Analytical and Bioanalytical Chemistry

, Volume 411, Issue 8, pp 1591–1599 | Cite as

Simultaneous metabolic mapping of different anatomies by 1H HR-MAS chemical shift imaging

  • Alan WongEmail author
  • Covadonga Lucas-Torres
Research Paper


Localized information on a specimen is considered indispensable for deciphering biological activity. Magnetic resonance spectroscopy is a notable method because of its versatility; however, one limitation is the spectral quality on a static sample. This study explores an amalgamated method with two magnetic resonance experiments: high-resolution magic-angle spinning (HR-MAS) for high-quality spectral acquisition from a spinning sample and chemical shift imaging (CSI) for spatial localization. The advantage of HR-MAS CSI is its amenity for simultaneously profiling the metabolome—with good spectral data—at different spatial regions in a single experiment. Herein, 1H HR-MAS CSI (including a T2-contrast CSI) was described and performed on various food tissues and an intact organism. Different data analyses such as multivariate and quantification were explored to identify the metabolic variants in different anatomical regions and in one case, to assist in a spatial allocation. The limitation and drawback of the experiment are also discussed.

Graphical abstract


Metabolomics HR-MAS NMR Chemical shift imaging CSI Localized metabolic profiling Metabolic mapping 



We are grateful to Dr. Franck Fayon and his team (Orleans, France) for their initial assistance on the experimental setup and also to Dr. Gaspard Huber (CEA-Saclay, France) for the discussions and reviewing the manuscript.


This work was financially supported by Agence Nationale de la Recherché (ANR-16-CE11-0023-01 and ANR-12-JSV5-0005-01).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

216_2019_1603_MOESM1_ESM.pdf (1.1 mb)
ESM 1 (PDF 1138 kb)


  1. 1.
    Beckonert O, Coen M, Keun HC, Wang Y, Ebbels TMD, Holmes E, et al. High-resolution magic-angle-spinning NMR spectroscopy for metabolic profiling of intact tissues. Nat Protoc. 2010;5:1019–32. Scholar
  2. 2.
    Fuss TL, Cheng LL. Evaluation of cancer metabolomics using ex vivo high resolution magic angle spinning (HRMAS) magnetic resonance spectroscopy (MRS). Metabolites. 2016;6:1–22. Scholar
  3. 3.
    Sitter B, Bathen TF, Tessem M, Gribbestad IS. High-resolution magic angle spinning (HR MAS) MR spectroscopy in metabolic characterization of human cancer. Prog Nucl Magn Reson Spectrosc. 2009;54:239–54. Scholar
  4. 4.
    Vermathen M, Müller J, Furrer J, Müller N, Vermathen P. 1H HR-MAS NMR spectroscopy to study the metabolome of the protozoan parasite Giardia lamblia. Talanta. 2018;188:429–41. Scholar
  5. 5.
    Farooq H, Courtier-murias D, Soong R, Bermel W, Kingery WM, Simpson AJ. HR-MAS NMR spectroscopy: a practical guide for natural samples. Curr Org Chem. 2013;17:3013–31. Scholar
  6. 6.
    Valentini M, Ritota M, Cafiero C, Cozzolino S, Leita L, Sequi P. The HRMAS-NMR tool in foodstuff characterisation. Magn Reson Chem. 2011;49:S121–5. Scholar
  7. 7.
    Mazzei P, Piccolo A, Valentini M. Intact food analysis by means of HRMAS-NMR spectroscopy. In: Webb GA (ed) Modern magnetic resonance. Springer International Publishing; 2017. pp. 1–16.Google Scholar
  8. 8.
    Li W. Multidimensional HRMAS NMR: a platform for in vivo studies using intact bacterial cells. Analyst. 2006;131:777–81. Scholar
  9. 9.
    Righi V, Constantinou C, Kesarwani M, Rahme LG, Tzika AA. Live-cell high resolution magic angle spinning magnetic resonance spectroscopy for in vivo analysis of Pseudomonas aeruginosa metabolomics. Biomed Rep. 2013;1:707–12. Scholar
  10. 10.
    Righi V, Apidianakis Y, Mintzopoulos D, Astrakas L, Rahme LG, Tzika AA. In vivo high-resolution magic angle spinning magnetic resonance spectroscopy of Drosophila melanogaster at 14.1 T shows trauma in aging and in innate immune-deficiency is linked to reduced insulin signaling. Int J Mol Med. 2010;26:175–84. Scholar
  11. 11.
    Sarou-Kanian V, Joudiou N, Louat F, Yon M, Szeremeta F, Même S, et al. Metabolite localization in living drosophila using high resolution magic angle spinning NMR. Sci Rep. 2015;5:1–5. Scholar
  12. 12.
    Wind RA, Hu JZ, Rommereim DN. High-resolution 1H NMR spectroscopy in a live mouse subjected to 1.5 Hz magic angle spinning. Magn Reson Med. 2003;50:1113–9. Scholar
  13. 13.
    Wind RA, Hu JZ, Majors PD. Localized in vivo isotropic– anisotropic correlation 1H NMR spectroscopy using ultra-slow magic angle spinning. Magn Reson Med. 2006;55:41–9. Scholar
  14. 14.
    Pampel A, Zick K, Glauner H. Studying lateral diffusion in lipid bilayer by combining a magic angle spinning NMR probe with a microimaging gradient system. J Am Chem Soc. 2004;126:9534–5. Scholar
  15. 15.
    Yon M, Sarou-kanian V, Scheler U, Bouler J, Bujoli B, Massiot D, et al. Solid-state 31P and 1H chemical MR micro-imaging of hard tissues and biomaterials with magic angle spinning at very high magnetic field. Sci Rep. 2017;7:8224. Scholar
  16. 16.
    Clausen MR, Edelenbos M, Bertram HC. Mapping the variation of the carrot metabolome using 1H NMR spectroscopy and consensus PCA. J Agric Food Chem. 2014;62:4392–8. Scholar
  17. 17.
    Gunstone FD. The lipid handbook, 2nd ed. London; 1995. pp. 518–157.Google Scholar
  18. 18.
    Hoppel C. The role of carnitine in normal and altered fatty acid metabolism. Am J Kidney Dis. 2003;41:S4–S12. Scholar
  19. 19.
    Schönfeld P, Wojtczak L. Short- and medium-chain fatty acids in energy metabolism: the cellular perspective. J Lipid Res. 2016;57:943–54. Scholar
  20. 20.
    Kapranas A, Snart CJP, Williams H, Hardy ICW, Barrett DA. Metabolomics of aging assessed in individual parasitoid wasps. Sci Rep. 2016;6:34848. Scholar
  21. 21.
    Welsh JH. Composition and mode of action of some invertebrate venoms. Annu Rev. 1963;4:293–305. Scholar
  22. 22.
    Martínez-Yusta A, Guillén MD. A study by 1H nuclear magnetic resonance of the influence on the frying medium composition of some soybean oil-food combinations in deep-frying. Food Res Int. 2014;55:347–55. Scholar
  23. 23.
    Siri-Tarino PW, Sun Q, Hu FB, Krauss RM. Saturated fat, carbohydrate, and cardiovascular disease. Am J Clin Nutr. 2010;91:502–9. Scholar
  24. 24.
    Lucas-Torres C, Huber G, Ichikawa A, Nishiyama Y, Wong A. HR-μMAS NMR-based metabolomics: localized metabolic profiling of a garlic clove with μg tissues. Anal Chem. 2018;90:13736–43. Scholar
  25. 25.
    Worley B, Powers R. Multivariate analysis in metabolomics. Curr Metabolomics. 2015;1:92–107. Scholar
  26. 26.
    Wind RA, Hu JZ. In vivo and ex vivo high-resolution 1H NMR in biological systems using low-speed magic angle spinning. Prog Nucl Magn Reson Spectrosc. 2006;49:207–59. Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.NIMBE, CEA, CNRS, CEA SaclayUniversité Paris-SaclayGif-sur-YvetteFrance

Personalised recommendations