Monitoring of Quality Changes in Salmon and Salmon Rest Raw Materials by NMR

Living reference work entry


High-resolution nuclear magnetic resonance (HR-NMR) spectroscopy is extensively utilized to monitor the food quality. This chapter describes how HR-NMR can be an effective and comprehensive tool to assess the quality of Atlantic salmon though the analysis of water-soluble metabolites. A yet unpublished case study of salmon muscle NMR analysis performed by the authors is reported together with a description of the results of the most recent publications in the field. The onset of salmon rigor mortis is estimated by measuring the ATP/IMP ratio. It is described how to detect premortem stress by quantifying glucose, lactic acid, and other molecules. The procedures to assess freshness of various salmon fractions, such as K- and H-index, or the levels of nicotinamide adenine dinucleotide are compared and discussed. The fish safety is evaluated by monitoring the formation of biogenic amines. Salmon taste, flavor, odor, and nutritional value are also estimated by quantifying the main water-soluble metabolites. Finally, a new Umami index is proposed within the chapter, to estimate the level of fish palatability provided by the umami taste compounds.


Biogenic amines Fish freshness Fish stress NMR metabolomics Salmon quality Umami 


  1. 1.
    FAO. The state of world fisheries and aquaculture. Opportunities and challenges. Rome: Food and Agriculture Organization of the United Nations; 2014.Google Scholar
  2. 2.
    Erikson U, et al. Use of NMR in fish processing optimization: a review of recent progress. Magn Reson Chem. 2012;50(7):471–80.CrossRefGoogle Scholar
  3. 3.
    Sitter B, Krane J, Gribbestad IS, Jørgensen L, Aursand M. Quality evaluation of Atlantic halibut (Hippoglossus hippoglossus L) during ice storage using 1H NMR spectroscopy. In: Hills BP, Belton PS, Webb GA, editors. Advances in magnetic resonance in food science. Cambridge, MA: The Royal Society of Chemistry; 1999. p. 226–37.CrossRefGoogle Scholar
  4. 4.
    Erikson U. Muscle quality of Atlantic salmon (Salmo salar) as affected by handling stress. In: Department of biotechnology, faculty of chemistry and biology. Trondheim: NTNU; 1997.Google Scholar
  5. 5.
    Ciampa A. Development of methodologies for fish freshness assessment using metabonomics applications. In: Scienze e Biotecnologie degli Alimenti. Bologna: Universita di Bologna; 2013.Google Scholar
  6. 6.
    Erikson U, Beyer A, Sigholt T. Muscle high-energy phosphates and stress affect K-values during ice storage of Atlantic salmon (Salmo salar). J Food Sci. 1997;62(1):43–7.CrossRefGoogle Scholar
  7. 7.
    Olafsdottir G, et al. Methods to evaluate fish freshness in research and industry. Trends Food Sci Technol. 1997;8(8):258–65.CrossRefGoogle Scholar
  8. 8.
    Delbarre-Ladrat C, et al. Trends in postmortem aging in fish: understanding of proteolysis and disorganization of the myofibrillar structure. Crit Rev Food Sci Nutr. 2006;46(5):409–21.CrossRefGoogle Scholar
  9. 9.
    Sigurgisladottir S, et al. Salmon quality: methods to determine the quality parameters. Rev Fish Sci. 1997;5(3):223–52.CrossRefGoogle Scholar
  10. 10.
    Samuelsson LM, Larsson DJ. Contributions from metabolomics to fish research. Mol Biosyst. 2008;4(10):974–9.CrossRefGoogle Scholar
  11. 11.
    Bulsing JM, Sanders JK, Hall LD. Spin-echo methods for resolution control of lanthanide-shifted nmr spectra. J Chem Soc Chem Commun. 1981;23:1201–3.CrossRefGoogle Scholar
  12. 12.
    Piotto M, Saudek V, Sklenář V. Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J Biomol NMR. 1992;2(6):661–5.CrossRefGoogle Scholar
  13. 13.
    Shumilina E, et al. NMR approach for monitoring post-mortem changes in Atlantic salmon fillets stored at 0 and 4 C. Food Chem. 2015;184:12–22.CrossRefGoogle Scholar
  14. 14.
    Shumilina E, et al. Quality changes of salmon by-products during storage: assessment and quantification by NMR. Food Chem. 2016;211:803–11.CrossRefGoogle Scholar
  15. 15.
    Wishart DS, et al. HMDB 3.0—the human metabolome database in 2013. Nucleic Acids Res. 2012;gks1065.Google Scholar
  16. 16.
    Ulrich EL, et al. BioMagResBank. Nucleic Acids Res. 2008;36(suppl 1):D402–8.Google Scholar
  17. 17.
    Beckonert O, et al. Metabolic profiling, metabolomic and metabonomic procedures for NMR spectroscopy of urine, plasma, serum and tissue extracts. Nat Protoc. 2007;2(11):2692–703.CrossRefGoogle Scholar
  18. 18.
    Solanky KS, et al. Metabolic changes in Atlantic salmon exposed to Aeromonas salmonicida detected by 1H-nuclear magnetic resonance spectroscopy of plasma. Dis Aquat Organ. 2005;65(2):107–14.CrossRefGoogle Scholar
  19. 19.
    Karakach TK, et al. 1H-NMR and mass spectrometric characterization of the metabolic response of juvenile Atlantic salmon (Salmo salar) to long-term handling stress. Metabolomics. 2009;5(1):123–37.CrossRefGoogle Scholar
  20. 20.
    Gribbestad IS, Aursand M, Martinez I. High-resolution 1 H magnetic resonance spectroscopy of whole fish, fillets and extracts of farmed Atlantic salmon (Salmo salar) for quality assessment and compositional analyses. Aquaculture. 2005;250(1):445–57.CrossRefGoogle Scholar
  21. 21.
    Castejon D, et al. 1H-HRMAS NMR study of smoked Atlantic salmon (Salmo salar). Magn Reson Chem. 2010;48(9):693–703.CrossRefGoogle Scholar
  22. 22.
    Aursand M, et al. Nuclear magnetic resonance. In: Rehbein Hartmut and Oehlenschläger Jörg(eds.),. Fishery products: quality, safety and authenticity. Wiley-Blackwell. 2009. pp. 252–72.Google Scholar
  23. 23.
    Tejada M. ATP-derived products and K-value determination. In: Rehbein H, Oehlenschlager J, editors. Fishery products: quality, safety and authenticity. Chichester: John Wiley & Sons; 2009. p. 68–88.CrossRefGoogle Scholar
  24. 24.
    Love RM, Lavety J, Steel P. The connective tissues of fish. II. Gaping in commercial species of frozen fish in relation to rigor mortis. Int J Food Sci Technol. 1969;4(1):39–44.CrossRefGoogle Scholar
  25. 25.
    Cappeln G, Jessen F. ATP, IMP, and glycogen in cod muscle at onset and during development of rigor mortis depend on the sampling location. J Food Sci. 2002;67(3):991–5.CrossRefGoogle Scholar
  26. 26.
    Stroud GD. Rigor in fish. Torry Research Station, Ministry of Technology, FAO. Torry Advisory Note 36. The effect on quality. 1981. Notes
  27. 27.
    Berg T, Erikson U, Nordtvedt T. Rigor mortis assessment of Atlantic salmon (Salmo salar) and effects of stress. J Food Sci. 1997;62(3):439–46.CrossRefGoogle Scholar
  28. 28.
    Aue W, Karhan J, Ernst R. Homonuclear broad band decoupling and two-dimensional J-resolved NMR spectroscopy. J Chem Phys. 1976;64(10):4226–7.CrossRefGoogle Scholar
  29. 29.
    Ludwig C, Viant MR. Two-dimensional J-resolved NMR spectroscopy: review of a key methodology in the metabolomics toolbox. Phytochem Anal. 2010;21(1):22–32.CrossRefGoogle Scholar
  30. 30.
    Selye H. The evolution of the stress concept: the originator of the concept traces its development from the discovery in 1936 of the alarm reaction to modern therapeutic applications of syntoxic and catatoxic hormones. Am Sci. 1973;61(6):692–9.Google Scholar
  31. 31.
    Barton BA. Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol. 2002;42(3):517–25.CrossRefGoogle Scholar
  32. 32.
    Barton BA, Iwama GK. Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Ann Rev Fish Dis. 1991;1:3–26.CrossRefGoogle Scholar
  33. 33.
    Pickering AD. Stress and fish. Pickering, London: Academic Press;1981.Google Scholar
  34. 34.
    Iwama GK, et al. Fish stress and health in aquaculture. Vol. 62. Cambridge: Cambridge University Press; 2011.Google Scholar
  35. 35.
    Nicholson JK, et al. 750 MHz 1H and 1H-13C NMR spectroscopy of human blood plasma. Anal Chem. 1995;67(5):793–811.CrossRefGoogle Scholar
  36. 36.
    Samuelsson LM, et al. Using NMR metabolomics to identify responses of an environmental estrogen in blood plasma of fish. Aquat Toxicol. 2006;78(4):341–9.CrossRefGoogle Scholar
  37. 37.
    Bonga SW. The stress response in fish. Physiol Rev. 1997;77(3):591–625.Google Scholar
  38. 38.
    Saito T, Arai K, Matuyoshi M. A new method for estimating the freshness of fish. Bull Jap Soc Sci Fish. 1959;24:749–50.CrossRefGoogle Scholar
  39. 39.
    Ehira S. A biochemical study on the freshness of fish. Bull Tokai Reg Fish Res Lab. 1976;88:1–132.Google Scholar
  40. 40.
    Jones N, J. Murray. Nicotinamide Adenine Dinucleotide (Nad) And Reduced Nad In Living And Chill-Stored Dying Muscle Of Cod, Gadus Callarias.日本水産学会誌. 1966. 32(2): 197–203.Google Scholar
  41. 41.
    Howell N, et al. High-resolution NMR and Magnetic Resonance Imaging (MRI) studies on fresh and frozen cod (Gadus morhua) and haddock (Melanogrammus aeglefinus). J Sci Food Agric. 1996;72(1):49–56.CrossRefGoogle Scholar
  42. 42.
    Ciampa A, et al. Changes in the amino acid composition of Bogue (Boops boops) fish during storage at different temperatures by 1H-NMR spectroscopy. Nutrients. 2012;4(6):542–53.CrossRefGoogle Scholar
  43. 43.
    Heude C, et al. Rapid assessment of fish freshness and quality by 1H HR-MAS NMR spectroscopy. Food Anal Methods. 2015;8(4):907–15.CrossRefGoogle Scholar
  44. 44.
    Maniara G, et al. Method performance and validation for quantitative analysis by 1H and 31P NMR spectroscopy. Applications to analytical standards and agricultural chemicals. Anal Chem. 1998;70(23):4921–8.CrossRefGoogle Scholar
  45. 45.
    Brækkan OR. A comparative study of vitamins in the trunk muscles of fishes. In: Reports on technological research concerning Norwegian fish industry. Bergen; 1959.Google Scholar
  46. 46.
    Askar A, H. Treptow. Biogene Amine in Lebensmitteln. Vorkommen, Bedeutung und Bestimmung; 1986.Google Scholar
  47. 47.
    ten Brink B, et al. Occurrence and formation of biologically active amines in foods. Int J Food Microbiol. 1990;11(1):73–84.CrossRefGoogle Scholar
  48. 48.
    Arnold SH, Brown WD. Histamine toxicity from fish products. Adv Food Res. 1978;24:113–54.CrossRefGoogle Scholar
  49. 49.
    Santos MS. Biogenic amines: their importance in foods. Int J Food Microbiol. 1996;29(2):213–31.CrossRefGoogle Scholar
  50. 50.
    Hoogwerf BJ, Laine D, Greene E. Urine C-peptide and creatinine (Jaffe method) excretion in healthy young adults on varied diets: sustained effects of varied carbohydrate, protein, and meat content. Am J Clin Nutr. 1986;43(3):350–60.Google Scholar
  51. 51.
    Bouckenooghe T, Remacle C, Reusens B. Is taurine a functional nutrient? Curr Opin Clin Nutr Metab Care. 2006;9(6):728–33.CrossRefGoogle Scholar
  52. 52.
    Zulli A. Taurine in cardiovascular disease. Curr Opin Clin Nutr Metab Care. 2011;14(1):57–60.CrossRefGoogle Scholar
  53. 53.
    Lourenco R, Camilo M. Taurine: a conditionally essential amino acid in humans? An overview in health and disease. Nutr Hosp. 2002;17(6):262–70.Google Scholar
  54. 54.
    Yamaguchi S, Ninomiya K. What is umami? Food Rev Intl. 1998;14(2–3):123–38.CrossRefGoogle Scholar
  55. 55.
    Di Natale C, Olafsdottir G. Electronic nose and electronic tongue. In: Rehbein H, Oehlenschlager J, editors. Fishery products: quality, safety and authenticity. Chichester: John Wiley & Sons; 2009. p. 105–26.CrossRefGoogle Scholar
  56. 56.
    Van Waarde A. Biochemistry of non-protein nitrogenous compounds in fish including the use of amino acids for anaerobic energy production. Comp Biochem Physiol Part B Comp Biochem. 1988;91(2):207–28.CrossRefGoogle Scholar
  57. 57.
    Hebard, C., G. Flick, and R. Martin, Occurrence and significance of trimethylamine oxide and its derivatives in fish and shellfish, in Chemistry and biochemistry of marine food products, R. Martin, et al., Editors. 1982, AVI Publishing Company: Westport, USA. p. 149-304.Google Scholar

Authors and Affiliations

  1. 1.Department of BiotechnologyNorwegian University of Science and Technology (NTNU)TrondheimNorway
  2. 2.Processing technologySINTEF Fisheries and AquacultureTrondheimNorway

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