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Published in: Cardiovascular Diabetology 1/2020

01-12-2020 | Insulins | Original investigation

Non-alcoholic steatohepatitis and progression of carotid atherosclerosis in patients with type 2 diabetes: a Korean cohort study

Authors: Hyeok-Hee Lee, Yongin Cho, Young Ju Choi, Byung Wook Huh, Byung-Wan Lee, Eun Seok Kang, Seok Won Park, Bong-Soo Cha, Eun Jig Lee, Yong-ho Lee, Kap Bum Huh

Published in: Cardiovascular Diabetology | Issue 1/2020

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Abstract

Background

There is increasing concern regarding cardiovascular risk in individuals with non-alcoholic fatty liver disease. This study was conducted to evaluate whether hepatic steatosis with or without fibrosis is associated with the progression of carotid atherosclerosis in patients with type 2 diabetes.

Methods

From a longitudinal cohort, we enrolled 1120 patients with type 2 diabetes who underwent repeated carotid artery ultrasonography every 1–2 years. Ultrasonographic findings at baseline and after 6–8 years were compared. Presence of hepatic steatosis was mainly assessed by abdominal ultrasonography; patients with hepatic steatosis were further evaluated for hepatic fibrosis according to fibrosis-4 index. We investigated the association between liver status and atherosclerosis progression.

Results

Of 1120 patients, 636 (56.8%) were classified as having hepatic steatosis at baseline. After 6–8 years, 431 (38.5%) showed atherosclerosis progression. Hepatic steatosis was significantly associated with atherosclerosis progression (adjusted odds ratio[AOR]: 1.370, 95% CI 1.025–1.832; p < 0.05). Among patients with hepatic steatosis, only individuals with fibrosis showed significant association with atherosclerosis progression (AOR: 1.615, 95% CI 1.005–2.598; p < 0.05). The association between hepatic fibrosis and atherosclerosis progression was significant in all metabolic subgroups regardless of age, body mass index, presence of metabolic syndrome, or insulin sensitivity (all p < 0.05). Furthermore, subjects with hepatic steatosis & fibrosis and ≥ 4 components of metabolic syndrome criteria showed markedly increased risk of atherosclerosis progression (AOR: 2.430, 95% CI 1.087–5.458; p < 0.05).

Conclusions

Hepatic steatosis with fibrosis is independently associated with the progression of carotid atherosclerosis in patients with type 2 diabetes.
Literature
1.
go back to reference Loomba R, Sanyal AJ. The global NAFLD epidemic. Nat Rev Gastroenterol Hepatol. 2013;10(11):686–90.PubMedCrossRef Loomba R, Sanyal AJ. The global NAFLD epidemic. Nat Rev Gastroenterol Hepatol. 2013;10(11):686–90.PubMedCrossRef
2.
go back to reference Vanni E, Marengo A, Mezzabotta L, Bugianesi E. Systemic complications of nonalcoholic fatty liver disease: when the liver is not an innocent bystander. Semin Liver Dis. 2015;35(3):236–49.PubMedCrossRef Vanni E, Marengo A, Mezzabotta L, Bugianesi E. Systemic complications of nonalcoholic fatty liver disease: when the liver is not an innocent bystander. Semin Liver Dis. 2015;35(3):236–49.PubMedCrossRef
3.
go back to reference Kim SK, Choi YJ, Huh BW, Park SW, Lee EJ, Cho YW, et al. Nonalcoholic fatty liver disease is associated with increased carotid intima-media thickness only in type 2 diabetic subjects with insulin resistance. J Clin Endocrinol Metab. 2014;99(5):1879–84.PubMedCrossRef Kim SK, Choi YJ, Huh BW, Park SW, Lee EJ, Cho YW, et al. Nonalcoholic fatty liver disease is associated with increased carotid intima-media thickness only in type 2 diabetic subjects with insulin resistance. J Clin Endocrinol Metab. 2014;99(5):1879–84.PubMedCrossRef
4.
go back to reference Kim HC, Kim DJ, Huh KB. Association between nonalcoholic fatty liver disease and carotid intima-media thickness according to the presence of metabolic syndrome. Atherosclerosis. 2009;204(2):521–5.PubMedCrossRef Kim HC, Kim DJ, Huh KB. Association between nonalcoholic fatty liver disease and carotid intima-media thickness according to the presence of metabolic syndrome. Atherosclerosis. 2009;204(2):521–5.PubMedCrossRef
5.
go back to reference Fracanzani AL, Tiraboschi S, Pisano G, Consonni D, Baragetti A, Bertelli C, et al. Progression of carotid vascular damage and cardiovascular events in non-alcoholic fatty liver disease patients compared to the general population during 10 years of follow-up. Atherosclerosis. 2016;246:208–13.PubMedCrossRef Fracanzani AL, Tiraboschi S, Pisano G, Consonni D, Baragetti A, Bertelli C, et al. Progression of carotid vascular damage and cardiovascular events in non-alcoholic fatty liver disease patients compared to the general population during 10 years of follow-up. Atherosclerosis. 2016;246:208–13.PubMedCrossRef
6.
go back to reference Bhatia LS, Curzen NP, Calder PC, Byrne CD. Non-alcoholic fatty liver disease: a new and important cardiovascular risk factor? Eur Heart J. 2012;33(10):1190–200.PubMedCrossRef Bhatia LS, Curzen NP, Calder PC, Byrne CD. Non-alcoholic fatty liver disease: a new and important cardiovascular risk factor? Eur Heart J. 2012;33(10):1190–200.PubMedCrossRef
7.
8.
go back to reference Machado MV, Diehl AM. Pathogenesis of nonalcoholic steatohepatitis. Gastroenterology. 2016;150(8):1769–77.PubMedCrossRef Machado MV, Diehl AM. Pathogenesis of nonalcoholic steatohepatitis. Gastroenterology. 2016;150(8):1769–77.PubMedCrossRef
9.
go back to reference Ekstedt M, Franzen LE, Mathiesen UL, Thorelius L, Holmqvist M, Bodemar G, et al. Long-term follow-up of patients with NAFLD and elevated liver enzymes. Hepatology. 2006;44(4):865–73.PubMedCrossRef Ekstedt M, Franzen LE, Mathiesen UL, Thorelius L, Holmqvist M, Bodemar G, et al. Long-term follow-up of patients with NAFLD and elevated liver enzymes. Hepatology. 2006;44(4):865–73.PubMedCrossRef
10.
go back to reference Schindhelm RK, Dekker JM, Nijpels G, Bouter LM, Stehouwer CD, Heine RJ, et al. Alanine aminotransferase predicts coronary heart disease events: a 10-year follow-up of the Hoorn Study. Atherosclerosis. 2007;191(2):391–6.PubMedCrossRef Schindhelm RK, Dekker JM, Nijpels G, Bouter LM, Stehouwer CD, Heine RJ, et al. Alanine aminotransferase predicts coronary heart disease events: a 10-year follow-up of the Hoorn Study. Atherosclerosis. 2007;191(2):391–6.PubMedCrossRef
11.
go back to reference Targher G, Byrne CD, Lonardo A, Zoppini G, Barbui C. Non-alcoholic fatty liver disease and risk of incident cardiovascular disease: a meta-analysis. J Hepatol. 2016;65(3):589–600.PubMedCrossRef Targher G, Byrne CD, Lonardo A, Zoppini G, Barbui C. Non-alcoholic fatty liver disease and risk of incident cardiovascular disease: a meta-analysis. J Hepatol. 2016;65(3):589–600.PubMedCrossRef
12.
go back to reference Oni E, Budoff MJ, Zeb I, Li D, Veledar E, Polak JF, et al. Nonalcoholic fatty liver disease is associated with arterial distensibility and carotid intima-media thickness: (from the multi-ethnic study of atherosclerosis). Am J Cardiol. 2019;124(4):534–8.PubMedCrossRef Oni E, Budoff MJ, Zeb I, Li D, Veledar E, Polak JF, et al. Nonalcoholic fatty liver disease is associated with arterial distensibility and carotid intima-media thickness: (from the multi-ethnic study of atherosclerosis). Am J Cardiol. 2019;124(4):534–8.PubMedCrossRef
13.
go back to reference Madan SA, John F, Pyrsopoulos N, Pitchumoni CS. Nonalcoholic fatty liver disease and carotid artery atherosclerosis in children and adults: a meta-analysis. Eur J Gastroenterol Hepatol. 2015;27(11):1237–48.PubMedCrossRef Madan SA, John F, Pyrsopoulos N, Pitchumoni CS. Nonalcoholic fatty liver disease and carotid artery atherosclerosis in children and adults: a meta-analysis. Eur J Gastroenterol Hepatol. 2015;27(11):1237–48.PubMedCrossRef
14.
go back to reference Sookoian S, Pirola CJ. Non-alcoholic fatty liver disease is strongly associated with carotid atherosclerosis: a systematic review. J Hepatol. 2008;49(4):600–7.PubMedCrossRef Sookoian S, Pirola CJ. Non-alcoholic fatty liver disease is strongly associated with carotid atherosclerosis: a systematic review. J Hepatol. 2008;49(4):600–7.PubMedCrossRef
15.
go back to reference Sinn DH, Cho SJ, Gu S, Seong D, Kang D, Kim H, et al. Persistent nonalcoholic fatty liver disease increases risk for carotid atherosclerosis. Gastroenterology. 2016;151(3):481–8 e1.CrossRef Sinn DH, Cho SJ, Gu S, Seong D, Kang D, Kim H, et al. Persistent nonalcoholic fatty liver disease increases risk for carotid atherosclerosis. Gastroenterology. 2016;151(3):481–8 e1.CrossRef
16.
go back to reference Chalasani N, Younossi Z, Lavine JE, Charlton M, Cusi K, Rinella M, 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):328–57.PubMedCrossRef Chalasani N, Younossi Z, Lavine JE, Charlton M, Cusi K, Rinella M, 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):328–57.PubMedCrossRef
18.
go back to reference Lee YH, Cho Y, Lee BW, Park CY, Lee DH, Cha BS, et al. Nonalcoholic fatty liver disease in diabetes. Part I: epidemiology and diagnosis. Diabetes Metab J. 2019;43(1):31–45.PubMedCrossRef Lee YH, Cho Y, Lee BW, Park CY, Lee DH, Cha BS, et al. Nonalcoholic fatty liver disease in diabetes. Part I: epidemiology and diagnosis. Diabetes Metab J. 2019;43(1):31–45.PubMedCrossRef
19.
go back to reference Wagenknecht LE, Zaccaro D, Espeland MA, Karter AJ, O’Leary DH, Haffner SM. Diabetes and progression of carotid atherosclerosis: the insulin resistance atherosclerosis study. Arterioscler Thromb Vasc Biol. 2003;23(6):1035–41.PubMedCrossRef Wagenknecht LE, Zaccaro D, Espeland MA, Karter AJ, O’Leary DH, Haffner SM. Diabetes and progression of carotid atherosclerosis: the insulin resistance atherosclerosis study. Arterioscler Thromb Vasc Biol. 2003;23(6):1035–41.PubMedCrossRef
20.
go back to reference Baek JH, Kim H, Kim KY, Jung J. Insulin resistance and the risk of diabetes and dysglycemia in Korean general adult population. Diabetes Metab J. 2018;42(4):296–307.PubMedPubMedCentralCrossRef Baek JH, Kim H, Kim KY, Jung J. Insulin resistance and the risk of diabetes and dysglycemia in Korean general adult population. Diabetes Metab J. 2018;42(4):296–307.PubMedPubMedCentralCrossRef
21.
go back to reference Choe EY, Lee YH, Choi YJ, Huh BW, Lee BW, Kim SK, et al. Waist-to-calf circumstance ratio is an independent predictor of hepatic steatosis and fibrosis in patients with type 2 diabetes. J Gastroenterol Hepatol. 2018;33(5):1082–91.PubMedCrossRef Choe EY, Lee YH, Choi YJ, Huh BW, Lee BW, Kim SK, et al. Waist-to-calf circumstance ratio is an independent predictor of hepatic steatosis and fibrosis in patients with type 2 diabetes. J Gastroenterol Hepatol. 2018;33(5):1082–91.PubMedCrossRef
23.
go back to reference Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D. A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. Modification of Diet in Renal Disease Study Group. Ann Intern Med. 1999;130(6):461–70.PubMedCrossRef Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D. A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. Modification of Diet in Renal Disease Study Group. Ann Intern Med. 1999;130(6):461–70.PubMedCrossRef
25.
go back to reference Sharma R, Vikram NK, Misra A. Comparison of short insulin tolerance test with HOMA Method for assessment of insulin sensitivity in Asian Indians in north India. Diabetes Res Clin Pract. 2008;82(1):e9–12.PubMedCrossRef Sharma R, Vikram NK, Misra A. Comparison of short insulin tolerance test with HOMA Method for assessment of insulin sensitivity in Asian Indians in north India. Diabetes Res Clin Pract. 2008;82(1):e9–12.PubMedCrossRef
26.
go back to reference Lee MY, Koh JH, Nam SM, Jung PM, Sung JK, Kim SY, et al. Short insulin tolerance test can determine the effects of thiazolidinediones treatment in type 2 diabetes. Yonsei Med J. 2008;49(6):901–8.PubMedPubMedCentralCrossRef Lee MY, Koh JH, Nam SM, Jung PM, Sung JK, Kim SY, et al. Short insulin tolerance test can determine the effects of thiazolidinediones treatment in type 2 diabetes. Yonsei Med J. 2008;49(6):901–8.PubMedPubMedCentralCrossRef
27.
go back to reference Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation. 2009;120(16):1640–5.PubMedCrossRef Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation. 2009;120(16):1640–5.PubMedCrossRef
28.
go back to reference World Health Organization. Regional Office for the Western P. The Asia-Pacific perspective: redefining obesity and its treatment: Sydney: Health Communications Australia; 2000. World Health Organization. Regional Office for the Western P. The Asia-Pacific perspective: redefining obesity and its treatment: Sydney: Health Communications Australia; 2000.
29.
go back to reference Lee YH, Bang H, Park YM, Bae JC, Lee BW, Kang ES, et al. Non-laboratory-based self-assessment screening score for non-alcoholic fatty liver disease: development, validation and comparison with other scores. PLoS ONE. 2014;9(9):e107584.PubMedPubMedCentralCrossRef Lee YH, Bang H, Park YM, Bae JC, Lee BW, Kang ES, et al. Non-laboratory-based self-assessment screening score for non-alcoholic fatty liver disease: development, validation and comparison with other scores. PLoS ONE. 2014;9(9):e107584.PubMedPubMedCentralCrossRef
30.
go back to reference Vallet-Pichard A, Mallet V, Nalpas B, Verkarre V, Nalpas A, Dhalluin-Venier V, et al. FIB-4: an inexpensive and accurate marker of fibrosis in HCV infection. Comparison with liver biopsy and fibrotest. Hepatology. 2007;46(1):32–6.PubMedCrossRef Vallet-Pichard A, Mallet V, Nalpas B, Verkarre V, Nalpas A, Dhalluin-Venier V, et al. FIB-4: an inexpensive and accurate marker of fibrosis in HCV infection. Comparison with liver biopsy and fibrotest. Hepatology. 2007;46(1):32–6.PubMedCrossRef
31.
go back to reference Qi Y, Fan J, Liu J, Wang W, Wang M, Sun J, et al. Cholesterol-overloaded HDL particles are independently associated with progression of carotid atherosclerosis in a cardiovascular disease-free population: a community-based cohort study. J Am Coll Cardiol. 2015;65(4):355–63.PubMedCrossRef Qi Y, Fan J, Liu J, Wang W, Wang M, Sun J, et al. Cholesterol-overloaded HDL particles are independently associated with progression of carotid atherosclerosis in a cardiovascular disease-free population: a community-based cohort study. J Am Coll Cardiol. 2015;65(4):355–63.PubMedCrossRef
32.
go back to reference Sotaniemi EA, Arranto AJ, Pelkonen O, Pasanen M. Age and cytochrome P450-linked drug metabolism in humans: an analysis of 226 subjects with equal histopathologic conditions. Clin Pharmacol Ther. 1997;61(3):331–9.PubMedCrossRef Sotaniemi EA, Arranto AJ, Pelkonen O, Pasanen M. Age and cytochrome P450-linked drug metabolism in humans: an analysis of 226 subjects with equal histopathologic conditions. Clin Pharmacol Ther. 1997;61(3):331–9.PubMedCrossRef
33.
go back to reference Elfaki I, Mir R, Almutairi FM, Duhier FMA. Cytochrome P450: polymorphisms and roles in cancer, diabetes and atherosclerosis. Asian Pac J Cancer Prev. 2018;19(8):2057–70.PubMedPubMedCentral Elfaki I, Mir R, Almutairi FM, Duhier FMA. Cytochrome P450: polymorphisms and roles in cancer, diabetes and atherosclerosis. Asian Pac J Cancer Prev. 2018;19(8):2057–70.PubMedPubMedCentral
34.
go back to reference Luoma PV. Cytochrome P450–physiological key factor against cholesterol accumulation and the atherosclerotic vascular process. Ann Med. 2007;39(5):359–70.PubMedCrossRef Luoma PV. Cytochrome P450–physiological key factor against cholesterol accumulation and the atherosclerotic vascular process. Ann Med. 2007;39(5):359–70.PubMedCrossRef
35.
go back to reference Li T, Matozel M, Boehme S, Kong B, Nilsson LM, Guo G, et al. Overexpression of cholesterol 7α-hydroxylase promotes hepatic bile acid synthesis and secretion and maintains cholesterol homeostasis. Hepatology. 2011;53(3):996–1006.PubMedCrossRef Li T, Matozel M, Boehme S, Kong B, Nilsson LM, Guo G, et al. Overexpression of cholesterol 7α-hydroxylase promotes hepatic bile acid synthesis and secretion and maintains cholesterol homeostasis. Hepatology. 2011;53(3):996–1006.PubMedCrossRef
36.
go back to reference Lorenz MW, Markus HS, Bots ML, Rosvall M, Sitzer M. Prediction of clinical cardiovascular events with carotid intima-media thickness: a systematic review and meta-analysis. Circulation. 2007;115(4):459–67.PubMedCrossRef Lorenz MW, Markus HS, Bots ML, Rosvall M, Sitzer M. Prediction of clinical cardiovascular events with carotid intima-media thickness: a systematic review and meta-analysis. Circulation. 2007;115(4):459–67.PubMedCrossRef
37.
go back to reference Gariani K, Philippe J, Jornayvaz F. Non-alcoholic fatty liver disease and insulin resistance: from bench to bedside. Diabetes Metab. 2013;39(1):16–26.PubMedCrossRef Gariani K, Philippe J, Jornayvaz F. Non-alcoholic fatty liver disease and insulin resistance: from bench to bedside. Diabetes Metab. 2013;39(1):16–26.PubMedCrossRef
38.
go back to reference Park BH, Yoon JM, Kim JH, Moon JH, Lee YH, Jang SM, et al. Pathologic impact of insulin resistance and sensitivity on the severity of liver histopathology in pediatric non-alcoholic steatohepatitis. Yonsei Med J. 2017;58(4):756–62.PubMedPubMedCentralCrossRef Park BH, Yoon JM, Kim JH, Moon JH, Lee YH, Jang SM, et al. Pathologic impact of insulin resistance and sensitivity on the severity of liver histopathology in pediatric non-alcoholic steatohepatitis. Yonsei Med J. 2017;58(4):756–62.PubMedPubMedCentralCrossRef
39.
go back to reference Brar PC, Chun A, Fan X, Jani V, Craft M, Bhatla P, et al. Impaired myocardial deformation and ventricular vascular coupling in obese adolescents with dysglycemia. Cardiovasc Diabetol. 2019;18(1):172.PubMedPubMedCentralCrossRef Brar PC, Chun A, Fan X, Jani V, Craft M, Bhatla P, et al. Impaired myocardial deformation and ventricular vascular coupling in obese adolescents with dysglycemia. Cardiovasc Diabetol. 2019;18(1):172.PubMedPubMedCentralCrossRef
40.
go back to reference Al Rifai M, Silverman MG, Nasir K, Budoff MJ, Blankstein R, Szklo M, et al. The association of nonalcoholic fatty liver disease, obesity, and metabolic syndrome, with systemic inflammation and subclinical atherosclerosis: the Multi-Ethnic Study of Atherosclerosis (MESA). Atherosclerosis. 2015;239(2):629–33.PubMedPubMedCentralCrossRef Al Rifai M, Silverman MG, Nasir K, Budoff MJ, Blankstein R, Szklo M, et al. The association of nonalcoholic fatty liver disease, obesity, and metabolic syndrome, with systemic inflammation and subclinical atherosclerosis: the Multi-Ethnic Study of Atherosclerosis (MESA). Atherosclerosis. 2015;239(2):629–33.PubMedPubMedCentralCrossRef
41.
go back to reference Fargion S, Porzio M, Fracanzani AL. Nonalcoholic fatty liver disease and vascular disease: state-of-the-art. World J Gastroenterol. 2014;20(37):13306–24.PubMedPubMedCentralCrossRef Fargion S, Porzio M, Fracanzani AL. Nonalcoholic fatty liver disease and vascular disease: state-of-the-art. World J Gastroenterol. 2014;20(37):13306–24.PubMedPubMedCentralCrossRef
42.
go back to reference Kathirvel E, Chen P, Morgan K, French SW, Morgan TR. Oxidative stress and regulation of anti-oxidant enzymes in cytochrome P4502E1 transgenic mouse model of non-alcoholic fatty liver. J Gastroenterol Hepatol. 2010;25(6):1136–43.PubMedCrossRef Kathirvel E, Chen P, Morgan K, French SW, Morgan TR. Oxidative stress and regulation of anti-oxidant enzymes in cytochrome P4502E1 transgenic mouse model of non-alcoholic fatty liver. J Gastroenterol Hepatol. 2010;25(6):1136–43.PubMedCrossRef
43.
go back to reference DeFilippis AP, Blaha MJ, Martin SS, Reed RM, Jones SR, Nasir K, et al. Nonalcoholic fatty liver disease and serum lipoproteins: the Multi-Ethnic Study of Atherosclerosis. Atherosclerosis. 2013;227(2):429–36.PubMedPubMedCentralCrossRef DeFilippis AP, Blaha MJ, Martin SS, Reed RM, Jones SR, Nasir K, et al. Nonalcoholic fatty liver disease and serum lipoproteins: the Multi-Ethnic Study of Atherosclerosis. Atherosclerosis. 2013;227(2):429–36.PubMedPubMedCentralCrossRef
44.
go back to reference Marra F, Gastaldelli A, Svegliati Baroni G, Tell G, Tiribelli C. Molecular basis and mechanisms of progression of non-alcoholic steatohepatitis. Trends Mol Med. 2008;14(2):72–81.PubMedCrossRef Marra F, Gastaldelli A, Svegliati Baroni G, Tell G, Tiribelli C. Molecular basis and mechanisms of progression of non-alcoholic steatohepatitis. Trends Mol Med. 2008;14(2):72–81.PubMedCrossRef
45.
go back to reference Targher G, Chonchol M, Miele L, Zoppini G, Pichiri I, Muggeo M. Nonalcoholic fatty liver disease as a contributor to hypercoagulation and thrombophilia in the metabolic syndrome. Semin Thromb Hemost. 2009;35(3):277–87.PubMedCrossRef Targher G, Chonchol M, Miele L, Zoppini G, Pichiri I, Muggeo M. Nonalcoholic fatty liver disease as a contributor to hypercoagulation and thrombophilia in the metabolic syndrome. Semin Thromb Hemost. 2009;35(3):277–87.PubMedCrossRef
46.
go back to reference Tuttolomondo A, Petta S, Casuccio A, Maida C, Corte VD, Daidone M, et al. Reactive hyperemia index (RHI) and cognitive performance indexes are associated with histologic markers of liver disease in subjects with non-alcoholic fatty liver disease (NAFLD): a case control study. Cardiovasc Diabetol. 2018;17(1):28.PubMedPubMedCentralCrossRef Tuttolomondo A, Petta S, Casuccio A, Maida C, Corte VD, Daidone M, et al. Reactive hyperemia index (RHI) and cognitive performance indexes are associated with histologic markers of liver disease in subjects with non-alcoholic fatty liver disease (NAFLD): a case control study. Cardiovasc Diabetol. 2018;17(1):28.PubMedPubMedCentralCrossRef
47.
go back to reference Gummesson A, Strömberg U, Schmidt C, Kullberg J, Angerås O, Lindgren S, et al. Non-alcoholic fatty liver disease is a strong predictor of coronary artery calcification in metabolically healthy subjects: a cross-sectional, population-based study in middle-aged subjects. PLoS ONE. 2018;13(8):e0202666.PubMedPubMedCentralCrossRef Gummesson A, Strömberg U, Schmidt C, Kullberg J, Angerås O, Lindgren S, et al. Non-alcoholic fatty liver disease is a strong predictor of coronary artery calcification in metabolically healthy subjects: a cross-sectional, population-based study in middle-aged subjects. PLoS ONE. 2018;13(8):e0202666.PubMedPubMedCentralCrossRef
48.
go back to reference Arslan U, Turkoglu S, Balcioglu S, Tavil Y, Karakan T, Cengel A. Association between nonalcoholic fatty liver disease and coronary artery disease. Coron Artery Dis. 2007;18(6):433–6.PubMedCrossRef Arslan U, Turkoglu S, Balcioglu S, Tavil Y, Karakan T, Cengel A. Association between nonalcoholic fatty liver disease and coronary artery disease. Coron Artery Dis. 2007;18(6):433–6.PubMedCrossRef
49.
go back to reference Guo YC, Zhou Y, Gao X, Yao Y, Geng B, Cui QH, 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):2269–76.PubMedPubMedCentralCrossRef Guo YC, Zhou Y, Gao X, Yao Y, Geng B, Cui QH, 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):2269–76.PubMedPubMedCentralCrossRef
50.
go back to reference Rampally V, Biri SK, Nair IK, Vadlakonda A. Determination of association between nonalcoholic fatty liver disease and carotid artery atherosclerosis among nondiabetic individuals. J Family Med Prim Care. 2020;9(2):1182–6.PubMedPubMedCentralCrossRef Rampally V, Biri SK, Nair IK, Vadlakonda A. Determination of association between nonalcoholic fatty liver disease and carotid artery atherosclerosis among nondiabetic individuals. J Family Med Prim Care. 2020;9(2):1182–6.PubMedPubMedCentralCrossRef
51.
go back to reference Fruchart JC, Santos RD, Aguilar-Salinas C, Aikawa M, Al Rasadi K, Amarenco P, et al. The selective peroxisome proliferator-activated receptor alpha modulator (SPPARMα) paradigm: conceptual framework and therapeutic potential: a consensus statement from the International Atherosclerosis Society (IAS) and the Residual Risk Reduction Initiative (R3i) Foundation. Cardiovasc Diabetol. 2019;18(1):71.PubMedPubMedCentralCrossRef Fruchart JC, Santos RD, Aguilar-Salinas C, Aikawa M, Al Rasadi K, Amarenco P, et al. The selective peroxisome proliferator-activated receptor alpha modulator (SPPARMα) paradigm: conceptual framework and therapeutic potential: a consensus statement from the International Atherosclerosis Society (IAS) and the Residual Risk Reduction Initiative (R3i) Foundation. Cardiovasc Diabetol. 2019;18(1):71.PubMedPubMedCentralCrossRef
52.
go back to reference Rafiq N, Bai C, Fang Y, Srishord M, McCullough A, Gramlich T, et al. Long-term follow-up of patients with nonalcoholic fatty liver. Clin Gastroenterol Hepatol. 2009;7(2):234–8.PubMedCrossRef Rafiq N, Bai C, Fang Y, Srishord M, McCullough A, Gramlich T, et al. Long-term follow-up of patients with nonalcoholic fatty liver. Clin Gastroenterol Hepatol. 2009;7(2):234–8.PubMedCrossRef
54.
go back to reference Kim JH, Moon JS, Byun SJ, Lee JH, Kang DR, Sung KC, et al. Fatty liver index and development of cardiovascular disease in Koreans without pre-existing myocardial infarction and ischemic stroke: a large population-based study. Cardiovasc Diabetol. 2020;19(1):51.PubMedPubMedCentralCrossRef Kim JH, Moon JS, Byun SJ, Lee JH, Kang DR, Sung KC, et al. Fatty liver index and development of cardiovascular disease in Koreans without pre-existing myocardial infarction and ischemic stroke: a large population-based study. Cardiovasc Diabetol. 2020;19(1):51.PubMedPubMedCentralCrossRef
55.
go back to reference Lonardo A, Nascimbeni F, Mantovani A, Targher G. Hypertension, diabetes, atherosclerosis and NASH: cause or consequence? J Hepatol. 2018;68(2):335–52.CrossRefPubMed Lonardo A, Nascimbeni F, Mantovani A, Targher G. Hypertension, diabetes, atherosclerosis and NASH: cause or consequence? J Hepatol. 2018;68(2):335–52.CrossRefPubMed
56.
go back to reference Villela-Nogueira CA, Leite NC, Cardoso CR, Salles GF. NAFLD and increased aortic stiffness: parallel or common physiopathological mechanisms? Int J Mol Sci. 2016;17(4):460.PubMedCentralCrossRef Villela-Nogueira CA, Leite NC, Cardoso CR, Salles GF. NAFLD and increased aortic stiffness: parallel or common physiopathological mechanisms? Int J Mol Sci. 2016;17(4):460.PubMedCentralCrossRef
57.
go back to reference Dam-Larsen S, Becker U, Franzmann MB, Larsen K, Christoffersen P, Bendtsen F. Final results of a long-term, clinical follow-up in fatty liver patients. Scand J Gastroenterol. 2009;44(10):1236–43.PubMedCrossRef Dam-Larsen S, Becker U, Franzmann MB, Larsen K, Christoffersen P, Bendtsen F. Final results of a long-term, clinical follow-up in fatty liver patients. Scand J Gastroenterol. 2009;44(10):1236–43.PubMedCrossRef
58.
go back to reference Farrell GC, Larter CZ. Nonalcoholic fatty liver disease: from steatosis to cirrhosis. Hepatology. 2006;43(S1):S99–112.PubMedCrossRef Farrell GC, Larter CZ. Nonalcoholic fatty liver disease: from steatosis to cirrhosis. Hepatology. 2006;43(S1):S99–112.PubMedCrossRef
59.
go back to reference Xiao G, Zhu S, Xiao X, Yan L, Yang J, Wu G. Comparison of laboratory tests, ultrasound, or magnetic resonance elastography to detect fibrosis in patients with nonalcoholic fatty liver disease: a meta-analysis. Hepatology. 2017;66(5):1486–501.PubMedCrossRef Xiao G, Zhu S, Xiao X, Yan L, Yang J, Wu G. Comparison of laboratory tests, ultrasound, or magnetic resonance elastography to detect fibrosis in patients with nonalcoholic fatty liver disease: a meta-analysis. Hepatology. 2017;66(5):1486–501.PubMedCrossRef
60.
go back to reference Wong VW, Adams LA, de Ledinghen V, Wong GL, Sookoian S. Noninvasive biomarkers in NAFLD and NASH—current progress and future promise. Nat Rev Gastroenterol Hepatol. 2018;15(8):461–78.PubMedCrossRef Wong VW, Adams LA, de Ledinghen V, Wong GL, Sookoian S. Noninvasive biomarkers in NAFLD and NASH—current progress and future promise. Nat Rev Gastroenterol Hepatol. 2018;15(8):461–78.PubMedCrossRef
Metadata
Title
Non-alcoholic steatohepatitis and progression of carotid atherosclerosis in patients with type 2 diabetes: a Korean cohort study
Authors
Hyeok-Hee Lee
Yongin Cho
Young Ju Choi
Byung Wook Huh
Byung-Wan Lee
Eun Seok Kang
Seok Won Park
Bong-Soo Cha
Eun Jig Lee
Yong-ho Lee
Kap Bum Huh
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2020
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/s12933-020-01064-x

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