The magic angle view to food: magic-angle spinning (MAS) NMR spectroscopy in food science
Nuclear Magnetic Resonance (NMR) spectroscopy has been used in food science and nutritional studies for decades and is one of the major analytical platforms in metabolomics. Many foods are solid or at least semi-solid, which denotes that the molecular motions are restricted as opposed to in pure liquids. While the majority of NMR spectroscopy is performed on liquid samples and a solid material gives rise to constraints in terms of many chemical analyses, the magic angle thrillingly enables the application of NMR spectroscopy also on semi-solid and solid materials. This paper attempts to review how magic-angle spinning (MAS) NMR is used from ‘farm-to-fork’ in food science.
KeywordsSemi-solid food characterization Food composition Foodomics Food metabolites Meat Dairy Plant-based food Taste compounds Cheese Food authenticity Intact tissue Food structure Fruit ripening Grain filling, vegetables, plant biochemistry
Abbreviations and definitions
Two-dimensional. Term used for techniques, which give data plotted in a space defined by two frequency axes rather than one and with the intensities constituting a third dimension
Comprehensive multiphase NMR combining both 1H HR-MAS, diffusion restriction and 13C CP MAS type of experiments in one probe
Cross polarization. CP is technique employed in solid-state NMR to transfer magnetization from one type of spin to another type of spin through space. This is achieved by applying a pulse simultaneously on the two different spins
Carr–Purcell–Meiboom–Gill. CPMG is a pulse sequence that utilizes a T2 relaxation filter to remove or attenuate broad resonances from of molecules with a short T2 relaxation. This enables broadening of macromolecules beyond detection, allowing improved detection of small molecules
Delays alternating with nutations for tailored excitation (Morris and Freeman 1978).
Dynamic nuclear polarisation. Highly sensitive NMR technique where spectra are recorded under hyperpolarisation of the sample
Differential scanning calorimetry
Fourier transform InfraRed spectroscopy
Hierarchical cluster analysis. HCA is method that is used to classify and cluster samples or variables based on their similarities and dissimilarities
High resolution MAS. A term defined by the vendor for NMR probe heads optimized for 1H NMRof gel-state samples (not crystalline, but soft solids, swollen materials or gels), where standard liquid pulse sequences (1D and 2D, HSQC, TOCSY) can be applied under magic angle spinning conditions
High pressure liquid chromatography
Heteronuclear single quantum correlation. HSQC is a 2D experiment used in NMR spectroscopy. In a 1H-13C HSQC experiment, information about the correlation between the aliphatic carbon and its attached protons are obtained, which can facilitate in spectral assignment
Hadamard encoded intermolecular multiple-quantum coherence
Magic angle spinning. MAS is a technique used in solid-state NMR spectroscopy and consists of spinning the sample at the magic angle θm (54.74°) with respect to the direction of the magnetic field to enhance the spectral resolution
Multivariate data analysis. MVDA is typically used to explore variations and trends in data across a high number of variables. As NMR spectral data consist of a high number of variables, MVDA is a useful tool to explore NMR spectral data
Nuclear Overhauser enhancement spectroscopy. An NMR experiment that takes advantage of the Nuclear Overhauser effect, consisting of dipole–dipole interactions through space
Orthogonal partial least squares. O-PLS is an adaption of PLS that separates the systematic variation in X into variation that is related or unrelated to Y
Phase-altered spinning sideband. Scheme for two-dimensional sideband separation in MAS NMR. The scheme can produce spinning sideband-free solid-state NMR spectra (Antzutkin et al. 1995)
Principal component analysis
Phase-corrected magic angle turning. Scheme for two-dimensional sideband separation in MAS NMR. The scheme can produce spinning sideband-free solid-state NMR spectra (Hu et al. 1995)
Partial least squares projections to latent structures is the supervised extension of PCA where the data matrix, X, is related to Y by regression
Partial least squares discriminant analysis. PLS-DA is a supervised method that uses a categorical response variable
Poly(methyl methacrylate). Polymer material used for MAS rotors
Polyoxymethylene. Polymer material used for MAS rotors
Proton relaxation induced spectral-editing. A 13C cross-polarization experiment that takes advantage of differences in the 1H relaxation to obtain information on molecular dynamics. If multiple components are present in the proton relaxation processes, proton magnetisation can be prepared in such a way that the magnetisation of protons having different relaxation times is separated (Tang et al. 2000)
Quantitative NMR. qNMR refers to the use of NMR to determine the exact concentration of one or more chemical species
: Refocused-insensitive nuclei enhanced by polarization transfer. RINEPT is technique employed in solution NMR to elucidates scalar (or J-) couplings between 1H and 13C nuclei. The technique has occasionally been adopted to solid-state NMR to transfer magnetization from one type of spin to another type of spin through bonds (Arnold et al. 2015)
The procedure for optimizing the magnetic field homogeneity prior to acquisition of a spectrum
Single pulse. The most basic NMR experiment is called a single pulse experiment. The experiment begins with the system at equilibrium and thus magnetization is oriented along the z axis. The first step is a 90° x pulse, which means that an excitation field is applied along the x axis by one of the radio frequency coils
Secure water suppression enhanced through T1 effects. Modified version of the WET pulse sequence where each selective pulse is broken up in the DANTE fashion, inserting bipolar pulsed-field gradients in the delays (Wu and Otting 2005)
Total correlation spectroscopy. TOCSY is a 2D experiment that enables the detection of cross peaks of coupled protons. Cross peaks are observed both for nuclei which are directly coupled and also between nuclei which are connected by a chain of couplings. This makes it useful for identifying the larger interconnected networks of spin couplings.
Water suppression by gradient-tailored excitation. In WATERGATE the gradient echo sequence combines a selective 180-degrees radiofrequency pulse and two field gradient pulses to achieve a highly selective and effective water suppression (Piotto et al. 1992).
Water suppression enhanced through T1 effects. This pulse sequence uses shaped, selective pulses and pulsed magnetic field gradients to suppress one or more solvent signals. The WET scheme is based on a series of water-selective excitation pulses followed by pulsed field gradients to defocus the transverse water magnetization (Smallcombe et al. 1995).
Wide line separation NMR. WISE is an NMR experiment based on the use of cross-polarization to characterize molecular dynamics (Schmidt-Rohr et al. 1992).
HMJ contributed with literature search and drafted approx. 65% of the text. HCB contributed with literature search and drafted approx. 35% of the text. Both authors revised and approved the final version of the manuscript.
Compliance with ethical standards
Conflict of interest
The authors Henrik Max Jensen and Hanne Christine Bertram declare no conflict of interest.
This article does not contain any studies with human participants or animals performed by any of the authors.
- Ardenkjaer-Larsen, J.-H., Boebinger, G. S., Comment, A., Duckett, S., Edison, A. S., Engelke, F., Griesinger, C., Griffin, R. G., Hilty, C., Maeda, H., Parigi, G., Prisner, T., Ravera, E., Bentum, J. v., Vega, S., Webb, A., Luchinat, C., Schwalbe, H., & Frydman, L. (2015). Facing and overcoming challenges in bio-molecular NMR spectroscopy. Angewandte Chemie International Edition, 54, 2–26.CrossRefGoogle Scholar
- Aursand, M., Gribbestad, I. S., & Martinez, I. (2008). Omega-3 fatty acids content of intact muscle of farmed Atlantic salmon (Salmo solar) examined by 1H MAS NMR spectroscopy. In G. A. Webb (Ed.), Modern magnetic resonance: Part 1: Applications in chemistry, biological and marine sciences (1st edn., pp. 941–945). Dordrecht: Springer.Google Scholar
- Bankefors, J., Kaszowska, M., Schlectriem, C., Pickova, J., Brännas, E., Edebo, L., Kiessling, A., & Sandström, C. (2011). A comparison of the metabolic profile on intact tissue and extracts of muscle and liver of juvenile Atlantic salmon (Salmo solar L.)—Application to a short feeding study. Food Chemistry, 129, 1397–1405.CrossRefGoogle Scholar
- Bardet, M., Foray, M. F., & Guillermo, A. (2006). High-resolution solid-state NMR spectroscopy as an analytical tool to study plant seeds. In G. A. Webb (Ed.), Modern magnetic resonance, Part 3: Applications in materials science and food sciences (pp. 1777–1781). Dordrecht: Springer.CrossRefGoogle Scholar
- Bertram, H. C., Duarte, I. F., Gil, A. M., Knudsen, K. E. B., & Laerke, H. N. (2007). Metabolic profiling of liver from hypercholesterolemic pigs fed rye or wheat fiber and from normal pigs. High-resolution magic angle spinning H-1 NMR spectroscopic study. Analytical Chemistry, 79, 168–175.PubMedCrossRefGoogle Scholar
- Bertram, H. C., Hu, J. Z., Rommerein, D. N., Wind, R. A., & Andersen, H. J. (2004d). Dynamic high-resolution 1H and 31P NMR spectroscopy and 1H T2 measurements in postmortem rabbit muscles using slow magic angle spinning. Journal of Agricultural and Food Chemistry, 52, 2681–2688.PubMedCrossRefGoogle Scholar
- Bertram, H. C., Whittaker, A. K., Andersen, H. J., & Karlsson, A. H. (2004a). The use of simultaneous 1H & 31P magic angle spinning nuclear magnetic resonance measurements to characterize energy metabolism during the conversion of muscle to meat. International Journal of Food Science and Technology, 39, 661–670.CrossRefGoogle Scholar
- Brescia, M. A., & Sacco, A. (2006). Magic angle spinning NMR of flours and doughs. In G. A. Webb (Ed.), Modern magnetic resonance, Part 3: Applications in materials science and food sciences (pp. 1735–1741). Dordrecht: Springer.Google Scholar
- Calucci, L., & Geppi., M. (2006). High-resolution solid-state of gluten and dough. In G. A. Webb (Ed.), Modern magnetic resonance, Part 3: Applications in materials science and food sciences (pp. 1747–1754). Dordrecht: Springer.Google Scholar
- Chatterjee, S., Matas, A., Isaacson, T., Kehlet, C., Rose, J., & Stark, R. (2016). Solid-state 13C NMR delineates the architectural design of biopolymers in native and engineered tomato fruit cuticles. Biomolecules, 17, 215–224.Google Scholar
- Corsaro, C., Mallamace, D., Vasi, S., Ferrantelli, V., Dugo, G., & Cicero, N.(2015). 1H HR-MAS NMR spectroscopy and the metabolite determination of typical foods in Mediterranean diet. Journal of Analytical Methods in Chemistry. https://doi.org/10.1155/2015/175696.CrossRefPubMedPubMedCentralGoogle Scholar
- Friebolin, H. (1998). Basic one- and two-dimensional NMR spectroscopy (3rd ed.). Chichester: Wiley-VCH. ISBN 3-527-29513-5.Google Scholar
- Gaëlle, S., Kervarec, N., & Cérantola, S., & Connan, D. B. (2015). HR MAS NMR analysis and identification of molecules of interest via conventional 1D and 2D NMR: sample preparation and optimization of experimental conditions. In S. Stengel (Ed.), Chapter 12 in ‘Methods in molecular biology’ (Vol. 1308, pp. 191–205). Dordrecht: Springer.Google Scholar
- Gil, M., Duarte, I. F., Delgadillo, I., Colquhoun, I. J., Casuscelli, F., Humpfer, E., & Spraul, M. (2000). Study of the compositional changes of mango during ripening by use of nuclear magnetic resonance spectroscopy. Journal of Agricultural and Food Chemistry, 48, 1524–1536.PubMedCrossRefGoogle Scholar
- Gobet, M., Rondeau-Mouro, C., Buchin, S., Qu´er´, L., Guichard, J.-L., Foucat, E., L., & Moreau, C. (2010). Distribution and mobility of phosphates and sodium ions in cheese by solid-state 31P and double-quantum filtered 23Na NMR spectroscopy. Magnetic Resonance in Chemistry, 48, 297–303.PubMedCrossRefGoogle Scholar
- Hennebelle, M., Roy, M., St-Pierre, V., Courchesne-Loyer, A., Fortier, M., Bouzier-Sore, A.-K., Gallis, J.-L., Beauvieux, M.-C., & Cunnane, S. C. (2015). Energy restriction does not prevent insulin resistance but does prevent liver steatosis in aging rats on Western-style diet. Nutrition, 31, 523–530.PubMedCrossRefGoogle Scholar
- Hoult, D. I. (1976). Solvent peak saturation with single-phase and quadrature Fourier transformation. Journal of Magnetic Resonance, 21, 337–347.Google Scholar
- Lamichhane, S., Yde, C. C., Mielby, L. H., Kidmose, U., Møller, J. R., Hammershoej, M., & Bertram, H. C. (2015). High-resolution magic-angle spinning studies of semi-hard Danbo (30+) cheese-impact of processing conditions and relation to sensory perception. In: F. Capozzi, L. Laghi, & P. S. Belton (Eds.), Magnetic resonance in food science: Defining food by magnetic resonance (pp. 171–180). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
- Larsen, F. H., Kasprzak, M. M., Lærke, H. N., Knudsen, K. E. B., Pedersen, S., Jørgensen, A. S., & Blennow, A. (2013). Hydration properties and phosphorous speciation in native, gelatinized and enzymatically modified potato starch analyzed by solid-state MAS NMR. Carbohydrate Polymers, 97, 502–511.PubMedCrossRefGoogle Scholar
- Martins, J. G. (2009). EPA but not DHA appears to be responsible for the efficacy of omega-3 long chain polyunsaturated fatty acid supplementation in depression: evidence from a meta-analysis of randomized controlled trials. Journal of the American College of Nutrition, 28(5), 525–542.PubMedCrossRefGoogle Scholar
- Morris, G. A., & Freeman, R. (1978). Selective excitation in fourier transform nuclear magnetic resonance. Journal of Magnetic Resonance, 29, 433–462.Google Scholar
- Mutungi, C., Passauer, L., Onyango, C., Jaros, D., & Rohm, H. (2012). Debranched cassava starch crystallinity determination by Raman spectroscopy: Correlation of features in Raman spectra with X-ray diffraction and 13C CP/MAS NMR spectroscopy. Carbohydrate Polymers, 87, 598–606.CrossRefGoogle Scholar
- Nestor, G., Bankefors, J., Schlectriem, C., Brännas, E., Pickova, J., & Sandström, C. (2010). High-resolution 1H magic angle spinning NMR spectroscopy of intact arctic char (Salvelinus alpinus) muscle. Quantitative analysis of n-3 fatty acids, EPA and DHA. Journal of Agricultural and Food Chemistry, 58, 10799–10803.PubMedCrossRefGoogle Scholar
- Paris, M., Bizot, H., Emery, J., Buzaré, J. Y., & Buléon, A. (2001b). NMR local range investigations in amorphous starchy substrates: II—Dynamical heterogeneity probed by 1H/13C magnetization transfer and 2D WISE solid state NMR. International Journal of Biological Macromolecules, 29, 137–143.PubMedCrossRefGoogle Scholar
- Park, S., Baker, J. O., Himmel, M. E., Parilla, P. A., & Johnson, D. K. (2010). Cellulose crystallinity index: Measurement techniques and their impact in interpreting cellulase performance. Biotechnology for Biofuels, 3, 10. https://doi.org/10.1186/1754-6834-3-10.CrossRefPubMedPubMedCentralGoogle Scholar
- Pearson, K. (1901). On lines and planes of closest fit to systems of points in space. Philosophical Magazine, 2, 559–572.Google Scholar
- Pecher, O., Halat, D. M., Lee, J., Liu, Z. G., Griffith, K. J., Braun, M., & Grey, C. P. (2017). Enhanced efficiency of solid-state NMR investigations of energy materials using an external automatic tuning/matching (eATM) robot. Journal of Magnetic Resonance, 275, 127–136.PubMedCrossRefGoogle Scholar
- Piterina, A. V., Barlett, J., & Pembroke, J. T. (2009). 13C-NMR assessment of the pattern of organic matter transformation during domestic wastewater treatment by autothermal aerobic digestion (ATAD). International Journal of Environmental Research and Public Health, 6, 2288–2306.PubMedPubMedCentralCrossRefGoogle Scholar
- Ragauskas, A. J., Beckham, G. T., Biddy, M. J., Chandra, R., Chen, F., Davis, M. F., Davison, B. H., Dixon, R. A., Gilna, P., Keller, M., Langan, P., Naskar, A. K., Saddler, J. N., Tschaplinski, T. J., Tiskan, G. A., & Wyman, C. E. (2014) Lignin valorization: improving lignin processing in the biorefinery. Science 344, https://doi.org/10.1126/science.1246843.
- Ravanbakhsh, S., Liu, P., Bjordahl, T. C., Mandal, R., Grant, J. R., Wilson, M., Eisner, R., Sinelnikov, I., Hu, X., Luchinat, C., Greiner, R., & Wishart, D. S. (2015). Accurate, fully-automated NMR spectral profiling for metabolomics. PLoS ONE. https://doi.org/10.1371/journal.pone.0124219.CrossRefPubMedPubMedCentralGoogle Scholar
- Sacco, D., Bolsi, I. N., Massini, R., Spraul, M., Humpfer, E., & Stefano Ghelli, S. (1998). Preliminary investigation on the characterization of Durum wheat flours coming from some areas of south italy by means of 1H high-resolution magic angle spinning nuclear magnetic resonance. Journal of Agricultural and Food Chemistry, 46, 4242–4249.CrossRefGoogle Scholar
- Song, C., & Zhao, S. (2007). “Omega-3 fatty acid eicosapentaenoic acid. A new treatment for psychiatric and neurodegenerative diseases: A review of clinical investigations”. Expert Opinion on Investigational Drugs, 16, 1627–1638. https://doi.org/10.1517/135437126.96.36.1997.CrossRefPubMedGoogle Scholar
- Song, E.-H., Kim, H.-J., Jeong, J., Chung, H.-J., Kim, H.-Y., Bang, E., & Hong, Y-S. (2016). A 1H HR-MAS NMR-based metabolomic study for metabolic characterization of rice grain from various Oryza sativa L. cultivars. Journal of Agricultural and Food Chemistry, 64, 3009–3016.PubMedCrossRefGoogle Scholar
- Soong, J. L., Reuss, D., Pinney, C., Boyack, T., Haddix, M.L., Stewart, C.E., & Cotrufo, M. F. (2014). Design and operation of a continuous 13C and 15N labeling chamber for uniform or differential, metabolic and structural, plant isotope labeling. Journal of Visualized Experiments, 83, e51117. https://doi.org/10.3791/51117 CrossRefGoogle Scholar
- Tang, H., & Wang, Y. (2006). ‘High-resolution solid-state NMR spectroscopy of starch polysaccharides’. In G. A. Webb (Ed.), Modern magnetic resonance, Part 3: Applications in materials science and food sciences (pp. 1761–1769). New York: Springer.Google Scholar
- Vermathen, M., Marzorati, M., Diserens, G., Baumgartner, D., Good, C., Gasser, F., & Vermathen, P. (2017). Metabolic profiling of apples from different production systems before and after controlled atmosphere (CA) storage studied by H-1 high resolution-magic angle spinning (HR-MAS) NMR. Food Chemistry, 233, 391–400.PubMedCrossRefGoogle Scholar
- Yu, B., Vengadesan, G., Wang, H., Jashi, L., Yefremov, T., Gaba, V., Shomer, I., & Stark, R. E. (2006). Magic-angle spinning NMR studies of cell wall bound aromatic-aaliphatic biopolyesters associated with strengthening of intercellular adhesion in potato (Solanum tuberosum) tuber paranchyma. Biomacromolecules, 7, 937–944.PubMedCrossRefGoogle Scholar