Composition of adipose tissue and marrow fat in humans by 1H NMR at 7 Tesla

Proton NMR spectroscopy at 7 Tesla (7T) was evaluated as a new method to quantify human fat composition noninvasively. In validation experiments, the composition of a known mixture of triolein, tristearin, and trilinolein agreed well with measurements by 1H NMR spectroscopy. Triglycerides in calf subcutaneous tissue and tibial bone marrow were examined in 20 healthy subjects by 1H spectroscopy. Ten well-resolved proton resonances from triglycerides were detected using stimulated echo acquisition mode sequence and small voxel (∼0.1 ml), and T1 and T2 were measured. Triglyceride composition was not different between calf subcutaneous adipose tissue and tibial marrow for a given subject, and its variation among subjects, as a result of diet and genetic differences, fell in a narrow range. After correction for differential relaxation effects, the marrow fat composition was 29.1 ± 3.5% saturated, 46.4 ± 4.8% monounsaturated, and 24.5 ± 3.1% diunsaturated, compared with adipose fat composition, 27.1 ± 4.2% saturated, 49.6 ± 5.7% monounsaturated, and 23.4 ± 3.9% diunsaturated. Proton spectroscopy at 7T offers a simple, fast, noninvasive, and painless method for obtaining detailed information about lipid composition in humans, and the sensitivity and resolution of the method may facilitate longitudinal monitoring of changes in lipid composition in response to diet, exercise, and disease. Proton NMR spectroscopy at 7 Tesla (7T) was evaluated as a new method to quantify human fat composition noninvasively. In validation experiments, the composition of a known mixture of triolein, tristearin, and trilinolein agreed well with measurements by 1H NMR spectroscopy. Triglycerides in calf subcutaneous tissue and tibial bone marrow were examined in 20 healthy subjects by 1H spectroscopy. Ten well-resolved proton resonances from triglycerides were detected using stimulated echo acquisition mode sequence and small voxel (∼0.1 ml), and T1 and T2 were measured. Triglyceride composition was not different between calf subcutaneous adipose tissue and tibial marrow for a given subject, and its variation among subjects, as a result of diet and genetic differences, fell in a narrow range. After correction for differential relaxation effects, the marrow fat composition was 29.1 ± 3.5% saturated, 46.4 ± 4.8% monounsaturated, and 24.5 ± 3.1% diunsaturated, compared with adipose fat composition, 27.1 ± 4.2% saturated, 49.6 ± 5.7% monounsaturated, and 23.4 ± 3.9% diunsaturated. Proton spectroscopy at 7T offers a simple, fast, noninvasive, and painless method for obtaining detailed information about lipid composition in humans, and the sensitivity and resolution of the method may facilitate longitudinal monitoring of changes in lipid composition in response to diet, exercise, and disease. Adipose mass and the anatomic distribution of adipose tissue strongly influence the risk of multiple diseases. The fatty acid composition of adipose tissue may also influence predisposition to various disorders including cancer (1Simonsen N. van't Veer P. Strain J.J. Martin-Moreno J.M. Huttunen J.K. Navajas J.F. Martin B.C. Thamm M. Kardinaal A.F. Kok F.J. et al.Adipose tissue omega-3 and omega-6 fatty acid content and breast cancer in the EURAMIC study. European Community Multicenter Study on Antioxidants, Myocardial Infarction, and Breast Cancer.Am. J. Epidemiol. 1998; 147: 342-352Crossref PubMed Scopus (136) Google Scholar, 2Shannon J. King I.B. Moshofsky R. Lampe J.W. 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Barnard M.L. Bryant D.J. Taylor-Robinson S.D. Simbrunner J. Coutts G.A. Burl M. Bloom S.R. Sales K.D. et al.An in vivo 13C magnetic resonance spectroscopic study of the relationship between diet and adipose tissue composition.Lipids. 1996; 31: PubMed Scopus Google Scholar, S. A. In vivo of fatty acids in human adipose tissue using natural abundance 1H 13C MRS at 1.5 clinical applications to dietary 2003; PubMed Scopus (39) Google Scholar). The chemical shift of 13C is a major compared with 1H is by the requirement for and a shift resolution in the 1H in at the fatty acid composition of adipose tissue was on 1H in vivo at the chemical shift of signals from protons adjacent to double of analysis K. J. J. proton magnetic resonance spectroscopy of in adipose tissue at resolution in in Lipid Res. 2008; 49: Full Text Full Text PDF PubMed Scopus Google was the of spectroscopic from adjacent resonances with a of at In (8Zancanaro C. Nano R. Marchioro C. Sbarbati A. Boicelli A. Osculati F. Magnetic resonance spectroscopy investigations of brown adipose tissue and isolated brown adipocytes.J. Lipid Res. 1994; 35: 2191-2199Abstract Full Text PDF PubMed Google Scholar), triglyceride was from the protons at by using the protons as the resonances a of at The may result in and the of with resonances in different known as chemical shift The to triglyceride composition using proton spectroscopy would have applications in clinical In study, the by and K. J. J. proton magnetic resonance spectroscopy of in adipose tissue at resolution in in Lipid Res. 2008; 49: Full Text Full Text PDF PubMed Scopus Google to fatty acid composition by 1H NMR spectroscopy in was in and to healthy human The fatty acid composition of bone marrow by NMR in study was in with D.K.W. Lam S.L. Griffith J.F. Chan A.B.W. Chen Z. Tsang P.H. Leung P.C. Analysis of bone marrow fatty acid composition using high-resolution proton NMR spectroscopy.Chem. Phys. Lipids. 2008; 151: 103-109Crossref PubMed Scopus (45) Google not P. D. J. Lipid composition of human bone marrow as by Lipid Res. Full Text PDF Google of fatty acid composition by The NMR determination of saturated fatty acids in subcutaneous fat agreed well with analysis of subcutaneous about of fatty for about were by compared with in The by to quantify fat composition by 1H NMR (8Zancanaro C. Nano R. Marchioro C. Sbarbati A. Boicelli A. Osculati F. Magnetic resonance spectroscopy investigations of brown adipose tissue and isolated brown adipocytes.J. Lipid Res. 1994; 35: 2191-2199Abstract Full Text PDF PubMed Google Scholar, 9Miyake Y. Yokomizo K. Matsuzaki N. Determination of unsaturated fatty acid composition by high-resolution nuclear magnetic resonance spectroscopy.J. Am. Oil Chem. Soc. 1998; 75: 1091-1094Crossref Google Scholar, 10Guillen M.D. Ruiz A. 1H nuclear magnetic resonance as a fast tool for determining the composition of acyl chains in acylglycerol mixtures.Eur. J. Lipid Sci. Technol. 2003; 105: 502-507Crossref Scopus (100) Google Scholar, 11Knothe G. Kenar J.A. Determination of the fatty acid profile by 1H-NMR spectroscopy.Eur. J. Lipid Sci. Technol. 2004; 106: 88-96Crossref Scopus (347) Google Scholar, 12Yeung D.K.W. Lam S.L. Griffith J.F. Chan A.B.W. Chen Z. Tsang P.H. Leung P.C. Analysis of bone marrow fatty acid composition using high-resolution proton NMR spectroscopy.Chem. Phys. Lipids. 2008; 151: 103-109Crossref PubMed Scopus (45) Google Scholar, K. J. J. proton magnetic resonance spectroscopy of in adipose tissue at resolution in in Lipid Res. 2008; 49: Full Text Full Text PDF PubMed Scopus Google are easily to human at 1H NMR be The was by the was from to the study. healthy and diabetes or known were or in a 7T were with a to the of a human and echo were of the calf of echo and of stimulated echo acquisition mode voxel (∼0.1 ml), 20 of of and to to was to 1H from tibial bone marrow and subcutaneous fat resonances for relaxation effects, T1 and T2 were in of the T1 was using with in the of to with 7 and T2 was by using from 20 to with were to in the The was or and it was by subjects were the and at the subjects or were from the of the to quantify lipid composition, were by of of double and trilinolein in the and with composition of different of triglyceride were by and in the and were in in were in the of a with magnetic resonance spectroscopy voxel The triglyceride composition was as The 1H chemical shift of in vivo fat resonances from bone marrow and subcutaneous tissue was the was at were by the with of on and for resonance were with its T1 and Lipid composition was evaluated correction for relaxation adipose tissue is of fatty acids as of of double linoleic and A. Relationship of diet to the fatty acid composition of human adipose tissue and J. Clin. Nutr. PubMed Scopus Google Scholar, M. M.A. acid composition of adipose tissue in between subcutaneous J. Clin. Nutr. PubMed Scopus Google Scholar). fatty acids for well of the fatty acids in human adipose fatty fatty and fatty acids for the of these than A. Relationship of diet to the fatty acid composition of human adipose tissue and J. Clin. Nutr. PubMed Scopus Google Scholar). 7 resonances be resolved, as to in from to resonances information about triglyceride the protons at the protons at and at to the and the and protons and are resonances to protons at to a double at protons at and double protons at with the proton at was the fatty acids detected or 2 double of fatty acids for of fat in humans on acid is in it of the triglycerides A. Relationship of diet to the fatty acid composition of human adipose tissue and J. Clin. Nutr. PubMed Scopus Google Scholar). and to the of fatty acids are saturated, monounsaturated, and unsaturated The is diunsaturated, be directly from the of the resonance of the protons with to the resonance of protons to the is from the of proton resonance to the double 2 The the of saturated fatty is as the of fatty acids are be from the of the resonances 3 The in of the for acid for acid for acid for acid and 7 for linoleic acid analysis is to the analysis K. J. J. proton magnetic resonance spectroscopy of in adipose tissue at resolution in in Lipid Res. 2008; 49: Full Text Full Text PDF PubMed Scopus Google with the a for unsaturated fat with double bonds was than a Ten lipid resonances are observed in the 7T 1H from for the the proton of the chemical shift is about the lipid resonances were well-resolved at 7T and to high-resolution in K. J. J. proton magnetic resonance spectroscopy of in adipose tissue at resolution in in Lipid Res. 2008; 49: Full Text Full Text PDF PubMed Scopus Google Scholar). The in the 1H of subcutaneous fat with and it is in bone marrow from a small voxel (∼0.1 The resonance chemical and from marrow and subcutaneous fat are in and resonance and ± ± ± ± protons to ± ± protons to ± ± protons to ± ± ± ± are to the resonance to correction for by to are the ± in a new The are to the resonance to correction for by to are the ± The of analysis was by in a by and in various from with the the known of trilinolein in the mixture is between the and the with of and were for the not the the known in the and mixture The of the known the was evaluated by also a with of and of fat composition in human subcutaneous tissue and tibial the were for in T1 and T2 as from and experiments, 3 the T1 and T2 from the voxel in subcutaneous with the the T2 between tibial marrow and subcutaneous tissue from on the The T1 and T2 at are in by the protons at different in have different with from and from subcutaneous fat T1 and T2 about on in with tibial bone be because of the of proton these T1 and T2 are for T2 have been for animal fat using spectroscopy sequence K. J. J. proton magnetic resonance spectroscopy of in adipose tissue at resolution in in Lipid Res. 2008; 49: Full Text Full Text PDF PubMed Scopus Google at the of bone marrow and calf subcutaneous fat from a healthy by at the voxel well in the fat of the subcutaneous tissue and the 1H is are to of the resonance and as a with the resonance with T2 than the T2 resonances as and to resonance the of the and is not of of in resonances to the fatty acid ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± are ± and are for the stimulated echo acquisition mode sequence in a new The are ± and are for the stimulated echo acquisition mode sequence The of saturated, and fat are in with the of fatty acid and The composition of bone marrow and adipose fat was not with 29.1 ± 3.5% saturated, 46.4 ± 4.8% monounsaturated, and 24.5 ± 3.1% for as compared with 27.1 ± 4.2% saturated, 49.6 ± 5.7% monounsaturated, and 23.4 ± 3.9% for subcutaneous was between tibial marrow and subcutaneous fat in the is the of for the 20 subjects as in In a composition of ± from fatty acid with and ± from fatty acid with was for bone as compared with subcutaneous fat with a composition of 23.4 ± 3.9% for and ± for fat composition in marrow and subcutaneous ± ± ± ± ± ± ± ± ± ± as of saturated, monounsaturated, and as well as the of are are the ± in a new The as of saturated, monounsaturated, and as well as the of are are the ± 1H NMR from human adipose tissue were at The of the 1H at 7T were with of high-resolution (8Zancanaro C. Nano R. Marchioro C. Sbarbati A. Boicelli A. Osculati F. Magnetic resonance spectroscopy investigations of brown adipose tissue and isolated brown adipocytes.J. Lipid Res. 1994; 35: 2191-2199Abstract Full Text PDF PubMed Google Scholar, 9Miyake Y. Yokomizo K. Matsuzaki N. Determination of unsaturated fatty acid composition by high-resolution nuclear magnetic resonance spectroscopy.J. Am. Oil Chem. Soc. 1998; 75: 1091-1094Crossref Google Scholar, 10Guillen M.D. Ruiz A. 1H nuclear magnetic resonance as a fast tool for determining the composition of acyl chains in acylglycerol mixtures.Eur. J. Lipid Sci. Technol. 2003; 105: 502-507Crossref Scopus (100) Google Scholar, 11Knothe G. Kenar J.A. Determination of the fatty acid profile by 1H-NMR spectroscopy.Eur. J. Lipid Sci. Technol. 2004; 106: 88-96Crossref Scopus (347) Google Scholar, 12Yeung D.K.W. Lam S.L. Griffith J.F. Chan A.B.W. Chen Z. Tsang P.H. Leung P.C. Analysis of bone marrow fatty acid composition using high-resolution proton NMR spectroscopy.Chem. Phys. Lipids. 2008; 151: 103-109Crossref PubMed Scopus (45) Google or in at 7T K. J. J. proton magnetic resonance spectroscopy of in adipose tissue at resolution in in Lipid Res. 2008; 49: Full Text Full Text PDF PubMed Scopus Google Scholar). the was chemical shift in humans is compared with 1.5 T or 3.0 The to protons adjacent to double bonds noninvasive of the fatty acid composition of adipose 13C NMR of human adipose tissue (15Beckmann N. Brocard J.J. Keller U. Seelig J. Relationship between the degree of unsaturation of dietary fatty acids and adipose tissue fatty acids assessed by natural-abundance 13C magnetic resonance spectroscopy in man.Magn. Reson. Med. 1992; 27: 97-106Crossref PubMed Scopus (26) Google Scholar, 16Dimand R.J. Moonen C.T. Chu S.C. Bradbury E.M. Kurland G. Cox K.L. Adipose tissue abnormalities in cystic fibrosis: noninvasive determination of mono- and polyunsaturated fatty acids by carbon-13 topical magnetic resonance spectroscopy.Pediatr. Res. 1988; 24: 243-246Crossref PubMed Scopus (17) Google Scholar, 17Moonen C.T. Dimand R.J. Cox K.L. The noninvasive determination of linoleic acid content of human adipose tissue by natural abundance carbon-13 nuclear magnetic resonance.Magn. Reson. Med. 1988; 6: 140-157Crossref PubMed Scopus (64) Google Scholar, 18Thomas E.L. Frost G. Barnard M.L. Bryant D.J. Taylor-Robinson S.D. Simbrunner J. Coutts G.A. Burl M. Bloom S.R. Sales K.D. et al.An in vivo 13C magnetic resonance spectroscopic study of the relationship between diet and adipose tissue composition.Lipids. 1996; 31: PubMed Scopus Google Scholar, S. A. In vivo of fatty acids in human adipose tissue using natural abundance 1H 13C MRS at 1.5 clinical applications to dietary 2003; PubMed Scopus (39) Google of fat composition, compared with a 1H the unsaturated in a are from the in in vivo at 1.5 abundance 13C NMR is by relatively resolution and compared with 1H spectroscopy for human study. 7T are not However, because the of 7T in is and 1H spectroscopy is routine on it to of 1H spectroscopy at 7T for clinical proton resonances in the chemical shift of are The resonances in the narrow of information about the abundance of protons between or adjacent to double correction for of the of saturated, monounsaturated, and fatty The analysis of lipid composition was by to The of saturated in triglycerides as by 1H NMR spectroscopy at about is in with However, the of fatty acids are was in study, compared with about fatty acids are A. Relationship of diet to the fatty acid composition of human adipose tissue and J. Clin. Nutr. PubMed Scopus Google Scholar, R.J. relationship between the fatty acid composition of the diet and of the adipose tissue in J. Clin. Nutr. PubMed Scopus Google Scholar). the of fatty acids to be was about in study compared with about in may in or with chemical the lipid resonances may the of the signals in vivo are the of 1H from several different fatty acids with different chemical a not the observed high-resolution analytical 1H NMR was to marrow fat composition from in and may in the study of the NMR method the of saturated fatty compared with of the D.K.W. Lam S.L. Griffith J.F. Chan A.B.W. Chen Z. Tsang P.H. Leung P.C. Analysis of bone marrow fatty acid composition using high-resolution proton NMR spectroscopy.Chem. Phys. Lipids. 2008; 151: 103-109Crossref PubMed Scopus (45) Google Scholar). as K. J. J. proton magnetic resonance spectroscopy of in adipose tissue at resolution in in Lipid Res. 2008; 49: Full Text Full Text PDF PubMed Scopus Google Scholar), correction for T2 is also and than correction for T1 a of the in T2 correction among the resonances and for it at 20 and is as as at to about correction for T1 for the resonances at 2 The T1 correction is not the is with of is the calf subcutaneous fat relatively proton relaxation than the marrow a on subcutaneous be from the in the between these of adipose as in the in subcutaneous tissue is as with fat of different with and the bone marrow as the tibial and to the Because of the resolution from bone marrow is to from subcutaneous as in is to between analysis of fat and marrow compared with from the or are of diet, and on fatty acid composition R.J. relationship between the fatty acid composition of the diet and of the adipose tissue in J. Clin. Nutr. PubMed Scopus Google Scholar, K. S. and in the fatty acid composition of human subcutaneous J. PubMed Scopus Google Scholar). adipose tissue a of fat and saturated fat compared with subcutaneous fat from the and K. S. and in the fatty acid composition of human subcutaneous J. PubMed Scopus Google Scholar). were not in the current study. Nevertheless, the for subcutaneous fat and for bone from 1H MRS study for 20 subjects is in with a for the of polyunsaturated to fatty acid by in vivo 13C study S. A. In vivo of fatty acids in human adipose tissue using natural abundance 1H 13C MRS at 1.5 clinical applications to dietary 2003; PubMed Scopus (39) Google of calf subcutaneous tissue of subjects The of 1H MRS is it is fast than a for as in is easily localized a and is easily or The resolution and sensitivity of the current 1H analysis also the detection of fat composition variation among healthy subjects be to the in diet and it is the method may be in detection of changes in the composition of fatty acids in response to diet, exercise, and diseases. in would noninvasive human lipid been on fat mass distribution by and techniques than fat In analysis of in fat composition between and subjects, on the calf subcutaneous fat in is than in The to the of fatty acid composition to saturated, monounsaturated, and was on the of polyunsaturated or double in human adipose tissue than to the 1H NMR were to quantify unsaturated fatty acids from fatty acids high-resolution analytical M.D. Ruiz A. 1H nuclear magnetic resonance as a fast tool for determining the composition of acyl chains in acylglycerol mixtures.Eur. 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Lipids. 2008; 151: 103-109Crossref PubMed Scopus (45) Google Scholar). in humans, would the to quantify linoleic and However, at the resolution in these a mixture of is from a of these the of fatty acids as saturated, monounsaturated, or a a chemical shift in the 1H may be it is on of resonances the of interest is to the was not evaluated in study, the of a small voxel (∼0.1 well the bone marrow analysis of resonances a narrow chemical shift to chemical shift the the resonance of protons to the is not by the at resonances at be at the of protons to a double T2 for and for subcutaneous than the resonance sequence the of than and on proton to the and was for the of fat composition in In to composition the well-resolved resonances of human tibial bone marrow and calf subcutaneous fat at 7T could also be as to quantify J. F. of in skeletal muscle by high-resolution spectroscopic using fat as the with Reson. Med. 2008; PubMed Scopus (17) Google Scholar), have interest the to to insulin and D. muscle lipid in insulin and type 2 2004; PubMed Scopus Google Scholar). In 1H MRS study at 7T the acquisition of 1H NMR from subcutaneous fat and from bone marrow is in healthy and the may be to assess triglyceride may facilitate longitudinal monitoring of changes in lipid composition in response to diet, exercise, and disease.

Composition of adipose tissue and marrow fat in humans by 1H NMR at 7 Tesla | Litlas