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Published in: Cardiovascular Diabetology 1/2024

Open Access 01-12-2024 | Type 2 Diabetes | Research

Non-alcoholic fatty liver disease biomarkers estimate cardiovascular risk based on coronary artery calcium score in type 2 diabetes: a cross-sectional study with two independent cohorts

Authors: Damien Denimal, Maharajah Ponnaiah, Anne-Caroline Jeannin, Franck Phan, Agnès Hartemann, Samia Boussouar, Etienne Charpentier, Alban Redheuil, Fabienne Foufelle, Olivier Bourron

Published in: Cardiovascular Diabetology | Issue 1/2024

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Abstract

Background

Studies have demonstrated that coronary artery calcification on one hand and non-alcoholic fatty liver disease (NAFLD) on the other hand are strongly associated with cardiovascular events. However, it remains unclear whether NAFLD biomarkers could help estimate cardiovascular risk in individuals with type 2 diabetes (T2D). The primary objective of the present study was to investigate whether the biomarkers of NAFLD included in the FibroMax® panels are associated with the degree of coronary artery calcification in patients with T2D.

Methods

A total of 157 and 460 patients with T2D were included from the DIACART and ACCoDiab cohorts, respectively. The coronary artery calcium score (CACS) was measured in both cohorts using computed tomography. FibroMax® panels (i.e., SteatoTest®, FibroTest®, NashTest®, and ActiTest®) were determined from blood samples as scores and stages in the DIACART cohort and as stages in the ACCoDiab cohort.

Results

CACS significantly increased with the FibroTest® stages in both the DIACART and ACCoDiab cohorts (p-value for trend = 0.0009 and 0.0001, respectively). In DIACART, the FibroTest® score was positively correlated with CACS in univariate analysis (r = 0.293, p = 0.0002) and remained associated with CACS independently of the traditional cardiovascular risk factors included in the SCORE2-Diabetes model [β = 941 ± 425 (estimate ± standard error), p = 0.028]. In the ACCoDiab cohort, the FibroTest® F3-F4 stage was positively correlated with CACS in point-biserial analysis (rpbi = 0.104, p = 0.024) and remained associated with CACS after adjustment for the traditional cardiovascular risk factors included in the SCORE2-Diabetes model (β = 234 ± 97, p = 0.016). Finally, the prediction of CACS was improved by adding FibroTest® to the traditional cardiovascular risk factors included in the SCORE2-Diabetes model (goodness-of-fit of prediction models multiplied by 4.1 and 6.7 in the DIACART and ACCoDiab cohorts, respectively). In contrast, no significant relationship was found between FibroMax® panels other than FibroTest® and CACS in either cohort.

Conclusions

FibroTest® is independently and positively associated with the degree of coronary artery calcification in patients with T2D, suggesting that FibroTest® could be a relevant biomarker of coronary calcification and cardiovascular risk.
Trial registration: ClinicalTrials.gov identifiers NCT02431234 and NCT03920683.
Literature
1.
go back to reference The Emerging Risk Factors Collaboration. Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies. Lancet. 2010;375:2215–22.CrossRefPubMedCentral The Emerging Risk Factors Collaboration. Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies. Lancet. 2010;375:2215–22.CrossRefPubMedCentral
2.
go back to reference Young LH, Wackers FJT, Chyun DA, Davey JA, Barrett EJ, Taillefer R, et al. Cardiac outcomes after screening for asymptomatic coronary artery disease in patients with type 2 diabetes: the DIAD study: a randomized controlled trial. JAMA. 2009;301(15):1547–55.CrossRefPubMedPubMedCentral Young LH, Wackers FJT, Chyun DA, Davey JA, Barrett EJ, Taillefer R, et al. Cardiac outcomes after screening for asymptomatic coronary artery disease in patients with type 2 diabetes: the DIAD study: a randomized controlled trial. JAMA. 2009;301(15):1547–55.CrossRefPubMedPubMedCentral
3.
go back to reference Keech A, Simes RJ, Barter P, Best J, Scott R, Taskinen MR, et al. Effects of long-term fenofibrate therapy on cardiovascular events in 9795 people with type 2 diabetes mellitus (the FIELD study): randomised controlled trial. Lancet. 2005;366(9500):1849–61.CrossRefPubMed Keech A, Simes RJ, Barter P, Best J, Scott R, Taskinen MR, et al. Effects of long-term fenofibrate therapy on cardiovascular events in 9795 people with type 2 diabetes mellitus (the FIELD study): randomised controlled trial. Lancet. 2005;366(9500):1849–61.CrossRefPubMed
4.
go back to reference Colhoun HM, Betteridge DJ, Durrington PN, Hitman GA, Neil HAW, Livingstone SJ, et al. Primary prevention of cardiovascular disease with atorvastatin in type 2 diabetes in the Collaborative Atorvastatin Diabetes Study (CARDS): multicentre randomised placebo-controlled trial. Lancet. 2004;364(9435):685–96.CrossRefPubMed Colhoun HM, Betteridge DJ, Durrington PN, Hitman GA, Neil HAW, Livingstone SJ, et al. Primary prevention of cardiovascular disease with atorvastatin in type 2 diabetes in the Collaborative Atorvastatin Diabetes Study (CARDS): multicentre randomised placebo-controlled trial. Lancet. 2004;364(9435):685–96.CrossRefPubMed
5.
go back to reference Patel A, MacMahon S, Chalmers J, Neal B, Billot L, ADVANCE Collaborative Group, et al. Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes. N Engl J Med. 2008;358(24):2560–72.CrossRefPubMed Patel A, MacMahon S, Chalmers J, Neal B, Billot L, ADVANCE Collaborative Group, et al. Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes. N Engl J Med. 2008;358(24):2560–72.CrossRefPubMed
6.
go back to reference Gerstein HC, Miller ME, Byington RP, Goff DC, Bigger JT, Action to Control Cardiovascular Risk in Diabetes Study Group, et al. Effects of intensive glucose lowering in type 2 diabetes. N Engl J Med. 2008;358(24):2545–59.CrossRefPubMed Gerstein HC, Miller ME, Byington RP, Goff DC, Bigger JT, Action to Control Cardiovascular Risk in Diabetes Study Group, et al. Effects of intensive glucose lowering in type 2 diabetes. N Engl J Med. 2008;358(24):2545–59.CrossRefPubMed
7.
go back to reference Frye RL, August P, Brooks MM, Hardison RM, Kelsey SF, BARI 2D Study Group, et al. A randomized trial of therapies for type 2 diabetes and coronary artery disease. N Engl J Med. 2009;360(24):2503–15.CrossRefPubMed Frye RL, August P, Brooks MM, Hardison RM, Kelsey SF, BARI 2D Study Group, et al. A randomized trial of therapies for type 2 diabetes and coronary artery disease. N Engl J Med. 2009;360(24):2503–15.CrossRefPubMed
8.
go back to reference Dziopa K, Asselbergs FW, Gratton J, Chaturvedi N, Schmidt AF. Cardiovascular risk prediction in type 2 diabetes: a comparison of 22 risk scores in primary care settings. Diabetologia. 2022;65(4):644–56.CrossRefPubMedPubMedCentral Dziopa K, Asselbergs FW, Gratton J, Chaturvedi N, Schmidt AF. Cardiovascular risk prediction in type 2 diabetes: a comparison of 22 risk scores in primary care settings. Diabetologia. 2022;65(4):644–56.CrossRefPubMedPubMedCentral
9.
go back to reference SCORE2-Diabetes Working Group and the ESC Cardiovascular Risk Collaboration. SCORE2-Diabetes: 10-year cardiovascular risk estimation in type 2 diabetes in Europe. Eur Heart J. 2023;44(28):2544–56. SCORE2-Diabetes Working Group and the ESC Cardiovascular Risk Collaboration. SCORE2-Diabetes: 10-year cardiovascular risk estimation in type 2 diabetes in Europe. Eur Heart J. 2023;44(28):2544–56.
10.
go back to reference The Task Force for diabetes, pre-diabetes, and cardiovascular diseases of the European Society of Cardiology (ESC) and the European Association for the Study of Diabetes (EASD). 2019 ESC guidelines on diabetes, pre-diabetes, and cardiovascular diseases developed in collaboration with the EASD. Eur Heart J. 2020;41(2):255–323. The Task Force for diabetes, pre-diabetes, and cardiovascular diseases of the European Society of Cardiology (ESC) and the European Association for the Study of Diabetes (EASD). 2019 ESC guidelines on diabetes, pre-diabetes, and cardiovascular diseases developed in collaboration with the EASD. Eur Heart J. 2020;41(2):255–323.
11.
go back to reference Elkeles RS, Godsland IF, Feher MD, Rubens MB, Roughton M, Nugara F, et al. Coronary calcium measurement improves prediction of cardiovascular events in asymptomatic patients with type 2 diabetes: the PREDICT study. Eur Heart J. 2008;29(18):2244–51.CrossRefPubMed Elkeles RS, Godsland IF, Feher MD, Rubens MB, Roughton M, Nugara F, et al. Coronary calcium measurement improves prediction of cardiovascular events in asymptomatic patients with type 2 diabetes: the PREDICT study. Eur Heart J. 2008;29(18):2244–51.CrossRefPubMed
12.
go back to reference Ichikawa K, Miyoshi T, Osawa K, Miki T, Toda H, Ejiri K, et al. Prognostic value of non-alcoholic fatty liver disease for predicting cardiovascular events in patients with diabetes mellitus with suspected coronary artery disease: a prospective cohort study. Cardiovasc Diabetol. 2021;20(1):8.CrossRefPubMedPubMedCentral Ichikawa K, Miyoshi T, Osawa K, Miki T, Toda H, Ejiri K, et al. Prognostic value of non-alcoholic fatty liver disease for predicting cardiovascular events in patients with diabetes mellitus with suspected coronary artery disease: a prospective cohort study. Cardiovasc Diabetol. 2021;20(1):8.CrossRefPubMedPubMedCentral
13.
go back to reference Agarwal S, Cox AJ, Herrington DM, Jorgensen NW, Xu J, Freedman BI, et al. Coronary calcium score predicts cardiovascular mortality in diabetes. Diabetes Care. 2013;36(4):972–7.CrossRefPubMedPubMedCentral Agarwal S, Cox AJ, Herrington DM, Jorgensen NW, Xu J, Freedman BI, et al. Coronary calcium score predicts cardiovascular mortality in diabetes. Diabetes Care. 2013;36(4):972–7.CrossRefPubMedPubMedCentral
14.
go back to reference Malik S, Zhao Y, Budoff M, Nasir K, Blumenthal RS, Bertoni AG, et al. Coronary artery calcium score for long-term risk classification in individuals with type 2 diabetes and metabolic syndrome from the Multi-Ethnic Study of Atherosclerosis. JAMA Cardiol. 2017;2(12):1332–40.CrossRefPubMedPubMedCentral Malik S, Zhao Y, Budoff M, Nasir K, Blumenthal RS, Bertoni AG, et al. Coronary artery calcium score for long-term risk classification in individuals with type 2 diabetes and metabolic syndrome from the Multi-Ethnic Study of Atherosclerosis. JAMA Cardiol. 2017;2(12):1332–40.CrossRefPubMedPubMedCentral
15.
go back to reference American Diabetes Association Professional Practice Committee. Cardiovascular disease and risk management: Standards of medical care in diabetes—2022. American Diabetes Association Professional Practice Committee. Cardiovascular disease and risk management: Standards of medical care in diabetes—2022.
16.
go back to reference Castera L, Laouenan C, Vallet-Pichard A, Vidal-Trécan T, Manchon P, Paradis V, et al. High prevalence of NASH and advanced fibrosis in type 2 diabetes: a prospective study of 330 outpatients undergoing liver biopsies for elevated ALT, using a low threshold. Diabetes Care. 2023;46(7):1354–62.CrossRefPubMed Castera L, Laouenan C, Vallet-Pichard A, Vidal-Trécan T, Manchon P, Paradis V, et al. High prevalence of NASH and advanced fibrosis in type 2 diabetes: a prospective study of 330 outpatients undergoing liver biopsies for elevated ALT, using a low threshold. Diabetes Care. 2023;46(7):1354–62.CrossRefPubMed
17.
go back to reference Rinella ME, Lazarus JV, Ratziu V, Francque SM, Sanyal AJ, Kanwal F, et al. A multisociety Delphi consensus statement on new fatty liver disease nomenclature. J Hepatol. 2023;79(6):1542–56.CrossRefPubMed Rinella ME, Lazarus JV, Ratziu V, Francque SM, Sanyal AJ, Kanwal F, et al. A multisociety Delphi consensus statement on new fatty liver disease nomenclature. J Hepatol. 2023;79(6):1542–56.CrossRefPubMed
18.
go back to reference Zeb I, Li D, Budoff MJ, Katz R, Lloyd-Jones D, Agatston A, et al. Nonalcoholic fatty liver disease and incident cardiac events. J Am Coll Cardiol. 2016;67(16):1965–6.CrossRefPubMed Zeb I, Li D, Budoff MJ, Katz R, Lloyd-Jones D, Agatston A, et al. Nonalcoholic fatty liver disease and incident cardiac events. J Am Coll Cardiol. 2016;67(16):1965–6.CrossRefPubMed
19.
go back to reference Ekstedt M, Hagström H, Nasr P, Fredrikson M, Stål P, Kechagias S, et al. Fibrosis stage is the strongest predictor for disease-specific mortality in NAFLD after up to 33 years of follow-up. Hepatology. 2015;61(5):1547–54.CrossRefPubMed Ekstedt M, Hagström H, Nasr P, Fredrikson M, Stål P, Kechagias S, et al. Fibrosis stage is the strongest predictor for disease-specific mortality in NAFLD after up to 33 years of follow-up. Hepatology. 2015;61(5):1547–54.CrossRefPubMed
20.
go back to reference Kim D, Kim WR, Kim HJ, Therneau TM. Association between noninvasive fibrosis markers and mortality among adults with nonalcoholic fatty liver disease in the United States. Hepatology. 2013;57(4):1357–65.CrossRefPubMed Kim D, Kim WR, Kim HJ, Therneau TM. Association between noninvasive fibrosis markers and mortality among adults with nonalcoholic fatty liver disease in the United States. Hepatology. 2013;57(4):1357–65.CrossRefPubMed
21.
go back to reference Sung KC, Wild SH, Kwag HJ, Byrne CD. Fatty liver, insulin resistance, and features of metabolic syndrome: relationships with coronary artery calcium in 10,153 people. Diabetes Care. 2012;35(11):2359–64.CrossRefPubMedPubMedCentral Sung KC, Wild SH, Kwag HJ, Byrne CD. Fatty liver, insulin resistance, and features of metabolic syndrome: relationships with coronary artery calcium in 10,153 people. Diabetes Care. 2012;35(11):2359–64.CrossRefPubMedPubMedCentral
22.
go back to reference Lee MK, Park HJ, Jeon WS, Park SE, Park CY, Lee WY, et al. Higher association of coronary artery calcification with non-alcoholic fatty liver disease than with abdominal obesity in middle-aged Korean men: the Kangbuk Samsung Health Study. Cardiovasc Diabetol. 2015;14:88.CrossRefPubMedPubMedCentral Lee MK, Park HJ, Jeon WS, Park SE, Park CY, Lee WY, et al. Higher association of coronary artery calcification with non-alcoholic fatty liver disease than with abdominal obesity in middle-aged Korean men: the Kangbuk Samsung Health Study. Cardiovasc Diabetol. 2015;14:88.CrossRefPubMedPubMedCentral
23.
go back to reference VanWagner LB, Ning H, Lewis CE, Shay CM, Wilkins J, Carr JJ, et al. Associations between nonalcoholic fatty liver disease and subclinical atherosclerosis in middle-aged adults: the Coronary Artery Risk Development in Young Adults Study. Atherosclerosis. 2014;235(2):599–605.CrossRefPubMedPubMedCentral VanWagner LB, Ning H, Lewis CE, Shay CM, Wilkins J, Carr JJ, et al. Associations between nonalcoholic fatty liver disease and subclinical atherosclerosis in middle-aged adults: the Coronary Artery Risk Development in Young Adults Study. Atherosclerosis. 2014;235(2):599–605.CrossRefPubMedPubMedCentral
24.
go back to reference Sinn DH, Kang D, Chang Y, Ryu S, Gu S, Kim H, et al. Non-alcoholic fatty liver disease and progression of coronary artery calcium score: a retrospective cohort study. Gut. 2017;66(2):323–9.CrossRefPubMed Sinn DH, Kang D, Chang Y, Ryu S, Gu S, Kim H, et al. Non-alcoholic fatty liver disease and progression of coronary artery calcium score: a retrospective cohort study. Gut. 2017;66(2):323–9.CrossRefPubMed
25.
go back to reference Koulaouzidis G, Charisopoulou D, Kukla M, Marlicz W, Rydzewska G, Koulaouzidis A, et al. Association of non-alcoholic fatty liver disease with coronary artery calcification progression: a systematic review and meta-analysis. Gastroenterol Rev. 2021;16(3):196–206.CrossRef Koulaouzidis G, Charisopoulou D, Kukla M, Marlicz W, Rydzewska G, Koulaouzidis A, et al. Association of non-alcoholic fatty liver disease with coronary artery calcification progression: a systematic review and meta-analysis. Gastroenterol Rev. 2021;16(3):196–206.CrossRef
26.
go back to reference Poynard T, Lassailly G, Diaz E, Clement K, Caïazzo R, Tordjman J, et al. Performance of biomarkers FibroTest, ActiTest, SteatoTest, and NashTest in patients with severe obesity: meta analysis of individual patient data. PLoS ONE. 2012;7(3): e30325.CrossRefPubMedPubMedCentralADS Poynard T, Lassailly G, Diaz E, Clement K, Caïazzo R, Tordjman J, et al. Performance of biomarkers FibroTest, ActiTest, SteatoTest, and NashTest in patients with severe obesity: meta analysis of individual patient data. PLoS ONE. 2012;7(3): e30325.CrossRefPubMedPubMedCentralADS
27.
go back to reference Bourron O, Phan F, Diallo MH, Hajage D, Aubert CE, Carlier A, et al. Circulating Receptor Activator of Nuclear Factor kB Ligand and triglycerides are associated with progression of lower limb arterial calcification in type 2 diabetes: a prospective, observational cohort study. Cardiovasc Diabetol. 2020;19(1):140.CrossRefPubMedPubMedCentral Bourron O, Phan F, Diallo MH, Hajage D, Aubert CE, Carlier A, et al. Circulating Receptor Activator of Nuclear Factor kB Ligand and triglycerides are associated with progression of lower limb arterial calcification in type 2 diabetes: a prospective, observational cohort study. Cardiovasc Diabetol. 2020;19(1):140.CrossRefPubMedPubMedCentral
28.
go back to reference Stefan N, Schulze MB. Metabolic health and cardiometabolic risk clusters: implications for prediction, prevention, and treatment. Lancet Diabetes Endocrinol. 2023;11(6):426–40.CrossRefPubMed Stefan N, Schulze MB. Metabolic health and cardiometabolic risk clusters: implications for prediction, prevention, and treatment. Lancet Diabetes Endocrinol. 2023;11(6):426–40.CrossRefPubMed
29.
go back to reference European Association for the Study of the Liver Clinical Practice Guideline Panel. EASL Clinical Practice Guidelines on non-invasive tests for evaluation of liver disease severity and prognosis—2021 update. J Hepatol. 2021;75(3):659–89. European Association for the Study of the Liver Clinical Practice Guideline Panel. EASL Clinical Practice Guidelines on non-invasive tests for evaluation of liver disease severity and prognosis—2021 update. J Hepatol. 2021;75(3):659–89.
30.
go back to reference Park JG, Jung J, Verma KK, Kang MK, Madamba E, Lopez S, et al. Liver stiffness by magnetic resonance elastography is associated with increased risk of cardiovascular disease in patients with non-alcoholic fatty liver disease. Aliment Pharmacol Ther. 2021;53(9):1030–7.CrossRefPubMedPubMedCentral Park JG, Jung J, Verma KK, Kang MK, Madamba E, Lopez S, et al. Liver stiffness by magnetic resonance elastography is associated with increased risk of cardiovascular disease in patients with non-alcoholic fatty liver disease. Aliment Pharmacol Ther. 2021;53(9):1030–7.CrossRefPubMedPubMedCentral
31.
go back to reference Lee J, Kim HS, Cho YK, Kim EH, Lee MJ, Bae IY, et al. Association between noninvasive assessment of liver fibrosis and coronary artery calcification progression in patients with nonalcoholic fatty liver disease. Sci Rep. 2020;10(1):18323.CrossRefPubMedPubMedCentral Lee J, Kim HS, Cho YK, Kim EH, Lee MJ, Bae IY, et al. Association between noninvasive assessment of liver fibrosis and coronary artery calcification progression in patients with nonalcoholic fatty liver disease. Sci Rep. 2020;10(1):18323.CrossRefPubMedPubMedCentral
32.
go back to reference Perdomo CM, Ezponda A, Núñez-Córdoba JM, Herrero JI, Bastarrika G, Frühbeck G, et al. Transient elastography and serum markers of liver fibrosis associate with epicardial adipose tissue and coronary artery calcium in NAFLD. Sci Rep. 2022;12(1):6564.CrossRefPubMedPubMedCentralADS Perdomo CM, Ezponda A, Núñez-Córdoba JM, Herrero JI, Bastarrika G, Frühbeck G, et al. Transient elastography and serum markers of liver fibrosis associate with epicardial adipose tissue and coronary artery calcium in NAFLD. Sci Rep. 2022;12(1):6564.CrossRefPubMedPubMedCentralADS
33.
go back to reference McKimmie RL, Daniel KR, Carr JJ, Bowden DW, Freedman BI, Register TC, et al. Hepatic steatosis and subclinical cardiovascular disease in a cohort enriched for type 2 diabetes: The Diabetes Heart Study. Am J Gastroenterol. 2008;103(12):3029–35.CrossRefPubMedPubMedCentral McKimmie RL, Daniel KR, Carr JJ, Bowden DW, Freedman BI, Register TC, et al. Hepatic steatosis and subclinical cardiovascular disease in a cohort enriched for type 2 diabetes: The Diabetes Heart Study. Am J Gastroenterol. 2008;103(12):3029–35.CrossRefPubMedPubMedCentral
34.
go back to reference Perazzo H, Munteanu M, Ngo Y, Lebray P, Seurat N, Rutka F, et al. Prognostic value of liver fibrosis and steatosis biomarkers in type 2 diabetes and dyslipidaemia. Aliment Pharmacol Ther. 2014;40(9):1081–93.CrossRefPubMed Perazzo H, Munteanu M, Ngo Y, Lebray P, Seurat N, Rutka F, et al. Prognostic value of liver fibrosis and steatosis biomarkers in type 2 diabetes and dyslipidaemia. Aliment Pharmacol Ther. 2014;40(9):1081–93.CrossRefPubMed
35.
go back to reference Targher G, Byrne CD, Tilg H. NAFLD and increased risk of cardiovascular disease: clinical associations, pathophysiological mechanisms and pharmacological implications. Gut. 2020;69(9):1691–705.CrossRefPubMed Targher G, Byrne CD, Tilg H. NAFLD and increased risk of cardiovascular disease: clinical associations, pathophysiological mechanisms and pharmacological implications. Gut. 2020;69(9):1691–705.CrossRefPubMed
37.
go back to reference Westenfeld R, Schäfer C, Krüger T, Haarmann C, Schurgers LJ, Reutelingsperger C, et al. Fetuin-A protects against atherosclerotic calcification in CKD. J Am Soc Nephrol JASN. 2009;20(6):1264–74.CrossRefPubMed Westenfeld R, Schäfer C, Krüger T, Haarmann C, Schurgers LJ, Reutelingsperger C, et al. Fetuin-A protects against atherosclerotic calcification in CKD. J Am Soc Nephrol JASN. 2009;20(6):1264–74.CrossRefPubMed
38.
go back to reference Liu S, Xiao J, Zhao Z, Wang M, Wang Y, Xin Y. Systematic review and meta-analysis of circulating fetuin-A levels in nonalcoholic fatty liver disease. J Clin Transl Hepatol. 2021;9(1):3–14.PubMed Liu S, Xiao J, Zhao Z, Wang M, Wang Y, Xin Y. Systematic review and meta-analysis of circulating fetuin-A levels in nonalcoholic fatty liver disease. J Clin Transl Hepatol. 2021;9(1):3–14.PubMed
39.
go back to reference Kahraman A, Sowa JP, Schlattjan M, Sydor S, Pronadl M, Wree A, et al. Fetuin-A mRNA expression is elevated in NASH compared with NAFL patients. Clin Sci. 2013;125(8):391–400.CrossRef Kahraman A, Sowa JP, Schlattjan M, Sydor S, Pronadl M, Wree A, et al. Fetuin-A mRNA expression is elevated in NASH compared with NAFL patients. Clin Sci. 2013;125(8):391–400.CrossRef
40.
go back to reference Sato M, Kamada Y, Takeda Y, Kida S, Ohara Y, Fujii H, et al. Fetuin-A negatively correlates with liver and vascular fibrosis in nonalcoholic fatty liver disease subjects. Liver Int. 2015;35(3):925–35.CrossRefPubMed Sato M, Kamada Y, Takeda Y, Kida S, Ohara Y, Fujii H, et al. Fetuin-A negatively correlates with liver and vascular fibrosis in nonalcoholic fatty liver disease subjects. Liver Int. 2015;35(3):925–35.CrossRefPubMed
41.
go back to reference Namakchian M, Rabizadeh S, Seifouri S, Asadigandomani H, Bafrani MA, Seifouri K, et al. Fibrosis score 4 index has an independent relationship with coronary artery diseases in patients with metabolic-associated fatty liver disease. Diabetol Metab Syndr. 2023;15(1):57.CrossRefPubMedPubMedCentral Namakchian M, Rabizadeh S, Seifouri S, Asadigandomani H, Bafrani MA, Seifouri K, et al. Fibrosis score 4 index has an independent relationship with coronary artery diseases in patients with metabolic-associated fatty liver disease. Diabetol Metab Syndr. 2023;15(1):57.CrossRefPubMedPubMedCentral
42.
go back to reference Poynard T, Paradis V, Mullaert J, Deckmyn O, Gault N, Marcault E, et al. Prospective external validation of a new non-invasive test for the diagnosis of non-alcoholic steatohepatitis in patients with type 2 diabetes. Aliment Pharmacol Ther. 2021;54(7):952–66.CrossRefPubMedPubMedCentral Poynard T, Paradis V, Mullaert J, Deckmyn O, Gault N, Marcault E, et al. Prospective external validation of a new non-invasive test for the diagnosis of non-alcoholic steatohepatitis in patients with type 2 diabetes. Aliment Pharmacol Ther. 2021;54(7):952–66.CrossRefPubMedPubMedCentral
43.
go back to reference Bril F, McPhaul MJ, Caulfield MP, Castille JM, Poynard T, Soldevila-Pico C, et al. Performance of the SteatoTest, ActiTest, NashTest and FibroTest in a multiethnic cohort of patients with type 2 diabetes mellitus. J Investig Med Off Publ Am Fed Clin Res. 2019;67(2):303–11. Bril F, McPhaul MJ, Caulfield MP, Castille JM, Poynard T, Soldevila-Pico C, et al. Performance of the SteatoTest, ActiTest, NashTest and FibroTest in a multiethnic cohort of patients with type 2 diabetes mellitus. J Investig Med Off Publ Am Fed Clin Res. 2019;67(2):303–11.
44.
go back to reference European Association for the Study of the Liver (EASL), European Association for the Study of Diabetes (EASD), European Association for the Study of Obesity (EASO). EASL–EASD–EASO clinical practice guidelines for the management of non-alcoholic fatty liver disease. Diabetologia. 2016;59(6):1121–40. European Association for the Study of the Liver (EASL), European Association for the Study of Diabetes (EASD), European Association for the Study of Obesity (EASO). EASL–EASD–EASO clinical practice guidelines for the management of non-alcoholic fatty liver disease. Diabetologia. 2016;59(6):1121–40.
45.
go back to reference Poynard T, Deckmyn O, Peta V, Paradis V, Gautier JF, Brzustowski A, et al. Prospective direct comparison of non-invasive liver tests in outpatients with type 2 diabetes using intention-to-diagnose analysis. Aliment Pharmacol Ther. 2023;58(9):888–902.CrossRefPubMed Poynard T, Deckmyn O, Peta V, Paradis V, Gautier JF, Brzustowski A, et al. Prospective direct comparison of non-invasive liver tests in outpatients with type 2 diabetes using intention-to-diagnose analysis. Aliment Pharmacol Ther. 2023;58(9):888–902.CrossRefPubMed
Metadata
Title
Non-alcoholic fatty liver disease biomarkers estimate cardiovascular risk based on coronary artery calcium score in type 2 diabetes: a cross-sectional study with two independent cohorts
Authors
Damien Denimal
Maharajah Ponnaiah
Anne-Caroline Jeannin
Franck Phan
Agnès Hartemann
Samia Boussouar
Etienne Charpentier
Alban Redheuil
Fabienne Foufelle
Olivier Bourron
Publication date
01-12-2024
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2024
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/s12933-024-02161-x

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