Skip to main content
Erschienen in: European Radiology 8/2022

21.03.2022 | Magnetic Resonance

Improved free-breathing liver fat and iron quantification using a 2D chemical shift–encoded MRI with flip angle modulation and motion-corrected averaging

verfasst von: Jitka Starekova, Ruiyang Zhao, Timothy J. Colgan, Kevin M. Johnson, Jennifer L. Rehm, Shane A. Wells, Scott B. Reeder, Diego Hernando

Erschienen in: European Radiology | Ausgabe 8/2022

Einloggen, um Zugang zu erhalten

Abstract

Objectives

3D chemical shift–encoded (CSE) MRI enables accurate and precise quantification of proton density fat fraction (PDFF) and R2*, biomarkers of hepatic fat and iron deposition. Unfortunately, 3D CSE-MRI requires reliable breath-holding. Free-breathing 2D CSE-MRI with sequential radiofrequency excitation is a motion-robust alternative but suffers from low signal-to-noise-ratio (SNR). To overcome this limitation, this work explores the combination of flip angle–modulated (FAM) 2D CSE imaging with a non-local means (NLM) motion-corrected averaging technique.

Methods

In this prospective study, 35 healthy subjects (27 children/8 adults) were imaged on a 3T MRI-system. Multi-echo 3D CSE (“3D”) and 2D CSE FAM (“FAM”) images were acquired during breath-hold and free-breathing, respectively, to obtain PDFF and R2* maps of the liver. Multi-repetition FAM was postprocessed with direct averaging (DA)– and NLM-based averaging and compared to 3D CSE using Bland-Altmann and regression analysis. Image qualities of PDFF and R2* maps were reviewed by two radiologists using a Likert-like scale (score 1–5, 5 = best).

Results

Compared to 3D CSE, multi-repetition FAM-NLM showed excellent agreement (regression slope = 1.0, R2 = 0.996) for PDFF and good agreement (regression slope 1.08–1.15, R2 ≥ 0.899) for R2*. Further, multi-repetition FAM-NLM PDFF and R2* maps had fewer artifacts (score 3.8 vs. 3.2, p < 0.0001 for PDFF; score 3.2 vs. 2.6, p < 0.001 for R2*) and better overall image quality (score 4.0 vs. 3.5, p < 0.0001 for PDFF; score 3.4 vs. 2.7, p < 0.0001 for R2*).

Conclusions

Free-breathing FAM-NLM provides superior image quality of the liver compared to the conventional breath-hold 3D CSE-MRI, while minimizing bias for PDFF and R2* quantification.

Key Points

2D CSE FAM-NLM is a free-breathing method for liver fat and iron quantification and viable alternative for patients unable to hold their breath.
2D CSE FAM-NLM is a feasible alternative to breath-hold 3D CSE methods, with low bias in proton density fat fraction (PDFF) and no clinically significant bias in R2*.
Quantitatively, multiple repetitions in 2D CSE FAM-NLM lead to improved SNR.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat Reeder SB, Cruite I, Hamilton G, Sirlin CB (2011) Quantitative assessment of liver fat with magnetic resonance imaging and spectroscopy. J Magn Reson Imaging 34:729–749CrossRef Reeder SB, Cruite I, Hamilton G, Sirlin CB (2011) Quantitative assessment of liver fat with magnetic resonance imaging and spectroscopy. J Magn Reson Imaging 34:729–749CrossRef
2.
Zurück zum Zitat Yokoo T, Serai SD, Pirasteh A et al (2018) Linearity, bias, and precision of hepatic proton density fat fraction measurements by using MR imaging: a meta-analysis. Radiology 286:486–498CrossRef Yokoo T, Serai SD, Pirasteh A et al (2018) Linearity, bias, and precision of hepatic proton density fat fraction measurements by using MR imaging: a meta-analysis. Radiology 286:486–498CrossRef
3.
Zurück zum Zitat Reeder SB, Hu HH, Sirlin CB (2012) Proton density fat-fraction: a standardized MR-based biomarker of tissue fat concentration. J Magn Reson Imaging 36:1011–1014CrossRef Reeder SB, Hu HH, Sirlin CB (2012) Proton density fat-fraction: a standardized MR-based biomarker of tissue fat concentration. J Magn Reson Imaging 36:1011–1014CrossRef
4.
Zurück zum Zitat Caussy C, Reeder SB, Sirlin CB, Loomba R (2018) Noninvasive, quantitative assessment of liver fat by MRI-PDFF as an endpoint in NASH trials. Hepatology 68:763–772CrossRef Caussy C, Reeder SB, Sirlin CB, Loomba R (2018) Noninvasive, quantitative assessment of liver fat by MRI-PDFF as an endpoint in NASH trials. Hepatology 68:763–772CrossRef
5.
Zurück zum Zitat Younossi ZM, Koenig AB, Abdelatif D et al (2016) Global epidemiology of nonalcoholic fatty liver disease—meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology 64:73–84CrossRef Younossi ZM, Koenig AB, Abdelatif D et al (2016) Global epidemiology of nonalcoholic fatty liver disease—meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology 64:73–84CrossRef
6.
Zurück zum Zitat Hernando D, Levin YS, Sirlin CB, Reeder SB (2014) Quantification of liver iron with MRI: State of the art and remaining challenges. J Magn Reson Imaging 40:1003–1021CrossRef Hernando D, Levin YS, Sirlin CB, Reeder SB (2014) Quantification of liver iron with MRI: State of the art and remaining challenges. J Magn Reson Imaging 40:1003–1021CrossRef
7.
Zurück zum Zitat 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 265:133–142CrossRef 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 265:133–142CrossRef
8.
Zurück zum Zitat Starekova J, Reeder SB (2020) Liver fat quantification: where do we stand? Abdom Radiol (NY) 45:3386–3399 Starekova J, Reeder SB (2020) Liver fat quantification: where do we stand? Abdom Radiol (NY) 45:3386–3399
9.
Zurück zum Zitat Zhao R, Zhang Y, Wang X et al (2020) Motion-robust, high-SNR liver fat quantification using a 2D sequential acquisition with a variable flip angle approach. Magn Reson Med 84:2004–2017CrossRef Zhao R, Zhang Y, Wang X et al (2020) Motion-robust, high-SNR liver fat quantification using a 2D sequential acquisition with a variable flip angle approach. Magn Reson Med 84:2004–2017CrossRef
10.
Zurück zum Zitat 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 42:1241–1248CrossRef 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 42:1241–1248CrossRef
11.
Zurück zum Zitat 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 79:370–382CrossRef 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 79:370–382CrossRef
12.
Zurück zum Zitat Luo H, Zhu A, Wiens CN et al (2021) Free-breathing liver fat and quantification using motion-corrected averaging based on a nonlocal means algorithm. Magn Reson Med 85:653–666CrossRef Luo H, Zhu A, Wiens CN et al (2021) Free-breathing liver fat and quantification using motion-corrected averaging based on a nonlocal means algorithm. Magn Reson Med 85:653–666CrossRef
13.
Zurück zum Zitat Moriguchi H, Lewin JS, Duerk JL (2003) Dixon techniques in spiral trajectories with off-resonance correction: a new approach for fat signal suppression without spatial-spectral RF pulses. Magn Reson Med 50:915–924CrossRef Moriguchi H, Lewin JS, Duerk JL (2003) Dixon techniques in spiral trajectories with off-resonance correction: a new approach for fat signal suppression without spatial-spectral RF pulses. Magn Reson Med 50:915–924CrossRef
14.
Zurück zum Zitat Börnert P, Koken P, Eggers H (2010) Spiral water-fat imaging with integrated off-resonance correction on a clinical scanner. J Magn Reson Imaging 32:1262–1267CrossRef Börnert P, Koken P, Eggers H (2010) Spiral water-fat imaging with integrated off-resonance correction on a clinical scanner. J Magn Reson Imaging 32:1262–1267CrossRef
15.
Zurück zum Zitat Pipe JG (1999) Motion correction with PROPELLER MRI: application to head motion and free-breathing cardiac imaging. Magn Reson Med 42:963–969CrossRef Pipe JG (1999) Motion correction with PROPELLER MRI: application to head motion and free-breathing cardiac imaging. Magn Reson Med 42:963–969CrossRef
16.
Zurück zum Zitat Moran CJ, Brodsky EK, Bancroft LH et al (2014) High-resolution 3D radial bSSFP with IDEAL. Magn Reson Med 71:95–104CrossRef Moran CJ, Brodsky EK, Bancroft LH et al (2014) High-resolution 3D radial bSSFP with IDEAL. Magn Reson Med 71:95–104CrossRef
17.
Zurück zum Zitat Hernando D, Sharma SD, Aliyari Ghasabeh M et al (2017) Multisite, multivendor validation of the accuracy and reproducibility of proton-density fat-fraction quantification at 1.5 T and 3T using a fat-water phantom. Magn Reson Med 77:1516–1524 Hernando D, Sharma SD, Aliyari Ghasabeh M et al (2017) Multisite, multivendor validation of the accuracy and reproducibility of proton-density fat-fraction quantification at 1.5 T and 3T using a fat-water phantom. Magn Reson Med 77:1516–1524
18.
Zurück zum Zitat 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 58:354–364CrossRef 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 58:354–364CrossRef
19.
Zurück zum Zitat Pooler BD, Hernando D, Ruby JA et al (2018) Validation of a motion-robust 2D sequential technique for quantification of hepatic proton density fat fraction during free breathing. J Magn Reson Imaging 48:1578–1585CrossRef Pooler BD, Hernando D, Ruby JA et al (2018) Validation of a motion-robust 2D sequential technique for quantification of hepatic proton density fat fraction during free breathing. J Magn Reson Imaging 48:1578–1585CrossRef
20.
Zurück zum Zitat Rehm JL, Wolfgram PM, Hernando D et al (2015) Proton density fat-fraction is an accurate biomarker of hepatic steatosis in adolescent girls and young women. Eur Radiol 25:2921–2930 Rehm JL, Wolfgram PM, Hernando D et al (2015) Proton density fat-fraction is an accurate biomarker of hepatic steatosis in adolescent girls and young women. Eur Radiol 25:2921–2930
21.
Zurück zum Zitat di Martino M, Pacifico L, Bezzi M et al (2016) Comparison of magnetic resonance spectroscopy, proton density fat fraction and histological analysis in the quantification of liver steatosis in children and adolescents. World J Gastroenterol 22:8812–8819CrossRef di Martino M, Pacifico L, Bezzi M et al (2016) Comparison of magnetic resonance spectroscopy, proton density fat fraction and histological analysis in the quantification of liver steatosis in children and adolescents. World J Gastroenterol 22:8812–8819CrossRef
22.
Zurück zum Zitat Kwee TC, Takahara T, Koh DM et al (2008) Comparison and reproducibility of ADC measurements in breathhold, respiratory triggered, and free-breathing diffusion-weighted MR imaging of the liver. J Magn Reson Imaging 28:1141–1148CrossRef Kwee TC, Takahara T, Koh DM et al (2008) Comparison and reproducibility of ADC measurements in breathhold, respiratory triggered, and free-breathing diffusion-weighted MR imaging of the liver. J Magn Reson Imaging 28:1141–1148CrossRef
23.
Zurück zum Zitat Hamilton G, Middleton MS, Hooker JC et al (2015) In vivo breath-hold 1H MRS simultaneous estimation of liver proton density fat fraction, and T1 and T2 of water and fat, with a multi-TR, multi-TE sequence. J Magn Reson Imaging 42:1538–1543CrossRef Hamilton G, Middleton MS, Hooker JC et al (2015) In vivo breath-hold 1H MRS simultaneous estimation of liver proton density fat fraction, and T1 and T2 of water and fat, with a multi-TR, multi-TE sequence. J Magn Reson Imaging 42:1538–1543CrossRef
24.
Zurück zum Zitat Hernando D, Hamilton G, Roldan-Alzate A, Reeder SB (2014) Fully automated processing of multi-echo spectroscopy data for liver fat quantification. . In Proceedings of the Annual Meeting of the International Society for Magnetic Resonance in Medicine, Milan(10-16 May), Abstract 2884 Hernando D, Hamilton G, Roldan-Alzate A, Reeder SB (2014) Fully automated processing of multi-echo spectroscopy data for liver fat quantification. . In Proceedings of the Annual Meeting of the International Society for Magnetic Resonance in Medicine, Milan(10-16 May), Abstract 2884
25.
Zurück zum Zitat Hines CDG, Frydrychowicz A, Hamilton G et al (2011) T1 independent, T2* 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 33:873–881CrossRef Hines CDG, Frydrychowicz A, Hamilton G et al (2011) T1 independent, T2* 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 33:873–881CrossRef
26.
Zurück zum Zitat Holdsworth SJ, MacPherson SJ, Yeom KW et al (2018) Clinical evaluation of silent T1-weighted MRI and silent MR angiography of the brain. AJR Am J Roentgenol 210:404–411 Holdsworth SJ, MacPherson SJ, Yeom KW et al (2018) Clinical evaluation of silent T1-weighted MRI and silent MR angiography of the brain. AJR Am J Roentgenol 210:404–411
27.
Zurück zum Zitat Kenkel D, Barth BK, Piccirelli M et al (2017) Simultaneous multislice diffusion-weighted imaging of the kidney. Invest Radiol 52:163–169CrossRef Kenkel D, Barth BK, Piccirelli M et al (2017) Simultaneous multislice diffusion-weighted imaging of the kidney. Invest Radiol 52:163–169CrossRef
28.
Zurück zum Zitat Campo CA, Hernando D, Schubert T et al (2017) Standardized approach for ROI-based measurements of proton density fat fraction and R2* in the liver. AJR Am J Roentgenol 209:592–603 Campo CA, Hernando D, Schubert T et al (2017) Standardized approach for ROI-based measurements of proton density fat fraction and R2* in the liver. AJR Am J Roentgenol 209:592–603
29.
Zurück zum Zitat Fernandez-Seara MA, Wehrli FW (2000) Postprocessing technique to correct for background gradients in image-based R*(2) measurements. Magn Reson Med 44:358–366CrossRef Fernandez-Seara MA, Wehrli FW (2000) Postprocessing technique to correct for background gradients in image-based R*(2) measurements. Magn Reson Med 44:358–366CrossRef
30.
Zurück zum Zitat Hernando D, Vigen KK, Shimakawa A, Reeder SB (2012) R2* mapping in the presence of macroscopic B0 field variations. Magn Reson Med 68:830–840CrossRef Hernando D, Vigen KK, Shimakawa A, Reeder SB (2012) R2* mapping in the presence of macroscopic B0 field variations. Magn Reson Med 68:830–840CrossRef
31.
Zurück zum Zitat Zhong X, Armstrong T, Nickel MD et al (2020) Effect of respiratory motion on free-breathing 3D stack-of-radial liver R*2 relaxometry and improved quantification accuracy using self-gating. Magn Reson Medicine 83:1964–1978CrossRef Zhong X, Armstrong T, Nickel MD et al (2020) Effect of respiratory motion on free-breathing 3D stack-of-radial liver R*2 relaxometry and improved quantification accuracy using self-gating. Magn Reson Medicine 83:1964–1978CrossRef
32.
Zurück zum Zitat Armstrong T, Ly Kv., Ghahremani S, et al (2019) Free-breathing 3-D quantification of infant body composition and hepatic fat using a stack-of-radial magnetic resonance imaging technique. Pediatric Radiology 49:876–888 Armstrong T, Ly Kv., Ghahremani S, et al (2019) Free-breathing 3-D quantification of infant body composition and hepatic fat using a stack-of-radial magnetic resonance imaging technique. Pediatric Radiology 49:876–888
33.
Zurück zum Zitat Rohani SC, Morin CE, Zhong X et al (2021, 2021) Hepatic iron quantification using a free-breathing 3D radial gradient echo technique and validation with a 2D biopsy-calibrated R2* relaxometry method. J Magn Reson Imaging. https://doi.org/10.1002/jmri.27921 Rohani SC, Morin CE, Zhong X et al (2021, 2021) Hepatic iron quantification using a free-breathing 3D radial gradient echo technique and validation with a 2D biopsy-calibrated R2* relaxometry method. J Magn Reson Imaging. https://​doi.​org/​10.​1002/​jmri.​27921
34.
Zurück zum Zitat Doneva M, Börnert P, Eggers H et al (2010) Compressed sensing for chemical shift-based water-fat separation. Magn Reson Med 64:1749–1759CrossRef Doneva M, Börnert P, Eggers H et al (2010) Compressed sensing for chemical shift-based water-fat separation. Magn Reson Med 64:1749–1759CrossRef
35.
Zurück zum Zitat Noureddin M, Lam J, Peterson MR et al (2013) Utility of magnetic resonance imaging versus histology for quantifying changes in liver fat in nonalcoholic fatty liver disease trials. Hepatology 58:1930–1940CrossRef Noureddin M, Lam J, Peterson MR et al (2013) Utility of magnetic resonance imaging versus histology for quantifying changes in liver fat in nonalcoholic fatty liver disease trials. Hepatology 58:1930–1940CrossRef
36.
Zurück zum Zitat Kim B, Kim SY, Kim KW et al (2018) MRI in donor candidates for living donor liver transplant: technical and practical considerations. J Magn Reson Imaging 48:1453–1467CrossRef Kim B, Kim SY, Kim KW et al (2018) MRI in donor candidates for living donor liver transplant: technical and practical considerations. J Magn Reson Imaging 48:1453–1467CrossRef
Metadaten
Titel
Improved free-breathing liver fat and iron quantification using a 2D chemical shift–encoded MRI with flip angle modulation and motion-corrected averaging
verfasst von
Jitka Starekova
Ruiyang Zhao
Timothy J. Colgan
Kevin M. Johnson
Jennifer L. Rehm
Shane A. Wells
Scott B. Reeder
Diego Hernando
Publikationsdatum
21.03.2022
Verlag
Springer Berlin Heidelberg
Erschienen in
European Radiology / Ausgabe 8/2022
Print ISSN: 0938-7994
Elektronische ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-022-08682-x

Weitere Artikel der Ausgabe 8/2022

European Radiology 8/2022 Zur Ausgabe

Update Radiologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.