Document Type: Review Article

Authors

1 DDS, MSc, Department of Oral and Maxillofacial Radiology, Faculty of Dentistry, Kerman University of Medical Sciences, Kerman, Iran

2 DVM, Ph.D., Assistant Professor, Department of Food Hygiene and Public Health, Faculty of Veterinary Medicine, Shahid Bahonar University of Kerman, Kerman, Iran

3 MSc, Department of Radiology, School of Paramedical Sciences, Shiraz University of Medical Sciences, Shiraz, Iran

4 DDS, MSc, Assistant Professor, Department of Pediatric Dentistry, Faculty of Dentistry, Shiraz University of Medical Sciences, Shiraz, Iran

Abstract

Modern challenges of food science require a new understanding of the determinants of food quality and safety. Application of advanced imaging modalities such as magnetic resonance imaging (MRI) has seen impressive successes and fast growth over the past decade. Since MRI does not have any harmful ionizing radiation, it can be considered as a magnificent tool for the quality control of food products. MRI allows the structure of foods to be imaged noninvasively and nondestructively. Magnetic resonance images can present information about several processes and material properties in foods. This review will provide an overview of the most prominent applications of MRI in food research.

Keywords

  1. Grunert KG. Food quality and safety: consumer perception and demand. European Review of Agricultural Economics. 2005;32:369-91. doi.org/10.1093/eurrag/jbi011.
  2. Xiong Z, Sun DW, Pu H, Gao W, Dai Q. Applications of Emerging Imaging Techniques for Meat Quality and Safety Detection and Evaluation: A Review. Crit Rev Food Sci Nutr. 2015:0. PubMed PMID: 25975703.
  3. Bushong SC. Magnetic resonance imaging: physical and biological principles. 3rd ed. United States of America: Mosby; 2003.
  4. Van As H, van Duynhoven J. MRI of plants and foods. J Magn Reson. 2013;229:25-34. doi.org/10.1016/j.jmr.2012.12.019. PubMed PMID: 23369439.
  5. Collewet G, Bogner P, Allen P, Busk H, Dobrowolski A, Olsen E, et al. Determination of the lean meat percentage of pig carcasses using magnetic resonance imaging. Meat Sci. 2005;70:563-72. doi.org/10.1016/j.meatsci.2005.02.005. PubMed PMID: 22063881.
  6. Kremer PV, Forster M, Scholz AM. Use of magnetic resonance imaging to predict the body composition of pigs in vivo. Animal. 2013;7:879-84. doi.org/10.1017/S1751731112002340. PubMed PMID: 23228200.
  7. Mohrmann M, Roehe R, Susenbeth A, Baulain U, Knap PW, Looft H, et al. Association between body composition of growing pigs determined by magnetic resonance imaging, deuterium dilution technique, and chemical analysis. Meat Sci. 2006;72:518-31. doi.org/10.1016/j.meatsci.2005.08.020. PubMed PMID: 22061736.
  8. Monziols M, Collewet G, Bonneau M, Mariette F, Davenel A, Kouba M. Quantification of muscle, subcutaneous fat and intermuscular fat in pig carcasses and cuts by magnetic resonance imaging. Meat Sci. 2006;72:146-54. doi.org/10.1016/j.meatsci.2005.06.018. PubMed PMID: 22061385.
  9. Dransfield E. The taste of fat. Meat Sci. 2008;80:37-42. doi.org/10.1016/j.meatsci.2008.05.030. PubMed PMID: 22063168.
  10. Collewett G, Toussaint C, Davenel A, Akoka S, Médale F, Fauconneau B, et al. Magnetic resonance imaging as a tool to quantify the adiposity distribution in fish. Special Publication-Royal Society of Chemistry. 2001;262:252-8. doi.org/10.1039/9781847551252-00252.
  11. Davenel A, Bazin C, Quellec S, Challois S, Gispert M, Mercat M, et al. High throughput determination of intramuscular fat content by magnetic resonance imaging. Journees de la recherche porcine en France. 2012;44:53-4.
  12. Clerjon S, Bonny JM. Diffusion-weighted NMR micro-imaging of lipids: Application to food products. 2011.
  13. Clerjon S, Kondjoyan A, Bonny JM, Portanguen S, Chevarin C, Thomas A, et al. Oil uptake by beef during pan frying: impact on fatty acid composition. Meat Sci. 2012;91:79-87. doi.org/10.1016/j.meatsci.2011.12.009. PubMed PMID: 22265369.
  14. Horigane A, Motoi H, Irie K, Yoshida M. Observation of the structure, moisture distribution, and oil distribution in the coating of tempura by NMR micro imaging. Journal of food science. 2003;68:2034-9. doi.org/10.1111/j.1365-2621.2003.tb07014.x.
  15. Brix O, Apablaza P, Baker A, Taxt T, Grüner R. Chemical shift based MR imaging and gas chromatography for quantification and localization of fat in Atlantic mackerel. Journal of experimental marine biology and ecology. 2009;376:68-75. doi.org/10.1016/j.jembe.2009.06.006.
  16. Wu J-L, Zhang J-L, Du X-X, Shen Y-J, Lao X, Zhang M-L, et al. Evaluation of the distribution of adipose tissues in fish using magnetic resonance imaging (MRI). Aquaculture. 2015;448:112-22. doi.org/10.1016/j.aquaculture.2015.06.002.
  17. Ballerini L, Hogberg A, Borgefors G, Bylund A-C, Lindgard A, Lundstrom K, et al. A segmentation technique to determine fat content in NMR images of beef meat. IEEE transactions on Nuclear Science. 2002;49:195-9. doi.org/10.1109/TNS.2002.998751.
  18. Toussaint C, Fauconneau B, Médale F, Collewet G, Akoka S, Haffray P, et al. Description of the heterogeneity of lipid distribution in the flesh of brown trout (Salmo trutta) by MR imaging. Aquaculture. 2005;243:255-67. doi.org/10.1016/j.aquaculture.2004.09.029.
  19. Aaslyng MD, Bejerholm C, Ertbjerg P, Bertram HC, Andersen HJ. Cooking loss and juiciness of pork in relation to raw meat quality and cooking procedure. Food quality and preference. 2003;14:277-88. doi.org/10.1016/S0950-3293(02)00086-1.
  20. Bouhrara M, Clerjon S, Damez JL, Chevarin C, Portanguen S, Kondjoyan A, et al. Dynamic MRI and thermal simulation to interpret deformation and water transfer in meat during heating. J Agric Food Chem. 2011;59:1229-35. doi.org/10.1021/jf103384d. PubMed PMID: 21265572.
  21. Bouhrara M, Lehallier B, Clerjon S, Damez JL, Bonny JM. Mapping of muscle deformation during heating: in situ dynamic MRI and nonlinear registration. Magn Reson Imaging. 2012;30:422-30. doi.org/10.1016/j.mri.2011.10.002. PubMed PMID: 22133287.
  22. Hansen CL, van der Berg F, Ringgaard S, Stodkilde-Jorgensen H, Karlsson AH. Diffusion of NaCl in meat studied by (1)H and (23)Na magnetic resonance imaging. Meat Sci. 2008;80:851-6. doi.org/10.1016/j.meatsci.2008.04.003. PubMed PMID: 22063607.
  23. Ruiz-Cabrera MA, Gou P, Foucat L, Renou JP, Daudin JD. Water transfer analysis in pork meat supported by NMR imaging. Meat Sci. 2004;67:169-78. doi.org/10.1016/j.meatsci.2003.10.005. PubMed PMID: 22061130.
  24. Veliyulin E, Egelandsdal B, Marica F, Balcom BJ. Quantitative 23Na magnetic resonance imaging of model foods. J Agric Food Chem. 2009;57:4091-5. doi.org/10.1021/jf9000605. PubMed PMID: 21314196.
  25. Vestergaard C, Risum J, Adler-Nissen J. Quantification of salt concentrations in cured pork by computed tomography. Meat Sci. 2004;68:107-13. doi.org/10.1016/j.meatsci.2004.02.011. PubMed PMID: 22062013.
  26. Vestergaard C, Risum J, Adler-Nissen J. (23)Na-MRI quantification of sodium and water mobility in pork during brine curing. Meat Sci. 2005;69:663-72. doi.org/10.1016/j.meatsci.2004.11.001. PubMed PMID: 22063144.
  27. Aursand IG, Erikson U, Veliyulin E. Water properties and salt uptake in Atlantic salmon fillets as affected by ante-mortem stress, rigor mortis, and brine salting: a low-field 1 H NMR and 1 H/23 Na MRI study. Food chemistry. 2010;120:482-9. doi.org/10.1016/j.foodchem.2009.10.041.
  28. Aursand IG, Veliyulin E, Bocker U, Ofstad R, Rustad T, Erikson U. Water and salt distribution in Atlantic salmon (Salmo salar) studied by low-field 1H NMR, 1H and 23Na MRI and light microscopy: effects of raw material quality and brine salting. J Agric Food Chem. 2009;57:46-54. doi.org/10.1021/jf802158u. PubMed PMID: 19090754.
  29. Erikson U, Veliyulin E, Singstad T, Aursand M. Salting and Desalting of Fresh and Frozen-thawed Cod (Gadus morhua) Fillets: A Comparative Study Using 23Na NMR, 23Na MRI, Low-field 1H NMR, and Physicochemical Analytical Methods. Journal of food science. 2004;69:FEP107-FEP14. doi.org/10.1111/j.1365-2621.2004.tb13362.x.
  30. Veliyulin E, Aursand IG. (1)H and (23)Na MRI studies of Atlantic salmon (Salmo salar) and Atlantic cod (Gadus morhua) fillet pieces salted in different brine concentrations. J Sci Food Agric. 2007;87(14):2676-83. doi.org/10.1002/jsfa.3030. PubMed PMID: 20836176.
  31. Bonny J, Laurent W, Renou J. Characterisation of meat structure by NMR imaging at high field. Special publication-royal society of chemistry. 2001;262:17-21. doi.org/10.1039/9781847551252-00017.
  32. Laurent W, Bonny J, Renou J. Muscle characterisation by NMR imaging and spectroscopic techniques. Food chemistry. 2000;69:419-26. doi.org/10.1016/S0308-8146(00)00051-0.
  33. Pérez-Palacios T, Antequera T, Durán ML, Caro A, Rodríguez PG, Palacios R. MRI-based analysis of feeding background effect on fresh Iberian ham. Food chemistry. 2011;126:1366-72. doi.org/10.1016/j.foodchem.2010.11.101.
  34. Bonny JM, Renou JP. Water diffusion features as indicators of muscle structure ex vivo. Magn Reson Imaging. 2002;20:395-400. doi.org/10.1016/S0730-725X(02)00515-5. PubMed PMID: 12206864.
  35. amez J, Clerjon S, Labas R, Danon J, Peyrin F, Bonny J, editors. Microstructure characterization of meat by quantitative MRI. 12-17 August 2012. Montreal: 58th International Congress of Meat Science and Technology; 2012.
  36. Shaarani SM, Nott KP, Hall LD. Combination of NMR and MRI quantitation of moisture and structure changes for convection cooking of fresh chicken meat. Meat Sci. 2006;72:398-403. doi.org/10.1016/j.meatsci.2005.07.017. PubMed PMID: 22061723.
  37. Van Duynhoven J, Goudappel GW, Weglarz W. Noninvasive assessment of moisture migration in food products by MRI. In: Codd S, Seymour JD et al., eds. Magnetic resonance microscopy. Weinheim: Wiley-VCH; 2009. pp. 331–351.
  38. Gonzalez J, McCarthy K, McCarthy M. Textural and structural changes in lasagna after cooking. Journal of texture studies. 2000;31:93-108. doi.org/10.1111/j.1745-4603.2000.tb00286.x.
  39. Thybo AK, Szczypiński PM, Karlsson AH, Dønstrup S, Stødkilde-Jørgensen HS, Andersen HJ. Prediction of sensory texture quality attributes of cooked potatoes by NMR-imaging (MRI) of raw potatoes in combination with different image analysis methods. Journal of Food Engineering. 2004;61:91-100. doi.org/10.1016/S0260-8774(03)00190-0.
  40. Lai H-M, Hwang S-C. Water status of cooked white salted noodles evaluated by MRI. Food research international. 2004;37:957-66. doi.org/10.1016/j.foodres.2004.06.008.
  41. Hills BP, Remigereau B. NMR studies of changes in subcellular water compartmentation in parenchyma apple tissue during drying and freezing. International Journal of Food Science & Technology. 1997;32:51-61. doi.org/10.1046/j.1365-2621.1997.00381.x.
  42. Hindmarsh J, Buckley C, Russell A, Chen X, Gladden L, Wilson D, et al. Imaging droplet freezing using MRI. Chemical engineering science. 2004;59:2113-22. doi.org/10.1016/j.ces.2003.12.031.
  43. Mahdjoub R, Chouvenc P, Seurin MJ, Andrieu J, Briguet A. Sucrose solution freezing studied by magnetic resonance imaging. Carbohydr Res. 2006;341:492-8. doi.org/10.1016/j.carres.2006.01.005. PubMed PMID: 16430876.
  44. Chaland B, Mariette F, Marchal P, De Certaines J. 1H nuclear magnetic resonance relaxometric characterization of fat and water states in soft and hard cheese. J Dairy Res. 2000;67:609-18. doi.org/10.1017/S0022029900004398. PubMed PMID: 11131073.
  45. Mahdjoub R, Molegnana J, Seurin MJ, Briguet A. High resolution magnetic resonance imaging evaluation of cheese. Journal of food science. 2003;68:1982-4. doi.org/10.1111/j.1365-2621.2003.tb07005.x.
  46. Hwang S-S, Cheng Y-C, Chang C, Lur H-S, Lin T-T. Magnetic resonance imaging and analyses of tempering processes in rice kernels. Journal of Cereal Science. 2009;50:36-42. doi.org/10.1016/j.jcs.2008.10.012.
  47. Cornillon P, Salim LC. Characterization of water mobility and distribution in low- and intermediate-moisture food systems. Magn Reson Imaging. 2000;18:335-41. doi.org/10.1016/S0730-725X(99)00139-3. PubMed PMID: 10745143.
  48. Mariette F. Investigations of food colloids by NMR and MRI. Current Opinion in Colloid & Interface Science. 2009;14:203-11. doi.org/10.1016/j.cocis.2008.10.006.
  49. Miquel ME, Hall LD. Measurement by MRI of storage changes in commercial chocolate confectionery products. Food research international. 2002;35:993-8. doi.org/10.1016/S0963-9969(02)00160-6.
  50. JHA SN, MATSUOKA T. Non-Destructive Techniques for Quality Evaluation of Intact Fruits and Vegetables. Food Science and Technology Research. 2000;6:248-51. doi.org/10.3136/fstr.6.248.
  51. Milczarek RR, McCarthy MJ. Low-field MR Sensors for Fruit Inspection. In: Codd SL, Seymour JD, eds. Magnetic Resonance Microscopy. Weinheim, Wiley-VCH; 2009. p. 289-299.
  52. Van As H. Intact plant MRI for the study of cell water relations, membrane permeability, cell-to-cell and long distance water transport. J Exp Bot. 2007;58:743-56. doi.org/10.1093/jxb/erl157. PubMed PMID: 17175554.
  53. Hills B, Clark C. Quality assessment of horticultural products by NMR. Annual Reports on NMR spectroscopy. 2003;50:75-120. doi.org/10.1016/S0066-4103(03)50002-3.
  54. Clark CJ, MacFall JS. Quantitative magnetic resonance imaging of ‘Fuyu’ persimmon fruit during development and ripening. Magn Reson Imaging. 2003;21:679-85. doi.org/10.1016/S0730-725X(03)00082-1. PubMed PMID: 12915200.
  55. Musse M, Quellec S, Cambert M, Devaux M-F, Lahaye M, Mariette F. Monitoring the postharvest ripening of tomato fruit using quantitative MRI and NMR relaxometry. Postharvest Biology and Technology. 2009;53:22-35. doi.org/10.1016/j.postharvbio.2009.02.004.
  56. Joyce DC, Hockings PD, Mazucco RA, Shorter AJ. 1H-Nuclear magnetic resonance imaging of ripening’Kensington Pride’mango fruit. Functional plant biology. 2002;29:873-9. doi.org/10.1071/PP01150.
  57. Shaarani SM, Cardenas-Blanco A, Amin MG, Soon NG, Hall LD. Monitoring development and ripeness of oil palm fruit (Elaeis guneensis) by MRI and bulk NMR. International Journal of Agriculture and Biology (Pakistan). 2010;12:101–105.
  58. Khoshroo A, Keyhani A, Zoroofi R, Yaghoobi G, editors. NNondestructive inspection of pomegranate maturity using magnetic resonance imaging and neural networks. April; 2011. France: CIGR Section VI International Symposium on Towards a Sustainable Food Chain Food Process, Bioprocess Food Qual Manag Nantes; 2011.
  59. Galed G, Fernandez-Valle ME, Martinez A, Heras A. Application of MRI to monitor the process of ripening and decay in citrus treated with chitosan solutions. Magn Reson Imaging. 2004;22:127-37. doi.org/10.1016/j.mri.2003.05.006. PubMed PMID: 14972402.
  60. Barreiro P, Ortiz C, Ruiz-Altisent M, Ruiz-Cabello J, Fernandez-Valle ME, Recasens I, et al. Mealiness assessment in apples and peaches using MRI techniques. Magn Reson Imaging. 2000;18:1175-81. doi.org/10.1016/S0730-725X(00)00179-X. PubMed PMID: 11118773.
  61. Otero L, Préstamo G. Effects of pressure processing on strawberry studied by nuclear magnetic resonance. Innovative Food Science & Emerging Technologies. 2009;10:434-40. doi.org/10.1016/j.ifset.2009.04.004.
  62. Haishi T, Koizumi H, Arai T, Koizumi M, Kano H. Rapid Detection of Infestation of Apple Fruits by the Peach Fruit Moth, Carposina sasakii Matsumura, Larvae Using a 0.2-T Dedicated Magnetic Resonance Imaging Apparatus. Appl Magn Reson. 2011;41:1-18. doi.org/10.1007/s00723-011-0222-8. PubMed PMID: 21957330. PubMed PMCID: 3162149.
  63. Lammertyn J, Dresselaers T, Van Hecke P, Jancsok P, Wevers M, Nicolai BM. MRI and x-ray CT study of spatial distribution of core breakdown in ‘Conference’ pears. Magn Reson Imaging. 2003;21:805-15. doi.org/10.1016/S0730-725X(03)00105-X. PubMed PMID: 14559346.
  64. Létal J, Jirak D, Šuderlová L, Hájek M. MRI ‘texture’analysis of MR images of apples during ripening and storage. LWT-Food Science and Technology. 2003;36:719-27. doi.org/10.1016/S0023-6438(03)00099-9.
  65. Burdon J, Clark C. Effect of postharvest water loss on ‘Hayward’kiwifruit water status. Postharvest Biology and Technology. 2001;22:215-25. doi.org/10.1016/S0925-5214(01)00095-3.