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Published in: European Radiology 8/2018

01-08-2018 | Gastrointestinal

Quantitative susceptibility mapping in combination with water-fat separation for simultaneous liver iron and fat fraction quantification

Authors: Huimin Lin, Hongjiang Wei, Naying He, Caixia Fu, Shu Cheng, Jun Shen, Baisong Wang, Xu Yan, Chunlei Liu, Fuhua Yan

Published in: European Radiology | Issue 8/2018

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Abstract

Purposes

To evaluate the feasibility of simultaneous quantification of liver iron concentration (LIC) and fat fraction (FF) using water-fat separation and quantitative susceptibility mapping (QSM).

Methods

Forty-five patients suspected of liver iron overload (LIO) were included. A volumetric interpolated breath-hold examination sequence for QSM and FF, a fat-saturated gradient echo sequence for R2*, a spin echo sequence for LIC measurements and MRS analyses for FF (FF-MRS) were performed. Magnetic susceptibility and FF were calculated using a water-fat separation method (FF-MRI). Correlation and receiver operating characteristic analyses were performed.

Results

Magnetic susceptibility showed strong correlation with LIC (rs=0.918). The optimal susceptibility cut-off values were 0.34, 0.63, 1.29 and 2.23 ppm corresponding to LIC thresholds of 1.8, 3.2, 7.0 and 15.0 mg/g dry weight. The area under the curve (AUC) were 0.948, 0.970, 1 and 1, respectively. No difference in AUC was found between susceptibility and R2* at all LIC thresholds. Correlation was found between FF-MRI and FF-MRS (R2=0.910).

Conclusions

QSM has a high diagnostic performance for LIC quantification, similar to that of R2*. FF-MRI provides simultaneous fat quantification. Findings suggest QSM in combination with water-fat separation has potential value for evaluating LIO, especially in cases with coexisting steatosis.

Key Points

• Magnetic susceptibility showed strong correlation with LIC (r s =0.918).
• QSM showed high diagnostic performance for LIC, similar to that of R 2 * .
• Simultaneously estimated FF-MRI showed strong correlation with MR-Spectroscopy-based FF (R 2 =0.910).
• QSM combining water-fat separation has quantitative value for LIO with coexisted steatosis.
Appendix
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Literature
1.
go back to reference Brittenham GM, Badman DG, National Institute of D, Digestive, Kidney Diseases W (2003) Noninvasive measurement of iron: report of an NIDDK workshop. Blood 101:15–19CrossRefPubMed Brittenham GM, Badman DG, National Institute of D, Digestive, Kidney Diseases W (2003) Noninvasive measurement of iron: report of an NIDDK workshop. Blood 101:15–19CrossRefPubMed
3.
go back to reference Chou ST, Fasano RM (2016) Management of Patients with Sickle Cell Disease Using Transfusion Therapy: Guidelines and Complications. Hematol Oncol Clin North Am 30:591–608CrossRefPubMed Chou ST, Fasano RM (2016) Management of Patients with Sickle Cell Disease Using Transfusion Therapy: Guidelines and Complications. Hematol Oncol Clin North Am 30:591–608CrossRefPubMed
5.
go back to reference Wood JC, Enriquez C, Ghugre N et al (2005) MRI R2 and R2* mapping accurately estimates hepatic iron concentration in transfusion-dependent thalassemia and sickle cell disease patients. Blood 106:1460–1465CrossRefPubMedPubMedCentral Wood JC, Enriquez C, Ghugre N et al (2005) MRI R2 and R2* mapping accurately estimates hepatic iron concentration in transfusion-dependent thalassemia and sickle cell disease patients. Blood 106:1460–1465CrossRefPubMedPubMedCentral
6.
7.
go back to reference Kuhn JP, Hernando D, Munoz 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 265:133–142CrossRefPubMedPubMedCentral Kuhn JP, Hernando D, Munoz 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 265:133–142CrossRefPubMedPubMedCentral
8.
go back to reference Moirand R, Mortaji AM, Loreal O, Paillard F, Brissot P, Deugnier Y (1997) A new syndrome of liver iron overload with normal transferrin saturation. Lancet 349:95–97CrossRefPubMed Moirand R, Mortaji AM, Loreal O, Paillard F, Brissot P, Deugnier Y (1997) A new syndrome of liver iron overload with normal transferrin saturation. Lancet 349:95–97CrossRefPubMed
9.
go back to reference George DK, Goldwurm S, MacDonald GA et al (1998) Increased hepatic iron concentration in nonalcoholic steatohepatitis is associated with increased fibrosis. Gastroenterology 114:311–318CrossRefPubMed George DK, Goldwurm S, MacDonald GA et al (1998) Increased hepatic iron concentration in nonalcoholic steatohepatitis is associated with increased fibrosis. Gastroenterology 114:311–318CrossRefPubMed
10.
go back to reference Wood MJ, Powell LW, Dixon JL, Ramm GA (2012) Clinical cofactors and hepatic fibrosis in hereditary hemochromatosis: the role of diabetes mellitus. Hepatology 56:904–911CrossRefPubMed Wood MJ, Powell LW, Dixon JL, Ramm GA (2012) Clinical cofactors and hepatic fibrosis in hereditary hemochromatosis: the role of diabetes mellitus. Hepatology 56:904–911CrossRefPubMed
11.
go back to reference Kuhn JP, Meffert P, Heske C et al (2017) Prevalence of Fatty Liver Disease and Hepatic Iron Overload in a Northeastern German Population by Using Quantitative MR Imaging. Radiology 284:706–716CrossRefPubMedPubMedCentral Kuhn JP, Meffert P, Heske C et al (2017) Prevalence of Fatty Liver Disease and Hepatic Iron Overload in a Northeastern German Population by Using Quantitative MR Imaging. Radiology 284:706–716CrossRefPubMedPubMedCentral
13.
go back to reference Henninger B, Zoller H, Rauch S et al (2015) R2* relaxometry for the quantification of hepatic iron overload: biopsy-based calibration and comparison with the literature. Rofo 187:472–479CrossRefPubMed Henninger B, Zoller H, Rauch S et al (2015) R2* relaxometry for the quantification of hepatic iron overload: biopsy-based calibration and comparison with the literature. Rofo 187:472–479CrossRefPubMed
14.
go back to reference Sanches-Rocha L, Serpa B, Figueiredo E, Hamerschlak N, Baroni R (2013) Comparison between multi-echo T2* with and without fat saturation pulse for quantification of liver iron overload. Magn Reson Imaging 31:1704–1708CrossRefPubMed Sanches-Rocha L, Serpa B, Figueiredo E, Hamerschlak N, Baroni R (2013) Comparison between multi-echo T2* with and without fat saturation pulse for quantification of liver iron overload. Magn Reson Imaging 31:1704–1708CrossRefPubMed
15.
go back to reference Krafft AJ, Loeffler RB, Song R et al (2016) Does fat suppression via chemically selective saturation affect R2*-MRI for transfusional iron overload assessment? A clinical evaluation at 1.5T and 3T. Magn Reson Med 76:591–601CrossRefPubMed Krafft AJ, Loeffler RB, Song R et al (2016) Does fat suppression via chemically selective saturation affect R2*-MRI for transfusional iron overload assessment? A clinical evaluation at 1.5T and 3T. Magn Reson Med 76:591–601CrossRefPubMed
16.
go back to reference Meloni A, Tyszka JM, Pepe A, Wood JC (2015) Effect of inversion recovery fat suppression on hepatic R2* quantitation in transfusional siderosis. AJR Am J Roentgenol 204:625–629CrossRefPubMedPubMedCentral Meloni A, Tyszka JM, Pepe A, Wood JC (2015) Effect of inversion recovery fat suppression on hepatic R2* quantitation in transfusional siderosis. AJR Am J Roentgenol 204:625–629CrossRefPubMedPubMedCentral
17.
go back to reference Powell EE, Ali A, Clouston AD et al (2005) Steatosis is a cofactor in liver injury in hemochromatosis. Gastroenterology 129:1937–1943CrossRefPubMed Powell EE, Ali A, Clouston AD et al (2005) Steatosis is a cofactor in liver injury in hemochromatosis. Gastroenterology 129:1937–1943CrossRefPubMed
18.
go back to reference Galimberti S, Trombini P, Bernasconi DP et al (2015) Simultaneous liver iron and fat measures by magnetic resonance imaging in patients with hyperferritinemia. Scand J Gastroenterol 50:429–438CrossRefPubMed Galimberti S, Trombini P, Bernasconi DP et al (2015) Simultaneous liver iron and fat measures by magnetic resonance imaging in patients with hyperferritinemia. Scand J Gastroenterol 50:429–438CrossRefPubMed
19.
go back to reference Franca M, Alberich-Bayarri A, Marti-Bonmati L et al (2017) Accurate simultaneous quantification of liver steatosis and iron overload in diffuse liver diseases with MRI. Abdom Radiol (NY) 42:1434–1443CrossRef Franca M, Alberich-Bayarri A, Marti-Bonmati L et al (2017) Accurate simultaneous quantification of liver steatosis and iron overload in diffuse liver diseases with MRI. Abdom Radiol (NY) 42:1434–1443CrossRef
20.
go back to reference Henninger B, Zoller H, Kannengiesser S, Zhong X, Jaschke W, Kremser C (2017) 3D Multiecho Dixon for the Evaluation of Hepatic Iron and Fat in a Clinical Setting. J Magn Reson Imaging 46:793–800CrossRefPubMed Henninger B, Zoller H, Kannengiesser S, Zhong X, Jaschke W, Kremser C (2017) 3D Multiecho Dixon for the Evaluation of Hepatic Iron and Fat in a Clinical Setting. J Magn Reson Imaging 46:793–800CrossRefPubMed
21.
go back to reference Taylor BA, Loeffler RB, Song R, McCarville MB, Hankins JS, Hillenbrand CM (2012) Simultaneous field and R2 mapping to quantify liver iron content using autoregressive moving average modeling. J Magn Reson Imaging 35:1125–1132CrossRefPubMed Taylor BA, Loeffler RB, Song R, McCarville MB, Hankins JS, Hillenbrand CM (2012) Simultaneous field and R2 mapping to quantify liver iron content using autoregressive moving average modeling. J Magn Reson Imaging 35:1125–1132CrossRefPubMed
22.
go back to reference Liu C, Wei H, Gong NJ, Cronin M, Dibb R, Decker K (2015) Quantitative susceptibility mapping: contrast mechanisms and clinical applications. Tomography 1:3–17CrossRefPubMedPubMedCentral Liu C, Wei H, Gong NJ, Cronin M, Dibb R, Decker K (2015) Quantitative susceptibility mapping: contrast mechanisms and clinical applications. Tomography 1:3–17CrossRefPubMedPubMedCentral
23.
go back to reference Wei H, Xie L, Dibb R et al (2016) Imaging whole-brain cytoarchitecture of mouse with MRI-based quantitative susceptibility mapping. Neuroimage 137:107–115CrossRefPubMedPubMedCentral Wei H, Xie L, Dibb R et al (2016) Imaging whole-brain cytoarchitecture of mouse with MRI-based quantitative susceptibility mapping. Neuroimage 137:107–115CrossRefPubMedPubMedCentral
24.
go back to reference Sharma SD, Fischer R, Schoennagel BP et al (2017) MRI-based quantitative susceptibility mapping (QSM) and R2* mapping of liver iron overload: Comparison with SQUID-based biomagnetic liver susceptometry. Magn Reson Med 78:264–270CrossRefPubMed Sharma SD, Fischer R, Schoennagel BP et al (2017) MRI-based quantitative susceptibility mapping (QSM) and R2* mapping of liver iron overload: Comparison with SQUID-based biomagnetic liver susceptometry. Magn Reson Med 78:264–270CrossRefPubMed
25.
go back to reference Yu H, Shimakawa A, McKenzie CA, Brodsky E, Brittain JH, Reeder SB (2008) Multiecho water-fat separation and simultaneous R2* estimation with multifrequency fat spectrum modeling. Magn Reson Med 60:1122–1134CrossRefPubMedPubMedCentral Yu H, Shimakawa A, McKenzie CA, Brodsky E, Brittain JH, Reeder SB (2008) Multiecho water-fat separation and simultaneous R2* estimation with multifrequency fat spectrum modeling. Magn Reson Med 60:1122–1134CrossRefPubMedPubMedCentral
26.
go back to reference Pineda N, Sharma P, Xu Q, Hu X, Vos M, Martin DR (2009) Measurement of hepatic lipid: high-speed T2-corrected multiecho acquisition at 1H MR spectroscopy--a rapid and accurate technique. Radiology 252:568–576CrossRefPubMed Pineda N, Sharma P, Xu Q, Hu X, Vos M, Martin DR (2009) Measurement of hepatic lipid: high-speed T2-corrected multiecho acquisition at 1H MR spectroscopy--a rapid and accurate technique. Radiology 252:568–576CrossRefPubMed
27.
go back to reference Hamilton G, Yokoo T, Bydder M et al (2011) In vivo characterization of the liver fat 1H MR spectrum. NMR Biomed 24:784–790CrossRefPubMed Hamilton G, Yokoo T, Bydder M et al (2011) In vivo characterization of the liver fat 1H MR spectrum. NMR Biomed 24:784–790CrossRefPubMed
28.
go back to reference Wu B, Li W, Guidon A, Liu C (2012) Whole brain susceptibility mapping using compressed sensing. Magn Reson Med 67:137–147CrossRefPubMed Wu B, Li W, Guidon A, Liu C (2012) Whole brain susceptibility mapping using compressed sensing. Magn Reson Med 67:137–147CrossRefPubMed
29.
go back to reference Wei H, Dibb R, Zhou Y et al (2015) Streaking artifact reduction for quantitative susceptibility mapping of sources with large dynamic range. NMR Biomed 28:1294–1303CrossRefPubMedPubMedCentral Wei H, Dibb R, Zhou Y et al (2015) Streaking artifact reduction for quantitative susceptibility mapping of sources with large dynamic range. NMR Biomed 28:1294–1303CrossRefPubMedPubMedCentral
31.
go back to reference Feng Y, He T, Gatehouse PD et al (2013) Improved MRI R2 * relaxometry of iron-loaded liver with noise correction. Magn Reson Med 70:1765–1774CrossRefPubMed Feng Y, He T, Gatehouse PD et al (2013) Improved MRI R2 * relaxometry of iron-loaded liver with noise correction. Magn Reson Med 70:1765–1774CrossRefPubMed
32.
go back to reference DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44:837–845CrossRefPubMed DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44:837–845CrossRefPubMed
33.
go back to reference Sharma SD, Hernando D, Horng DE, Reeder SB (2015) Quantitative susceptibility mapping in the abdomen as an imaging biomarker of hepatic iron overload. Magn Reson Med 74:673–683CrossRefPubMed Sharma SD, Hernando D, Horng DE, Reeder SB (2015) Quantitative susceptibility mapping in the abdomen as an imaging biomarker of hepatic iron overload. Magn Reson Med 74:673–683CrossRefPubMed
34.
go back to reference Longo R, Ricci C, Masutti F et al (1993) Fatty infiltration of the liver. Quantification by 1H localized magnetic resonance spectroscopy and comparison with computed tomography. Invest Radiol 28:297–302CrossRefPubMed Longo R, Ricci C, Masutti F et al (1993) Fatty infiltration of the liver. Quantification by 1H localized magnetic resonance spectroscopy and comparison with computed tomography. Invest Radiol 28:297–302CrossRefPubMed
35.
go back to reference Wood JC (2014) Guidelines for quantifying iron overload. Hematology Am Soc Hematol Educ Program 2014:210–215PubMed Wood JC (2014) Guidelines for quantifying iron overload. Hematology Am Soc Hematol Educ Program 2014:210–215PubMed
36.
go back to reference Olivieri NF, Brittenham GM (1997) Iron-chelating therapy and the treatment of thalassemia. Blood 89:739–761PubMed Olivieri NF, Brittenham GM (1997) Iron-chelating therapy and the treatment of thalassemia. Blood 89:739–761PubMed
37.
go back to reference Harrison SA, Bacon BR (2005) Relation of hemochromatosis with hepatocellular carcinoma: epidemiology, natural history, pathophysiology, screening, treatment, and prevention. Med Clin North Am 89:391–409CrossRefPubMed Harrison SA, Bacon BR (2005) Relation of hemochromatosis with hepatocellular carcinoma: epidemiology, natural history, pathophysiology, screening, treatment, and prevention. Med Clin North Am 89:391–409CrossRefPubMed
38.
go back to reference Kang BK, Yu ES, Lee SS et al (2012) 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 47:368–375CrossRefPubMed Kang BK, Yu ES, Lee SS et al (2012) 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 47:368–375CrossRefPubMed
39.
go back to reference Hong CW, Mamidipalli A, Hooker JC et al (2017) MRI proton density fat fraction is robust across the biologically plausible range of triglyceride spectra in adults with nonalcoholic steatohepatitis. J Magn Reson Imaging. https://doi.org/10.1002/jmri.25845 Hong CW, Mamidipalli A, Hooker JC et al (2017) MRI proton density fat fraction is robust across the biologically plausible range of triglyceride spectra in adults with nonalcoholic steatohepatitis. J Magn Reson Imaging. https://​doi.​org/​10.​1002/​jmri.​25845
40.
go back to reference Satkunasingham J, Besa C, Bane O et al (2015) Liver fat quantification: Comparison of dual-echo and triple-echo chemical shift MRI to MR spectroscopy. Eur J Radiol 84:1452–1458CrossRefPubMed Satkunasingham J, Besa C, Bane O et al (2015) Liver fat quantification: Comparison of dual-echo and triple-echo chemical shift MRI to MR spectroscopy. Eur J Radiol 84:1452–1458CrossRefPubMed
41.
go back to reference Zhong X, Nickel MD, Kannengiesser SA, Dale BM, Kiefer B, Bashir MR (2014) Liver fat quantification using a multi-step adaptive fitting approach with multi-echo GRE imaging. Magn Reson Med 72:1353–1365CrossRefPubMed Zhong X, Nickel MD, Kannengiesser SA, Dale BM, Kiefer B, Bashir MR (2014) Liver fat quantification using a multi-step adaptive fitting approach with multi-echo GRE imaging. Magn Reson Med 72:1353–1365CrossRefPubMed
42.
go back to reference Yokoo T, Browning JD (2014) Fat and iron quantification in the liver: past, present, and future. Top Magn Reson Imaging 23:73–94CrossRefPubMed Yokoo T, Browning JD (2014) Fat and iron quantification in the liver: past, present, and future. Top Magn Reson Imaging 23:73–94CrossRefPubMed
43.
go back to reference St Pierre TG, El-Beshlawy A, Elalfy M et al (2014) Multicenter validation of spin-density projection-assisted R2-MRI for the noninvasive measurement of liver iron concentration. Magn Reson Med 71:2215–2223CrossRefPubMed St Pierre TG, El-Beshlawy A, Elalfy M et al (2014) Multicenter validation of spin-density projection-assisted R2-MRI for the noninvasive measurement of liver iron concentration. Magn Reson Med 71:2215–2223CrossRefPubMed
44.
go back to reference Xie L, Sparks MA, Li W et al (2013) Quantitative susceptibility mapping of kidney inflammation and fibrosis in type 1 angiotensin receptor-deficient mice. NMR Biomed 26:1853–1863CrossRefPubMedPubMedCentral Xie L, Sparks MA, Li W et al (2013) Quantitative susceptibility mapping of kidney inflammation and fibrosis in type 1 angiotensin receptor-deficient mice. NMR Biomed 26:1853–1863CrossRefPubMedPubMedCentral
46.
go back to reference Luo XF, Xie XQ, Cheng S et al (2015) Dual-energy CT for patients suspected of having liver iron overload: can virtual iron content imaging accurately quantify liver iron content? Radiology 277:95–103CrossRefPubMed Luo XF, Xie XQ, Cheng S et al (2015) Dual-energy CT for patients suspected of having liver iron overload: can virtual iron content imaging accurately quantify liver iron content? Radiology 277:95–103CrossRefPubMed
47.
go back to reference Wang Y, Liu T (2015) Quantitative susceptibility mapping (QSM): Decoding MRI data for a tissue magnetic biomarker. Magn Reson Med 73:82–101CrossRefPubMed Wang Y, Liu T (2015) Quantitative susceptibility mapping (QSM): Decoding MRI data for a tissue magnetic biomarker. Magn Reson Med 73:82–101CrossRefPubMed
48.
go back to reference Henninger B, Kremser C, Rauch S et al (2012) Evaluation of MR imaging with T1 and T2* mapping for the determination of hepatic iron overload. Eur Radiol 22:2478–2486CrossRefPubMed Henninger B, Kremser C, Rauch S et al (2012) Evaluation of MR imaging with T1 and T2* mapping for the determination of hepatic iron overload. Eur Radiol 22:2478–2486CrossRefPubMed
Metadata
Title
Quantitative susceptibility mapping in combination with water-fat separation for simultaneous liver iron and fat fraction quantification
Authors
Huimin Lin
Hongjiang Wei
Naying He
Caixia Fu
Shu Cheng
Jun Shen
Baisong Wang
Xu Yan
Chunlei Liu
Fuhua Yan
Publication date
01-08-2018
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 8/2018
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-017-5263-4

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