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Research Article

Noninvasive liver fibrosis markers are independently associated with carotid atherosclerosis risk in patients with nonalcoholic fatty liver disease

, , , &
Received 22 Mar 2024, Accepted 02 Jun 2024, Published online: 22 Jun 2024

References

  • Powell EE, Wong VW, Rinella M. Non-alcoholic fatty liver disease. Lancet. 2021;397(10290):2212–2224. doi: 10.1016/S0140-6736(20)32511-3.
  • Liu H, Lu HY. Nonalcoholic fatty liver disease and cardiovascular disease. World J Gastroenterol. 2014;20(26):8407–8415. doi: 10.3748/wjg.v20.i26.8407.
  • Abdelmalek MF. Nonalcoholic fatty liver disease: another leap forward. Nat Rev Gastroenterol Hepatol. 2021;18(2):85–86. doi: 10.1038/s41575-020-00406-0.
  • Stefan N, Kantartzis K, Häring HU. Causes and metabolic consequences of Fatty liver. Endocr Rev. 2008;29(7):939–960. doi: 10.1210/er.2008-0009.
  • Sohn W, Kwon HJ, Chang Y, et al. Liver Fibrosis in Asians With Metabolic Dysfunction-Associated Fatty Liver Disease. Clin Gastroenterol Hepatol. 2022;20(5):e1135–e1148. doi: 10.1016/j.cgh.2021.06.042.
  • Song DS, Chang UI, Kang SG, et al. Noninvasive Serum Fibrosis Markers are Associated with Coronary Artery Calcification in Patients with Nonalcoholic Fatty Liver Disease. Gut Liver. 2019;13(6):658–668. doi: 10.5009/gnl18439.
  • Shao C, Xu L, Lei P, et al. Metabolomics to identify fingerprints of carotid atherosclerosis in nonobese metabolic dysfunction-associated fatty liver disease. J Transl Med. 2023;21(1):12. doi: 10.1186/s12967-022-03760-6.
  • Cleveland ER, Ning H, Vos MB, et al. Low Awareness of Nonalcoholic Fatty Liver Disease in a Population-Based Cohort Sample: the CARDIA Study. J Gen Intern Med. 2019;34(12):2772–2778. doi: 10.1007/s11606-019-05340-9.
  • Rundek T, Gardener H, Della-Morte D, et al. The relationship between carotid intima-media thickness and carotid plaque in the Northern Manhattan Study. Atherosclerosis. 2015;241(2):364–370. doi: 10.1016/j.atherosclerosis.2015.05.027.
  • Shimoda S, Kitamura A, Imano H, et al. Associations of carotid intima-media thickness and plaque heterogeneity with the risks of stroke subtypes and coronary artery disease in the japanese general population: the circulatory risk in communities study. J Am Heart Assoc. 2020;9(19):e017020. doi: 10.1161/JAHA.120.017020.
  • Fracanzani AL, 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;15(10):1604–1611.e1. doi: 10.1016/j.cgh.2017.04.045.
  • Jamalinia M, Zare F, Lankarani KB. Systematic review and meta-analysis: association between liver fibrosis and subclinical atherosclerosis in nonalcoholic fatty liver disease. Aliment Pharmacol Ther. 2023;58(4):384–394. doi: 10.1111/apt.17617.
  • Naimi RM, Hvistendahl M, Nerup N, et al. Effects of glepaglutide, a novel long-acting glucagon-like peptide-2 analogue, on markers of liver status in patients with short bowel syndrome: findings from a randomised phase 2 trial. EBioMedicine. 2019;46:444–451. doi: 10.1016/j.ebiom.2019.07.016.
  • Pirmoazen AM, Khurana A, El Kaffas A, et al. Quantitative ultrasound approaches for diagnosis and monitoring hepatic steatosis in nonalcoholic fatty liver disease. Theranostics. 2020;10(9):4277–4289. doi: 10.7150/thno.40249.
  • Siddiqui MS, Yamada G, Vuppalanchi R, et al. Diagnostic accuracy of noninvasive fibrosis models to detect change in fibrosis stage. Clin Gastroenterol Hepatol. 2019;17(9):1877–1885.e1875. doi: 10.1016/j.cgh.2018.12.031.
  • Ballestri S, Mantovani A, Di Girolamo M, et al. Liver fibrosis in nonalcoholic fatty liver disease patients: noninvasive evaluation and correlation with cardiovascular disease and mortality. Metab Target Organ Damage. 2023;3(1):1. doi: 10.20517/mtod.2022.23.
  • Chalasani N, Younossi Z, Lavine JE, et al. The diagnosis and management of nonalcoholic fatty liver disease: practice guidance from the American Association for the Study of Liver Diseases. Hepatology. 2018;67(1):328–357. doi: 10.1002/hep.29367.
  • Bril F, Ortiz-Lopez C, Lomonaco R, et al. Clinical value of liver ultrasound for the diagnosis of nonalcoholic fatty liver disease in overweight and obese patients. Liver Int. 2015;35(9):2139–2146. doi: 10.1111/liv.12840.
  • Stein JH, Korcarz CE, Hurst RT, et al. Use of carotid ultrasound to identify subclinical vascular disease and evaluate cardiovascular disease risk: a consensus statement from the American Society of Echocardiography Carotid Intima-Media Thickness Task Force. Endorsed by the Society for Vascular Medicine. J Am Soc Echocardiogr. 2008;21(2):93. doi: 10.1016/j.echo.2007.11.011.
  • Sterling RK, Lissen E, Clumeck N, et al. Development of a simple noninvasive index to predict significant fibrosis in patients with HIV/HCV coinfection. Hepatology. 2006;43(6):1317–1325. doi: 10.1002/hep.21178.
  • Wang HW, Peng CY, Lai HC, et al. New noninvasive index for predicting liver fibrosis in Asian patients with chronic viral hepatitis. Sci Rep. 2017;7(1):3259. doi: 10.1038/s41598-017-03589-w.
  • Wai CT, Greenson JK, Fontana RJ, et al. A simple noninvasive index can predict both significant fibrosis and cirrhosis in patients with chronic hepatitis C. Hepatology. 2003;38(2):518–526. doi: 10.1053/jhep.2003.50346.
  • Williams AL, Hoofnagle JH. Ratio of serum aspartate to alanine aminotransferase in chronic hepatitis. Relationship to cirrhosis. Gastroenterology. 1988;95(3):734–739. doi: 10.1016/s0016-5085(88)80022-2.
  • Tseng PL, Wang JH, Hung CH, et al. Comparisons of noninvasive indices based on daily practice parameters for predicting liver cirrhosis in chronic hepatitis B and hepatitis C patients in hospital and community populations. Kaohsiung J Med Sci. 2013;29(7):385–395. doi: 10.1016/j.kjms.2012.11.007.
  • Forns X, Ampurdanès S, Llovet JM, et al. Identification of chronic hepatitis C patients without hepatic fibrosis by a simple predictive model. Hepatology. 2002;36(4 Pt 1):986–992. doi: 10.1053/jhep.2002.36128.
  • Xanthakos SA, Jenkins TM, Kleiner DE, et al. High prevalence of nonalcoholic fatty liver disease in adolescents undergoing bariatric surgery. Gastroenterology. 2015;149(3):623–634.e628. doi: 10.1053/j.gastro.2015.05.039.
  • Sookoian S, Pirola CJ. Non-alcoholic fatty liver disease is strongly associated with carotid atherosclerosis: a systematic review. J Hepatol. 2008;49(4):600–607. doi: 10.1016/j.jhep.2008.06.012.
  • Schwimmer JB, Behling C, Angeles JE, et al. Magnetic resonance elastography measured shear stiffness as a biomarker of fibrosis in pediatric nonalcoholic fatty liver disease. Hepatology. 2017;66(5):1474–1485. doi: 10.1002/hep.29241.
  • Lusis AJ. Atherosclerosis. Nature. 2000;407(6801):233–241. doi: 10.1038/35025203.
  • Dulai PS, Singh S, Patel J, et al. Increased risk of mortality by fibrosis stage in nonalcoholic fatty liver disease: systematic review and meta-analysis. Hepatology. 2017;65(5):1557–1565. doi: 10.1002/hep.29085.
  • Angulo P, Kleiner DE, Dam-Larsen S, et al. Liver fibrosis, but no other histologic features, is associated with long-term outcomes of patients with nonalcoholic fatty liver disease. Gastroenterology. 2015;149(2):389–397.e10. doi: 10.1053/j.gastro.2015.04.043.
  • Taylor RS, Taylor RJ, Bayliss S, et al. Association between fibrosis stage and outcomes of patients with nonalcoholic fatty liver disease: a systematic review and meta-analysis. Gastroenterology. 2020;158(6):1611–1625.e1612. doi: 10.1053/j.gastro.2020.01.043.
  • Brouha SS, Nguyen P, Bettencourt R, et al. Increased severity of liver fat content and liver fibrosis in non-alcoholic fatty liver disease correlate with epicardial fat volume in type 2 diabetes: a prospective study. Eur Radiol. 2018;28(4):1345–1355. doi: 10.1007/s00330-017-5075-6.
  • Kim D, Kim WR, Kim HJ, et al. Association between noninvasive fibrosis markers and mortality among adults with nonalcoholic fatty liver disease in the United States. Hepatology. 2013;57(4):1357–1365. doi: 10.1002/hep.26156.
  • Hagström H, Nasr P, Ekstedt M, et al. Cardiovascular risk factors in non-alcoholic fatty liver disease. Liver Int. 2019;39(1):197–204. doi: 10.1111/liv.13973.
  • Lauridsen BK, Stender S, Kristensen TS, et al. Liver fat content, non-alcoholic fatty liver disease, and ischaemic heart disease: mendelian randomization and meta-analysis of 279 013 individuals. Eur Heart J. 2018;39(5):385–393. doi: 10.1093/eurheartj/ehx662.
  • Martínez-Arranz I, Bruzzone C, Noureddin M, et al. Metabolic subtypes of patients with NAFLD exhibit distinctive cardiovascular risk profiles. Hepatology. 2022;76(4):1121–1134. doi: 10.1002/hep.32427.
  • Fracanzani AL, Burdick L, Raselli S, et al. Carotid artery intima-media thickness in nonalcoholic fatty liver disease. Am J Med. 2008;121(1):72–78. doi: 10.1016/j.amjmed.2007.08.041.
  • Shabbirhussain BV, Singh S, Dixit VK, et al. Carotid intima media as predictor of liver fibrosis in type 2 diabetes mellitus with NAFLD. Diabetes Metab Syndr. 2022;16(7):102560. doi: 10.1016/j.dsx.2022.102560.
  • Bhatia L, Scorletti E, Curzen N, et al. Improvement in non-alcoholic fatty liver disease severity is associated with a reduction in carotid intima-media thickness progression. Atherosclerosis. 2016;246:13–20. doi: 10.1016/j.atherosclerosis.2015.12.028.
  • Sinn DH, Cho SJ, Gu S, et al. Persistent nonalcoholic fatty liver disease increases risk for carotid atherosclerosis. Gastroenterology. 2016;151(3):481–488.e481. doi: 10.1053/j.gastro.2016.06.001.
  • Lonardo A, Nascimbeni F, Mantovani A, et al. Hypertension, diabetes, atherosclerosis and NASH: cause or consequence? J Hepatol. 2018;68(2):335–352. doi: 10.1016/j.jhep.2017.09.021.
  • Chen Y, Xu M, Wang T, et al. Advanced fibrosis associates with atherosclerosis in subjects with nonalcoholic fatty liver disease. Atherosclerosis. 2015;241(1):145–150. doi: 10.1016/j.atherosclerosis.2015.05.002.
  • Arai T, Atsukawa M, Tsubota A, et al. Liver fibrosis is associated with carotid atherosclerosis in patients with liver biopsy-proven nonalcoholic fatty liver disease. Sci Rep. 2021;11(1):15938. doi: 10.1038/s41598-021-95581-8.
  • Ojima S, Kubozono T, Kawasoe S, et al. Fib4 index is a more relevant marker for pulse wave velocity but not for carotid intima-media thickness in a men population. Eur Heart J. 2020;41(Supplement_2):ehaa946.2896. doi: 10.1093/ehjci/ehaa946.2896.
  • Guo YC, Zhou Y, Gao X, et al. Association between nonalcoholic fatty liver disease and carotid artery disease in a community-based Chinese population: a cross-sectional study. Chin Med J (Engl). 2018;131(19):2269–2276. doi: 10.4103/0366-6999.241797.
  • Ciardullo S, Perseghin G. Statin use is associated with lower prevalence of advanced liver fibrosis in patients with type 2 diabetes. Metabolism. 2021;121:154752. doi: 10.1016/j.metabol.2021.154752.
  • Shao C, Ye J, Li F, et al. Early predictors of cardiovascular disease risk in nonalcoholic fatty liver disease: non-obese versus obese patients. Dig Dis Sci. 2020;65(6):1850–1860. doi: 10.1007/s10620-019-05926-7.
  • Kasper P, Martin A, Lang S, et al. NAFLD and cardiovascular diseases: a clinical review. Clin Res Cardiol. 2021;110(7):921–937. doi: 10.1007/s00392-020-01709-7.
  • Cichoż-Lach H, Michalak A. Oxidative stress as a crucial factor in liver diseases. World J Gastroenterol. 2014;20(25):8082–8091. doi: 10.3748/wjg.v20.i25.8082.
  • Podszun MC, Alawad AS, Lingala S, et al. Vitamin E treatment in NAFLD patients demonstrates that oxidative stress drives steatosis through upregulation of de-novo lipogenesis. Redox Biol. 2020;37:101710. doi: 10.1016/j.redox.2020.101710.
  • Hargrove L, Kennedy L, Demieville J, et al. Bile duct ligation-induced biliary hyperplasia, hepatic injury, and fibrosis are reduced in mast cell-deficient KitW-sh mice. Hepatology. 2017;65(6):1991–2004. doi: 10.1002/hep.29079.
  • Hall KC, Bernier SG, Jacobson S, et al. sGC stimulator praliciguat suppresses stellate cell fibrotic transformation and inhibits fibrosis and inflammation in models of NASH. Proc Natl Acad Sci U S A. 2019;116(22):11057–11062. doi: 10.1073/pnas.1821045116.
  • Dikalov SI, Dikalova AE. Crosstalk between mitochondrial hyperacetylation and oxidative stress in vascular dysfunction and hypertension. Antioxid Redox Signal. 2019;31(10):710–721. doi: 10.1089/ars.2018.7632.
  • Saiki P, Yoshihara M, Kawano Y, et al. Anti-inflammatory effects of heliangin from jerusalem artichoke (helianthus tuberosus) leaves might prevent atherosclerosis. Biomolecules. 2022;12(1):91. doi: 10.3390/biom12010091.
  • Lu H, Rateri DL, Feldman DL, et al. Renin inhibition reduces hypercholesterolemia-induced atherosclerosis in mice. J Clin Invest. 2008;118(3):984–993. doi: 10.1172/JCI32970.
  • Nussberger J, Aubert J-F, Bouzourene K, et al. Renin inhibition by aliskiren prevents atherosclerosis progression: comparison with irbesartan, atenolol, and amlodipine. Hypertension. 2008;51(5):1306–1311. doi: 10.1161/HYPERTENSIONAHA.108.110932.
  • Ramadan R, Dhawan SS, Binongo JNG, et al. Effect of angiotensin II type I receptor blockade with valsartan on carotid artery atherosclerosis: a double blind randomized clinical trial comparing valsartan and placebo (EFFERVESCENT). Am Heart J. 2016;174:68–79. doi: 10.1016/j.ahj.2015.12.021.
  • Chen G, Yang JC, Zhang GX, et al. Evaluation of six noninvasive methods for the detection of fibrosis in chinese patients with obesity and nonalcoholic fatty liver disease. Obes Surg. 2022;32(11):3619–3626. doi: 10.1007/s11695-022-06251-1.
  • Sigrist RMS, Liau J, Kaffas AE, et al. Ultrasound elastography: review of techniques and clinical applications. Theranostics. 2017;7(5):1303–1329. doi: 10.7150/thno.18650.
  • Lv T, Li M, Zeng N, et al. Systematic review and meta-analysis on the incidence and prevalence of autoimmune hepatitis in Asian, European, and American population. J Gastroenterol Hepatol. 2019;34(10):1676–1684. doi: 10.1111/jgh.14746.
  • Sandahl TD, Laursen TL, Munk DE, et al. The prevalence of Wilson’s disease: an update. Hepatology. 2020;71(2):722–732. doi: 10.1002/hep.30911.
  • Wang LJ, Zhou Y, Hu YQ, et al. Epidemiological characteristics and prevention strategies of viral hepatitis in Chongwen District of Beijing during 1997-2006. Zhonghua Yu Fang Yi Xue Za Zhi. 2008;42(8):592–595. doi: 10.3321/j.issn:0253-9624.2008.08.012.

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