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Pediatric Radiology
Published in: Pediatric Radiology 7/2018

01-07-2018 | Original Article

Free-breathing quantification of hepatic fat in healthy children and children with nonalcoholic fatty liver disease using a multi-echo 3-D stack-of-radial MRI technique

Authors: Tess Armstrong, Karrie V. Ly, Smruthi Murthy, Shahnaz Ghahremani, Grace Hyun J. Kim, Kara L. Calkins, Holden H. Wu

Published in: Pediatric Radiology | Issue 7/2018

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Abstract

Background

In adults, noninvasive chemical shift encoded Cartesian magnetic resonance imaging (MRI) and single-voxel magnetic resonance (MR) spectroscopy (SVS) accurately quantify hepatic steatosis but require breath-holding. In children, especially young and sick children, breath-holding is often limited or not feasible. Sedation can facilitate breath-holding but is highly undesirable. For these reasons, there is a need to develop free-breathing MRI technology that accurately quantifies steatosis in all children.

Objective

This study aimed to compare non-sedated free-breathing multi-echo 3-D stack-of-radial (radial) MRI versus standard breath-holding MRI and SVS techniques in a group of children for fat quantification with respect to image quality, accuracy and repeatability.

Materials and methods

Healthy children (n=10, median age [±interquartile range]: 10.9 [±3.3] years) and overweight children with nonalcoholic fatty liver disease (NAFLD) (n=9, median age: 15.2 [±3.2] years) were imaged at 3 Tesla using free-breathing radial MRI, breath-holding Cartesian MRI and breath-holding SVS. Acquisitions were performed twice to assess repeatability (within-subject mean difference, MDwithin). Images and hepatic proton-density fat fraction (PDFF) maps were scored for image quality. Free-breathing and breath-holding PDFF were compared using linear regression (correlation coefficient, r and concordance correlation coefficient, ρc) and Bland-Altman analysis (mean difference). P<0.05 was considered significant.

Results

In patients with NAFLD, free-breathing radial MRI demonstrated significantly less motion artifacts compared to breath-holding Cartesian (P<0.05). Free-breathing radial PDFF demonstrated a linear relationship (P<0.001) versus breath-holding SVS PDFF and breath-holding Cartesian PDFF with r=0.996 and ρc=0.994, and r=0.997 and ρc=0.995, respectively. The mean difference in PDFF between free-breathing radial MRI, breath-holding Cartesian MRI and breath-holding SVS was <0.7%. Repeated free-breathing radial MRI had MDwithin=0.25% for PDFF.

Conclusion

In this pediatric study, non-sedated free-breathing radial MRI provided accurate and repeatable hepatic PDFF measurements and improved image quality, compared to standard breath-holding MR techniques.
Appendix
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Literature
1.
2.
Schwimmer JB, Deutsch R, Kahen T et al (2006) Prevalence of fatty liver in children and adolescents. Pediatrics 118:1388–1393CrossRefPubMed
3.
Feldstein AE, Charatcharoenwitthaya P, Treeprasertsuk S et al (2009) The natural history of non-alcoholic fatty liver disease in children: a follow-up study for up to 20 years. Gut 58:1538–1544CrossRefPubMedCentralPubMed
4.
Pardee PE, Lavine JE, Schwimmer JB (2009) Diagnosis and treatment of pediatric nonalcoholic steatohepatitis and the implications for bariatric surgery. Semin Pediatr Surg 18:144–151CrossRefPubMedCentralPubMed
5.
Younossi ZM (2008) Review article: current management of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis. Aliment Pharmacol Ther 28:2–12CrossRefPubMed
6.
Uppal V, Mansoor S, Furuya KN (2016) Pediatric non-alcoholic fatty liver disease. Curr Gastroenterol Rep 18:24CrossRefPubMed
7.
Della Corte C, Vajro P, Socha P et al (2014) Pediatric non-alcoholic fatty liver disease: recent advances. Clin Res Hepatol Gastroenterol 38:419–422CrossRefPubMed
8.
Tapper EB, Lok AS-F (2017) Use of liver imaging and biopsy in clinical practice. N Engl J Med 377:756–768CrossRefPubMed
9.
Sumida Y, Nakajima A, Itoh Y (2014) Limitations of liver biopsy and non-invasive diagnostic tests for the diagnosis of nonalcoholic fatty liver disease/nonalcoholic steatohepatitis. World J Gastroenterol 20:475–485CrossRefPubMedCentralPubMed
10.
11.
Manning DS, Afdhal NH (2008) Diagnosis and quantitation of fibrosis. Gastroenterology 134:1670–1681CrossRefPubMed
12.
13.
14.
Szczepaniak LS, Nurenberg P, Leonard D 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–E468CrossRefPubMed
15.
Bohte AE, van Werven JR, Bipat S et al (2011) The diagnostic accuracy of US, CT, MRI and H-1-MRS for the evaluation of hepatic steatosis compared with liver biopsy: a meta-analysis. Eur Radiol 21:87–97CrossRefPubMed
16.
Georgoff P, Thomasson D, Louie A et al (2012) Hydrogen-1 MR spectroscopy for measurement and diagnosis of hepatic steatosis. AJR Am J Roentgenol 199:2–7CrossRefPubMedCentralPubMed
17.
Meisamy S, Hines CDG, Hamilton G 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 258:767–775CrossRefPubMedCentralPubMed
18.
Hines CDG, Yu H, Shimakawa A et al (2009) T1 independent, T2* corrected MRI with accurate spectral modeling for quantification of fat: validation in a fat-water-SPIO phantom. J Magn Reson Imaging 30:1215–1222CrossRefPubMedCentralPubMed
19.
Achmad E, Yokoo T, Hamilton G et al (2015) Feasibility of and agreement between MR imaging and spectroscopic estimation of hepatic proton density fat fraction in children with known or suspected nonalcoholic fatty liver disease. Abdom Imaging 40:3084–3090CrossRefPubMedCentralPubMed
20.
Reeder SB, Cruite I, Hamilton G et al (2011) Quantitative assessment of liver fat with magnetic resonance imaging and spectroscopy. J Magn Reson Imaging 34:729–749CrossRefPubMed
21.
Koh H, Kim S, Kim MJ et al (2015) Hepatic fat quantification magnetic resonance for monitoring treatment response in pediatric nonalcoholic steatohepatitis. World J Gastroenterol 21:9741–9748CrossRefPubMedCentralPubMed
22.
Schwimmer JB, Middleton MS, Behling C et al (2015) Magnetic resonance imaging and liver histology as biomarkers of hepatic steatosis in children with nonalcoholic fatty liver disease. Hepatology 61:1887–1895CrossRefPubMedCentralPubMed
23.
24.
Bashir MR, Zhong X, Nickel MD et al (2015) Quantification of hepatic steatosis with a multistep adaptive fitting MRI approach: prospective validation against MR spectroscopy. AJR Am J Roentgenol 204:297–306CrossRefPubMed
25.
Kühn J-P, Hernando D, Muñoz del Rio A et al (2012) Effect of multipeak spectral modeling of fat for liver iron and fat quantification: correlation of biopsy with MR imaging results. Radiology 265:133–142CrossRefPubMedCentralPubMed
26.
Idilman IS, Aniktar H, Idilman R et al (2013) Hepatic steatosis: quantification by proton density fat fraction with MR imaging versus liver biopsy. Radiology 267:767–775CrossRefPubMed
27.
Yokoo T, Shiehmorteza M, Hamilton G et al (2011) Estimation of hepatic proton-density fat fraction by using MR imaging at 3.0 T. Radiology 258:749–759CrossRefPubMedCentralPubMed
28.
Zhong X, Nickel MD, Kannengiesser SAR et al (2014) Liver fat quantification using a multi-step adaptive fitting approach with multi-echo GRE imaging. Magn Reson Med 72:1353–1365CrossRefPubMed
29.
Chavhan GB, Babyn PS, Vasanawala SS (2013) Abdominal MR imaging in children: motion compensation, sequence optimization, and protocol organization. Radiographics 33:703–719CrossRefPubMed
30.
Courtier J, Rao AG, Anupindi SA (2017) Advanced imaging techniques in pediatric body MRI. Pediatr Radiol 47:522–533CrossRefPubMed
31.
Jaimes C, Gee MS (2016) Strategies to minimize sedation in pediatric body magnetic resonance imaging. Pediatr Radiol 46:916–927CrossRefPubMed
32.
Arboleda C, Aguirre-Reyes D, García MP et al (2016) Total liver fat quantification using three-dimensional respiratory self-navigated MRI sequence. Magn Reson Med 76:1400–1409CrossRefPubMed
33.
Motosugi U, Hernando D, Bannas P et al (2015) Quantification of liver fat with respiratory-gated quantitative chemical shift encoded MRI. J Magn Reson Imaging 42:1241–1248CrossRefPubMedCentralPubMed
34.
Malamateniou C, Malik SJ, Counsell SJ et al (2013) Motion-compensation techniques in neonatal and fetal MR imaging. AJNR Am J Neuroradiol 34:1124–1136CrossRefPubMed
35.
Fujinaga Y, Kitou Y, Ohya A et al (2016) Advantages of radial volumetric breath-hold examination (VIBE) with k-space weighted image contrast reconstruction (KWIC) over Cartesian VIBE in liver imaging of volunteers simulating inadequate or no breath-holding ability. Eur Radiol 26:2790–2797CrossRefPubMed
36.
Armstrong T, Dregely I, Stemmer A et al (2018) Free-breathing liver fat quantification using a multiecho 3D stack-of-radial technique. Magn Reson Med 79:370–382CrossRefPubMed
37.
Block KT, Chandarana H, Milla S et al (2014) Towards routine clinical use of radial stack-of-stars 3D gradient-echo sequences for reducing motion sensitivity. J Korean Soc Magn Reson Med 18:87–106CrossRef
38.
Armstrong T, Martin T, Stemmer A, et al (2017) Free-breathing fat quantification in the liver using a multiecho 3D stack-of-radial technique: investigation of motion compensation and quantification accuracy. Proc. Int. Soc. Magn. Reson. Med. 25th. p 363
39.
Breuer FA, Blaimer M, Heidemann RM et al (2005) Controlled aliasing in parallel imaging results in higher acceleration (CAIPIRINHA) for multi-slice imaging. Magn Reson Med 53:1–8CrossRef
40.
Pineda N, Sharma P, Xu Q et al (2009) Measurement of hepatic lipid: high-speed T2-corrected multiecho acquisition at 1H MR spectroscopy--a rapid and accurate technique. Radiology 252:568–576CrossRefPubMed
41.
42.
Hernando D, Kellman P, Haldar JP et al (2010) Robust water/fat separation in the presence of large field inhomogeneities using a graph cut algorithm. Magn Reson Med 63:79–90PubMedCentralPubMed
43.
44.
Gleich DF (2009) Models and algorithms for pagerank sensitivity. Dissertation. Stanford University
45.
Liu CY, McKenzie CA, Yu H et al (2007) Fat quantification with IDEAL gradient echo imaging: correction of bias from T1 and noise. Magn Reson Med 58:354–364CrossRefPubMed
46.
Mann HB, Whitney DR (1947) On a test of whether one of two random variables is stochastically larger than the other. Ann Math Stat 18:50–60CrossRef
47.
Sawilowsky SS (2005) Misconceptions leading to choosing the t test over the Wilcoxon Mann-Whitney test for shift in location parameter. J Mod Appl Stat Methods 4:598–600CrossRef
48.
49.
Williams S (1996) Pearson’s correlation coefficient. N Z Med J 109:38PubMed
50.
Lin LI (1989) A concordance correlation coefficient to evaluate reproducibility. Biometrics 45:255–268CrossRefPubMed
51.
Bland JM, Altman DG (1999) Measuring agreement in method comparison studies. Stat Methods Med Res 8:135–160CrossRefPubMed
52.
Bartlett JW, Frost C (2008) Reliability, repeatability and reproducibility: analysis of measurement errors in continuous variables. Ultrasound Obstet Gynecol 31:466–475CrossRefPubMed
53.
Obuchowski NA, Reeves AP, Huang EP et al (2014) Quantitative imaging biomarkers: a review of statistical methods for computer algorithm comparisons. Stat Methods Med Res 24:68–106CrossRefPubMed
54.
55.
Yu H, McKenzie CA, Shimakawa A et al (2007) Multiecho reconstruction for simultaneous water-fat decomposition and T2* estimation. J Magn Reson Imaging 26:1153–1161CrossRefPubMed
56.
Venkatesh SK, Hennedige T, Johnson GB et al (2017) Imaging patterns and focal lesions in fatty liver: a pictorial review. Abdom Radiol 42:1374–1392CrossRef
57.
Lee H, Jun DW, Kang BK et al (2017) Estimating of hepatic fat amount using MRI proton density fat fraction in a real practice setting. Medicine (Baltimore) 96:e7778CrossRef
58.
Hamer OW, Aguirre DA, Casola G et al (2006) Fatty liver: imaging patterns and pitfalls. Radiographics 26:1637–1653CrossRefPubMed
59.
60.
Fazeli Dehkordy S, Wolfson T, William Hong C et al (2017) Liver fat reduction following bariatric weight loss surgery is greater in the right lobe of the liver. Proc. Int. Soc. Magn. Reson. Med. 25th. p 123
61.
Uecker M, Lai P, Murphy MJ et al (2014) ESPIRiT - an eigenvalue approach to autocalibrating parallel MRI: where SENSE meets GRAPPA. Magn Reson Med 71:990–1001CrossRefPubMedCentralPubMed
62.
Feng L, Axel L, Chandarana H et al (2016) XD-GRASP: golden-angle radial MRI with reconstruction of extra motion-state dimensions using compressed sensing. Magn Reson Med 75:775–788CrossRefPubMed
63.
Horng DE, Hernando D, Reeder SB (2017) Quantification of liver fat in the presence of iron overload. J Magn Reson Imaging 45:428–439CrossRefPubMed
64.
65.
Manco M, Alisi A, Real JMF et al (2011) Early interplay of intra-hepatic iron and insulin resistance in children with non-alcoholic fatty liver disease. J Hepatol 55:647–653CrossRefPubMed
66.
St Pierre TG, Clark PR, Chua-anusorn W et al (2005) Noninvasive measurement and imaging of liver iron concentrations using proton magnetic resonance. Blood 105:855–861CrossRefPubMed
67.
Doyle EK, Toy K, Valdez B et al (2018) Ultra-short echo time images quantify high liver iron. Magn Reson Med 79:1579–1585CrossRefPubMed
68.
Krafft AJ, Loeffler RB, Song R et al (2017) Quantitative ultrashort echo time imaging for assessment of massive iron overload at 1.5 and 3 tesla. Magn Reson Med 78:1839–1851CrossRefPubMed
69.
Tipirneni-Sajja A, Krafft AJ, McCarville MB et al (2017) Radial ultrashort TE imaging removes the need for breath-holding in hepatic iron overload quantification by R2* MRI. Am J Roentgenol 209:187–194CrossRef
Metadata
Title
Free-breathing quantification of hepatic fat in healthy children and children with nonalcoholic fatty liver disease using a multi-echo 3-D stack-of-radial MRI technique
Authors
Tess Armstrong
Karrie V. Ly
Smruthi Murthy
Shahnaz Ghahremani
Grace Hyun J. Kim
Kara L. Calkins
Holden H. Wu
Publication date
01-07-2018
Publisher
Springer Berlin Heidelberg
Published in
Pediatric Radiology / Issue 7/2018
Print ISSN: 0301-0449
Electronic ISSN: 1432-1998
DOI
https://doi.org/10.1007/s00247-018-4127-7

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