Association of noninvasive quantitative decline in liver fat content on MRI with histologic response in nonalcoholic steatohepatitis

Therapeutic Advances in Gastroenterology

Volumn 9, Issue 5, 2016, Pages 692-701

  Patel, Janki ^a   Bettencourt, Ricki ^b,c   Cui, Jeffrey ^b   Salotti, Joanie ^c   Hooker, Jonathan ^c   Bhatt, Archana ^b   Hernandez, Carolyn ^b   Nguyen, Phirum ^c   Aryafar, Hamed ^c   Valasek, Mark ^c   Haufe, William ^c   Hooker, Catherine ^c   Richards, Lisa ^c   Sirlin, Claude B ^c   Loomba, Rohit ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

advanced fibrosis; biomarker; fat mapping; magnetic resonance imaging (MRI); MRI proton density fat fraction (PDFF); nonalcoholic fatty liver disease; nonalcoholic steatohepatitis; noninvasive assessment

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; EZETIMIBE; GAMMA GLUTAMYLTRANSFERASE; PLACEBO;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG RESPONSE; FEMALE; HUMAN; HUMAN TISSUE; LIVER BIOPSY; LIVER HISTOLOGY; MALE; NONALCOHOLIC FATTY LIVER; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RANDOMIZED CONTROLLED TRIAL (TOPIC);

EID: 84981267545     PISSN: 1756283X     EISSN: 17562848     Source Type: Journal    
DOI: 10.1177/1756283X16656735     Document Type: Article

References (44)

1. Adams L., Lymp J., St Sauver J., Sanderson S., Lindor K., Feldstein A., et al. (2005) The natural history of nonalcoholic fatty liver disease: a population-based cohort study. Gastroenterology 129: 113-121.
2. Bohte A., van Werven J., Bipat S., Stoker J., (2011) The diagnostic accuracy of US, CT, MRI and 1h-MRS for the evaluation of hepatic steatosis compared with liver biopsy: a meta-analysis. Eur Radiol 21: 87-97.
3. Bravo A., Sheth S., Chopra S., (2001) Liver biopsy. N Engl J Med 344: 495-500.
4. Browning J., Szczepaniak L., Dobbins R., Nuremberg P., Horton J., Cohen J., et al. (2004) Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 40: 1387-1395.
5. Chalasani N., Younossi Z., Lavine J., Diehl A., Brunt E., Cusi K., et al. (2012) The diagnosis and management of non-alcoholic fatty liver disease: practice guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology 55: 2005-2023.
6. Charlton M., Burns J., Pedersen R., Watt K., Heimbach J., Dierkhising R., (2011) Frequency and outcomes of liver transplantation for nonalcoholic steatohepatitis in the United States. Gastroenterology 141: 1249-1253.
7. Doycheva I., Cui J., Nguyen P., Costa E., Hooker J., Hofflich H., et al. (2015) Noninvasive screening of diabetics in primary care for NAFLD and advanced fibrosis by MRI and MRE. Aliment Pharmacol Ther 43: 83-95.
8. Hines C., Frydrychowicz A., Hamilton G., Tudorascu D., Vigen K., Yu H., et al. (2011) T(1) independent, T(2) (∗) corrected chemical shift based fat-water separation with multi-peak fat spectral modeling is an accurate and precise measure of hepatic steatosis. J Magn Reson Imaging 33: 873-881.
9. Idilman I., Aniktar H., Idilman R., Kabacam G., Savas B., Elhan A., et al. (2013) Hepatic steatosis: quantification by proton density fat fraction with MR imaging versus liver biopsy. Radiology 267: 767-775.
10. Kang G., Cruite I., Shiehmorteza M., Wolfson T., Gamst A., Hamilton G., et al. (2011) Reproducibility of MRI-determined proton density fat fraction across two different MR scanner platforms. J Magn Reson Imaging 34: 928-934.
11. Keating S., Hackett D., Parker H., O'Connor H., Gerofi J., Sainsbury A., et al. (2015) Effect of aerobic exercise training dose on liver fat and visceral adiposity. J Hepatol 63: 174-182.
12. Kleiner D., Brunt E., van Natta M., Behling C., Contos M., Cummings O., et al. (2005) Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41: 1313-1321.
13. Le T., Chen J., Changchien C., Peterson M., Kono Y., Patton H., et al. (2012) Effect of colesevelam on liver fat quantified by magnetic resonance in nonalcoholic steatohepatitis: a randomized controlled trial. Hepatology 56: 922-932.
14. Liu C., McKenzie C., Yu H., Brittain J., Reeder S., (2007) Fat quantification with ideal gradient echo imaging: correction of bias from T(1) and noise. Magn Reson Med 58: 354-364.
15. Loomba R., Abraham M., Unalp A., Wilson L., Lavine J., Doo E., et al. (2012) Association between Diabetes, family history of diabetes, and risk of nonalcoholic steatohepatitis and fibrosis. Hepatology 56: 943-951.
16. Loomba R., Sanyal A., (2013) The global NAFLD epidemic. Nat Rev Gastroenterol Hepatol 10: 686-690.
17. Loomba R., Schork N., Chen C., Bettencourt R., Bhatt A., Ang B., et al. (2015) Heritability of hepatic fibrosis and steatosis based on a prospective twin study. Gastroenterology 149: 1784-1793.
18. Loomba R., Sirlin C., Ang B., Bettencourt R., Jain R., Salotti J., et al. (2014) Ezetimibe for the treatment of nonalcoholic steatohepatitis: assessment by novel MRI and MRE in a randomized trial (Mozart Trial). Hepatology 61: 1239-1250.
19. Loomba R., Wesley R., Pucino F., Liang T., Kleiner D., Lavine J., (2008) Placebo in nonalcoholic steatohepatitis: insight into natural history and implications for future clinical trials. Clin Gastroenterol Hepatol 6: 1243-1248.
20. Matteoni C., Younossi Z., Gramlich T., Boparai N., Liu Y., McCullough A., (1999) Nonalcoholic fatty liver disease: a spectrum of clinical and pathological severity. Gastroenterology 116: 1413-1419.
21. Meisamy S., Hines C., Hamilton G., Sirlin C., Mckenzie C., Yu H., et al. (2011) Quantification of hepatic steatosis with T1-independent, T2-corrected MR imaging with spectral modeling of fat: blinded comparison with MR spectroscopy. Radiology 258: 767-775.
22. Mishra P., Younossi Z., (2007) Abdominal ultrasound for diagnosis of nonalcoholic fatty liver disease (NAFLD). Am J Gastroenterol 102: 2716-2717.
23. Negrete L., Middleton M., Clark L., Wolfson T., Gamst A., Lam J., et al. (2014) Inter-examination precision of magnitude-based MRI for estimation of segmental hepatic proton density fat fraction in obese subjects. J Magn Reson Imaging 39: 1265-1271.
24. Neuschwander-Tetri B., Clark J., Bass N., van Natta M., Unalp-Arida A., Tonascia J., et al. (2010) Clinical, laboratory and histological associations in adults with nonalcoholic fatty liver disease. Hepatology 52: 913-924.
25. Noureddin M., Lam J., Peterson M., Middleton M., Hamilton G., Le T., et al. (2013) Utility of magnetic resonance imaging versus histology for quantifying changes in liver fat in nonalcoholic fatty liver disease trials. Hepatology 58: 1930-1940.
26. Patel N., Doycheva I., Peterson M., Hooker J., Kisselva T., Schnabl B., et al. (2014) Effect of weight loss on magnetic resonance imaging estimation of liver fat and volume in patients with nonalcoholic steatohepatitis. Clin Gastroenterol Hepatol 13: 561-568.e1.
27. Permutt Z., Le T., Peterson M., Seki E., Brenner D., Sirlin C., et al. (2012) 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 36: 22-29.
28. Prati D., Taioli E., Zanella A., Della Torre E., Butelli S., Del Vecchio E., et al. (2002) Updated definitions of healthy ranges for serum alanine aminotransferase levels. Ann Intern Med 137: 1-10.
29. Ratziu V., Charlotte F., Heurtier A., Gombert S., Giral P., Bruckert E., et al. (2005) Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology 128: 1898-1906.
30. Reeder S., Robson P., Yu H., Shimakawa A., Hines C., Mckenzie C., et al. (2009) Quantification of hepatic steatosis with mri: the effects of accurate fat spectral modeling. J Magn Reson Imaging 29: 1332-1339.
31. Reeder S., Sirlin C., (2010) Quantification of liver fat with magnetic resonance imaging. Magn Reson Imaging Clin N Am 18: 337-357, ix.
32. Saadeh S., Younossi Z., Remer E., Gramlich T., Ong J., Hurley M., et al. (2002) The utility of radiological imaging in nonalcoholic fatty liver disease. Gastroenterology 123: 745-750.
33. Schwenzer N., Springer F., Schraml C., Stefan N., Machann J., Schick F., (2009) Noninvasive assessment and quantification of liver steatosis by ultrasound, computed tomography and magnetic resonance. J Hepatol 51: 433-445.
34. Singh S., Allen A., Wang Z., Prokop L., Murad M., Loomba R., (2014) Fibrosis progression in nonalcoholic fatty liver vs nonalcoholic steatohepatitis: a systematic review and meta-analysis of paired-biopsy studies. Clin Gastroenterol Hepatol 13: 643-654.e9.
35. Sumida Y., Nakajima A., Itoh Y., (2014) Limitations of liver biopsy and noninvasive diagnostic tests for the diagnosis of nonalcoholic fatty liver disease/nonalcoholic steatohepatitis. World J Gastroenterol 20: 475-485.
36. Szczepaniak L., Nurenberg P., Leonard D., Browning J., Reingold J., Grundy S., et al. (2005) Magnetic resonance spectroscopy to measure hepatic triglyceride content: prevalence of hepatic steatosis in the general population. Am J Physiol Endocrinol Metab 288: e462-e468.
37. Tang A., Desai A., Hamilton G., Wolfson T., Gamst A., Lam J., et al. (2015) Accuracy of MR imaging-estimated proton density fat fraction for classification of dichotomized histologic steatosis grades in nonalcoholic fatty liver disease. Radiology 274: 416-425.
38. Tang A., Tan J., Sun M., Hamilton G., Bydder M., Wolfson T., et al. (2013) Nonalcoholic fatty liver disease: MR imaging of liver proton density fat fraction to assess hepatic steatosis. Radiology 267: 422-431.
39. Vernon G., Baranova A., Younossi Z., (2011) Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment Pharmacol Ther 34: 274-285.
40. Williams C., Stengel J., Asike M., Torres D., Shaw J., Contreras M., et al. (2011) Prevalence of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis among a largely middle-aged population utilizing ultrasound and liver biopsy: a prospective study. Gastroenterology 140: 124-131.
41. Wong V., Chu W., Wong G., Chan R., Chim A., Ong A., et al. (2012) 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 61: 409-415.
42. Yokoo T., Bydder M., Hamilton G., Middleton M., Gamst A., Wolfson T., et al. (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.
43. Yokoo T., Shiehmorteza M., Hamilton G., Wolfson T., Schroeder M., Middleton M., et al. (2011) Estimation of hepatic proton-density fat fraction by using MR imaging at 3.0 T. Radiology 258: 749-759.
44. Zarrinpar A., Gupta S., Maurya M., Subramaniam S., Loomba R., (2015) Serum micrornas explain discordance of non-alcoholic fatty liver disease in monozygotic and dizygotic twins: a prospective study. Gut. doi: 10.1136/gutjnl-2015-309456. 22 2015 [Epub ahead of print].