The diagnostic accuracy of US, CT, MRI and 1H-MRS for the evaluation of hepatic steatosis compared with liver biopsy: a meta-analysis

Angulo P (2002) Nonalcoholic fatty liver disease. N Engl J Med 346:1221–1231 Williams R (2006) Global challenges in liver disease. Hepatology 44:521–526 Adams LA, Lymp JF, St Sauver J, Sanderson SO, Lindor KD, Feldstein A, Angulo P (2005) The natural history of nonalcoholic fatty liver disease: a population-based cohort study. Gastroenterology 129:113–121 Farrell GC, Larter CZ (2006) Nonalcoholic fatty liver disease: from steatosis to cirrhosis. Hepatology 43:S99–S112 Rector RS, Thyfault JP, Wei Y, Ibdah JA (2008) Non-alcoholic fatty liver disease and the metabolic syndrome: an update. World J Gastroenterol 14:185–192 Adinolfi LE, Gambardella M, Andreana A, Tripodi MF, Utili R, Ruggiero G (2001) Steatosis accelerates the progression of liver damage of chronic hepatitis C patients and correlates with specific HCV genotype and visceral obesity. Hepatology 33:1358–1364 Rubbia-Brandt L, Fabris P, Paganin S, Leandro G, Male PJ, Giostra E, Carlotto A, Bozzola L, Smedile A, Negro F (2004) Steatosis affects chronic hepatitis C progression in a genotype specific way. Gut 53:406–412 Ploeg RJ, D’Alessandro AM, Knechtle SJ, Stegall MD, Pirsch JD, Hoffmann RM, Sasaki T, Sollinger HW, Belzer FO, Kalayoglu M (1993) Risk factors for primary dysfunction after liver transplantation–a multivariate analysis. Transplantation 55:807–813 Vetelainen R, van Vliet A, Gouma DJ, van Gulik TM (2007) Steatosis as a risk factor in liver surgery. Ann Surg 245:20–30 Bravo AA, Sheth SG, Chopra S (2001) Liver biopsy. N Engl J Med 344:495–500 Charatcharoenwitthaya P, Lindor KD (2007) Role of radiologic modalities in the management of non-alcoholic steatohepatitis. Clin Liver Dis 11:37–54 Hamer OW, Aguirre DA, Casola G, Lavine JE, Woenckhaus M, Sirlin CB (2006) Fatty liver: imaging patterns and pitfalls. Radiographics 26:1637–1653 Joseph AE, Saverymuttu SH (1991) Ultrasound in the assessment of diffuse parenchymal liver disease. Clin Radiol 44:219–221 Whiting P, Rutjes AW, Reitsma JB, Bossuyt PM, Kleijnen J (2003) The development of QUADAS: a tool for the quality assessment of studies of diagnostic accuracy included in systematic reviews. BMC Med Res Methodol 3:25 Limanond P, Raman SS, Lassman C, Sayre J, Ghobrial RM, Busuttil RW, Saab S, Lu DS (2004) Macrovesicular hepatic steatosis in living related liver donors: correlation between CT and histologic findings. Radiology 230:276–280 van Werven JR, Hoogduin JM, Nederveen AJ, van Vliet AA, Wajs E, Vandenberk P, Stroes ES, Stoker J (2009) Reproducibility of 3.0 Tesla magnetic resonance spectroscopy for measuring hepatic fat content. J Magn Reson Imaging 30:444–448 Reitsma JB, Glas AS, Rutjes AW, Scholten RJ, Bossuyt PM, Zwinderman AH (2005) Bivariate analysis of sensitivity and specificity produces informative summary measures in diagnostic reviews. J Clin Epidemiol 58:982–990 Glas AS, Lijmer JG, Prins MH, Bonsel GJ, Bossuyt PM (2003) The diagnostic odds ratio: a single indicator of test performance. J Clin Epidemiol 56:1129–1135 Bahl M, Qayyum A, Westphalen AC, Noworolski SM, Chu PW, Ferrell L, Tien PC, Bass NM, Merriman RB (2008) Liver steatosis: investigation of opposed-phase T1-weighted liver MR signal intensity loss and visceral fat measurement as biomarkers. Radiology 249:160–166 Caturelli E, Squillante MM, Andriulli A, Cedrone A, Cellerino C, Pompili M, Manoja ER, Rapaccini GL (1992) Hypoechoic lesions in the ‘bright liver’: a reliable indicator of fatty change. A prospective study. Gastroenterol Hepatol 7:469–472 Chen C-H, Lin S-T, Yang C-C, Yeh Y-H, Kuo C-L, Nien C-K (2008) The accuracy of sonography in predicting steatosis and fibrosis in chronic hepatitis C. Dig Dis Sci 53:1699–1706 Cho CS, Curran S, Schwartz LH, Kooby DA, Klimstra DS, Shia J, Munoz A, Fong Y, Jarnagin WR, DeMatteo RP, Blumgart LH, D’Angelica MI (2008) Preoperative radiographic assessment of hepatic steatosis with histologic correlation. J Am Coll Surg 206:480–488 Crum-Cianflone N, Dilay A, Collins G, Asher D, Campin R, Medina S, Goodman Z, Parker R, Lifson A, Capozza T, Bavaro M, Hale B, Hames C (2009) Nonalcoholic fatty liver disease Among HIV-infected persons. J Acquir Immune Defic Syndr 50:464–473 D’Assignies G, Ruel M, Khiat A, Lepanto L, Chagnon M, Kauffmann C, Tang A, Gaboury L, Boulanger Y (2009) Noninvasive quantitation of human liver steatosis using magnetic resonance and bioassay methods. Eur Radiol 19:2033–2040 Dasarathy S, Dasarathy J, Khiyami A, Joseph R, Lopez R, McCullough AJ (2009) Validity of real time ultrasound in the diagnosis of hepatic steatosis: a prospective study. J Hepatol 51:1061–1067 de Korte PJ, van der Loos TL, van den Tweel JG, Cremers PT, Veldhuijzen van Zanten GO, Lustermans FA (1986) Interpretation of a ‘bright’ liver in ultrasound examination. Neth J Med 29:5–7 de Moura Almeida A, Cotrim HP, Barbosa DB, de Athayde LG, Santos AS, Bitencourt AG, de Freitas LA, Rios A, Alves E (2008) Fatty liver disease in severe obese patients: diagnostic value of abdominal ultrasound. World J Gastroenterol 14:1415–1418 Dietrich CF, Wehrmann T, Zeuzem S, Braden B, Caspary WF, Lembcke B (1999) Analysis of hepatic echo patterns in chronic hepatitis C. Ultraschall Med 20:9–14 Friedrich-Rust M, Muller C, Winckler A, Kriener S, Herrmann E, Holtmeier J, Poynard T, Vogl TJ, Zeuzem S, Hammerstingl R, Sarrazin C (2010) Assessment of liver fibrosis and steatosis in PBC with FibroScan, MRI, MR-spectroscopy, and Serum Markers. J Clin Gastroenterol 44:58–65 Graif M, Yanuka M, Baraz M, Blank A, Moshkovitz M, Kessler A, Gilat T, Weiss J, Walach E, Amazeen P, Irving CS (2000) Quantitative estimation of attenuation in ultrasound video images: correlation with histology in diffuse liver disease. Invest Radiol 35:319–324 Hamaguchi M, Kojima T, Itoh Y, Harano Y, Fujii K, Nakajima T, Kato T, Takeda N, Okuda J, Ida K, Kawahito Y, Yoshikawa T, Okanoue T (2007) The severity of ultrasonographic findings in nonalcoholic fatty liver disease reflects the metabolic syndrome and visceral fat accumulation. Am J Gastroenterol 102:2708–2715 Hepburn MJ, Vos JA, Fillman EP, Lawitz EJ (2005) The accuracy of the report of hepatic steatosis on ultrasonography in patients infected with hepatitis C in a clinical setting: a retrospective observational study. BMC Gastroenterol 5:14 Hirche TO, Ignee A, Hirche H, Schneider A, Dietrich CF (2007) Evaluation of hepatic steatosis by ultrasound in patients with chronic hepatitis C virus infection. Liver Int 27:748–757 Hultcrantz R, Gabrielsson N (1993) Patients with persistent elevation of aminotransferases: investigation with ultrasonography, radionuclide imaging and liver biopsy. J Intern Med 233:7–12 Iwasaki M, Takada Y, Hayashi M, Minamiguchi S, Haga H, Maetani Y, Fujii K, Kiuchi T, Tanaka K (2004) Noninvasive evaluation of graft steatosis in living donor liver transplantation. Transplantation 78:1501–1505 Joseph AE, Saverymuttu SH, al-Sam S, Cook MG, Maxwell JD (1991) Comparison of liver histology with ultrasonography in assessing diffuse parenchymal liver disease. Clin Radiol 43:26–31 Kichian K, McLean R, Gramlich LM, Bailey RJ, Bain VG (2003) Nonalcoholic fatty liver disease in patients investigated for elevated liver enzymes. Can J Gastroenterol 17:38–42 Kim DY, Park SH, Lee SS, Kim HJ, Kim SY, Kim MY, Lee Y, Kim TK, Khalili K, Bae MH, Lee JY, Lee SG, Yu ES (2010) Contrast-enhanced computed tomography for the diagnosis of fatty liver: prospective study with same-day biopsy used as the reference standard. Eur Radiol 20:359–366 Kim SH, Jeong ML, Jong HK, Kwang GK, Joon KH, Kyoung HL, Seong HP, Yi N-J, Suh K-S, Su KA, Young JK, Kyu RS, Hye SL, Byung IC (2005) Appropriateness of a donor liver with respect to macrosteatosis: application of artificial neural networks to US images—Initial experience. Radiology 234:793–803 Kim SH, Lee JM, Han JK, Lee JY, Lee KH, Han CJ, Jo JY, Yi NJ, Suh KS, Shin KS, Jo SY, Choi BI (2006) Hepatic macrosteatosis: predicting appropriateness of liver donation by using MR imaging–correlation with histopathologic findings. Radiology 240:116–129 Krššák M, Hofer H, Wrba F, Meyerspeer M, Brehm A, Lohninger A, Steindl-Munda P, Moser E, Ferenci P, Roden M (Epub 2009) Non-invasive assessment of hepatic fat accumulation in chronic hepatitis C by (1)H magnetic resonance spectroscopy. Eur J Radiol. doi:10.1016/j.ejrad.2009.03.062 Kutcher R, Smith GS, Sen F, Gelman SF, Mitsudo S, Thung SN, Reinus JF (1998) Comparison of sonograms and liver histologic findings in patients with chronic hepatitis C virus infection. J Ultrasound Med 17:321–325 Lee JY, Kim KM, Lee SG, Yu E, Lim YS, Lee HC, Chung YH, Lee YS, Suh DJ (2007) Prevalence and risk factors of non-alcoholic fatty liver disease in potential living liver donors in Korea: a review of 589 consecutive liver biopsies in a single center. J Hepatol 47:239–244 Lee SW, Park SH, Kim KW, Choi EK, Shin YM, Kim PN, Lee KH, Yu ES, Hwang S, Lee SG (2007) Unenhanced CT for assessment of macrovesicular hepatic steatosis in living liver donors: comparison of visual grading with liver attenuation index. Radiology 244:479–485 Lossner C, Cuno S, Kleine S, Kleine FD (1988) Value of ultrasound tomography in the diagnosis and follow-up of fatty liver. [German]. Dtsch Z Verdau Stoffwechselkr 48:22–26 Mathiesen UL, Franzen LE, Aselius H, Resjo M, Jacobsson L, Foberg U, Fryden A, Bodemar G (2002) 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 34:516–522 McPherson S, Jonsson JR, Cowin GJ, O’Rourke P, Clouston AD, Volp A, Horsfall L, Jothimani D, Fawcett J, Galloway GJ, Benson M, Powell EE (2009) Magnetic resonance imaging and spectroscopy accurately estimate the severity of steatosis provided the stage of fibrosis is considered. J Hepatol 51:389–397 Mennesson N, Dumortier J, Hervieu V, Milot L, Guillaud O, Scoazec JY, Pilleul F (2009) Liver steatosis quantification using magnetic resonance imaging: a prospective comparative study with liver biopsy. J Comput Assist Tomogr 33:672–677 O’Rourke TR, Welsh FK, Tekkis PP, Lyle N, Mustajab A, John TG, Peppercorn D, Rees M (2009) Accuracy of liver-specific magnetic resonance imaging as a predictor of chemotherapy-associated hepatic cellular injury prior to liver resection. Eur J Surg Oncol 35:1085–1091 Orlacchio A, Bolacchi F, Cadioli M, Bergamini A, Cozzolino V, Angelico M, Simonetti G (2008) Evaluation of the severity of chronic hepatitis C with 3-T1H-MR spectroscopy. AJR Am J Roentgenol 190:1331–1339 Palmentieri B, de Sio I, La Mura V, Masarone M, Vecchione R, Bruno S, Torella R, Persico M (2006) The role of bright liver echo pattern on ultrasound B-mode examination in the diagnosis of liver steatosis. Dig Liver Dis 38:485–489 Park SH, Kim PN, Kim KW, Lee SW, Yoon SE, Park SW, Ha HK, Lee MG, Hwang S, Lee SG, Yu ES, Cho EY (2006) Macrovesicular hepatic steatosis in living liver donors: use of CT for quantitative and qualitative assessment. Radiology 239:105–112 Perez NE, Siddiqui FA, Mutchnick MG, Dhar R, Tobi M, Ullah N, Saksouk FA, Wheeler DE, Ehrinpreis MN (2007) Ultrasound diagnosis of fatty liver in patients with chronic liver disease: a retrospective observational study. J Clin Gastroenterol 41:624–629 Rinella ME, Alonso E, Rao S, Whitington P, Fryer J, Abecassis M, Superina R, Flamm SL, Blei AT (2001) Body mass index as a predictor of hepatic steatosis in living liver donors. Liver Transplant 7:409–414 Rinella ME, McCarthy R, Thakrar K, Finn JP, Rao SM, Koffron AJ, Abecassis M, Blei AT (2003) Dual-echo, chemical shift gradient-echo magnetic resonance imaging to quantify hepatic steatosis: implications for living liver donation. Liver Transplant 9:851–856 Saadeh S, Younossi ZM, Remer EM, Gramlich T, Ong JP, Hurley M, Mullen KD, Cooper JN, Sheridan MJ (2002) The utility of radiological imaging in nonalcoholic fatty liver disease. Gastroenterology 123:745–750 Saverymuttu SH, Joseph AE, Maxwell JD (1986) Ultrasound scanning in the detection of hepatic fibrosis and steatosis. Br Med J Clin Res Ed 292:13–15 Tobari M, Hashimoto E, Yatsuji S, Torii N, Shiratori K (2009) Imaging of nonalcoholic steatohepatitis: advantages and pitfalls of ultrasonography and computed tomography. Intern Med 48:739–746 Webb M, Yeshua H, Zelber-Sagi S, Santo E, Brazowski E, Halpern Z, Oren R (2009) Diagnostic value of a computerized hepatorenal index for sonographic quantification of liver steatosis. AJR Am J Roentgenol 192:909–914 Yajima Y, Ohta K, Narui T, Abe R, Suzuki H, Ohtsuki M (1983) Ultrasonographical diagnosis of fatty liver: significance of the liver-kidney contrast. Tohoku J Exp Med 139:43–50 Yamashiki N, Sugawara Y, Tamura S, Kaneko J, Matsui Y, Togashi J, Ohki T, Yoshida H, Omata M, Makuuchi M, Kokudo N (2009) Noninvasive estimation of hepatic steatosis in living liver donors: usefulness of visceral fat area measurement. Transplantation 88:575–581 Yoshimitsu K, Kuroda Y, Nakamuta M, Taketomi A, Irie H, Tajima T, Hirakawa M, Ishigami K, Ushijima Y, Yamada T, Honda H (2008) Noninvasive estimation of hepatic steatosis using plain CT vs. chemical-shift MR imaging: significance for living donors. J Magn Reson Imaging 28:678–684 Yu W, Hu S, Qi Y, Li B (2009) The correlation between sonographic diagnosis and laparoscopic observations on fatty liver. J Laparoendosc Adv Surg Tech 19:163–169 Strauss S, Gavish E, Gottlieb P, Katsnelson L (2007) Interobserver and intraobserver variability in the sonographic assessment of fatty liver. Am J Roentgenol 189:W320–W323 Ma X, Holalkere NS, Kambadakone RA, Mino-Kenudson M, Hahn PF, Sahani DV (2009) Imaging-based quantification of hepatic fat: methods and clinical applications. Radiographics 29:1253–1277 Borra RJ, Salo S, Dean K, Lautamaki R, Nuutila P, Komu M, Parkkola R (2009) Nonalcoholic fatty liver disease: rapid evaluation of liver fat content with in-phase and out-of-phase MR imaging. Radiology 250:130–136 Guiu B, Petit JM, Loffroy R, Ben SD, Aho S, Masson D, Hillon P, Krause D, Cercueil JP (2009) Quantification of liver fat content: comparison of triple-echo chemical shift gradient-echo imaging and in vivo proton MR spectroscopy. Radiology 250:95–102 Guiu B, Loffroy R, Petit JM, Aho S, Ben SD, Masson D, Hillon P, Cercueil JP, Krause D (2009) Mapping of liver fat with triple-echo gradient echo imaging: validation against 3.0-T proton MR spectroscopy. Eur Radiol 19:1786–1793 Irwan R, Edens MA, Sijens PE (2008) Assessment of the variations in fat content in normal liver using a fast MR imaging method in comparison with results obtained by spectroscopic imaging. Eur Radiol 18:806–813 Kim H, Taksali SE, Dufour S, Befroy D, Goodman TR, Petersen KF, Shulman GI, Caprio S, Constable RT (2008) Comparative MR study of hepatic fat quantification using single-voxel proton spectroscopy, two-point dixon and three-point IDEAL. Magn Reson Med 59:521–527 O’Regan DP, Callaghan MF, Wylezinska-Arridge M, Fitzpatrick J, Naoumova RP, Hajnal JV, Schmitz SA (2008) Liver fat content and T2*: simultaneous measurement by using breath-hold multiecho MR imaging at 3.0 T–feasibility. Radiology 247:550–557 Reeder SB, Robson PM, Yu H, Shimakawa A, Hines CD, McKenzie CA, Brittain JH (2009) Quantification of hepatic steatosis with MRI: the effects of accurate fat spectral modeling. J Magn Reson Imaging 29:1332–1339 Yokoo T, Bydder M, Hamilton G, Middleton MS, Gamst AC, Wolfson T, Hassanein T, Patton HM, Lavine JE, Schwimmer JB, Sirlin CB (2009) Nonalcoholic fatty liver disease: diagnostic and fat-grading accuracy of low-flip-angle multiecho gradient-recalled-echo MR imaging at 1.5 T. Radiology 251:67–76 Szczepaniak LS, Nurenberg P, Leonard D, Browning JD, Reingold JS, Grundy S, Hobbs HH, Dobbins RL (2005) Magnetic resonance spectroscopy to measure hepatic triglyceride content: prevalence of hepatic steatosis in the general population. Am J Physiol Endocrinol Metab 288:E462–468 Guiu B, Loffroy R, Hillon P, Petit JM (2009) Magnetic resonance imaging and spectroscopy for quantification of hepatic steatosis: urgent need for standardization! J Hepatol 51:1082–1083 Kleiner DE, Brunt EM, Van NM, Behling C, Contos MJ, Cummings OW, Ferrell LD, Liu YC, Torbenson MS, Unalp-Arida A, Yeh M, McCullough AJ, Sanyal AJ (2005) Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41:1313–1321