Semi-Quantitative Ultrasonographic Evaluation of NAFLD

Author(s): Stefano Ballestri*, Claudio Tana, Maria Di Girolamo, Maria Cristina Fontana, Mariano Capitelli, Amedeo Lonardo, Giorgio Cioni

Journal Name: Current Pharmaceutical Design

Volume 26 , Issue 32 , 2020


Become EABM
Become Reviewer
Call for Editor

Abstract:

Nonalcoholic fatty liver disease (NAFLD) embraces histopathological entities ranging from the relatively benign simple steatosis to the progressive form nonalcoholic steatohepatitis (NASH), which is associated with fibrosis and an increased risk of progression to cirrhosis and hepatocellular carcinoma. NAFLD is the most common liver disease and is associated with extrahepatic comorbidities including a major cardiovascular disease burden.

The non-invasive diagnosis of NAFLD and the identification of subjects at risk of progressive liver disease and cardio-metabolic complications are key in implementing personalized treatment schedules and follow-up strategies.

In this review, we highlight the potential role of ultrasound semiquantitative scores for detecting and assessing steatosis severity, progression of NAFLD, and cardio-metabolic risk.

Ultrasonographic scores of fatty liver severity act as sensors of cardio-metabolic health and may assist in selecting patients to submit to second-line non-invasive imaging techniques and/or liver biopsy.

Keywords: Atherosclerosis, cardiometabolic risk, conventional ultrasound, hepatic fibrosis, hepatic steatosis, liver biopsy, metabolic derangements.

[1]
Ballestri S, Mantovani A, Nascimbeni F, Lugari S, Lonardo A. Extra-hepatic manifestations and complications of NAFLD. Future Med Chem 2019; 11: 2171-92.
[http://dx.doi.org/10.4155/fmc-2019-0003] [PMID: 31538528]
[2]
Nascimbeni F, Ballestri S, Machado MV, et al. Clinical relevance of liver histopathology and different histological classifications of NASH in adults. Expert Rev Gastroenterol Hepatol 2018; 12(4): 351-67.
[http://dx.doi.org/10.1080/17474124.2018.1415756] [PMID: 29224471]
[3]
Lonardo A, Ballestri S, Marchesini G, Angulo P, Loria P. Nonalcoholic fatty liver disease: a precursor of the metabolic syndrome. Dig Liver Dis 2015; 47(3): 181-90.
[http://dx.doi.org/10.1016/j.dld.2014.09.020] [PMID: 25739820]
[4]
Ballestri S, Zona S, Targher G, et al. Nonalcoholic fatty liver disease is associated with an almost twofold increased risk of incident type 2 diabetes and metabolic syndrome. Evidence from a systematic review and meta-analysis. J Gastroenterol Hepatol 2016; 31(5): 936-44.
[http://dx.doi.org/10.1111/jgh.13264] [PMID: 26667191]
[5]
Mantovani A, Byrne CD, Bonora E, Targher G. Nonalcoholic Fatty liver disease and risk of incident type 2 diabetes: a meta-analysis. Diabetes Care 2018; 41(2): 372-82.
[http://dx.doi.org/10.2337/dc17-1902] [PMID: 29358469]
[6]
Ballestri S, Lonardo A, Bonapace S, Byrne CD, Loria P, Targher G. Risk of cardiovascular, cardiac and arrhythmic complications in patients with non-alcoholic fatty liver disease. World J Gastroenterol 2014; 20(7): 1724-45.
[http://dx.doi.org/10.3748/wjg.v20.i7.1724] [PMID: 24587651]
[7]
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.
[http://dx.doi.org/10.1016/j.jhep.2016.05.013] [PMID: 27212244]
[8]
Stahl EP, Dhindsa DS, Lee SK, Sandesara PB, Chalasani NP, Sperling LS. Nonalcoholic Fatty liver disease and the heart: JACC state-of-the-art review. J Am Coll Cardiol 2019; 73(8): 948-63.
[http://dx.doi.org/10.1016/j.jacc.2018.11.050] [PMID: 30819364]
[9]
Tana C, Ballestri S, Ricci F, et al. Cardiovascular risk in non-alcoholic fatty liver disease: mechanisms and therapeutic implications. Int J Environ Res Public Health 2019; 16(17): 3104.
[http://dx.doi.org/10.3390/ijerph16173104] [PMID: 31455011]
[10]
Lonardo A, Bellentani S, et al. Non-alcoholic fatty liver disease (NAFLD) study group. Epidemiological modifiers of non-alcoholic fatty liver disease: Focus on high-risk groups. Dig Liver Dis 2015; 47: 997-1006.
[11]
Machado MV, Cortez-Pinto H. Non-invasive diagnosis of non-alcoholic fatty liver disease. A critical appraisal. J Hepatol 2013; 58(5): 1007-19.
[http://dx.doi.org/10.1016/j.jhep.2012.11.021] [PMID: 23183525]
[12]
Castera L, Friedrich-Rust M, Loomba R. Noninvasive assessment of liver disease in patients with nonalcoholic fatty liver disease. Gastroenterology 2019; 156(5): 1264-81.e4.
[http://dx.doi.org/10.1053/j.gastro.2018.12.036] [PMID: 30660725]
[13]
Ballestri S, Nascimbeni F, Lugari S, Lonardo A, Francica G. A critical appraisal of the use of ultrasound in hepatic steatosis. Expert Rev Gastroenterol Hepatol 2019; 13(7): 667-81.
[http://dx.doi.org/10.1080/17474124.2019.1621164] [PMID: 31104523]
[14]
Hamaguchi M, Kojima T, Itoh Y, et al. The severity of ultrasonographic findings in nonalcoholic fatty liver disease reflects the metabolic syndrome and visceral fat accumulation. Am J Gastroenterol 2007; 102(12): 2708-15.
[http://dx.doi.org/10.1111/j.1572-0241.2007.01526.x] [PMID: 17894848]
[15]
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): 2139-46.
[http://dx.doi.org/10.1111/liv.12840] [PMID: 25847730]
[16]
Ballestri S, Nascimbeni F, Baldelli E, et al. Ultrasonographic fatty liver indicator detects mild steatosis and correlates with metabolic/histological parameters in various liver diseases. Metabolism 2017; 72: 57-65.
[http://dx.doi.org/10.1016/j.metabol.2017.04.003] [PMID: 28641784]
[17]
Liang RJ, Wang HH, Lee WJ, Liew PL, Lin JT, Wu MS. Diagnostic value of ultrasonographic examination for nonalcoholic steatohepatitis in morbidly obese patients undergoing laparoscopic bariatric surgery. Obes Surg 2007; 17(1): 45-56.
[http://dx.doi.org/10.1007/s11695-007-9005-6] [PMID: 17355768]
[18]
Ballestri S, Lonardo A, Romagnoli D, et al. Ultrasonographic fatty liver indicator, a novel score which rules out NASH and is correlated with metabolic parameters in NAFLD. Liver Int 2012; 32(8): 1242-52.
[http://dx.doi.org/10.1111/j.1478-3231.2012.02804.x] [PMID: 22520641]
[19]
Ballestri S, Romagnoli D, Nascimbeni F, Francica G, Lonardo A. Role of ultrasound in the diagnosis and treatment of nonalcoholic fatty liver disease and its complications. Expert Rev Gastroenterol Hepatol 2015; 9(5): 603-27.
[http://dx.doi.org/10.1586/17474124.2015.1007955] [PMID: 25694178]
[20]
Zhang YN, Fowler KJ, Hamilton G, et al. Liver fat imaging-a clinical overview of ultrasound, CT, and MR imaging. Br J Radiol 2018; 91(1089)20170959
[http://dx.doi.org/10.1259/bjr.20170959] [PMID: 29722568]
[21]
van Werven JR, Marsman HA, Nederveen AJ, et al. Assessment of hepatic steatosis in patients undergoing liver resection: comparison of US, CT, T1-weighted dual-echo MR imaging, and point-resolved 1H MR spectroscopy. Radiology 2010; 256(1): 159-68.
[http://dx.doi.org/10.1148/radiol.10091790] [PMID: 20574093]
[22]
Saadeh S, Younossi ZM, Remer EM, et al. The utility of radiological imaging in nonalcoholic fatty liver disease. Gastroenterology 2002; 123(3): 745-50.
[http://dx.doi.org/10.1053/gast.2002.35354] [PMID: 12198701]
[23]
Dasarathy S, Dasarathy J, Khiyami A, Joseph R, Lopez R, McCullough AJ. Validity of real time ultrasound in the diagnosis of hepatic steatosis: a prospective study. J Hepatol 2009; 51(6): 1061-7.
[http://dx.doi.org/10.1016/j.jhep.2009.09.001] [PMID: 19846234]
[24]
Hernaez R, Lazo M, Bonekamp S, et al. Diagnostic accuracy and reliability of ultrasonography for the detection of fatty liver: a meta-analysis. Hepatology 2011; 54(3): 1082-90.
[http://dx.doi.org/10.1002/hep.24452] [PMID: 21618575]
[25]
Karlas T, Petroff D, Sasso M, et al. Individual patient data meta-analysis of controlled attenuation parameter (CAP) technology for assessing steatosis. J Hepatol 2017; 66(5): 1022-30.
[http://dx.doi.org/10.1016/j.jhep.2016.12.022] [PMID: 28039099]
[26]
Pu K, Wang Y, Bai S, et al. Diagnostic accuracy of controlled attenuation parameter (CAP) as a non-invasive test for steatosis in suspected non-alcoholic fatty liver disease: a systematic review and meta-analysis. BMC Gastroenterol 2019; 19(1): 51.
[http://dx.doi.org/10.1186/s12876-019-0961-9] [PMID: 30961539]
[27]
Ferraioli G, Tinelli C, De Silvestri A, et al. The clinical value of controlled attenuation parameter for the noninvasive assessment of liver steatosis. Liver Int 2016; 36(12): 1860-6.
[http://dx.doi.org/10.1111/liv.13207] [PMID: 27439331]
[28]
Mathiesen UL, Franzén LE, Aselius H, et al. Increased liver echogenicity at ultrasound examination reflects degree of steatosis but not of fibrosis in asymptomatic patients with mild/moderate abnormalities of liver transaminases. Dig Liver Dis 2002; 34(7): 516-22.
[http://dx.doi.org/10.1016/S1590-8658(02)80111-6] [PMID: 12236486]
[29]
Palmentieri B, de Sio I, La Mura V, et al. The role of bright liver echo pattern on ultrasound B-mode examination in the diagnosis of liver steatosis. Dig Liver Dis 2006; 38(7): 485-9.
[http://dx.doi.org/10.1016/j.dld.2006.03.021] [PMID: 16716779]
[30]
Xu L, Lu W, Li P, Shen F, Mi YQ, Fan JG. A comparison of hepatic steatosis index, controlled attenuation parameter and ultrasound as noninvasive diagnostic tools for steatosis in chronic hepatitis B. Dig Liver Dis 2017; 49(8): 910-7.
[http://dx.doi.org/10.1016/j.dld.2017.03.013] [PMID: 28433586]
[31]
Paige JS, Bernstein GS, Heba E, et al. A pilot comparative study of quantitative ultrasound, conventional ultrasound, and MRI for predicting histology-determined steatosis grade in adult nonalcoholic fatty liver disease. AJR Am J Roentgenol 2017; 208(5)W168-77
[http://dx.doi.org/10.2214/AJR.16.16726] [PMID: 28267360]
[32]
Zardi EM, De Sio I, Ghittoni G, et al. Which clinical and sonographic parameters may be useful to discriminate NASH from steatosis? J Clin Gastroenterol 2011; 45(1): 59-63.
[http://dx.doi.org/10.1097/MCG.0b013e3181dc25e3] [PMID: 20502351]
[33]
Nelson SM, Hoskins JD, Lisanti C, Chaudhuri J. Ultrasound fatty liver indicator: a simple tool for differentiating steatosis from nonalcoholic steatohepatitis: validity in the average obese population. J Ultrasound Med 2019. Epub ahead of print
[http://dx.doi.org/10.1002/jum.15154] [PMID: 31647137]
[34]
Liu HK, Yang MC, Su YT, et al. Novel ultrasonographic fatty liver indicator can predict hepatitis in children with non-alcoholic fatty liver disease. Front Pediatr 2019; 6: 416.
[http://dx.doi.org/10.3389/fped.2018.00416] [PMID: 30671426]
[35]
García-Monzón C, Vargas-Castrillón J, Porrero JL, et al. Prevalence and risk factors for biopsy-proven non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in a prospective cohort of adult patients with gallstones. Liver Int 2015; 35(8): 1983-91.
[http://dx.doi.org/10.1111/liv.12813] [PMID: 25708133]
[36]
Costa-Silva L, Ferolla SM, Lima AS, Vidigal PVT, Ferrari TCA. MR elastography is effective for the non-invasive evaluation of fibrosis and necroinflammatory activity in patients with nonalcoholic fatty liver disease. Eur J Radiol 2018; 98: 82-9.
[http://dx.doi.org/10.1016/j.ejrad.2017.11.003] [PMID: 29279175]
[37]
Siddiqui MS, Vuppalanchi R, Van Natta ML, et al. NASH Clinical Research Network. Vibration-controlled transient elastography to assess fibrosis and steatosis in patients with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 2019; 17(1): 156-163.e2.
[http://dx.doi.org/10.1016/j.cgh.2018.04.043] [PMID: 29705261]
[38]
Besutti G, Valenti L, Ligabue G, et al. Accuracy of imaging methods for steatohepatitis diagnosis in non-alcoholic fatty liver disease patients: A systematic review. Liver Int 2019; 39(8): 1521-34.
[http://dx.doi.org/10.1111/liv.14118] [PMID: 30972903]
[39]
Berzigotti A, Castera L. Update on ultrasound imaging of liver fibrosis. J Hepatol 2013; 59(1): 180-2.
[http://dx.doi.org/10.1016/j.jhep.2012.12.028] [PMID: 23333447]
[40]
Berzigotti A, Piscaglia F. EFSUMB Education and Professional Standards Committee. Ultrasound in portal hypertension--part 2--and EFSUMB recommendations for the performance and reporting of ultrasound examinations in portal hypertension. Ultraschall Med 2012; 33(1): 8-32.
[PMID: 22322479]
[41]
Tana C, Tana M, Rossi S, Silingardi M, Schiavone C. Hepatic artery resistive index (HARI) and non-alcoholic fatty liver disease (NAFLD) fibrosis score in NAFLD patients: cut-off suggestive of non-alcoholic steatohepatitis (NASH) evolution. J Ultrasound 2016; 19(3): 183-9.
[http://dx.doi.org/10.1007/s40477-016-0203-8] [PMID: 27635163]
[42]
Tana C, Schiavone C, Ticinesi A, et al. Hepatic artery resistive index as surrogate marker for fibrosis progression in NAFLD patients: A clinical perspective. Int J Immunopathol Pharmacol 2018; 322058738418781373
[http://dx.doi.org/10.1177/2058738418781373] [PMID: 29873275]
[43]
Jiang W, Huang S, Teng H, et al. Diagnostic accuracy of point shear wave elastography and transient elastography for staging hepatic fibrosis in patients with non-alcoholic fatty liver disease: a meta-analysis. BMJ Open 2018; 8(8) e021787
[http://dx.doi.org/10.1136/bmjopen-2018-021787] [PMID: 30139901]
[44]
Herrmann E, de Lédinghen V, Cassinotto C, et al. Assessment of biopsy-proven liver fibrosis by two-dimensional shear wave elastography: An individual patient data-based meta-analysis. Hepatology 2018; 67(1): 260-72.
[http://dx.doi.org/10.1002/hep.29179] [PMID: 28370257]
[45]
Ferraioli G, Wong VW, Castera L, et al. Liver ultrasound elastography: an update to the world federation for ultrasound in medicine and biology guidelines and recommendations. Ultrasound Med Biol 2018; 44(12): 2419-40.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2018.07.008] [PMID: 30209008]
[46]
Eddowes PJ, Sasso M, Allison M, et al. Accuracy of fibroscan controlled attenuation parameter and liver stiffness measurement in assessing steatosis and fibrosis in patients with nonalcoholic fatty liver disease. Gastroenterology 2019; 156(6): 1717-30.
[http://dx.doi.org/10.1053/j.gastro.2019.01.042] [PMID: 30689971]
[47]
Berzigotti A, Ferraioli G, Bota S, Gilja OH, Dietrich CF. Novel ultrasound-based methods to assess liver disease: The game has just begun. Dig Liver Dis 2018; 50(2): 107-12.
[http://dx.doi.org/10.1016/j.dld.2017.11.019] [PMID: 29258813]
[48]
Berzigotti A. Non-invasive evaluation of portal hypertension using ultrasound elastography. J Hepatol 2017; 67(2): 399-411.
[http://dx.doi.org/10.1016/j.jhep.2017.02.003] [PMID: 28223101]
[49]
Park CC, Nguyen P, Hernandez C, et al. Magnetic resonance elastography vs transient elastography in detection of fibrosis and noninvasive measurement of steatosis in patients with biopsy-proven nonalcoholic fatty liver disease. Gastroenterology 2017; 152(3): 598-607.e2.
[http://dx.doi.org/10.1053/j.gastro.2016.10.026] [PMID: 27911262]
[50]
Wang CC, Tseng TC, Hsieh TC, et al. Severity of fatty liver on ultrasound correlates with metabolic and cardiovascular risk. Kaohsiung J Med Sci 2012; 28(3): 151-60.
[http://dx.doi.org/10.1016/j.kjms.2011.10.005] [PMID: 22385608]
[51]
Cuenza LR, Razon TLJ, Dayrit JC. Correlation between severity of ultrasonographic nonalcoholic fatty liver disease and cardiometabolic risk among Filipino wellness patients. J Cardiovasc Thorac Res 2017; 9(2): 85-9.
[http://dx.doi.org/10.15171/jcvtr.2017.14] [PMID: 28740627]
[52]
Mustapic S, Ziga S, Matic V, et al. Ultrasound grade of liver steatosis is independently associated with the risk of metabolic syndrome. Can J Gastroenterol Hepatol 2018; 20188490242
[http://dx.doi.org/10.1155/2018/8490242] [PMID: 30211140]
[53]
Liao YY, Yang KC, Lee MJ, Huang KC, Chen JD, Yeh CK. Multifeature analysis of an ultrasound quantitative diagnostic index for classifying nonalcoholic fatty liver disease. Sci Rep 2016; 6: 35083.
[http://dx.doi.org/10.1038/srep35083] [PMID: 27734972]
[54]
Liao YY, Yeh CK, Huang KC, Tsui PH, Yang KC. Metabolic characteristics of a novel ultrasound quantitative diagnostic index for nonalcoholic fatty liver disease. Sci Rep 2019; 9(1): 7922.
[http://dx.doi.org/10.1038/s41598-019-44453-3] [PMID: 31138858]
[55]
Lin YH, Liao YY, Yeh CK, Yang KC, Tsui PH. Ultrasound entropy imaging of nonalcoholic fatty liver disease: association with metabolic syndrome. Entropy (Basel) 2018; 20: 893.
[http://dx.doi.org/10.3390/e20120893]
[56]
Ballestri S, Nascimbeni F, Baldelli E, Marrazzo A, Romagnoli D, Lonardo A. NAFLD as a sexual dimorphic disease: role of gender and reproductive status in the development and progression of nonalcoholic fatty liver disease and inherent cardiovascular risk. Adv Ther 2017; 34(6): 1291-326.
[http://dx.doi.org/10.1007/s12325-017-0556-1] [PMID: 28526997]
[57]
Lonardo A, Nascimbeni F, Ballestri S, et al. Sex differences in nonalcoholic fatty liver disease: state of the art and identification of research gaps. Hepatology 2019; 70(4): 1457-69.
[http://dx.doi.org/10.1002/hep.30626] [PMID: 30924946]
[58]
Cicero AF, D’Addato S, Reggi A, Marchesini G, Borghi C. Brisighella Heart Study. Gender difference in hepatic steatosis index and lipid accumulation product ability to predict incident metabolic syndrome in the historical cohort of the Brisighella Heart Study. Metab Syndr Relat Disord 2013; 11(6): 412-6.
[http://dx.doi.org/10.1089/met.2012.0147] [PMID: 23902132]
[59]
Oni ET, Agatston AS, Blaha MJ, et al. A systematic review: burden and severity of subclinical cardiovascular disease among those with nonalcoholic fatty liver; should we care? Atherosclerosis 2013; 230(2): 258-67.
[http://dx.doi.org/10.1016/j.atherosclerosis.2013.07.052] [PMID: 24075754]
[60]
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.
[http://dx.doi.org/10.1097/MEG.0000000000000429] [PMID: 26193052]
[61]
Fan Y, Wei F, Zhou Y, Zhang H. Association of non-alcoholic fatty liver disease with impaired endothelial function by flow-mediated dilation: A meta-analysis. Hepatol Res 2016; 46(3): E165-73.
[http://dx.doi.org/10.1111/hepr.12554] [PMID: 26179110]
[62]
Kapuria D, Takyar VK, Etzion O, Surana P, O’Keefe JH, Koh C. Association of hepatic steatosis with subclinical atherosclerosis: systematic review and meta-analysis. Hepatol Commun 2018; 2(8): 873-83.
[http://dx.doi.org/10.1002/hep4.1199] [PMID: 30094399]
[63]
Lee SB, Park GM, Lee JY, et al. Association between non-alcoholic fatty liver disease and subclinical coronary atherosclerosis: An observational cohort study. J Hepatol 2018; 68(5): 1018-24.
[http://dx.doi.org/10.1016/j.jhep.2017.12.012] [PMID: 29274406]
[64]
Lee YH, Wu YJ, Liu CC, et al. The severity of Fatty liver disease relating to metabolic abnormalities independently predicts coronary calcification. Radiol Res Pract 2011; 2011586785
[http://dx.doi.org/10.1155/2011/586785] [PMID: 22254139]
[65]
Kim MK, Ahn CW, Nam JS, Kang S, Park JS, Kim KR. Association between nonalcoholic fatty liver disease and coronary artery calcification in postmenopausal women. Menopause 2015; 22(12): 1323-7.
[http://dx.doi.org/10.1097/GME.0000000000000503] [PMID: 26154274]
[66]
Park HE, Kwak MS, Kim D, Kim MK, Cha MJ, Choi SY. Nonalcoholic fatty liver disease is associated with coronary artery calcification development: a longitudinal study. J Clin Endocrinol Metab 2016; 101(8): 3134-43.
[http://dx.doi.org/10.1210/jc.2016-1525] [PMID: 27253666]
[67]
Açikel M, Sunay S, Koplay M, Gündoğdu F, Karakelleoğlu S. Evaluation of ultrasonographic fatty liver and severity of coronary atherosclerosis, and obesity in patients undergoing coronary angiography. Anadolu Kardiyol Derg 2009; 9(4): 273-9.
[PMID: 19666428]
[68]
Inci MF, Özkan F, Ark B, et al. Sonographic evaluation for predicting the presence and severity of coronary artery disease. Ultrasound Q 2013; 29(2): 125-30.
[http://dx.doi.org/10.1097/RUQ.0b013e318291580e] [PMID: 23609339]
[69]
Choi DH, Lee SJ, Kang CD, et al. Nonalcoholic fatty liver disease is associated with coronary artery disease in Koreans. World J Gastroenterol 2013; 19(38): 6453-7.
[http://dx.doi.org/10.3748/wjg.v19.i38.6453] [PMID: 24151364]
[70]
Boddi M, Tarquini R, Chiostri M, et al. Nonalcoholic fatty liver in nondiabetic patients with acute coronary syndromes. Eur J Clin Invest 2013; 43(5): 429-38.
[http://dx.doi.org/10.1111/eci.12065] [PMID: 23480577]
[71]
Langroudi TF, Haybar H, Parsa SA, Mahjoorian M, Khaheshi I, Naderian M. The severity of coronary artery disease was not associated with non-alcoholic fatty liver disease in a series of 264 non-diabetic patients who underwent coronary angiography. Rom J Intern Med 2018; 56(3): 167-72.
[http://dx.doi.org/10.2478/rjim-2018-0009] [PMID: 29561732]
[72]
Song Y, Dang Y, Wang P, Tian G, Ruan L. CHD is associated with higher grades of NAFLD predicted by liver stiffness. J Clin Gastroenterol 2020; 54(3): 271-7.
[http://dx.doi.org/10.1097/MCG.0000000000001238] [PMID: 31305280]
[73]
Pisto P, Santaniemi M, Bloigu R, Ukkola O, Kesäniemi YA. Fatty liver predicts the risk for cardiovascular events in middle-aged population: a population-based cohort study. BMJ Open 2014; 4(3)e004973
[http://dx.doi.org/10.1136/bmjopen-2014-004973] [PMID: 24650811]
[74]
Emre A, Terzi S, Celiker E, et al. Impact of nonalcoholic fatty liver disease on myocardial perfusion in nondiabetic patients undergoing primary percutaneous coronary intervention for ST-segment elevation myocardial infarction. Am J Cardiol 2015; 116(12): 1810-4.
[http://dx.doi.org/10.1016/j.amjcard.2015.09.021] [PMID: 26506122]
[75]
Pacifico L, Cantisani V, Ricci P, et al. Nonalcoholic fatty liver disease and carotid atherosclerosis in children. Pediatr Res 2008; 63(4): 423-7.
[http://dx.doi.org/10.1203/PDR.0b013e318165b8e7] [PMID: 18356751]
[76]
Mohammadi A, Bazazi A, Maleki-Miyandoab T, Ghasemi-Rad M. Evaluation of relationship between grading of fatty liver and severity of atherosclerotic finding. Int J Clin Exp Med 2012; 5(3): 251-6.
[PMID: 22837800]
[77]
Rasool A, Dar W, Latief M, Dar I, Sofi N, Khan MA. Nonalcoholic fatty liver disease as an independent risk factor for carotid atherosclerosis. Brain Circ 2017; 3(1): 35-40.
[PMID: 30276302]
[78]
Lee JE, Lee YJ, Chung SY, Cho HW, Park BJ, Jung DH. Severity of nonalcoholic fatty liver disease is associated with subclinical cerebro-cardiovascular atherosclerosis risk in Korean men. PLoS One 2018; 13(3) e0193191
[http://dx.doi.org/10.1371/journal.pone.0193191] [PMID: 29565984]
[79]
Fracanzani AL, Tiraboschi S, Pisano G, 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.
[http://dx.doi.org/10.1016/j.atherosclerosis.2016.01.016] [PMID: 26803429]
[80]
Golabi P, Stepanova M, Pham HT, et al. Non-alcoholic steatofibrosis (NASF) can independently predict mortality in patients with non-alcoholic fatty liver disease (NAFLD). BMJ Open Gastroenterol 2018; 5(1)e000198
[http://dx.doi.org/10.1136/bmjgast-2018-000198] [PMID: 29607054]
[81]
Liu HH, Cao YX, Sun D, et al. Impact of Non-alcoholic fatty liver disease on cardiovascular outcomes in patients with stable coronary artery disease: A matched case-control study. Clin Transl Gastroenterol 2019; 10(2)e00011
[http://dx.doi.org/10.14309/ctg.0000000000000011] [PMID: 30829918]
[82]
Alkagiet S, Papagiannis A, Tziomalos K. Associations between nonalcoholic fatty liver disease and ischemic stroke. World J Hepatol 2018; 10(7): 474-8.
[http://dx.doi.org/10.4254/wjh.v10.i7.474] [PMID: 30079133]
[83]
Li H, Hu B, Wei L, et al. Non-alcoholic fatty liver disease is associated with stroke severity and progression of brainstem infarctions. Eur J Neurol 2018; 25(3): 577-e34.
[http://dx.doi.org/10.1111/ene.13556] [PMID: 29281159]
[84]
Mangla N, Ajmera VH, Caussy C, et al. Liver stiffness severity is associated with increased cardiovascular risk in patients with type 2 diabetes. Clin Gastroenterol Hepatol 2020; 18(3): 744-6.e1.
[http://dx.doi.org/10.1016/j.cgh.2019.05.003] [PMID: 31100460]
[85]
Nascimbeni F, Romagnoli D, Ballestri S, et al. Do nonalcoholic fatty liver disease and fetuin-a play different roles in symptomatic coronary artery disease and peripheral arterial disease? Diseases 2018; 6(1)E17
[http://dx.doi.org/10.3390/diseases6010017] [PMID: 29462898]
[86]
Zou Y, Li X, Wang C, et al. Association between non-alcoholic fatty liver disease and peripheral artery disease in patients with type 2 diabetes. Intern Med J 2017; 47(10): 1147-53.
[http://dx.doi.org/10.1111/imj.13549] [PMID: 28696562]
[87]
Mantovani A, Pernigo M, Bergamini C, et al. Nonalcoholic fatty liver disease is independently associated with early left ventricular diastolic dysfunction in patients with type 2 diabetes. PLoS One 2015; 10(8)e0135329
[http://dx.doi.org/10.1371/journal.pone.0135329] [PMID: 26252899]
[88]
Jung JY, Park SK, Ryoo JH, et al. Effect of non-alcoholic fatty liver disease on left ventricular diastolic function and geometry in the Korean general population. Hepatol Res 2017; 47(6): 522-32.
[http://dx.doi.org/10.1111/hepr.12770] [PMID: 27379875]
[89]
Wang Q, Ma W, Xia J. Nonalcoholic Fatty liver is associated with further left ventricular abnormalities in patients with type 2 diabetes mellitus: a 3-dimensional speckle-tracking study. J Ultrasound Med 2018; 37(8): 1899-911.
[http://dx.doi.org/10.1002/jum.14536] [PMID: 29363154]
[90]
Patel J, Bettencourt R, Cui J, et al. Association of noninvasive quantitative decline in liver fat content on MRI with histologic response in nonalcoholic steatohepatitis. Therap Adv Gastroenterol 2016; 9(5): 692-701.
[http://dx.doi.org/10.1177/1756283X16656735] [PMID: 27582882]
[91]
Ajmera V, Park CC, Caussy C, et al. Magnetic resonance imaging proton density fat fraction associates with progression of fibrosis in patients with non-alcoholic fatty liver disease. Gastroenterology 2018; 155(2): 307-310.e2.
[http://dx.doi.org/10.1053/j.gastro.2018.04.014] [PMID: 29660324]
[92]
Kim M, Kang BK, Jun DW. Comparison of conventional sonographic signs and magnetic resonance imaging proton density fat fraction for assessment of hepatic steatosis. Sci Rep 2018; 8(1): 7759.
[http://dx.doi.org/10.1038/s41598-018-26019-x] [PMID: 29773823]
[93]
De Lucia Rolfe E, Brage S, Sleigh A, et al. Validity of ultrasonography to assess hepatic steatosis compared to magnetic resonance spectroscopy as a criterion method in older adults. PLoS One 2018; 13(11) e0207923
[http://dx.doi.org/10.1371/journal.pone.0207923] [PMID: 30475885]
[94]
Lonardo A, Lugari S, Ballestri S, Nascimbeni F, Baldelli E, Maurantonio M. A round trip from nonalcoholic fatty liver disease to diabetes: molecular targets to the rescue? Acta Diabetol 2019; 56(4): 385-96.
[http://dx.doi.org/10.1007/s00592-018-1266-0] [PMID: 30519965]
[95]
Cho HJ, Hwang S, Park JI, et al. Improvement of nonalcoholic fatty liver disease reduces the risk of type 2 diabetes mellitus. Gut Liver 2019; 13(4): 440-9.
[http://dx.doi.org/10.5009/gnl18382] [PMID: 30970431]
[96]
Heo NY. Nonalcoholic fatty liver disease is a stepping stone in the path toward diabetes mellitus. Gut Liver 2019; 13(4): 383-4.
[http://dx.doi.org/10.5009/gnl19192] [PMID: 31284360]
[97]
Gelli C, Tarocchi M, Abenavoli L, Di Renzo L, Galli A, De Lorenzo A. Effect of a counseling-supported treatment with the Mediterranean diet and physical activity on the severity of the non-alcoholic fatty liver disease. World J Gastroenterol 2017; 23(17): 3150-62.
[http://dx.doi.org/10.3748/wjg.v23.i17.3150] [PMID: 28533672]
[98]
Misciagna G, Del Pilar Díaz M, Caramia DV, et al. Effect of a Low glycemic index mediterranean diet on non-alcoholic fatty liver disease. a randomized controlled clinici trial. J Nutr Health Aging 2017; 21(4): 404-12.
[http://dx.doi.org/10.1007/s12603-016-0809-8] [PMID: 28346567]
[99]
Anania C, Perla FM, Olivero F, Pacifico L, Chiesa C. Mediterranean diet and nonalcoholic fatty liver disease. World J Gastroenterol 2018; 24(19): 2083-94.
[http://dx.doi.org/10.3748/wjg.v24.i19.2083] [PMID: 29785077]
[100]
Scaglioni F, Marino M, Ciccia S, et al. Short-term multidisciplinary non-pharmacological intervention is effective in reducing liver fat content assessed non-invasively in patients with nonalcoholic fatty liver disease (NAFLD). Clin Res Hepatol Gastroenterol 2013; 37(4): 353-8.
[http://dx.doi.org/10.1016/j.clinre.2012.10.009] [PMID: 23273500]
[101]
Paul J, Venugopal RV, Peter L, Shetty KNK, Shetti MP. Measurement of controlled attenuation parameter: a surrogate marker of hepatic steatosis in patients of nonalcoholic fatty liver disease on lifestyle modification - a prospective follow-up study. Arq Gastroenterol 2018; 55(1): 7-13.
[http://dx.doi.org/10.1590/s0004-2803.201800000-07] [PMID: 29561981]
[102]
Bhatia L, Scorletti E, Curzen N, Clough GF, Calder PC, Byrne CD. Improvement in non-alcoholic fatty liver disease severity is associated with a reduction in carotid intima-media thickness progression. Atherosclerosis 2016; 246: 13-20.
[http://dx.doi.org/10.1016/j.atherosclerosis.2015.12.028] [PMID: 26748347]
[103]
Clemente MG, Mandato C, Poeta M, Vajro P. Pediatric non-alcoholic fatty liver disease: Recent solutions, unresolved issues, and future research directions. World J Gastroenterol 2016; 22(36): 8078-93.
[http://dx.doi.org/10.3748/wjg.v22.i36.8078] [PMID: 27688650]
[104]
Vos MB, Abrams SH, Barlow SE, et al. NASPGHAN Clinical Practice Guideline for the Diagnosis and Treatment of Nonalcoholic Fatty Liver Disease in Children: Recommendations from the Expert Committee on NAFLD (ECON) and the North American Society of Pediatric Gastroenterology, Hepatology and Nutrition (NASPGHAN). J Pediatr Gastroenterol Nutr 2017; 64(2): 319-34.
[http://dx.doi.org/10.1097/MPG.0000000000001482] [PMID: 28107283]
[105]
Fitzpatrick E, Dhawan A. Childhood and adolescent nonalcoholic fatty liver disease: is it different from adults? J Clin Exp Hepatol 2019; 9(6): 716-22.
[http://dx.doi.org/10.1016/j.jceh.2019.05.005] [PMID: 31889753]
[106]
Chiloiro M, Riezzo G, Chiarappa S, et al. Relationship among fatty liver, adipose tissue distribution and metabolic profile in moderately obese children: an ultrasonographic study. Curr Pharm Des 2008; 14(26): 2693-8.
[http://dx.doi.org/10.2174/138161208786264197] [PMID: 18991688]
[107]
Shannon A, Alkhouri N, Carter-Kent C, et al. Ultrasonographic quantitative estimation of hepatic steatosis in children With NAFLD. J Pediatr Gastroenterol Nutr 2011; 53(2): 190-5.
[http://dx.doi.org/10.1097/MPG.0b013e31821b4b61] [PMID: 21788761]
[108]
Kang BK, Kim M, Shin SJ, Kim YJ. Correlation of clinical and histopathologic parameters with ultrasonographic grades in pediatric non-alcoholic fatty liver disease. J Korean Med Sci 2019; 34(47)e298
[http://dx.doi.org/10.3346/jkms.2019.34.e298] [PMID: 31808322]
[109]
Bonci E, Chiesa C, Versacci P, Anania C, Silvestri L, Pacifico L. Association of nonalcoholic fatty liver disease with subclinical cardiovascular changes: A systematic review and meta-analysis. BioMed Res Int 2015; 2015213737
[http://dx.doi.org/10.1155/2015/213737] [PMID: 26273598]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 26
ISSUE: 32
Year: 2020
Published on: 23 September, 2020
Page: [3915 - 3927]
Pages: 13
DOI: 10.2174/1381612826666200417142444
Price: $65

Article Metrics

PDF: 20
HTML: 4
EPUB: 1