOI:10.3390/biom13091356
6. Mellemkjær A, Kjær M, Grønbæk H, Thomsen K. Management of cardiovascular risk in patients with metabolic dysfunction-associated steatotic liver disease. Eur J Intern Med. 2023;S0953-6205(23)00409-0. DOI:10.1016/j.ejim.2023.11.012
7. Platek A, Szymanska A. Metabolic dysfunction-associated steatotic liver disease as a cardiovascular risk factor. Clin Exp Hepatol. 2023;9(3):187-92. DOI:10.5114/ceh.2023.130744
8. Yanai H, Adachi H, Hakoshima M, et al. Metabolic-dysfunction-associated steatotic liver disease – its pathophysiology, association with atherosclerosis and cardiovascular disease, and treatments. Int J Mol Sci. 2023;24(20):15473. DOI:10.3390/ijms242015473
9. Chan K, Ong E, Chung C, 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
10. Takahashi Y, Dungubat E, Kusano H, Fukusato T. Pathology and pathogenesis of metabolic dysfunction-associated steatotic liver disease-associated hepatic tumors. Biomedicines. 2023;11(10):2761. DOI:10.3390/biomedicines11102761
11. Krolevec TS, Livzan MA. Metabolic-associated fatty liver disease (NAFLD) as a cancer risk factor. Experimental and Clinical Gastroenterology. 2023;3:120-7 (in Russian). DOI:10.31146/1682-8658-ecg-211-3-120-127
12. Meroni M, Longo M, Paolini E, Dongiovanni P. A narrative review about cognitive impairment in metabolic Dysfunction-Associated liver disease (MASLD): Another matter to face through a holistic approach. J Adv Res. 2024:S2090-1232(24)00069-9. DOI:10.1016/j.jare.2024.02.007
13. Maev IV, Andreev DN, Kucheryavyy YA. Metabolically associated fatty liver disease – a disease of the 21st century: A review. Consilium Medicum. 2022;24(5):325-32 (in Russian). DOI:10.26442/20751753.2022.5.201532
14. Connor C. Fatty infiltration of the liver and the development of cirrhosis in diabetes and chronic alcoholism. Am J Pathol. 1938;14(3):347-64.9.
15. Ludwig J, Viggiano T, McGill D, Oh B. Nonalcoholic steatohepatitis: Mayo Clinic experiences with a hitherto unnamed disease. Mayo Clin Proc. 1980;55(7):434-8.
16. Fouad Y, Waked I, Bollipo S, et al. What’s in a name? Renaming “NAFLD” to “MAFLD”. Liver Int. 2020;40(6):1254-61. DOI:10.1111/liv.14478
17. Kim G-A, Moon J, Kim W. Critical appraisal of metabolic dysfunction-associated steatotic liver disease: Implication of Janus-faced modernity. Clin Mol Hepatol. 2023;29(4):831-43. DOI:10.3350/cmh.2023.0277
18. Rao G, Peng X, Li X, et al. Unmasking the enigma of lipid metabolism in metabolic dysfunction-associated steatotic liver disease: from mechanism to the clinic. Front Med (Lausanne). 2023;10:1294267. DOI:10.3389/fmed.2023.1294267
19. Lim S, Kim J-W, Targher G. Links between metabolic syndrome and metabolic dysfunction-associated fatty liver disease. Trends Endocrinol Metab. 2021;32(7):500-14. DOI:10.1016/j.tem.2021.04.008
20. Buzzetti E, Pinzani M, Tsochatzis E. The multiple-hit pathogenesis of non-alcoholic fatty liver disease (NAFLD). Metabolism. 2016;65(8):1038-48. DOI:10.1016/j.metabol.2015.12.012
21. Ratziu V, Bellentani S, Cortez-Pinto H, et al. A position statement on NAFLD/NASH based on the EASL 2009 special conference. J Hepatol. 2010;53(2):372-84. DOI:10.1016/j.jhep.2010.04.008
22. Hutchison A, Tavaglione F, Romeo S, Charlton M. Endocrine aspects of metabolic dysfunction-associated steatotic liver disease (MASLD): Beyond insulin resistance. J Hepatol. 2023;79(6):1524-41. DOI:10.1016/j.jhep.2023.08.030
23. Shin S, Kim J, Lee J, et al. Mitochondrial quality control: its role in metabolic dysfunction-associated steatotic liver disease (MASLD). J Obes Metab Syndr. 2023;32(4):289-302. DOI:10.7570/jomes23054
24. Venkatesan N, Doskey L, Malhi H. The role of endoplasmic reticulum in lipotoxicity during metabolic dysfunction-associated steatotic liver disease (MASLD) pathogenesis. Am J Pathol. 2023;193(12):1887-99. DOI:10.1016/j.ajpath.2023.08.007
25. Vesković M, Šutulović N, Hrnčić D, et al. The interconnection between hepatic insulin resistance and metabolic dysfunction-associated steatotic liver disease – the transition from an adipocentric to liver-centric approach. Curr Issues Mol Biol. 2023;45(11):9084-102. DOI:10.3390/cimb45110570
26. Zhu B, Wei Y, Zhang M, et al. Metabolic dysfunction-associated steatotic liver disease: ferroptosis related mechanisms and potential drugs. Front Pharmacol. 2023;14:1286449. DOI:10.3389/fphar.2023.1286449
27. Ziamanesh F, Mohammadi M, Ebrahimpour S, et al. Unraveling the link between insulin resistance and non-alcoholic fatty liver disease (or metabolic dysfunction-associated steatotic liver disease): A narrative review. J Diabetes Metab Disord. 2023;22(2):1083-94. DOI:10.1007/s40200-023-01293-3
28. Bellentani S, Tiribelli C. Is it time to change NAFLD and NASH nomenclature? Lancet Gastroenterol Hepatol. 2017;2(8):547-8. DOI:10.1016/S2468-1253(17)30146-2
29. Loria P, Lonardo A, Carulli N. Should nonalcoholic fatty liver disease be renamed? Dig Dis. 2005;23(1):72-82. DOI:10.1159/000084728
30. Eslam M, Newsome PN, Sarin SK, et al. A new definition for metabolic dysfunction-associated fatty liver disease: an international expert consensus statement. J Hepatol. 2020;73(1):202-9. DOI:10.1016/j.jhep.2020.03.039
31. Cukanov VV, Vasyutin AV, Tonkih YL. New aspects of non-alcoholic fatty liver disease. Doktor.Ru. 2021;20(4):33-9 (in Russian). DOI:10.31550/1727-2378-2021-20-4-33-39
32. De A, Bhagat N, Mehta M, et al. Metabolic dysfunction-associated steatotic liver disease (MASLD) definition is better than MAFLD criteria for lean patients with NAFLD. J Hepatol. 2024;80(2):e61-2. DOI:10.1016/j.jhep.2023.07.031
33. Rinella M, Lazarus J, Ratziu V, et al. A multisociety Delphi consensus statement on new fatty liver disease nomenclature. Hepatology. 2023;78(6):1966-86. DOI:10.1097/HEP.0000000000000520
34. EASL SLD Summit 2023. EASL-The Home of Hepatology. Available at: https://easl.eu/event/easl-sld-summit-2023/abstract-bursaries/ Accessed: 19.12.2023.
35. EASL Congress 2023. EASL-The Home of Hepatology. Available at: https://easl.eu/event/easl-congress-2023/ Accessed: 19.12.2023.
36. AASLD. New MASLD Nomenclature. Available at: https://www.aasld.org/new-masld-nomenclature. Accessed: 19.12.2023.
37. Ciardullo S, Carbone M, Invernizzi P, Perseghin G. Exploring the landscape of steatotic liver disease in the general US population. Liver Int. 2023;43(11):2425-33. DOI:10.1111/liv.15695
38. Li M, Xie W. Are there all-cause mortality differences between metabolic dysfunction-associated steatotic liver disease subtypes? J Hepatol. 2023:S0168-8278(23)04989-9. DOI:10.1016/j.jhep.2023.07.012

Авторы

Ч.С. Павлов¹, Д.А. Теплюк¹, Л.Б. Лазебник², А.С. Аметов³, Е.Ю. Пашкова^3,4, С.М. Сороколетов^4,5, Ю.П. Успенский⁶, С.В. Туркина⁷, Е.В. Пономаренко*⁸, А.С. Маслаков⁸

¹ФГАОУ ВО «Первый Московский государственный медицинский университет им. И.М. Сеченова» Минздрава России (Сеченовский Университет), Москва, Россия;
²ФГБОУ ВО «Российский университет медицины» Минздрава России, Москва, Россия;
³ФГБОУ ДПО «Российская медицинская академия непрерывного профессионального образования» Минздрава России, Москва, Россия;
⁴ГБУЗ «Городская клиническая больница им С.П. Боткина» Департамента здравоохранения г. Москвы, Москва, Россия;
⁵Международная академия фундаментального образования, Санкт-Петербург, Россия;
⁶ФГБОУ ВО «Северо-Западный государственный медицинский университет им. И.И. Мечникова» Минздрава России, Санкт-Петербург, Россия;
⁷ФГБОУ ВО «Волгоградский государственный медицинский университет» Минздрава России, Волгоград, Россия;
⁸ООО «Опелла Хелскеа», Москва, Россия
*elizaveta.ponomarenko@sanofi.com

________________________________________________

Chavdar S. Pavlov¹, Daria A. Teplyuk¹, Leonid B. Lazebnik², Aleksandr S. Ametov³, Evgeniia Yu. Pashkova^3,4, Sergey M. Sorokoletov^4,5, Yury P. Uspenskiy⁶, Svetlana V. Turkina⁷, Elizaveta V. Ponomarenko*⁸, Aleksandr S. Maslakov⁸

¹Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia;
²Russian University Of Medicine, Moscow, Russia;
³Russian Medical Academy of Continuous Professional Education, Moscow, Russia;
⁴Botkin City Clinical Hospital, Moscow, Russia;
⁵International Academy of Main Education (IAME), Saint Petersburg, Russia;
⁶Mechnikov North-Western State Medical University, Saint Petersburg, Russia;
⁷Volgograd State Medical University, Volgograd, Russia;
⁸Opella Healthcare LLC, Moscow, Russia
*elizaveta.ponomarenko@sanofi.com

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