Magnetic resonance imaging and liver histology as biomarkers of hepatic steatosis in children with nonalcoholic fatty liver disease

Hepatology

Volumn 61, Issue 6, 2015, Pages 1887-1895

  Schwimmer, Jeffrey B ^a,b,c   Middleton, Michael S ^c   Behling, Cynthia ^a,d   Newton, Kimberly P ^a,b   Awai, Hannah I ^a,b,c   Paiz, Melissa N ^a   Lam, Jessica ^c,e   Hooker, Jonathan C ^c   Hamilton, Gavin ^c   Fontanesi, John ^f   Sirlin, Claude B ^c  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b RADY CHILDREN'S HOSPITAL   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Sharp Fertility Center   (United States)

^e LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTATE AMINOTRANSFERASE; FAT; GAMMA GLUTAMYLTRANSFERASE; BIOLOGICAL MARKER;

ADOLESCENT; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ARTICLE; CHILD; CLINICAL ASSESSMENT; CLINICAL EVALUATION; CLINICAL FEATURE; COMPARATIVE STUDY; CORRELATIONAL STUDY; DIAGNOSTIC ACCURACY; FAT CONTENT; FATTY LIVER; FEMALE; HUMAN; HUMAN TISSUE; LIVER BIOPSY; LIVER FIBROSIS; LIVER HISTOLOGY; MAJOR CLINICAL STUDY; MALE; NONALCOHOLIC FATTY LIVER; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTON DENSITY FAT FRACTION; QUANTITATIVE ANALYSIS; RADIOLOGICAL PARAMETERS; RECEIVER OPERATING CHARACTERISTIC; SENSITIVITY AND SPECIFICITY; CASE CONTROL STUDY; CLINICAL TRIAL; LIVER; PATHOLOGY; PROSPECTIVE STUDY;

ADOLESCENT; BIOLOGICAL MARKERS; CASE-CONTROL STUDIES; CHILD; FEMALE; HUMANS; LIVER; MAGNETIC RESONANCE IMAGING; MALE; NON-ALCOHOLIC FATTY LIVER DISEASE; PROSPECTIVE STUDIES;

EID: 84929607638     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.27666     Document Type: Article

References (44)

1. Schwimmer JB, Deutsch R, Kahen T, Lavine JE, Stanley C, Behling C. Prevalence of fatty liver in children and adolescents. Pediatrics 2006;118:1388-1393.
2. Feldstein AE, Charatcharoenwitthaya P, Treeprasertsuk S, Benson JT, Enders FB, Angulo P. The natural history of non-alcoholic fatty liver disease in children: a follow-up study for up to 20 years. Gut 2009;58:1538-1544.
3. Alexander J, Torbenson M, Wu TT, Yeh MM. Non-alcoholic fatty liver disease contributes to hepatocarcinogenesis in non-cirrhotic liver: a clinical and pathological study. J Gastroenterol Hepatol 2013;28:848-854.
4. Schwimmer JB, Pardee PE, Lavine JE, Blumkin AK, Cook S. Cardiovascular risk factors and the metabolic syndrome in pediatric nonalcoholic fatty liver disease. Circulation 2008;118:277-283.
5. Rubinstein E, Lavine JE, Schwimmer JB. Hepatic, cardiovascular, and endocrine outcomes of the histological subphenotypes of nonalcoholic fatty liver disease. Semin Liver Dis 2008;28:380-385.
6. Ekstedt M, Franzen LE, Mathiesen UL, Thorelius L, Holmqvist M, Bodemar G, et al. Long-term follow-up of patients with NAFLD and elevated liver enzymes. Hepatology 2006;44:865-873.
7. Sanches PL, de Piano A, Campos RM, Carnier J, de Mello MT, Elias N, et al. Association of nonalcoholic fatty liver disease with cardiovascular risk factors in obese adolescents: the role of interdisciplinary therapy. J Clin Lipidol 2014;8:265-272.
8. Kim NH, Park J, Kim SH, Kim YH, Kim DH, Cho GY, et al. Non-alcoholic fatty liver disease, metabolic syndrome and subclinical cardiovascular changes in the general population. Heart 2014;100:938-943.
9. Schwimmer JB, Behling C, Newbury R, Deutsch R, Nievergelt C, Schork NJ, et al. Histopathology of pediatric nonalcoholic fatty liver disease. Hepatology 2005;42:641-649.
10. Brunt EM. Nonalcoholic steatohepatitis: definition and pathology. Semin Liver Dis 2001;21:3-16.
11. Brunt EM, Janney CG, Di Bisceglie AM, Neuschwander-Tetri BA, Bacon BR. Nonalcoholic steatohepatitis: a proposal for grading and staging the histological lesions. Am J Gastroenterol 1999;94:2467-2474.
12. Awai HI, Newton KP, Sirlin CB, Behling C, Schwimmer JB. Evidence and recommendations for imaging liver fat in children, based on systematic review. Clin Gastroenterol Hepatol 2014;12:765-773.
13. Tang A, Tan J, Sun M, Hamilton G, Bydder M, Wolfson T, et al. Nonalcoholic fatty liver disease: MR imaging of liver proton density fat fraction to assess hepatic steatosis. Radiology 2013;267:422-431.
14. Wu CH, Ho MC, Jeng YM, Hsu CY, Liang PC, Hu RH, et al. Quantification of hepatic steatosis: a comparison of the accuracy among multiple magnetic resonance techniques. J Gastroenterol Hepatol 2014;29:807-813.
15. Permutt Z, Le TA, Peterson MR, Seki E, Brenner DA, Sirlin C, et al. Correlation between liver histology and novel magnetic resonance imaging in adult patients with non-alcoholic fatty liver disease-MRI accurately quantifies hepatic steatosis in NAFLD. Aliment Pharmacol Ther 2012;36:22-29.
16. Banerjee R, Pavlides M, Tunnicliffe EM, Piechnik SK, Sarania N, Philips R, et al. Multiparametric magnetic resonance for the non-invasive diagnosis of liver disease. J Hepatol 2014;60:69-77.
17. Levenson H, Greensite F, Hoefs J, Friloux L, Applegate G, Silva E, et al. Fatty infiltration of the liver: quantification with phase-contrast MR imaging at 1.5 T vs biopsy. AJR Am J Roentgenol 1991;156:307-312.
18. Westphalen AC, Qayyum A, Yeh BM, Merriman RB, Lee JA, Lamba A, et al. Liver fat: effect of hepatic iron deposition on evaluation with opposed-phase MR imaging. Radiology 2007;242:450-455.
19. Qayyum A, Chen DM, Breiman RS, Westphalen AC, Yeh BM, Jones KD, et al. Evaluation of diffuse liver steatosis by ultrasound, computed tomography, and magnetic resonance imaging: which modality is best? Clin Imaging 2009;33:110-115.
20. McPherson S, Jonsson JR, Cowin GJ, O'Rourke P, Clouston AD, Volp A, et al. Magnetic resonance imaging and spectroscopy accurately estimate the severity of steatosis provided the stage of fibrosis is considered. J Hepatol 2009;51:389-397.
21. Kang BK, Yu ES, Lee SS, Lee Y, Kim N, Sirlin CB, et al. Hepatic fat quantification: a prospective comparison of magnetic resonance spectroscopy and analysis methods for chemical-shift gradient echo magnetic resonance imaging with histologic assessment as the reference standard. Invest Radiol 2012;47:368-375.
22. 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.
23. Qayyum A, Goh JS, Kakar S, Yeh BM, Merriman RB, Coakley FV. Accuracy of liver fat quantification at MR imaging: comparison of out-of-phase gradient-echo and fat-saturated fast spin-echo techniques-initial experience. Radiology 2005;237:507-511.
24. Schwimmer JB. Definitive diagnosis and assessment of risk for nonalcoholic fatty liver disease in children and adolescents. Semin Liver Dis 2007;27:312-318.
25. 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;41:1313-1321.
26. Bydder M, Yokoo T, Hamilton G, Middleton MS, Chavez AD, Schwimmer JB, et al. Relaxation effects in the quantification of fat using gradient echo imaging. Magn Reson Imaging 2008;26:347-359.
27. Liu CY, McKenzie CA, Yu H, Brittain JH, Reeder SB. Fat quantification with IDEAL gradient echo imaging: correction of bias from T(1) and noise. Magn Reson Med 2007;58:354-364.
28. Yu H, McKenzie CA, Shimakawa A, Vu AT, Brau AC, Beatty PJ, et al. Multiecho reconstruction for simultaneous water-fat decomposition and T2* estimation. J Magn Reson Imaging 2007;26:1153-1161.
29. Yu H, Shimakawa A, McKenzie CA, Brodsky E, Brittain JH, Reeder SB. Multiecho water-fat separation and simultaneous R2* estimation with multifrequency fat spectrum modeling. Magn Reson Med 2008;60:1122-1134.
30. Goodman LAK, William H. Measures of association for cross classifications. IV: Simplification of asymptotic variances. J Am Stat Assoc 1972;67:415-421.
31. Schwimmer JB, Newton KP, Awai HI, Choi LJ, Garcia MA, Ellis LL, et al. Paediatric gastroenterology evaluation of overweight and obese children referred from primary care for suspected non-alcoholic fatty liver disease. Aliment Pharmacol Ther 2013;38:1267-1277.
32. Pacifico L, Martino MD, Catalano C, Panebianco V, Bezzi M, Anania C, et al. T1-weighted dual-echo MRI for fat quantification in pediatric nonalcoholic fatty liver disease. World J Gastroenterol 2011;17:3012-3019.
33. 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.
34. Hatta T, Fujinaga Y, Kadoya M, Ueda H, Murayama H, Kurozumi M, et al. Accurate and simple method for quantification of hepatic fat content using magnetic resonance imaging: a prospective study in biopsy-proven nonalcoholic fatty liver disease. J Gastroenterol 2010;45:1263-1271.
35. Lee SS, Park SH, Kim HJ, Kim SY, Kim MY, Kim DY, et al. Non-invasive assessment of hepatic steatosis: prospective comparison of the accuracy of imaging examinations. J Hepatol 2010;52:579-585.
36. Reeder SB, Cruite I, Hamilton G, Sirlin CB. Quantitative assessment of liver fat with magnetic resonance imaging and spectroscopy. J Magn Reson Imaging 2011;34:729-749.
37. Meisamy S, Hines CD, Hamilton G, Sirlin CB, McKenzie CA, Yu H, et al. Quantification of hepatic steatosis with T1-independent, T2-corrected MR imaging with spectral modeling of fat: blinded comparison with MR spectroscopy. Radiology 2011;258:767-775.
38. Fischer MA, Nanz D, Reiner CS, Montani M, Breitenstein S, Leschka S, et al. Diagnostic performance and accuracy of 3-D spoiled gradient-dual-echo MRI with water- and fat-signal separation in liver-fat quantification: comparison to liver biopsy. Invest Radiol 2010;45:465-470.
39. Yokoo T, Bydder M, Hamilton G, Middleton MS, Gamst AC, Wolfson T, et al. Nonalcoholic fatty liver disease: diagnostic and fat-grading accuracy of low-flip-angle multiecho gradient-recalled-echo MR imaging at 1.5 T. Radiology 2009;251:67-76.
40. Longo R, Ricci C, Masutti F, Vidimari R, Croce LS, Bercich L, et al. Fatty infiltration of the liver. Quantification by 1H localized magnetic resonance spectroscopy and comparison with computed tomography. Invest Radiol 1993;28:297-302.
41. Longo R, Pollesello P, Ricci C, Masutti F, Kvam BJ, Bercich L, et al. Proton MR spectroscopy in quantitative in vivo determination of fat content in human liver steatosis. J Magn Reson Imaging 1995;5:281-285.
42. van Werven JR, Marsman HA, Nederveen AJ, Smits NJ, ten Kate FJ, van Gulik TM, 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;256:159-168.
43. Szczepaniak LS, Nurenberg P, Leonard D, Browning JD, Reingold JS, Grundy S, et al. Magnetic resonance spectroscopy to measure hepatic triglyceride content: prevalence of hepatic steatosis in the general population. Am J Physiol Endocrinol Metab 2005;288:E462-E468.
44. Fishbein MH, Gardner KG, Potter CJ, Schmalbrock P, Smith MA. Introduction of fast MR imaging in the assessment of hepatic steatosis. Magn Reson Imaging 1997;15:287-293.