High-Density Lipoprotein Subfraction Changes in End-Stage Liver Failure
Yıl 2024,
Cilt: 10 Sayı: 3, 542 - 549, 19.09.2024
Zerrin Barut
Mutay Aydın Aslan
,
Tuğçe Çeker
,
Çağatay Yılmaz
,
Aleyna Öztüzün
Bürke Çırçırlı
Bora Dinç
,
İlker Aycan
Öz
BACKGROUND: This work was designed to ascertain high-density lipoprotein (HDL) subfractions and HDL-related enzyme alterations in end stage liver failure (ESLF).
METHODS: Twenty patients with ESLF and twenty control subjects (liver donors) were chosen for the study. Before the transplant, serum samples from each patient and control were evaluated. Continuous disc polyacrylamide gel electrophoresis was performed to determine HDL subfraction changes and ELISA was carried out to determine serum levels of lecithin–cholesterol acyltransferase (LCAT), apolipoprotein A-1 (ApoA-I) and cholesteryl ester transfer protein (CETP).
RESULTS: Liver failure patients had significantly higher levels of triglycerides (TG) and very low-density lipoprotein (VLDL) compared to healthy donors. Additionally, these patients showed significant increases in levels of aspartate aminotransaminase (AST), alkaline phosphatase (ALP), alanine aminotransaminase (ALT), and blood urea nitrogen (BUN), while albumin was notably lower compared to controls. Even though HDL cholesterol concentrations were not considerably altered between the two groups, ESLF patients had a marked raise in the HDL-large subfraction and a significant decline in the HDL-small subfraction in contrast to controls. Moreover, liver failure patients had considerably lower serum ApoA1 levels compared to healthy controls, but there was no significant difference in LCAT and CETP levels between the two groups.
CONCLUSION: HDL subfraction profile can distinguish between healthy donors and liver failure patients. The results also indicate that levels of ApoA-1, which performs a crucial function in HDL metabolism, are lower in ESLF. This decrease in HDL-small subfractions may be due to impaired anabolism resulting from hepatic failure.
Etik Beyan
This study was reviewed and approved by the Akdeniz University Clinical Research Ethics Committee (08/02/2023 – Reference number: 70904504/67).
Destekleyen Kurum
Akdeniz University Research Foundation
Proje Numarası
#TSA-2018-2785 ve #TTU-2021-5605
Kaynakça
- 1. Zuñiga-Aguilar E, Ramírez-Fernández O. Fibrosis and hepatic regeneration mechanism. Transl Gastroenterol Hepatol 2022; 7:9.
- 2. Jung YK, Yim HJ. Reversal of liver cirrhosis: current evidence and expectations. Korean J Intern Med 2017; 32(2):213-28.
- 3. Huang DQ, Terrault NA, Tacke F, Gluud LL, Arrese M, Bugianesi E, Loomba R. Global epidemiology of cirrhosis - aetiology, trends and predictions. Nat Rev Gastroenterol Hepatol 2023; 20(6):388-98.
- 4. Sarin SK, Kumar M, Eslam M, George J, Al Mahtab M, Akbar SMF, Jia J, Tian Q, Aggarwal R, Muljono DH, Omata M, Ooka Y, Han KH, Lee HW, Jafri W, Butt AS, Chong CH, Lim SG, Pwu RF, Chen DS.Liver diseases in the Asia-Pacific region: a Lancet Gastroenterology & Hepatology Commission. Lancet Gastroenterol Hepatol 2020; 5(2):167-28.
- 5. Zhou WC, Zhang QB, Qiao L. Pathogenesis of liver cirrhosis. World J Gastroenterol 2014; 20(23):7312-24.
- 6. Röhrl C, Stangl H. HDL endocytosis and resecretion. Biochim Biophys Acta 2013; 1831(11):1626-33.
- 7. Arvind A, Osganian SA, Cohen DE, Corey KE. Lipid and Lipoprotein Metabolism in Liver Disease. 2019 Jul 21. In: Feingold KR, Anawalt B, Blackman MR, Boyce A, Chrousos G, Corpas E, de Herder WW, Dhatariya K, Dungan K, Hofland J, Kalra S, Kaltsas G, Kapoor N, Koch C, Kopp P, Korbonits M, Kovacs CS, Kuohung W, Laferrère B, Levy M, McGee EA, McLachlan R, New M, Purnell J, Sahay R, Shah AS, Singer F, Sperling MA, Stratakis CA, Trence DL, Wilson DP, editors., Endotext. MDText.com, Inc.; 2000.
- 8. Wang D, Hiebl V, Xu T, Ladurner A, Atanasov AG, Heiss EH, Dirsch VM. Impact of natural products on the cholesterol transporter ABCA1. J Ethnopharmacol 2020; 249:112444.
- 9. Kent AP, Stylianou IM. Scavenger receptor class B member 1 protein: hepatic regulation and its effects on lipids, reverse cholesterol transport, and atherosclerosis. Hepat Med 2011; 3:29-44.
- 10. Wang Y, van der Tuin S, Tjeerdema N, van Dam AD, Rensen SS, Hendrikx T, Berbée JF, Atanasovska B, Fu J, Hoekstra M, Bekkering S, Riksen NP, Buurman WA, Greve JW, Hofker MH, Shiri-Sverdlov R, Meijer OC, Smit JW, Havekes LM, van Dijk KW, Rensen PC. Plasma cholesteryl ester transfer protein is predominantly derived from Kupffer cells. Hepatology 2015; 62(6):1710-22.
- 11. HDL Function and Size in Patients with On-Target LDL Plasma Levels and a First-Onset ACS. Cordero A, Muñoz-García N, Padró T, Vilahur G, Bertomeu-González V, Escribano D, Flores E, Zuazola P, Badimon L. Int J Mol Sci 2023; 24(6):5391.
- 12. Ahmed HM, Miller M, Nasir K, McEvoy JW, Herrington D, Blumenthal RS, Blaha MJ. Primary Low Level of High-Density Lipoprotein Cholesterol and Risks of Coronary Heart Disease, Cardiovascular Disease, and Death: Results From the Multi-Ethnic Study of Atherosclerosis. Am J Epidemiol 2016; 183(10):875-83.
- 13. Abe RJ, Abe JI, Nguyen MTH, Olmsted-Davis EA, Mamun A, Banerjee P, Cooke JP, Fang L, Pownall H, Le NT. Free Cholesterol Bioavailability and Atherosclerosis. Curr Atheroscler Rep 2022; 24(5):323-36.
- 14. Colombo GI, Bianconi V, Bonomi A, Simonelli S, Amato M, Frigerio B, Ravani A, Vitali C, Sansaro D, Coggi D, Mannarino MR, Savonen KP, Kurl S, Gigante B, Smit AJ, Giral P, Tremoli E, Calabresi L, Veglia F, Pirro M, Baldassarre D, On Behalf Of The Improve Study Group. The Association between HDL-C and Subclinical Atherosclerosis Depends on CETP Plasma Concentration: Insights from the IMPROVE Study. Biomedicines 2021; 9(3):286.
- 15. Calabresi L, Franceschini G. Lecithin:cholesterol acyltransferase, high-density lipoproteins, and atheroprotection in humans. Trends Cardiovasc Med 2010; 20(2):50-53.
- 16. Paul B, Lewinska M, Andersen JB. Lipid alterations in chronic liver disease and liver cancer. JHEP Rep 2022; 4(6):100479.
- 17. Perla FM, Prelati M, Lavorato M, Visicchio D, Anania C. The Role of Lipid and Lipoprotein Metabolism in Non-Alcoholic Fatty Liver Disease. Children (Basel) 2017; 4(6):46.
- 18. Iglesias A, Arranz M, Alvarez JJ, Perales J, Villar J, Herrera E, Lasunción MA. Cholesteryl ester transfer activity in liver disease and cholestasis, and its relation with fatty acid composition of lipoprotein lipids. Clin Chim Acta 1996 ; 248(2):157-74.
- 19. Loria P, Marchesini G, Nascimbeni F, Ballestri S, Maurantonio M, Carubbi F, Ratziu V, Lonardo A. Cardiovascular risk, lipidemic phenotype and steatosis. A comparative analysis of cirrhotic and non-cirrhotic liver disease due to varying etiology. Atherosclerosis 2014; 232(1):99-109.
- 20. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 1972; 18(6):499-502.
- 21. Doğan S, Aslan I, Eryılmaz R, Ensari CO, Bilecik T, Aslan M. Early postoperative changes of HDL subfraction profile and HDL-associated enzymes after laparoscopic sleeve gastrectomy. Obes Surg 2013; 23(12):1973-80.
- 22. Wiesner R, Edwards E, Freeman R, Harper A, Kim R, Kamath P, Kremers W, Lake J, Howard T, Merion RM, Wolfe RA, Krom R; United Network for Organ Sharing Liver Disease Severity Score Committee. Model for end-stage liver disease (MELD) and allocation of donor livers. Gastroenterology 2003; 124(1):91-6.
- 23. Tsoris A, Marlar CA. Use Of The Child Pugh Score In Liver Disease. (2023). In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2023 Jan-. Available from: https://www.ncbi.nlm.nih.gov/books/NBK542308/.
- 24. Singal AK, Kamath PS. Model for End-stage Liver Disease. J Clin Exp Hepatol 2013; 3(1):50-60.
- 25. Patel N, Sharma B, Samant H. Cryptogenic Cirrhosis. (2023). In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2023 Jan-. Available from: https://www.ncbi.nlm.nih.gov/books/NBK534228/.
- 26. Hadizadeh F, Faghihimani E, Adibi P. Nonalcoholic fatty liver disease: Diagnostic biomarkers. World J Gastrointest Pathophysiol 2017; 8(2):11-26.
- 27. Corey KE, Vuppalanchi R, Wilson LA, Cummings OW, Chalasani N; NASH CRN. NASH resolution is associated with improvements in HDL and triglyceride levels but not improvement in LDL or non-HDL-C levels. Aliment Pharmacol Ther 2015; 41(3):301-9.
- 28. Cotter TG, Rinella M. Nonalcoholic Fatty Liver Disease 2020: The State of the Disease. Gastroenterology 2020; 158(7):1851-64.
- 29. Bailey A, Mohiuddin SS. Biochemistry, High Density Lipoprotein. (2022) In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2023 Jan-. Available from: https://www.ncbi.nlm.nih.gov/books/NBK549802/.
- 30. Rosenson RS, Brewer HB Jr, Chapman MJ, Fazio S, Hussain MM, Kontush A, Krauss RM, Otvos JD, Remaley AT, Schaefer EJ. HDL measures, particle heterogeneity, proposed nomenclature, and relation to atherosclerotic cardiovascular events. Clin Chem 2011; 57(3):392-410.
- 31. Deprince A, Haas JT, Staels B. Dysregulated lipid metabolism links NAFLD to cardiovascular disease. Mol Metab 2020; 42:101092.
- 32. Day RC, Harry DS, Owen JS, Foo AY, McIntyre N. Lecithin-cholesterol acyltransferase and the lipoprotein abnormalities of parenchymal liver disease. Clin Sci (Lond) 1979; 56(6):575-83.
- 33. Simon JB, Scheig R. Serum cholesterol esterification in liver disease. N Engl J Med 1970; 283(16):841-6.
- 34. Privitera G, Spadaro L, Marchisello S, Fede G, Purrello F. Abnormalities of Lipoprotein Levels in Liver Cirrhosis: Clinical Relevance. Dig Dis Sci 2018; 63(1):16-26.
- 35. Kadayifci A, Tan V, Ursell PC, Merriman RB, Bass NM. Clinical and pathologic risk factors for atherosclerosis in cirrhosis: a comparison between NASH-related cirrhosis and cirrhosis due to other aetiologies. J Hepatol 2008; 49(4):595-9.
- 36. Berzigotti A, Bonfiglioli A, Muscari A, Bianchi G, Libassi S, Bernardi M, Zoli M. Reduced prevalence of ischemic events and abnormal supraortic flow patterns in patients with liver cirrhosis. Liver Int 2005; 25(2):331-6.
- 37. Sodré FL, Castanho VS, Castilho LN, de Barros-Mazon S, de Faria EC. High-density lipoprotein subfractions in normolipidemic individuals without clinical atherosclerosis lipoprotein subfractions in an adult population. J Clin Lab Anal 2006; 20(3):113-7.
- 38. Masulli M, Patti L, Riccardi G, Vaccaro O, Annuzzi G, Ebbesson SO, Fabsitz RR, Howard WJ, Otvos JD, Roman MJ, Wang H, Weissman NJ, Howard BV, Rivellese AA. Relation among lipoprotein subfractions and carotid atherosclerosis in Alaskan Eskimos (from the GOCADAN Study). Am J Cardiol 2009; 104(11):1516-21.
- 39. Rohatgi A, Westerterp M, von Eckardstein A, Remaley A, Rye KA. HDL in the 21st Century: A Multifunctional Roadmap for Future HDL Research. Circulation 2021; 143(23):2293-2309.
Son Dönem Karaciğer Yetmezliğinde Yüksek Yoğunluklu Lipoprotein Subfraksiyon Değişiklikleri
Yıl 2024,
Cilt: 10 Sayı: 3, 542 - 549, 19.09.2024
Zerrin Barut
Mutay Aydın Aslan
,
Tuğçe Çeker
,
Çağatay Yılmaz
,
Aleyna Öztüzün
Bürke Çırçırlı
Bora Dinç
,
İlker Aycan
Öz
AMAÇ: Bu çalışma, son dönem karaciğer yetmezliğinde (ESLF) yüksek yoğunluklu lipoprotein (HDL) alt fraksiyonlarını ve HDL ile ilişkili enzim değişikliklerini belirlemek için tasarlanmıştır.
YÖNTEMLER: Çalışma için 20 ESLF hastası ve 20 kontrol (karaciğer donörü) kişi seçildi. Nakil öncesinde her hasta ve kontrolden alınan serum örnekleri değerlendirildi. HDL alt fraksiyon değişikliklerini belirlemek için sürekli disk poliakrilamid jel elektroforezi yapıldı ve lesitin-kolesterol asiltransferaz (LCAT), apolipoprotein A-1 (ApoA-I) ve kolesteril ester transfer proteininin (CETP) serum seviyelerini belirlemek için ELISA yapıldı.
BULGULAR: Karaciğer yetmezliği olan hastalarda, sağlıklı donörlerle karşılaştırıldığında anlamlı derecede yüksek trigliserit (TG) ve çok düşük yoğunluklu lipoprotein (VLDL) seviyeleri vardı. Ek olarak, bu hastalarda aspartat aminotransaminaz (AST), alkalin fosfataz (ALP), alanin aminotransaminaz (ALT) ve kan üre nitrojeni (BUN) düzeylerinde önemli artışlar görülürken, albümin kontrollere kıyasla belirgin şekilde düşüktü. HDL kolesterol konsantrasyonları iki grup arasında önemli ölçüde değişmese de, ESLF hastalarında kontrollerin aksine HDL-büyük alt bölümünde belirgin bir artış ve HDL-küçük alt bölümünde önemli bir düşüş vardı. Ayrıca karaciğer yetmezliği olan hastaların serum ApoA1 düzeyleri sağlıklı kontrollere göre oldukça düşüktü ancak LCAT ve CETP düzeyleri açısından iki grup arasında anlamlı bir fark yoktu.
SONUÇ: HDL alt fraksiyon profili, sağlıklı donörler ile karaciğer yetmezliği olan hastaları birbirinden ayırabilir. Sonuçlar ayrıca HDL metabolizmasında çok önemli bir işlevi yerine getiren ApoA-1 düzeylerinin ESLF'de daha düşük olduğunu göstermektedir. HDL-küçük alt fraksiyonlarındaki bu azalma, hepatik yetmezlikten kaynaklanan bozulmuş anabolizmaya bağlı olabilir.
Proje Numarası
#TSA-2018-2785 ve #TTU-2021-5605
Kaynakça
- 1. Zuñiga-Aguilar E, Ramírez-Fernández O. Fibrosis and hepatic regeneration mechanism. Transl Gastroenterol Hepatol 2022; 7:9.
- 2. Jung YK, Yim HJ. Reversal of liver cirrhosis: current evidence and expectations. Korean J Intern Med 2017; 32(2):213-28.
- 3. Huang DQ, Terrault NA, Tacke F, Gluud LL, Arrese M, Bugianesi E, Loomba R. Global epidemiology of cirrhosis - aetiology, trends and predictions. Nat Rev Gastroenterol Hepatol 2023; 20(6):388-98.
- 4. Sarin SK, Kumar M, Eslam M, George J, Al Mahtab M, Akbar SMF, Jia J, Tian Q, Aggarwal R, Muljono DH, Omata M, Ooka Y, Han KH, Lee HW, Jafri W, Butt AS, Chong CH, Lim SG, Pwu RF, Chen DS.Liver diseases in the Asia-Pacific region: a Lancet Gastroenterology & Hepatology Commission. Lancet Gastroenterol Hepatol 2020; 5(2):167-28.
- 5. Zhou WC, Zhang QB, Qiao L. Pathogenesis of liver cirrhosis. World J Gastroenterol 2014; 20(23):7312-24.
- 6. Röhrl C, Stangl H. HDL endocytosis and resecretion. Biochim Biophys Acta 2013; 1831(11):1626-33.
- 7. Arvind A, Osganian SA, Cohen DE, Corey KE. Lipid and Lipoprotein Metabolism in Liver Disease. 2019 Jul 21. In: Feingold KR, Anawalt B, Blackman MR, Boyce A, Chrousos G, Corpas E, de Herder WW, Dhatariya K, Dungan K, Hofland J, Kalra S, Kaltsas G, Kapoor N, Koch C, Kopp P, Korbonits M, Kovacs CS, Kuohung W, Laferrère B, Levy M, McGee EA, McLachlan R, New M, Purnell J, Sahay R, Shah AS, Singer F, Sperling MA, Stratakis CA, Trence DL, Wilson DP, editors., Endotext. MDText.com, Inc.; 2000.
- 8. Wang D, Hiebl V, Xu T, Ladurner A, Atanasov AG, Heiss EH, Dirsch VM. Impact of natural products on the cholesterol transporter ABCA1. J Ethnopharmacol 2020; 249:112444.
- 9. Kent AP, Stylianou IM. Scavenger receptor class B member 1 protein: hepatic regulation and its effects on lipids, reverse cholesterol transport, and atherosclerosis. Hepat Med 2011; 3:29-44.
- 10. Wang Y, van der Tuin S, Tjeerdema N, van Dam AD, Rensen SS, Hendrikx T, Berbée JF, Atanasovska B, Fu J, Hoekstra M, Bekkering S, Riksen NP, Buurman WA, Greve JW, Hofker MH, Shiri-Sverdlov R, Meijer OC, Smit JW, Havekes LM, van Dijk KW, Rensen PC. Plasma cholesteryl ester transfer protein is predominantly derived from Kupffer cells. Hepatology 2015; 62(6):1710-22.
- 11. HDL Function and Size in Patients with On-Target LDL Plasma Levels and a First-Onset ACS. Cordero A, Muñoz-García N, Padró T, Vilahur G, Bertomeu-González V, Escribano D, Flores E, Zuazola P, Badimon L. Int J Mol Sci 2023; 24(6):5391.
- 12. Ahmed HM, Miller M, Nasir K, McEvoy JW, Herrington D, Blumenthal RS, Blaha MJ. Primary Low Level of High-Density Lipoprotein Cholesterol and Risks of Coronary Heart Disease, Cardiovascular Disease, and Death: Results From the Multi-Ethnic Study of Atherosclerosis. Am J Epidemiol 2016; 183(10):875-83.
- 13. Abe RJ, Abe JI, Nguyen MTH, Olmsted-Davis EA, Mamun A, Banerjee P, Cooke JP, Fang L, Pownall H, Le NT. Free Cholesterol Bioavailability and Atherosclerosis. Curr Atheroscler Rep 2022; 24(5):323-36.
- 14. Colombo GI, Bianconi V, Bonomi A, Simonelli S, Amato M, Frigerio B, Ravani A, Vitali C, Sansaro D, Coggi D, Mannarino MR, Savonen KP, Kurl S, Gigante B, Smit AJ, Giral P, Tremoli E, Calabresi L, Veglia F, Pirro M, Baldassarre D, On Behalf Of The Improve Study Group. The Association between HDL-C and Subclinical Atherosclerosis Depends on CETP Plasma Concentration: Insights from the IMPROVE Study. Biomedicines 2021; 9(3):286.
- 15. Calabresi L, Franceschini G. Lecithin:cholesterol acyltransferase, high-density lipoproteins, and atheroprotection in humans. Trends Cardiovasc Med 2010; 20(2):50-53.
- 16. Paul B, Lewinska M, Andersen JB. Lipid alterations in chronic liver disease and liver cancer. JHEP Rep 2022; 4(6):100479.
- 17. Perla FM, Prelati M, Lavorato M, Visicchio D, Anania C. The Role of Lipid and Lipoprotein Metabolism in Non-Alcoholic Fatty Liver Disease. Children (Basel) 2017; 4(6):46.
- 18. Iglesias A, Arranz M, Alvarez JJ, Perales J, Villar J, Herrera E, Lasunción MA. Cholesteryl ester transfer activity in liver disease and cholestasis, and its relation with fatty acid composition of lipoprotein lipids. Clin Chim Acta 1996 ; 248(2):157-74.
- 19. Loria P, Marchesini G, Nascimbeni F, Ballestri S, Maurantonio M, Carubbi F, Ratziu V, Lonardo A. Cardiovascular risk, lipidemic phenotype and steatosis. A comparative analysis of cirrhotic and non-cirrhotic liver disease due to varying etiology. Atherosclerosis 2014; 232(1):99-109.
- 20. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 1972; 18(6):499-502.
- 21. Doğan S, Aslan I, Eryılmaz R, Ensari CO, Bilecik T, Aslan M. Early postoperative changes of HDL subfraction profile and HDL-associated enzymes after laparoscopic sleeve gastrectomy. Obes Surg 2013; 23(12):1973-80.
- 22. Wiesner R, Edwards E, Freeman R, Harper A, Kim R, Kamath P, Kremers W, Lake J, Howard T, Merion RM, Wolfe RA, Krom R; United Network for Organ Sharing Liver Disease Severity Score Committee. Model for end-stage liver disease (MELD) and allocation of donor livers. Gastroenterology 2003; 124(1):91-6.
- 23. Tsoris A, Marlar CA. Use Of The Child Pugh Score In Liver Disease. (2023). In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2023 Jan-. Available from: https://www.ncbi.nlm.nih.gov/books/NBK542308/.
- 24. Singal AK, Kamath PS. Model for End-stage Liver Disease. J Clin Exp Hepatol 2013; 3(1):50-60.
- 25. Patel N, Sharma B, Samant H. Cryptogenic Cirrhosis. (2023). In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2023 Jan-. Available from: https://www.ncbi.nlm.nih.gov/books/NBK534228/.
- 26. Hadizadeh F, Faghihimani E, Adibi P. Nonalcoholic fatty liver disease: Diagnostic biomarkers. World J Gastrointest Pathophysiol 2017; 8(2):11-26.
- 27. Corey KE, Vuppalanchi R, Wilson LA, Cummings OW, Chalasani N; NASH CRN. NASH resolution is associated with improvements in HDL and triglyceride levels but not improvement in LDL or non-HDL-C levels. Aliment Pharmacol Ther 2015; 41(3):301-9.
- 28. Cotter TG, Rinella M. Nonalcoholic Fatty Liver Disease 2020: The State of the Disease. Gastroenterology 2020; 158(7):1851-64.
- 29. Bailey A, Mohiuddin SS. Biochemistry, High Density Lipoprotein. (2022) In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2023 Jan-. Available from: https://www.ncbi.nlm.nih.gov/books/NBK549802/.
- 30. Rosenson RS, Brewer HB Jr, Chapman MJ, Fazio S, Hussain MM, Kontush A, Krauss RM, Otvos JD, Remaley AT, Schaefer EJ. HDL measures, particle heterogeneity, proposed nomenclature, and relation to atherosclerotic cardiovascular events. Clin Chem 2011; 57(3):392-410.
- 31. Deprince A, Haas JT, Staels B. Dysregulated lipid metabolism links NAFLD to cardiovascular disease. Mol Metab 2020; 42:101092.
- 32. Day RC, Harry DS, Owen JS, Foo AY, McIntyre N. Lecithin-cholesterol acyltransferase and the lipoprotein abnormalities of parenchymal liver disease. Clin Sci (Lond) 1979; 56(6):575-83.
- 33. Simon JB, Scheig R. Serum cholesterol esterification in liver disease. N Engl J Med 1970; 283(16):841-6.
- 34. Privitera G, Spadaro L, Marchisello S, Fede G, Purrello F. Abnormalities of Lipoprotein Levels in Liver Cirrhosis: Clinical Relevance. Dig Dis Sci 2018; 63(1):16-26.
- 35. Kadayifci A, Tan V, Ursell PC, Merriman RB, Bass NM. Clinical and pathologic risk factors for atherosclerosis in cirrhosis: a comparison between NASH-related cirrhosis and cirrhosis due to other aetiologies. J Hepatol 2008; 49(4):595-9.
- 36. Berzigotti A, Bonfiglioli A, Muscari A, Bianchi G, Libassi S, Bernardi M, Zoli M. Reduced prevalence of ischemic events and abnormal supraortic flow patterns in patients with liver cirrhosis. Liver Int 2005; 25(2):331-6.
- 37. Sodré FL, Castanho VS, Castilho LN, de Barros-Mazon S, de Faria EC. High-density lipoprotein subfractions in normolipidemic individuals without clinical atherosclerosis lipoprotein subfractions in an adult population. J Clin Lab Anal 2006; 20(3):113-7.
- 38. Masulli M, Patti L, Riccardi G, Vaccaro O, Annuzzi G, Ebbesson SO, Fabsitz RR, Howard WJ, Otvos JD, Roman MJ, Wang H, Weissman NJ, Howard BV, Rivellese AA. Relation among lipoprotein subfractions and carotid atherosclerosis in Alaskan Eskimos (from the GOCADAN Study). Am J Cardiol 2009; 104(11):1516-21.
- 39. Rohatgi A, Westerterp M, von Eckardstein A, Remaley A, Rye KA. HDL in the 21st Century: A Multifunctional Roadmap for Future HDL Research. Circulation 2021; 143(23):2293-2309.