Diffusion-weighted stimulated echo acquisition mode (DW-STEAM) MR spectroscopy to measure fat unsaturation in regions with low proton-density fat fraction
Corresponding Author
Stefan Ruschke
Department of Diagnostic and Interventional Radiology, Technische Universität München, Munich, Germany
Correspondence to: Stefan Ruschke, M.Sc., Department of Diagnostic and Interventional Radiology, Klinikum rechts der Isar, Technische Universität München, Ismaninger Str. 22, 81675 Munich, Germany. E-mail: [email protected]Search for more papers by this authorHermine Kienberger
Bioanalytik Weihenstephan, Research Center for Nutrition and Food Sciences, Technische Universität München, Freising, Germany
Search for more papers by this authorThomas Baum
Department of Diagnostic and Interventional Radiology, Technische Universität München, Munich, Germany
Search for more papers by this authorMarcus Settles
Department of Diagnostic and Interventional Radiology, Technische Universität München, Munich, Germany
Search for more papers by this authorAxel Haase
Zentralinstitut für, Medizintechnik, Technische Universität München, Garching, Germany
Search for more papers by this authorMichael Rychlik
Bioanalytik Weihenstephan, Research Center for Nutrition and Food Sciences, Technische Universität München, Freising, Germany
Chair of Analytical Food Chemistry, Technische Universität München, Freising, Germany
Search for more papers by this authorErnst J. Rummeny
Department of Diagnostic and Interventional Radiology, Technische Universität München, Munich, Germany
Search for more papers by this authorDimitrios C. Karampinos
Department of Diagnostic and Interventional Radiology, Technische Universität München, Munich, Germany
Search for more papers by this authorCorresponding Author
Stefan Ruschke
Department of Diagnostic and Interventional Radiology, Technische Universität München, Munich, Germany
Correspondence to: Stefan Ruschke, M.Sc., Department of Diagnostic and Interventional Radiology, Klinikum rechts der Isar, Technische Universität München, Ismaninger Str. 22, 81675 Munich, Germany. E-mail: [email protected]Search for more papers by this authorHermine Kienberger
Bioanalytik Weihenstephan, Research Center for Nutrition and Food Sciences, Technische Universität München, Freising, Germany
Search for more papers by this authorThomas Baum
Department of Diagnostic and Interventional Radiology, Technische Universität München, Munich, Germany
Search for more papers by this authorMarcus Settles
Department of Diagnostic and Interventional Radiology, Technische Universität München, Munich, Germany
Search for more papers by this authorAxel Haase
Zentralinstitut für, Medizintechnik, Technische Universität München, Garching, Germany
Search for more papers by this authorMichael Rychlik
Bioanalytik Weihenstephan, Research Center for Nutrition and Food Sciences, Technische Universität München, Freising, Germany
Chair of Analytical Food Chemistry, Technische Universität München, Freising, Germany
Search for more papers by this authorErnst J. Rummeny
Department of Diagnostic and Interventional Radiology, Technische Universität München, Munich, Germany
Search for more papers by this authorDimitrios C. Karampinos
Department of Diagnostic and Interventional Radiology, Technische Universität München, Munich, Germany
Search for more papers by this authorAbstract
Purpose
To propose and optimize diffusion-weighted stimulated echo acquisition mode (DW-STEAM) for measuring fat unsaturation in the presence of a strong water signal by suppressing the water signal based on a shorter T2 and higher diffusivity of water relative to fat.
Methods
A parameter study for point-resolved spectroscopy (PRESS) and STEAM using oil phantoms was performed and correlated with gas chromatography (GC). Simulations of muscle tissue signal behavior using DW-STEAM and long–echo time (TE) PRESS and a parameter optimization for DW-STEAM were conducted. DW-STEAM and long-TE PRESS were applied in the gastrocnemius muscles of nine healthy subjects.
Results
STEAM with TE and mixing time (TM) up to 45 ms exhibited R2 correlations above 0.98 with GC and little T2-weighting and J-modulation for the quantified olefinic/methylene peak ratio. The optimal parameters for muscle tissue using DW-STEAM were b-value = 1800 s/mm2, TE = 33 ms, TM = 30 ms, and repetition time = 2300 ms. In vivo measured mean olefinic signal-to-noise ratios were 72 and 40, mean apparent olefinic water fractions were 0.19 and 0.11 for DW-STEAM and long-TE PRESS, respectively.
Conclusion
Optimized DW-STEAM MR spectroscopy is superior to long-TE PRESS for measuring fat unsaturation, if a strong water peak prevents the olefinic fat signal's quantification at shorter TEs and water's tissue specific ADC is substantially higher than fat. Magn Reson Med 75:32–41, 2016. © 2015 Wiley Periodicals, Inc.
Supporting Information
Additional Supporting Information may be found in the online version of this article.
Filename | Description |
---|---|
mrm25578-sup-0001-suppfig1.docx187.6 KB |
Supporting Information Figure 1. R2 correlation between STEAM-TE and GC results for area ratio F to B and ULtotal, fUL, and fPUL as described by Ye et al. (12). C1 refers to the α-olefinic contribution at 2.02 ppm of peak C only. The series parameters for STEAM-TE were as follows: TE = 12–200 ms, TM = 16 ms, and TR = 2300 ms. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- 1Ren J, Dimitrov I, Sherry AD, Malloy CR. Composition of adipose tissue and marrow fat in humans by 1H NMR at 7 Tesla. J Lipid Res 2008; 49: 2055–2062.
- 2Hamilton G, Yokoo T, Bydder M, Cruite I, Schroeder ME, Sirlin CB, Middleton MS. In vivo characterization of the liver fat (1)H MR spectrum. NMR Biomed 2011; 24: 784–790.
- 3Yeung DK, Griffith JF, Antonio GE, Lee FK, Woo J, Leung PC. Osteoporosis is associated with increased marrow fat content and decreased marrow fat unsaturation: a proton MR spectroscopy study. J Magn Reson Imaging 2005; 22: 279–285.
- 4Patsch JM, Li X, Baum T, Yap SP, Karampinos DC, Schwartz AV, Link TM. Bone marrow fat composition as a novel imaging biomarker in postmenopausal women with prevalent fragility fractures. J Bone Miner Res 2013; 28: 1721–1728.
- 5Velan SS, Said N, Durst C, et al. Distinct patterns of fat metabolism in skeletal muscle of normal-weight, overweight, and obese humans. Am J Physiol Regul Integr Comp Physiol 2008; 295: R1060–R1065.
- 6Manco M, Mingrone G, Greco AV, Capristo E, Gniuli D, De Gaetano A, Gasbarrini G. Insulin resistance directly correlates with increased saturated fatty acids in skeletal muscle triglycerides. Metabolism 2000; 49: 220–224.
- 7Carey DG, Jenkins AB, Campbell LV, Freund J, Chisholm DJ. Abdominal fat and insulin resistance in normal and overweight women: direct measurements reveal a strong relationship in subjects at both low and high risk of NIDDM. Diabetes 1996; 45: 633–638.
- 8Baum T, Yap SP, Karampinos DC, et al. Does vertebral bone marrow fat content correlate with abdominal adipose tissue, lumbar spine bone mineral density, and blood biomarkers in women with type 2 diabetes mellitus? J Magn Reson Imaging 2012; 35: 117–124.
- 9Thomas MA, Chung HK, Middlekauff H. Localized two-dimensional 1H magnetic resonance exchange spectroscopy: a preliminary evaluation in human muscle. Magn Reson Med 2005; 53: 495–502.
- 10Velan SS, Durst C, Lemieux SK, Raylman RR, Sridhar R, Spencer RG, Hobbs GR, Thomas MA. Investigation of muscle lipid metabolism by localized one- and two-dimensional MRS techniques using a clinical 3T MRI/MRS scanner. J Magn Reson Imaging 2007; 25: 192–199.
- 11Haase A, Frahm J, Hanicke W, Matthaei D. 1H NMR chemical shift selective (CHESS) imaging. Phys Med Biol 1985; 30: 341–344.
- 12Ye Q, Danzer CF, Fuchs A, Wolfrum C, Rudin M. Hepatic lipid composition differs between ob/ob and ob/+ control mice as determined by using in vivo localized proton magnetic resonance spectroscopy. MAGMA 2012; 25: 381–389.
- 13Lundbom J, Hakkarainen A, Fielding B, Soderlund S, Westerbacka J, Taskinen MR, Lundbom N. Characterizing human adipose tissue lipids by long echo time 1H-MRS in vivo at 1.5 Tesla: validation by gas chromatography. NMR Biomed 2010; 23: 466–472.
- 14Lundbom J, Heikkinen S, Fielding B, Hakkarainen A, Taskinen MR, Lundbom N. PRESS echo time behavior of triglyceride resonances at 1.5T: detecting omega-3 fatty acids in adipose tissue in vivo. J Magn Reson 2009; 201: 39–47.
- 15Troitskaia A, Fallone BG, Yahya A. Long echo time proton magnetic resonance spectroscopy for estimating relative measures of lipid unsaturation at 3 T. J Magn Reson Imaging 2013; 37: 944–949.
- 16Bingolbali A, Fallone BG, Yahya A. Comparison of optimized long echo time STEAM and PRESS proton MR spectroscopy of lipid olefinic protons at 3 Tesla. J Magn Reson Imaging 2015; 41: 481–486.
- 17Xiao L, Wu EX. Diffusion-weighted magnetic resonance spectroscopy: a novel approach to investigate intramyocellular lipids. Magn Reson Med 2011; 66: 937–944.
- 18Brandejsky V, Kreis R, Boesch C. Restricted or severely hindered diffusion of intramyocellular lipids in human skeletal muscle shown by in vivo proton MR spectroscopy. Magn Reson Med 2012; 67: 310–316.
- 19Wang AM, Cao P, Yee A, Chan D, Wu EX. Detection of extracellular matrix degradation in intervertebral disc degeneration by diffusion magnetic resonance spectroscopy. Magn Reson Med 2015; 73: 1703–1712.
- 20Lehnert A, Machann J, Helms G, Claussen CD, Schick F. Diffusion characteristics of large molecules assessed by proton MRS on a whole-body MR system. J Magn Reson Imaging 2004; 22: 39–46.
- 21Merboldt KD, Hanicke W, Frahm J. Self-diffusion NMR Imaging Using Stimulated Echoes. J MagnReson 1985; 64: 479–486.
- 22Yahya A, Fallone BG. T(2) determination of the J-coupled methyl protons of lipids: In vivo ilustration with tibial bone marrow at 3 T. J Magn Reson Imaging 2010; 31: 1514–1521.
- 23Hamilton G, Middleton MS, Bydder M, Yokoo T, Schwimmer JB, Kono Y, Patton HM, Lavine JE, Sirlin CB. Effect of PRESS and STEAM sequences on magnetic resonance spectroscopic liver fat quantification. J Magn Reson Imaging 2009; 30: 145–152.
- 24Lin C, Wendt RE 3rd, Evans HJ, Rowe RM, Hedrick TD, LeBlanc AD. Eddy current correction in volume-localized MR spectroscopy. J Magn Reson Imaging 1994; 4: 823–827.
- 25Ruschke S, Baum T, Kooijman H, Settles M, Haase A, Rummeny EJ, Karampinos DC. Eddy current correction in diffusion-weighted STEAM MRS in the presence of water and fat peaks. Proc Intl Soc Mag Reson Med 2014: 22; 2268.
- 26Firl N, Kienberger H, Rychlik M. Validation of the sensitive and accurate quantitation of the fatty acid distribution in bovine milk. Int Dairy J 2014; 35: 139–144.
- 27Gold GE, Han E, Stainsby J, Wright G, Brittain J, Beaulieu C. Musculoskeletal MRI at 3.0 T: relaxation times and image contrast. AJR Am J Roentgenol 2004; 183: 343–351.
- 28Wang L, Salibi N, Wu Y, Schweitzer ME, Regatte RR. Relaxation times of skeletal muscle metabolites at 7T. J Magn Reson Imaging 2009; 29: 1457–1464.
- 29Karampinos DC, King KF, Sutton BP, Georgiadis JG. Myofiber ellipticity as an explanation for transverse asymmetry of skeletal muscle diffusion MRI in vivo signal. Ann Biomed Eng 2009; 37: 2532–2546.
- 30Bydder M, Girard O, Hamilton G. Mapping the double bonds in triglycerides. J Magn Reson Imaging 2011; 29: 1041–1046.
- 31Price WS, Kuchel PW. Effect of nonrectangular field gradient pulses in the stejskal and tanner (diffusion) pulse sequence. J Magn Reson 1991; 94: 133–139.
- 32Steidle G, Schick F. Echoplanar diffusion tensor imaging of the lower leg musculature using eddy current nulled stimulated echo preparation. Magn Reson Med 2006; 55: 541–548.
- 33Karampinos DC, Banerjee S, King KF, Link TM, Majumdar S. Considerations in high-resolution skeletal muscle diffusion tensor imaging using single-shot echo planar imaging with stimulated-echo preparation and sensitivity encoding. NMR Biomed 2012; 25: 766–778.
- 34Schick F, Eismann B, Jung WI, Bongers H, Bunse M, Lutz O. Comparison of localized proton NMR signals of skeletal muscle and fat tissue in vivo: two lipid compartments in muscle tissue. Magn Reson Med 1993; 29: 158–167.
- 35Boesch C, Slotboom J, Hoppeler H, Kreis R. In vivo determination of intra-myocellular lipids in human muscle by means of localized 1H-MR-spectroscopy. Magn Reson Med 1997; 37: 484–493.
- 36Ren JM, Sherry AD, Malloy CR. H-1 MRS of intramyocellular lipids in soleus muscle at 7 T: spectral simplification by using long echo times without water suppression. Magn Reson Med 2010; 64: 662–671.
- 37Lundbom J, Hakkarainen A, Soderlund S, Westerbacka J, Lundbom N, Taskinen MR. Long-TE 1H MRS suggests that liver fat is more saturated than subcutaneous and visceral fat. NMR Biomed 2011; 24: 238–245.
- 38Walecki J, Michalak MJ, Michalak E, Bilinska ZT, Ruzyllo W. Usefulness of 1H MR spectroscopy in the evaluation of myocardial metabolism in patients with dilated idiopathic cardiomyopathy: pilot study. Acad Radiol 2003; 10: 1187–1192.
- 39Hammer S, de Vries AP, de Heer P, Bizino MB, Wolterbeek R, Rabelink TJ, Doornbos J, Lamb HJ. Metabolic imaging of human kidney triglyceride content: reproducibility of proton magnetic resonance spectroscopy. PLoS One 2013; 8: e62209.