Skip to main content
Top
Published in: Hepatology International 6/2020

01-12-2020 | Fatty Liver | Original Article

Association of arterial stiffness with the histological severity of nonalcoholic fatty liver disease

Authors: Hack-Lyoung Kim, Bo Kyung Koo, Sae Kyung Joo, Won Kim

Published in: Hepatology International | Issue 6/2020

Login to get access

Abstract

Background

Although arterial stiffness has been reported to be associated with nonalcoholic fatty liver disease (NAFLD), previous studies have relied only on noninvasive assessments for the diagnosis of NAFLD. This study attempted to investigate the association of arterial stiffness with the histological severity of NAFLD.

Methods

We analyzed data from a biopsy-proven prospective NAFLD cohort. Augmentation index corrected for a heart rate of 75 bpm (AI@75) was obtained using applanation tonometry of the radial artery.

Results

A total of 154 patients (mean age 55.2 years; females 55.8%) with biopsy-proven NAFLD were analyzed. Patients with higher AI@75 (≥ 76%) showed more severe grades of lobular and portal inflammation and hepatocellular ballooning, and more advanced stages of fibrosis compared to those with lower AI@75 (< 76%) (p < 0.05 for each). The presence of nonalcoholic steatohepatitis (NASH) (adjusted odds ratio [aOR] 2.48; 95% confidence interval [CI] 1.31–6.16; p = 0.008), lobular inflammation (aOR 2.03; 95% CI 1.09–3.78; p = 0.025) hepatocellular ballooning (aOR 2.82; 95% CI 1.23–6.43; p = 0.014), and significant fibrosis (≥ F2) (aOR 3.42; 95% CI 1.50–7.79; p = 0.003) were independently associated with higher AI@75 (≥ 76%) even after adjustment for confounders.

Conclusion

Arterial stiffness as indicated by higher AI@75 was associated with more severe NAFLD histology. This adds to the evidence for the association between increased arterial stiffness and NAFLD.
Appendix
Available only for authorised users
Literature
1.
go back to reference Chalasani N, Younossi Z, Lavine JE, Charlton M, Cusi K, Rinella M, Harrison SA, 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;67:328–357CrossRef Chalasani N, Younossi Z, Lavine JE, Charlton M, Cusi K, Rinella M, Harrison SA, 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;67:328–357CrossRef
2.
go back to reference Adams LA, Lymp JF, St Sauver J, Sanderson SO, Lindor KD, Feldstein A, et al. The natural history of nonalcoholic fatty liver disease: a population-based cohort study. Gastroenterology 2005;129:113–121CrossRef Adams LA, Lymp JF, St Sauver J, Sanderson SO, Lindor KD, Feldstein A, et al. The natural history of nonalcoholic fatty liver disease: a population-based cohort study. Gastroenterology 2005;129:113–121CrossRef
3.
go back to reference Vernon G, Baranova A, Younossi ZM. Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment Pharmacol Ther 2011;34:274–285CrossRef Vernon G, Baranova A, Younossi ZM. Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment Pharmacol Ther 2011;34:274–285CrossRef
4.
go back to reference Ong JP, Pitts A, Younossi ZM. Increased overall mortality and liver-related mortality in non-alcoholic fatty liver disease. J Hepatol 2008;49:608–612CrossRef Ong JP, Pitts A, Younossi ZM. Increased overall mortality and liver-related mortality in non-alcoholic fatty liver disease. J Hepatol 2008;49:608–612CrossRef
5.
go back to reference Huang RC, Beilin LJ, Ayonrinde O, Mori TA, Olynyk JK, Burrows S, et al. Importance of cardiometabolic risk factors in the association between nonalcoholic fatty liver disease and arterial stiffness in adolescents. Hepatology 2013;58:1306–1314CrossRef Huang RC, Beilin LJ, Ayonrinde O, Mori TA, Olynyk JK, Burrows S, et al. Importance of cardiometabolic risk factors in the association between nonalcoholic fatty liver disease and arterial stiffness in adolescents. Hepatology 2013;58:1306–1314CrossRef
6.
go back to reference Salvi P, Ruffini R, Agnoletti D, Magnani E, Comandini G, Praticò A, et al. Increased arterial stiffness in nonalcoholic fatty liver disease: the Cardio-GOOSE study. J Hypertens 2010;28:1699–1707CrossRef Salvi P, Ruffini R, Agnoletti D, Magnani E, Comandini G, Praticò A, et al. Increased arterial stiffness in nonalcoholic fatty liver disease: the Cardio-GOOSE study. J Hypertens 2010;28:1699–1707CrossRef
7.
go back to reference Tarnoki AD, Tarnoki DL, Bata P, Littvay L, Osztovits J, Jermendy G, et al. Heritability of non-alcoholic fatty liver disease and association with abnormal vascular parameters: a twin study. Liver Int 2012;32:1287–1293CrossRef Tarnoki AD, Tarnoki DL, Bata P, Littvay L, Osztovits J, Jermendy G, et al. Heritability of non-alcoholic fatty liver disease and association with abnormal vascular parameters: a twin study. Liver Int 2012;32:1287–1293CrossRef
8.
go back to reference Long MT, Wang N, Larson MG, Mitchell GF, Palmisano J, Vasan RS, et al. Nonalcoholic fatty liver disease and vascular function: cross-sectional analysis in the Framingham heart study. Arterioscler Thromb Vasc Biol 2015;35:1284–1291CrossRef Long MT, Wang N, Larson MG, Mitchell GF, Palmisano J, Vasan RS, et al. Nonalcoholic fatty liver disease and vascular function: cross-sectional analysis in the Framingham heart study. Arterioscler Thromb Vasc Biol 2015;35:1284–1291CrossRef
9.
go back to reference Vlachopoulos C, Manesis E, Baou K, Papatheodoridis G, Koskinas J, Tiniakos D, et al. Increased arterial stiffness and impaired endothelial function in nonalcoholic fatty liver disease: a pilot study. Am J Hypertens 2010;23:83–89 Vlachopoulos C, Manesis E, Baou K, Papatheodoridis G, Koskinas J, Tiniakos D, et al. Increased arterial stiffness and impaired endothelial function in nonalcoholic fatty liver disease: a pilot study. Am J Hypertens 2010;23:83–89
10.
go back to reference Sunbul M, Agirbasli M, Durmus E, Kivrak T, Akin H, Aydin Y, et al. Arterial stiffness in patients with non-alcoholic fatty liver disease is related to fibrosis stage and epicardial adipose tissue thickness. Atherosclerosis 2014;237:490–493CrossRef Sunbul M, Agirbasli M, Durmus E, Kivrak T, Akin H, Aydin Y, et al. Arterial stiffness in patients with non-alcoholic fatty liver disease is related to fibrosis stage and epicardial adipose tissue thickness. Atherosclerosis 2014;237:490–493CrossRef
11.
go back to reference Kim BJ, Kim NH, Kim BS, Kang JH. The association between nonalcoholic fatty liver disease, metabolic syndrome and arterial stiffness in nondiabetic, nonhypertensive individuals. Cardiology 2012;123:54–61CrossRef Kim BJ, Kim NH, Kim BS, Kang JH. The association between nonalcoholic fatty liver disease, metabolic syndrome and arterial stiffness in nondiabetic, nonhypertensive individuals. Cardiology 2012;123:54–61CrossRef
12.
go back to reference Cavalcante JL, Lima JA, Redheuil A, Al-Mallah MH. Aortic stiffness: current understanding and future directions. J Am Coll Cardiol 2011;57:1511–1522CrossRef Cavalcante JL, Lima JA, Redheuil A, Al-Mallah MH. Aortic stiffness: current understanding and future directions. J Am Coll Cardiol 2011;57:1511–1522CrossRef
13.
go back to reference Kim J, Song TJ, Song D, Lee KJ, Kim EH, Lee HS, et al. Brachial-ankle pulse wave velocity is a strong predictor for mortality in patients with acute stroke. Hypertension 2014;64:240–246CrossRef Kim J, Song TJ, Song D, Lee KJ, Kim EH, Lee HS, et al. Brachial-ankle pulse wave velocity is a strong predictor for mortality in patients with acute stroke. Hypertension 2014;64:240–246CrossRef
14.
go back to reference Chirinos JA, Zambrano JP, Chakko S, Veerani A, Schob A, Willens HJ, et al. Aortic pressure augmentation predicts adverse cardiovascular events in patients with established coronary artery disease. Hypertension 2005;45:980–985CrossRef Chirinos JA, Zambrano JP, Chakko S, Veerani A, Schob A, Willens HJ, et al. Aortic pressure augmentation predicts adverse cardiovascular events in patients with established coronary artery disease. Hypertension 2005;45:980–985CrossRef
15.
go back to reference Weber T, Auer J, O’Rourke MF, Kvas E, Lassnig E, Lamm G, et al. Increased arterial wave reflections predict severe cardiovascular events in patients undergoing percutaneous coronary interventions. Eur Heart J 2005;26:2657–2663CrossRef Weber T, Auer J, O’Rourke MF, Kvas E, Lassnig E, Lamm G, et al. Increased arterial wave reflections predict severe cardiovascular events in patients undergoing percutaneous coronary interventions. Eur Heart J 2005;26:2657–2663CrossRef
16.
go back to reference Mitchell GF, Hwang SJ, Vasan RS, Larson MG, Pencina MJ, Hamburg NM, et al. Arterial stiffness and cardiovascular events: the Framingham Heart Study. Circulation 2010;121:505–511CrossRef Mitchell GF, Hwang SJ, Vasan RS, Larson MG, Pencina MJ, Hamburg NM, et al. Arterial stiffness and cardiovascular events: the Framingham Heart Study. Circulation 2010;121:505–511CrossRef
17.
go back to reference Koo BK, Kim D, Joo SK, Kim JH, Chang MS, Kim BG, et al. Sarcopenia is an independent risk factor for non-alcoholic steatohepatitis and significant fibrosis. J Hepatol 2017;66:123–131CrossRef Koo BK, Kim D, Joo SK, Kim JH, Chang MS, Kim BG, et al. Sarcopenia is an independent risk factor for non-alcoholic steatohepatitis and significant fibrosis. J Hepatol 2017;66:123–131CrossRef
18.
go back to reference Sarin SK, Kumar M, Lau GK, Abbas Z, Chan HLY, Chen CJ, et al. Asian-Pacific clinical practice guidelines on the management of hepatitis B: a 2015 update. Hepatol Int 2016;10:1–98CrossRef Sarin SK, Kumar M, Lau GK, Abbas Z, Chan HLY, Chen CJ, et al. Asian-Pacific clinical practice guidelines on the management of hepatitis B: a 2015 update. Hepatol Int 2016;10:1–98CrossRef
19.
go back to reference Organization WH. International Association for the Study of Obesity, International Obesity Taskforce. The Asia-Pacific perspective: redefining obesity and its treatment. 2000:15–21 Organization WH. International Association for the Study of Obesity, International Obesity Taskforce. The Asia-Pacific perspective: redefining obesity and its treatment. 2000:15–21
20.
go back to reference Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, et al. Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation 2005;112:2735–2752CrossRef Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, et al. Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation 2005;112:2735–2752CrossRef
21.
go back to reference Kim D, Kim W, Joo SK, Han J, Kim JH, Harrison SA, et al. Association between body size-metabolic phenotype and nonalcoholic steatohepatitis and significant fibrosis. J Gastroenterol 2020;55:330–341CrossRef Kim D, Kim W, Joo SK, Han J, Kim JH, Harrison SA, et al. Association between body size-metabolic phenotype and nonalcoholic steatohepatitis and significant fibrosis. J Gastroenterol 2020;55:330–341CrossRef
22.
go back to reference Pauca AL, O’Rourke MF, Kon ND. Prospective evaluation of a method for estimating ascending aortic pressure from the radial artery pressure waveform. Hypertension 2001;38:932–937CrossRef Pauca AL, O’Rourke MF, Kon ND. Prospective evaluation of a method for estimating ascending aortic pressure from the radial artery pressure waveform. Hypertension 2001;38:932–937CrossRef
23.
go back to reference Wilkinson IB, MacCallum H, Flint L, Cockcroft JR, Newby DE, Webb DJ. The influence of heart rate on augmentation index and central arterial pressure in humans. J Physiol 2000;525(Pt 1):263–270CrossRef Wilkinson IB, MacCallum H, Flint L, Cockcroft JR, Newby DE, Webb DJ. The influence of heart rate on augmentation index and central arterial pressure in humans. J Physiol 2000;525(Pt 1):263–270CrossRef
24.
go back to reference Brunt EM, Kleiner DE, Wilson LA, Belt P, Neuschwander-Tetri BA. Nonalcoholic fatty liver disease (NAFLD) activity score and the histopathologic diagnosis in NAFLD: distinct clinicopathologic meanings. Hepatology 2011;53:810–820CrossRef Brunt EM, Kleiner DE, Wilson LA, Belt P, Neuschwander-Tetri BA. Nonalcoholic fatty liver disease (NAFLD) activity score and the histopathologic diagnosis in NAFLD: distinct clinicopathologic meanings. Hepatology 2011;53:810–820CrossRef
25.
go back to reference Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 2005;41:1313–1321CrossRef Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 2005;41:1313–1321CrossRef
26.
go back to reference Razek AA, Khashaba M, Abdalla A, Bayomy M, Barakat T. Apparent diffusion coefficient value of hepatic fibrosis and inflammation in children with chronic hepatitis. La Radiol Med 2014;119:903–909CrossRef Razek AA, Khashaba M, Abdalla A, Bayomy M, Barakat T. Apparent diffusion coefficient value of hepatic fibrosis and inflammation in children with chronic hepatitis. La Radiol Med 2014;119:903–909CrossRef
27.
go back to reference Razek AA, Abdalla A, Omran E, Fathy A, Zalata K. Diagnosis and quantification of hepatic fibrosis in children with diffusion weighted MR imaging. Eur J Radiol 2011;78:129–334CrossRef Razek AA, Abdalla A, Omran E, Fathy A, Zalata K. Diagnosis and quantification of hepatic fibrosis in children with diffusion weighted MR imaging. Eur J Radiol 2011;78:129–334CrossRef
28.
go back to reference Ekstedt M, Hagstrom 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;61:1547–1554CrossRef Ekstedt M, Hagstrom 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;61:1547–1554CrossRef
29.
go back to reference Vilar-Gomez E, Calzadilla-Bertot L, Wai-Sun Wong V, Castellanos M, Aller-de la Fuente R, Metwally M, Eslam M, et al. Fibrosis severity as a determinant of cause-specific mortality in patients with advanced nonalcoholic fatty liver disease: a multi-national cohort study. Gastroenterology 2018;155:443–457CrossRef Vilar-Gomez E, Calzadilla-Bertot L, Wai-Sun Wong V, Castellanos M, Aller-de la Fuente R, Metwally M, Eslam M, et al. Fibrosis severity as a determinant of cause-specific mortality in patients with advanced nonalcoholic fatty liver disease: a multi-national cohort study. Gastroenterology 2018;155:443–457CrossRef
30.
go back to reference McEniery CM, Cockcroft JR, Roman MJ, Franklin SS, Wilkinson IB. Central blood pressure: current evidence and clinical importance. Eur Heart J 2014;35:1719–1725CrossRef McEniery CM, Cockcroft JR, Roman MJ, Franklin SS, Wilkinson IB. Central blood pressure: current evidence and clinical importance. Eur Heart J 2014;35:1719–1725CrossRef
31.
go back to reference Shimizu M, Kario K. Role of the augmentation index in hypertension. Ther Adv Cardiovasc Dis 2008;2:25–35CrossRef Shimizu M, Kario K. Role of the augmentation index in hypertension. Ther Adv Cardiovasc Dis 2008;2:25–35CrossRef
32.
go back to reference Sharman JE, Lim R, Qasem AM, Coombes JS, Burgess MI, Franco J, et al. Validation of a generalized transfer function to noninvasively derive central blood pressure during exercise. Hypertension 2006;47:1203–1208CrossRef Sharman JE, Lim R, Qasem AM, Coombes JS, Burgess MI, Franco J, et al. Validation of a generalized transfer function to noninvasively derive central blood pressure during exercise. Hypertension 2006;47:1203–1208CrossRef
33.
go back to reference Leach NV, Dronca E, Vesa SC, Sampelean DP, Craciun EC, Lupsor M, et al. Serum homocysteine levels, oxidative stress and cardiovascular risk in non-alcoholic steatohepatitis. Eur J Intern Med 2014;25:762–767CrossRef Leach NV, Dronca E, Vesa SC, Sampelean DP, Craciun EC, Lupsor M, et al. Serum homocysteine levels, oxidative stress and cardiovascular risk in non-alcoholic steatohepatitis. Eur J Intern Med 2014;25:762–767CrossRef
34.
go back to reference Spahis S, Delvin E, Borys JM, Levy E. Oxidative stress as a critical factor in nonalcoholic fatty liver disease pathogenesis. Antioxid Redox Signal 2017;26:519–541CrossRef Spahis S, Delvin E, Borys JM, Levy E. Oxidative stress as a critical factor in nonalcoholic fatty liver disease pathogenesis. Antioxid Redox Signal 2017;26:519–541CrossRef
Metadata
Title
Association of arterial stiffness with the histological severity of nonalcoholic fatty liver disease
Authors
Hack-Lyoung Kim
Bo Kyung Koo
Sae Kyung Joo
Won Kim
Publication date
01-12-2020
Publisher
Springer India
Keyword
Fatty Liver
Published in
Hepatology International / Issue 6/2020
Print ISSN: 1936-0533
Electronic ISSN: 1936-0541
DOI
https://doi.org/10.1007/s12072-020-10108-z

Other articles of this Issue 6/2020

Hepatology International 6/2020 Go to the issue