Feasibility of omega-3 fatty acid fraction mapping using chemical shift encoding-based imaging at 3 T.
3 T
Dixon imaging
chemical shift encoding‐based imaging
fatty acids
omega‐3
water–fat imaging
ω‐3
Journal
NMR in biomedicine
ISSN: 1099-1492
Titre abrégé: NMR Biomed
Pays: England
ID NLM: 8915233
Informations de publication
Date de publication:
03 Jun 2024
03 Jun 2024
Historique:
revised:
21
04
2024
received:
12
12
2023
accepted:
06
05
2024
medline:
4
6
2024
pubmed:
4
6
2024
entrez:
3
6
2024
Statut:
aheadofprint
Résumé
The aim of this work is to develop an ω-3 fatty acid fraction mapping method at 3 T based on a chemical shift encoding model, to assess its performance in a phantom and in vitro study, and to further demonstrate its feasibility in vivo. A signal model was heuristically derived based on spectral appearance and theoretical considerations of the corresponding molecular structures to differentiate between ω-3 and non-ω-3 fatty acid substituents in triacylglycerols in addition to the number of double bonds (ndb), the number of methylene-interrupted double bonds (nmidb), and the mean fatty acid chain length (CL). First, the signal model was validated using single-voxel spectroscopy and a time-interleaved multi-echo gradient-echo (TIMGRE) sequence in gas chromatography-mass spectrometry (GC-MS)-calibrated oil phantoms. Second, the TIMGRE-based method was validated in vitro in 21 adipose tissue samples with corresponding GC-MS measurements. Third, an in vivo feasibility study was performed for the TIMGRE-based method in the gluteal region of two healthy volunteers. Phantom and in vitro data was analyzed using a Bland-Altman analysis. Compared with GC-MS, MRS showed in the phantom study significant correlations in estimating the ω-3 fraction (p < 0.001), ndb (p < 0.001), nmidb (p < 0.001), and CL (p = 0.001); MRI showed in the phantom study significant correlations (all p < 0.001) for the ω-3 fraction, ndb, and nmidb, but no correlation for CL. Also in the in vitro study, significant correlations (all p < 0.001) between MRI and GC-MS were observed for the ω-3 fraction, ndb, and nmidb, but not for CL. An exemplary ROI measurement in vivo in the gluteal subcutaneous adipose tissue yielded (mean ± standard deviation) 0.8% ± 1.9% ω-3 fraction. The present study demonstrated strong correlations between gradient-echo imaging-based ω-3 fatty acid fraction mapping and GC-MS in the phantom and in vitro study. Furthermore, feasibility was demonstrated for characterizing adipose tissue in vivo.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e5181Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : 446320752
Organisme : Philips Healthcare
Informations de copyright
© 2024 The Authors. NMR in Biomedicine published by John Wiley & Sons Ltd.
Références
Cameron AJ, Shaw JE, Zimmet PZ. The metabolic syndrome: prevalence in worldwide populations. Endocrinol Metab Clin North Am. 2004;33(2):351‐375. doi:10.1016/j.ecl.2004.03.005
Avgerinos KI, Spyrou N, Mantzoros CS, Dalamaga M. Obesity and cancer risk: emerging biological mechanisms and perspectives. Metabolism. 2019;92:121‐135. doi:10.1016/j.metabol.2018.11.001
Belladelli F, Montorsi F, Martini A. Metabolic syndrome, obesity and cancer risk. Curr Opin Urol. 2022;32(6):594‐597. doi:10.1097/MOU.0000000000001041
Kassi E, Pervanidou P, Kaltsas G, Chrousos G. Metabolic syndrome: definitions and controversies. BMC Med. 2011;9(1):48. doi:10.1186/1741‐7015‐9‐48
Phinney SD, Stern JS, Burke KE, Tang AB, Miller G, Holman RT. Human subcutaneous adipose tissue shows site‐specific differences in fatty acid composition. Am J Clin Nutr. 1994;60(5):725‐729. doi:10.1093/ajcn/60.5.725
Honecker J, Ruschke S, Seeliger C, et al. Transcriptome and fatty‐acid signatures of adipocyte hypertrophy and its non‐invasive MR‐based characterization in human adipose tissue. eBioMedicine. 2022;79:104020. doi:10.1016/j.ebiom.2022.104020
Lands WEM. Biochemistry and physiology of n‐3 fatty acids. FASEB J. 1992;6(8):2530‐2536. doi:10.1096/fasebj.6.8.1592205
Smith WL, Murphy RC. Chapter 9—The eicosanoids: cyclooxygenase, lipoxygenase and epoxygenase pathways. In: Ridgway ND, Mcleod RS, eds. Biochemistry of Lipids, Lipoproteins and Membranes. 6th ed. Elsevier; 2016:259‐296. doi:10.1016/B978‐0‐444‐63438‐2.00009‐2
De Gómez Dumm INT, Brenner RR. Oxidative desaturation of α‐linolenic, linoleic, and stearic acids by human liver microsomes. Lipids. 1975;10(6):315‐317. doi:10.1007/BF02532451
Simopoulos A. Omega‐3 fatty acids in health and disease and in growth and development. Am J Clin Nutr. 1991;54(3):438‐463. doi:10.1093/ajcn/54.3.438
Simopoulos AP. Omega‐3 fatty acids in inflammation and autoimmune diseases. J Am Coll Nutr. 2002;21(6):495‐505. doi:10.1080/07315724.2002.10719248
Lepretti M, Martucciello S, Aceves MAB, Putti R, Lionetti L. Omega‐3 fatty acids and insulin resistance: focus on the regulation of mitochondria and endoplasmic reticulum stress. Nutrients. 2018;10(3):350. doi:10.3390/nu10030350
Albert BB, Derraik JGB, Brennan CM, et al. Higher omega‐3 index is associated with increased insulin sensitivity and more favourable metabolic profile in middle‐aged overweight men. Sci Rep. 2014;4(1):6697. doi:10.1038/srep06697
López‐Alarcón M, Inda‐Icaza P, Márquez‐Maldonado MC, et al. A randomized control trial of the impact of LCPUFA‐ω3 supplementation on body weight and insulin resistance in pubertal children with obesity. Pediatr Obes. 2019;14(5):e12499. doi:10.1111/ijpo.12499
Hodson L, Skeaff CM, Fielding BA. Fatty acid composition of adipose tissue and blood in humans and its use as a biomarker of dietary intake. Prog Lipid Res. 2008;47(5):348‐380. doi:10.1016/j.plipres.2008.03.003
Sears B, Perry M. The role of fatty acids in insulin resistance. Lipids Health Dis. 2015;14(1):121. doi:10.1186/s12944‐015‐0123‐1
Abate N, Garg A, Peshock RM, Stray‐Gundersen J, Grundy SM. Relationships of generalized and regional adiposity to insulin sensitivity in men. J Clin Invest. 1995;96(1):88‐98. doi:10.1172/JCI118083
Frayn KN. Visceral fat and insulin resistance—causative or correlative? Br J Nutr. 2000;83(S1):S71‐S77. doi:10.1017/S0007114500000982
Peterson P, Trinh L, Månsson S. Quantitative 1H MRI and MRS of fatty acid composition. Magn Reson Med. 2021;85(1):49‐67. doi:10.1002/mrm.28471
Lundbom J, Heikkinen S, Fielding B, Hakkarainen A, Taskinen MR, Lundbom N. PRESS echo time behavior of triglyceride resonances at 1.5 T: detecting ω‐3 fatty acids in adipose tissue in vivo. J Magn Reson. 2009;201(1):39‐47. doi:10.1016/j.jmr.2009.07.026
Lundbom J, Hakkarainen A, Fielding B, et al. 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(5):466‐472. doi:10.1002/nbm.1483
Škoch A, Tošner Z, Hájek M. The in vivo J‐difference editing MEGA‐PRESS technique for the detection of n‐3 fatty acids. NMR Biomed. 2014;27(11):1293‐1299. doi:10.1002/nbm.3189
Gajdošík M, Hingerl L, Škoch A, et al. Ultralong TE in vivo 1H MR spectroscopy of omega‐3 fatty acids in subcutaneous adipose tissue at 7 T. J Magn Reson Imaging. 2019;50(1):71‐82. doi:10.1002/jmri.26605
Fallone CJ, McKay RT, Yahya A. Long TE STEAM and PRESS for estimating fat olefinic/methyl ratios and relative ω‐3 fat content at 3T. J Magn Reson Imaging. 2018;48(1):169‐177. doi:10.1002/jmri.25920
Ruschke S, Eggers H, Kooijman‐Kurfuerst H, et al. Correction of phase errors in quantitative water–fat imaging using a monopolar time‐interleaved multi‐echo gradient echo sequence. Magn Reson Med. 2017;78(3):984‐996. doi:10.1002/mrm.26485
Boehm C, Diefenbach MN, Makowski MR, Karampinos DC. Improved body quantitative susceptibility mapping by using a variable‐layer single‐min‐cut graph‐cut for field‐mapping. Magn Reson Med. 2021;85(3):1697‐1712. doi:10.1002/mrm.28515
Hamilton G, Schlein AN, Middleton MS, et al. In vivo triglyceride composition of abdominal adipose tissue measured by 1H MRS at 3T. J Magn Reson Imaging. 2017;45(5):1455‐1463. doi:10.1002/jmri.25453
Bydder M, Girard O, Hamilton G, Hamilton G. Mapping the double bonds in triglycerides. Magn Reson Imaging. 2011;29(8):1041‐1046. doi:10.1016/j.mri.2011.07.004
Bydder M, Hamilton G, Yokoo T, Sirlin CB. Optimal phased‐array combination for spectroscopy. Magn Reson Imaging. 2008;26(6):847‐850. doi:10.1016/j.mri.2008.01.050
Hamilton G, Yokoo T, Bydder M, et al. In vivo characterization of the liver fat 1H MR spectrum. NMR Biomed. 2011;24(7):784‐790. doi:10.1002/nbm.1622
Berglund J, Ahlström H, Kullberg J. Model‐based mapping of fat unsaturation and chain length by chemical shift imaging‐phantom validation and in vivo feasibility. Magn Reson Med. 2012;68(6):1815‐1827. doi:10.1002/mrm.24196
Ouwerkerk R, Hamimi A, Matta J, et al. Proton MR spectroscopy measurements of white and brown adipose tissue in healthy humans: relaxation parameters and unsaturated fatty acids. Radiology. 2021;299(2):396‐406. doi:10.1148/radiol.2021202676
Ruschke S, Karampinos D. ALFONSO: A versatiLe Formulation fOr N‐dimensional Signal mOdel fitting of MR spectroscopy data and its application in MRS of body lipids. Paper presented at: 31st Joint Annual Meeting of the International Society for Magnetic Resonance in Medicine and the European Society for Magnetic Resonance in Medicine and Biology; May 07–12, 2022; London, UK. doi:10.58530/2022/2776
Dennis JE, Gay DM, Welsch RE. Algorithm 573: NL2SOL—an adaptive nonlinear least‐squares algorithm [E4]. ACM Trans Math Softw. 1981;7(3):369‐383. doi:10.1145/355958.355966
Ecker J, Scherer M, Schmitz G, Liebisch G. A rapid GC‐MS method for quantification of positional and geometric isomers of fatty acid methyl esters. J Chromatogr B. 2012;897:98‐104. doi:10.1016/j.jchromb.2012.04.015
Hines CDG, Yu H, Shimakawa A, McKenzie CA, Brittain JH, Reeder SB. T1 independent, T2* corrected MRI with accurate spectral modeling for quantification of fat: validation in a fat‐water‐SPIO phantom. J Magn Reson Imaging. 2009;30(5):1215‐1222. doi:10.1002/jmri.21957
Bernard CP, Liney GP, Manton DJ, Turnbull LW, Langton CM. Comparison of fat quantification methods: a phantom study at 3.0T. J Magn Reson Imaging. 2008;27(1):192‐197. doi:10.1002/jmri.21201
Flachs P, Rossmeisl M, Bryhn M, Kopecky J. Cellular and molecular effects of n3 polyunsaturated fatty acids on adipose tissue biology and metabolism. Clin Sci. 2009;116(1):1‐16. doi:10.1042/CS20070456
Warensjö E, Risérus U, Vessby B. Fatty acid composition of serum lipids predicts the development of the metabolic syndrome in men. Diabetologia. 2005;48(10):1999‐2005. doi:10.1007/s00125‐005‐1897‐x
Lorente‐Cebrián S, Costa AGV, Navas‐Carretero S, Zabala M, Martínez JA, Moreno‐Aliaga MJ. Role of omega‐3 fatty acids in obesity, metabolic syndrome, and cardiovascular diseases: a review of the evidence. J Physiol Biochem. 2013;69(3):633‐651. doi:10.1007/s13105‐013‐0265‐4
Albracht‐Schulte K, Kalupahana NS, Ramalingam L, et al. Omega‐3 fatty acids in obesity and metabolic syndrome: a mechanistic update. J Nutr Biochem. 2018;58:1‐16. doi:10.1016/j.jnutbio.2018.02.012
Andersen CJ, Fernandez ML. Dietary strategies to reduce metabolic syndrome. Rev Endocr Metab Disord. 2013;14(3):241‐254. doi:10.1007/s11154‐013‐9251‐y
Alexandri E, Ahmed R, Siddiqui H, Choudhary MI, Tsiafoulis CG, Gerothanassis IP. High resolution NMR spectroscopy as a structural and analytical tool for unsaturated lipids in solution. Molecules. 2017;22(10):1663. doi:10.3390/molecules22101663
Garaulet M, Hernandez‐Morante JJ, Lujan J, Tebar FJ, Zamora S. Relationship between fat cell size and number and fatty acid composition in adipose tissue from different fat depots in overweight/obese humans. Int J Obes. 2006;30(6):899‐905. doi:10.1038/sj.ijo.0803219
Leaf D, Connor W, Barstad L, Sexton G. Incorporation of dietary n‐3 fatty acids into the fatty acids of human adipose tissue and plasma lipid classes. Am J Clin Nutr. 1995;62(1):68‐73. doi:10.1093/ajcn/62.1.68
Hwang JH, Bluml S, Leaf A, Ross BD. In vivo characterization of fatty acids in human adipose tissue using natural abundance 1H decoupled 13C MRS at 1.5 T: clinical applications to dietary therapy. NMR Biomed. 2003;16(3):160‐167. doi:10.1002/nbm.824
Ren 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(9):2055‐2062. doi:10.1194/jlr.D800010‐JLR200
Machann J, Stefan N, Wagner R, et al. Intra‐ and interindividual variability of fatty acid unsaturation in six different human adipose tissue compartments assessed by 1H‐MRS in vivo at 3 T. NMR Biomed. 2017;30(9):e3744. doi:10.1002/nbm.3744
Lindeboom L, Graaf RA. Measurement of lipid composition in human skeletal muscle and adipose tissue with 1H‐MRS homonuclear spectral editing. Magn Reson Med. 2018;79(2):619‐627. doi:10.1002/mrm.26740
Lin D, Zhou J, Cao Y, et al. Echo time optimization for in‐vivo measurement of unsaturated lipid resonances using J‐difference‐edited MRS. Magn Reson Med. 2023;90(6):2217‐2232. doi:10.1002/mrm.29807
Peterson P, Månsson S. Simultaneous quantification of fat content and fatty acid composition using MR imaging. Magn Reson Med. 2013;69(3):688‐697. doi:10.1002/mrm.24297
Leporq B, Lambert SA, Ronot M, Vilgrain V, Van Beers BE. Quantification of the triglyceride fatty acid composition with 3.0 T MRI. NMR Biomed. 2014;27(10):1211‐1221. doi:10.1002/nbm.3175
Schneider M, Janas G, Lugauer F, et al. Accurate fatty acid composition estimation of adipose tissue in the abdomen based on bipolar multi‐echo MRI. Magn Reson Med. 2019;81(4):2330‐2346. doi:10.1002/mrm.27557
Nemeth A, Segrestin B, Leporq B, et al. 3D chemical shift‐encoded MRI for volume and composition quantification of abdominal adipose tissue during an overfeeding protocol in healthy volunteers. J Magn Reson Imaging. 2019;49(6):1587‐1599. doi:10.1002/jmri.26532
Trinh L, Peterson P, Leander P, Brorson H, Månsson S. In vivo comparison of MRI‐based and MRS‐based quantification of adipose tissue fatty acid composition against gas chromatography. Magn Reson Med. 2020;84(5):2484‐2494. doi:10.1002/mrm.28300
Baboli M, Storey P, Sood TP, et al. Bilateral gradient‐echo spectroscopic imaging with correction of frequency variations for measurement of fatty acid composition in mammary adipose tissue. Magn Reson Med. 2021;86(1):33‐45. doi:10.1002/mrm.28692
Fallone CJ, Tessier AG, Field CJ, Yahya A. Resolving the omega‐3 methyl resonance with long echo time magnetic resonance spectroscopy in mouse adipose tissue at 9.4 T. NMR Biomed. 2021;34(2):e4455. doi:10.1002/nbm.4455
Saive E, Fairgrieve‐Park L, Yahya A. Estimating relative diglyceride to triglyceride content with localized MRS at 3 T. NMR Biomed. 2022;35(8):e4723. doi:10.1002/nbm.4723
Uche IK, Galiana G. Distinguishing lipid subtypes by amplifying contrast from J‐coupling. Sci Rep. 2019;9(1):3600. doi:10.1038/s41598‐019‐39780‐4
Branca RT, Warren WS. In vivo brown adipose tissue detection and characterization using water‐lipid intermolecular zero‐quantum coherences. Magn Reson Med. 2011;65(2):313‐319. doi:10.1002/mrm.22622
Branca RT, Zhang L, Warren WS, et al. In vivo noninvasive detection of brown adipose tissue through intermolecular zero‐quantum MRI. PLoS ONE. 2013;8(9):e74206. doi:10.1371/journal.pone.0074206
Lin L, Zhang Q, Wang N, et al. Evaluation of brown adipose tissue with intermolecular double‐quantum coherence magnetic resonance spectroscopy at 3.0 T. NMR Biomed. 2022;35(6):e4676. doi:10.1002/nbm.4676
Hamilton G, Middleton MS, Bydder M, et al. Effect of PRESS and STEAM sequences on magnetic resonance spectroscopic liver fat quantification. J Magn Reson Imaging. 2009;30(1):145‐152. doi:10.1002/jmri.21809
Gajdošík M, Chmelík M, Just‐Kukurová I, et al. In vivo relaxation behavior of liver compounds at 7 tesla, measured by single‐voxel proton MR spectroscopy. J Magn Reson Imaging. 2014;40(6):1365‐1374. doi:10.1002/jmri.24489
Bingölbali 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(2):481‐486. doi:10.1002/jmri.24532
Song KH, Baek HM, Lee DW, Choe BY. In vivo proton magnetic resonance spectroscopy of liver metabolites in non‐alcoholic fatty liver disease in rats: T2 relaxation times in methylene protons. Chem Phys Lipids. 2015;191:1‐7. doi:10.1016/j.chemphyslip.2015.07.005
Ruschke S, Kienberger H, Baum T, et al. Diffusion‐weighted stimulated echo acquisition mode (DW‐STEAM) MR spectroscopy to measure fat unsaturation in regions with low proton‐density fat fraction. Magn Reson Med. 2016;75(1):32‐41. doi:10.1002/mrm.25578