Noninvasive Quantitative Detection Methods of Liver Fat Content in Nonalcoholic Fatty Liver Disease

Shujing Lv, Sushan Jiang, Shousheng Liu, Quanjiang Dong, Yongning Xin, Shiying Xuan, Shujing Lv, Sushan Jiang, Shousheng Liu, Quanjiang Dong, Yongning Xin, Shiying Xuan

Abstract

Nonalcoholic fatty liver disease (NAFLD) ranges from simple steatosis to NAFLD-related liver cirrhosis and is a main cause of chronic liver diseases. Patients with nonalcoholic steatohepatitis and fibrosis are at a great risk of the progression to cirrhosis or hepatocellular carcinoma, both of which are tightly associated with liver-related mortality. Liver biopsy is still the gold standard for the diagnosis of NAFLD, but some defects, such as serious complications, sampling error and variability in histologic evaluation among pathologists, remain problematic. Therefore, noninvasive, repeatable and accurate diagnostic methods are urgently needed. Ultrasonography is a well-established and lower-cost imaging technique for the diagnosis of hepatic steatosis, especially suitable for population census, but limited by its low sensitivity to diagnose mild steatosis and being highly operator-dependent. Computed tomography also lacks the sensitivity to detect mild steatosis and small changes in fat content, and presents a potential radiation hazard. Controlled attenuation parameter based on the FibroScan® technology is a promising tool for noninvasive semiquantitative assessment of liver fat content, but the accuracy rate depends on the operator's expertise and is affected by age, width of the intercostal space, skin capsular distance and body mass index. Magnetic resonance imaging and magnetic resonance spectroscopy are regarded as the most accurate quantitative methods for measuring liver fat content in clinical practice, especially for longitudinal follow up of NAFLD patients. In this review, we mainly introduce the current imaging methods that are in use for evaluation of liver fat content and we discuss the advantages and disadvantages of each method.

Keywords: Hydrogen-1 magnetic resonance spectroscopy; Liver fat content; Nonalcoholic fatty liver disease; Noninvasive.

Conflict of interest statement

The authors have no conflict of interests related to this publication.

References

    1. Hannah WN, Jr, Harrison SA. Noninvasive imaging methods to determine severity of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis. Hepatology. 2016;64:2234–2243. doi: .
    1. Imajo K, Kessoku T, Honda Y, Tomeno W, Ogawa Y, Mawatari H, et al. Magnetic resonance imaging more accurately classifies steatosis and fibrosis in patients with nonalcoholic fatty liver disease than transient elastography. Gastroenterology. 2016;150:626–637.e7. doi: .
    1. Bazick J, Donithan M, Neuschwander-Tetri BA, Kleiner D, Brunt EM, Wilson L, et al. Clinical model for NASH and advanced fibrosis in adult patients with diabetes and NAFLD: Guidelines for referral in NAFLD. Diabetes Care. 2015;38:1347–1355. doi: .
    1. Deng J, Fishbein MH, Rigsby CK, Zhang G, Schoeneman SE, Donaldson JS. Quantitative MRI for hepatic fat fraction and T2* measurement in pediatric patients with non-alcoholic fatty liver disease. Pediatr Radiol. 2014;44:1379–1387. doi: .
    1. Bannas P, Kramer H, Hernando D, Agni R, Cunningham AM, Mandal R, et al. Quantitative magnetic resonance imaging of hepatic steatosis: Validation in ex vivo human livers. Hepatology. 2015;62:1444–1455. doi: .
    1. 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;61:1547–1554. doi: .
    1. Idilman IS, Aniktar H, Idilman R, Kabacam G, Savas B, Elhan A, et al. Hepatic steatosis: quantification by proton density fat fraction with MR imaging versus liver biopsy. Radiology. 2013;267:767–775. doi: .
    1. Pavlides M, Banerjee R, Sellwood J, Kelly CJ, Robson MD, Booth JC, et al. Multiparametric magnetic resonance imaging predicts clinical outcomes in patients with chronic liver disease. J Hepatol. 2016;64:308–315. doi: .
    1. Schwimmer JB, Middleton MS, Behling C, Newton KP, Awai HI, Paiz MN, et al. Magnetic resonance imaging and liver histology as biomarkers of hepatic steatosis in children with nonalcoholic fatty liver disease. Hepatology. 2015;61:1887–1895. doi: .
    1. Jiménez-Agüero R, Emparanza JI, Beguiristain A, Bujanda L, Alustiza JM, García E, et al. Novel equation to determine the hepatic triglyceride concentration in humans by MRI: diagnosis and monitoring of NAFLD in obese patients before and after bariatric surgery. BMC Med. 2014;12:137. doi: .
    1. Kan H, Kimura Y, Hyogo H, Fukuhara T, Fujino H, Naeshiro N, et al. Non-invasive assessment of liver steatosis in non-alcoholic fatty liver disease. Hepatol Res. 2014;44:E420–E427. doi: .
    1. Kłusek-Oksiuta M, Bialokoz-Kalinowska I, Tarasów E, Wojtkowska M, Werpachowska I, Lebensztejn DM. Chemerin as a novel non-invasive serum marker of intrahepatic lipid content in obese children. Ital J Pediatr. 2014;40:84. doi: .
    1. Kang GH, Cruite I, Shiehmorteza M, Wolfson T, Gamst AC, Hamilton G, et al. Reproducibility of MRI-determined proton density fat fraction across two different MR scanner platforms. J Magn Reson Imaging. 2011;34:928–934. doi: .
    1. Soliman AS, Yuan J, Vigen KK, White JA, Peters TM, McKenzie CA. Max-IDEAL: a max-flow based approach for IDEAL water/fat separation. Magn Reson Med. 2014;72:510–521. doi: .
    1. EASL-EASD-EASO Clinical Practice Guidelines for the management of non-alcoholic fatty liver disease. J. Hepatol. 2016;64:1388–1402. doi: .
    1. Krishan S, Jain D, Bathina Y, Kale A, Saraf N, Saigal S, et al. Non-invasive quantification of hepatic steatosis in living, related liver donors using dual-echo Dixon imaging and single-voxel proton spectroscopy. Clin Radiol. 2016;71:58–63. doi: .
    1. Zhang Q, Zhang HM, Qi WQ, Zhang YG, Zhao P, Jiao J, et al. 3.0T 1H magnetic resonance spectroscopy for assessment of steatosis in patients with chronic hepatitis C. World J Gastroenterol. 2015;21:6736–6744. doi: .
    1. Di Martino M, Pacifico L, Bezzi M, Di Miscio R, Sacconi B, Chiesa C, et al. Comparison of magnetic resonance spectroscopy, proton density fat fraction and histological analysis in the quantification of liver steatosis in children and adolescents. World J Gastroenterol. 2016;22:8812–8819. doi: .
    1. Sagi R, Reif S, Neuman G, Webb M, Phillip M, Shalitin S. Nonalcoholic fatty liver disease in overweight children and adolescents. Acta Paediatr. 2007;96:1209–1213. doi: .
    1. Noureddin M, Lam J, Peterson MR, Middleton M, Hamilton G, Le TA, et al. Utility of magnetic resonance imaging versus histology for quantifying changes in liver fat in nonalcoholic fatty liver disease trials. Hepatology. 2013;58:1930–1940. doi: .
    1. Wong VW, Chu WC, Wong GL, Chan RS, Chim AM, Ong A, et al. Prevalence of non-alcoholic fatty liver disease and advanced fibrosis in Hong Kong Chinese: a population study using proton-magnetic resonance spectroscopy and transient elastography. Gut. 2012;61:409–415. doi: .
    1. Guaraldi G, Besutti G, Stentarelli C, Zona S, Nocetti L, Loria P, et al. Magnetic resonance for quantitative assessment of liver steatosis: a new potential tool to monitor antiretroviral-drug-related toxicities. Antivir Ther. 2012;17:965–971. doi: .
    1. Keese D, Korkusuz H, Huebner F, Namgaladze D, Raschidi B, Vogl TJ. In vivo and ex vivo measurements: noninvasive assessment of alcoholic fatty liver using 1H-MR spectroscopy. Diagn Interv Radiol. 2016;22:13–21. doi: .
    1. de Lédinghen V, Vergniol J, Foucher J, Merrouche W, le Bail B. Non-invasive diagnosis of liver steatosis using controlled attenuation parameter (CAP) and transient elastography. Liver Int. 2012;32:911–918. doi: .
    1. de Lédinghen V, Vergniol J, Capdepont M, Chermak F, Hiriart JB, Cassinotto C, et al. Controlled attenuation parameter (CAP) for the diagnosis of steatosis: a prospective study of 5323 examinations. J Hepatol. 2014;60:1026–1031. doi: .
    1. Myers RP, Pollett A, Kirsch R, Pomier-Layrargues G, Beaton M, Levstik M, et al. Controlled Attenuation Parameter (CAP): a noninvasive method for the detection of hepatic steatosis based on transient elastography. Liver Int. 2012;32:902–910. doi: .
    1. Shen F, Zheng RD, Mi YQ, Wang XY, Pan Q, Chen GY, et al. Controlled attenuation parameter for non-invasive assessment of hepatic steatosis in Chinese patients. World J Gastroenterol. 2014;20:4702–4711. doi: .
    1. Fujimori N, Tanaka N, Shibata S, Sano K, Yamazaki T, Sekiguchi T, et al. Controlled attenuation parameter is correlated with actual hepatic fat content in patients with non-alcoholic fatty liver disease with none-to-mild obesity and liver fibrosis. Hepatol Res. 2016;46:1019–1027. doi: .
    1. de Lédinghen V, Hiriart JB, Vergniol J, Merrouche W, Bedossa P, Paradis V. Controlled attenuation parameter (CAP) with the XL probe of the Fibroscan®: A comparative study with the M probe and liver biopsy. Dig Dis Sci. 2017;62:2569–2577. doi: .
    1. Shen F, Zheng RD, Shi JP, Mi YQ, Chen GF, Hu X, et al. Impact of skin capsular distance on the performance of controlled attenuation parameter in patients with chronic liver disease. Liver Int. 2015;35:2392–2400. doi: .
    1. Eggers H, Börnert P. Chemical shift encoding-based water-fat separation methods. J Magn Reson Imaging. 2014;40:251–268. doi: .
    1. Arboleda C, Aguirre-Reyes D, García MP, Tejos C, Muñoz L, Miquel JF, et al. Total liver fat quantification using three-dimensional respiratory self-navigated MRI sequence. Magn Reson Med. 2016;76:1400–1409. doi: .
    1. Runge JH, Bakker PJ, Gaemers IC, Verheij J, Hakvoort TB, Ottenhoff R, et al. Measuring liver triglyceride content in mice: non-invasive magnetic resonance methods as an alternative to histopathology. MAGMA. 2014;27:317–327. doi: .
    1. Idilman IS, Keskin O, Celik A, Savas B, Elhan AH, Idilman R, et al. A comparison of liver fat content as determined by magnetic resonance imaging-proton density fat fraction and MRS versus liver histology in non-alcoholic fatty liver disease. Acta Radiol. 2016;57:271–278. doi: .
    1. Hayashi T, Saitoh S, Takahashi J, Tsuji Y, Ikeda K, Kobayashi M, et al. Hepatic fat quantification using the two-point Dixon method and fat color maps based on non-alcoholic fatty liver disease activity score. Hepatol Res. 2017;47:455–464. doi: .
    1. Chabanova E, Bille DS, Thisted E, Holm JC, Thomsen HS. (1)H MRS assessment of hepatic steatosis in overweight children and adolescents: comparison between 3T and open 1T MR-systems. Abdom Imaging. 2013;38:315–319. doi: .
    1. Lee SH, Lee YH, Hahn S, Suh JS. Fat fraction estimation of morphologically normal lumbar vertebrae using the two-point mDixon turbo spin-echo MRI with flexible echo times and multipeak spectral model of fat: Comparison between cancer and non-cancer patients. Magn Reson Imaging. 2016;34:1114–1120. doi: .
    1. Takatsu Y, Akasaka T, Miyati T. The Dixon technique and the frequency-selective fat suppression technique in three-dimensional T1 weighted MRI of the liver: a comparison of contrast-to-noise ratios of hepatocellular carcinomas-to-liver. Br J Radiol. 2015;88:20150117. doi: .
    1. Fischer MA, Raptis DA, Montani M, Graf R, Clavien PA, Nanz D, et al. Liver fat quantification by dual-echo MR imaging outperforms traditional histopathological analysis. Acad Radiol. 2012;19:1208–1214. doi: .
    1. Georgoff P, Thomasson D, Louie A, Fleischman E, Dutcher L, Mani H, et al. Hydrogen-1 MR spectroscopy for measurement and diagnosis of hepatic steatosis. AJR Am J Roentgenol. 2012;199:2–7. doi: .
    1. Heba ER, Desai A, Zand KA, Hamilton G, Wolfson T, Schlein AN, et al. Accuracy and the effect of possible subject-based confounders of magnitude-based MRI for estimating hepatic proton density fat fraction in adults, using MR spectroscopy as reference. J Magn Reson Imaging. 2016;43:398–406. doi: .

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