Abstract
This study investigated the antimicrobial activity of 405 nm light-emitting diode (LED) with and without riboflavin against Listeria monocytogenes in phosphate buffered saline (PBS) and on smoked salmon at different storage temperatures and evaluated its impact on food quality. The results show that riboflavin-mediated LED illumination in PBS 25 °C significantly inactivated L. monocytogenes cells by 6.2 log CFU/mL at 19.2 J/cm2, while illumination alone reduced 1.9 log CFU/mL of L. monocytogenes populations at 57.6 J/cm2. L. monocytogenes populations on illuminated smoked salmon decreased by 1.0–2.2 log CFU/cm2 at 1.27–2.76 kJ/cm2 at 4, 12, and 25 °C, regardless of the presence of riboflavin. Although illumination with and without riboflavin caused the lipid peroxidation and color change in smoked salmon, this study demonstrates the potential of a 405 nm LED to preserve the smoked salmon products, reducing the risk of listeriosis.
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Anyasi TA, Jideani AI, Mchau GR. Effect of organic acid pretreatment on some physical, functional and antioxidant properties of flour obtained from three unripe banana cultivars. Food Chemistry. 172: 515-522 (2015)
Ashoori M, Saedisomeolia A. Riboflavin (vitamin B2) and oxidative stress: a review. British Journal of Nutrition. 111: 1985-1991 (2014)
Aponiene K, Paskeviciute E, Reklaitis I, Luksiene Z. Reduction of microbial contamination of fruits and vegetables by hypericin-based photosensitization: Comparison with other emerging antimicrobial treatments. Journal of Food Engineering. 144: 29-35 (2015)
Ayala A, Muñoz MF, Argüelles S. Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxidative Medicine and Cellular Longevity. 2014: 360438 (2014)
Bermúdez-Aguirre D, Barbosa-Cánovas GV. Disinfection of selected vegetables under nonthermal treatment: Chlorine, acid citric, ultraviolet light and ozone. Food Control. 29: 82-90 (2013)
Catalá A. Lipid peroxidation of membrane phospholipids generates hydroxy-alkenals and oxidized phospholipids active in physiological and/or pathological conditions. Chemistry and Physics of Lipids. 157: 1-11 (2009)
Chau ML, Aung KT, Hapuarachchi HC, Lee PSV, Lim PY, Kang JSL, Ng Y, Yap HM, Yuk H G, Gutiérrez RA, Ng LC. Microbial survey of ready-to-eat salad ingredients sold at retial reveals the occurrence and the presistance of Listeria monocytogenes sequence type 2 and 87 in pre-packed smoked salmon. BMC Microbiology. 17: 46 (2017)
Colejo S, Alvarez-Ordóñez A, Prieto M, González-Raurich M, López M. Evaluation of ultraviolet light (UV), non-thermal atmospheric plasma (NTAP) and their combination for the control of foodborne pathogens in smoked salmon and their effect on quality attributes. Innovative Food Science and Emerging Technologies. 50: 84-93 (2018)
Ghate V, Ng KS, Zhou W, Yang H, Khoo GH, Yoon WB, Yuk HG. Antibacterial effect of light emitting diodes of visible wavelengths on selected foodborne pathogens at different illumination temperatures. International Journal of Food Microbiology. 166: 399-406 (2013)
Ghate V, Kumar A, Zhou W, Yuk HG. Irradiance and temperature influence the bactericidal effect of 460-nanometer light-emitting diodes on Salmonella in orange juice. Journal of Food Protection. 79: 553-560 (2016)
Ghate V, Kumar A, Kim MJ, Bang WS, Zhou W, Yuk HG. Effect of 460 nm light emitting diode illumination on survival of Salmonella spp. on fresh-cut pineapples at different irradiances and temperatures. Journal of Food Engineering. 196: 130–138 (2017)
German JB. Food processing and lipid oxidation. Advances in Experimental Medicine and Biology. 459: 23-50 (1999)
Heir E, Liland KH, Carlehög M, Holck AL. Reduction and inhibition of Listeria monocytogenes in cold-smoked salmon by Verdad N6, a buffered vinegar fermentate, and UV-C treatments. International Journal of Food Microbiology. 291: 48-58 (2019)
Josewin SW, Ghate V, Kim MJ, Yuk HG. Antibacterial effect of 460 nm light-emitting diode in combination with riboflavin against Listeria monocytogenes on smoked salmon. Food Control. 84: 354-361 (2018)
Kim MJ, Mikš-Krajnik M, Kumar A, Ghate V, Yuk HG. Antibacterial effect and mechanism of high-intensity 405±5 nm light emitting diode on Bacillus cereus, Listeria monocytogenes, and Staphylococcus aureus under refrigerated condition. Journal of Photochemistry and Photobiology B: Biology. 153: 33-39 (2015)
Kim MJ, Mikš-Krajnik M, Kumar A, Yuk HG. Inactivation by 405±5 nm light emitting diode on Escherichia coli O157: H7, Salmonella Typhimurium, and Shigella sonnei under refrigerated condition might be due to the loss of membrane integrity. Food Control. 59: 99-107 (2016)
Kim MJ, Bang WS, Yuk HG. 405±5 nm light emitting diode illumination causes photodynamic inactivation of Salmonella spp. on fresh-cut papaya without deterioration. Food Microbiology. 62: 124–132 (2017a)
Kim MJ, Ng BXA, Zwe YH, Yuk HG. Photodynamic inactivation of Salmonella enterica Enteritidis by 405±5-nm light-emitting diode and its application to control salmonellosis on cooked chicken. Food Control. 82: 305-315 (2017b)
Kim, MJ, Tang CH, Bang WS, Yuk HG. Antibacterial effect of 405±5 nm light emitting diode illumination against Escherichia coli O157: H7, Listeria monocytogenes, and Salmonella on the surface of fresh-cut mango and its influence on fruit quality. International Journal of Food Microbiology. 244: 82-89 (2017c)
Kim MJ, Yuk HG. (2017) Antibacterial mechanism of 405-nanometer light-emitting diode against Salmonella at refrigeration temperature. Applied and Environmental Microbiology. 83: e02582-16 (2017)
Kumar A, Ghate V, Kim M., Zhou W, Khoo GH, Yuk HG. Antibacterial efficacy of 405, 460 and 520 nm light emitting diodes on Lactobacillus plantarum, Staphylococcus aureus and Vibrio parahaemolyticus. Journal of Applied Microbiology. 120: 49-56 (2016)
Liang JY, Yuann JMP, Cheng CW, Jian HL, Lin CC, Chen LY. Blue light induced free radicals from riboflavin on E. coli DNA damage. Journal of Photochemistry and Photobiology B: Biology. 119: 60–64 (2013)
Liang JY, Cheng CW, Yu CH, Chen LY. Investigations of blue light-induced reactive oxygen species from flavin mononucleotide on inactivation of E. coli. Journal of Photochemistry and Photobiology B: Biology. 143: 82–88 (2015)
Li X, Kim MJ, Bang WS, Yuk HG. Anti-biofilm effect of 405-nm LEDs against Listeria monocytogenes in simulated ready-to-eat fresh salmon storage conditions. Food Control. 84: 513-521 (2018)
Luksiene Z, Zukauskas A. Prospects of photosensitization in control of pathogenic and harmful micro-organisms. Journal of Applied Microbiology. 107: 1415e1424 (2009)
Luksiene Z, Paskeviciute E. Novel approach to the microbial decontamination of strawberries: chlorophyllin-based photosensitization. Journal of Applied Microbiology. 110: 1274–1283 (2011)
Luksienė Z, Kokstaite R, Katauskis P, Skakauskas V. Novel approach to effective and uniform inactivation of Gram-positive Listeria monocytogenes and Gram-negative Salmonella enterica by photosensitization. Food Technology and Biotechnology. 51: 338-344 (2013)
Ma Y, Hou J, Hao W, Liu J, Meng L, Lu Z. Influence of riboflavin on the oxidation kinetics of unsaturated fatty acids at the air/aqueous interface revealed by sum frequency generation vibrational spectroscopy. Physical Chemistry Chemical Physics. 20: 17199-17207 (2018)
Mori M, Hamamoto A, Takahashi A, Nakano M, Wakikawa N, Tachibana S, Kinouchi Y. Development of a new water sterilization device with a 365 nm UV-LED. Medical and Biological Engineering and Computing. 45: 1237-1241 (2007)
Nakamura K, Ishiyama K, Sheng H, Ikai H, Kanno T, Niwano Y. Bactericidal activity and mechanism of photoirradiated polyphenols against Gram-positive and-negative bacteria. Journal of Agricultural and Food Chemistry. 63: 7707-7713 (2015)
Nicorescu I, Nguyen B, Chevalier S, Orange N. Effects of pulsed light on the organoleptic properties and shelf-life extension of pork and salmon. Food Control. 44: 138-145 (2014)
Oğuzhan P. Effect of salting and packaging on liquid-smoked rainbow trout fillets during refrigerated storage. African Journal of Microbiology Research. 50: 5719-5725 (2013)
Pang X, Wong C, Chung HJ, Yuk HG. Biofilm formation of Listeria monocytogenes and its resistance to quaternary ammonium compounds in a simulated salmon processing environment. Food Control. 98: 200-208 (2019)
Pedrós-Garrido S, Condón-Abanto S, Clemente I, Beltrán JA, Lyng JG, Bolton D, Brunton N, Whyte P. Efficacy of ultraviolet light (UV-C) and pulsed light (PL) for the microbiological decontamination of raw salmon (Salmo salar) and food contact surface materials. Innovative Food Science and Emerging Technologies. 50: 124-31 (2018)
Reddi E, Jori G. Steady-state and time-resolved spectroscopic studies of photodynamic sensitizers: porphyrins and phthalocyanines. Research on Chemical Intermediates. 10: 241-268 (1988)
Refsgaard HH, Brockhoff PB, Jensen B. Sensory and chemical changes in farmed Atlantic salmon (Salmo salar) during frozen storage. Journal of Agricultural and Food Chemistry. 46: 3473-3479 (1998)
Ricci A, Allende A, Bolton D, Chemaly M, Davies R, Fernandez Escamez PS, Girones R, Herman L, Koutsoumanis K, Nørrung B, Robertson L, Ru G, Sanaa M, Simmons M, Skandamis P, Snary E, Speybroeck N, Ter Kuile B, Threlfall J, Wahlstrom H, Takkinen J, Wagner M, Arcella D, Da Silva Felicio MT, Georgiadis M, Messens W. Lindqvist R. EFSA panel on biological hazards. Scientific opinion on the Listeria monocytogenes contamination of ready-to-eat foods and the risk for human health in the EU. EFSA Journal. 16: 5134 (2018)
Rørvik LM. Listeria monocytogenes in the smoked salmon industry. International Journal of Food Microbiology. 62: 183-190 (2000)
Takeungwongtrakul S., Benjakul, S. Astaxanthin degradation and lipid oxidation of Pacific white shrimp oil: kinetics study and stability as affected by storage conditions. International Aquatic Research. 8: 15-27 (2016)
Tocmo R, Krizman K, Khoo WJ, Phua LK, Kim M, Yuk HG. Listeria monocytogenes in vacuum‐packed smoked fish products: sccurrence, routes of contamination, and potential intervention measures. Comprehensive Reviews in Food Science and Food Safety. 13: 172-189 (2014)
Yagiz Y, Kristinsson HG, Balaban MO, Welt BA, Raghavan S, Marshall MR. Correlation between astaxanthin amount and a* value in fresh Atlantic salmon (Salmo salar) muscle during different irradiation doses. Food Chemistry. 120: 121-127 (2010)
Ye M, Neetoo H, Chen H. Effectiveness of chitosan-coated plastic films incorporating antimicrobials in inhibition of Listeria monocytogenes on cold-smoked salmon. International Journal of Food Microbiology. 127: 235-240 (2008)
Wold JP, Jakobsen T, Krane L. Atlantic salmon average fat content estimated by near‐infrared transmittance spectroscopy. Journal of Food Science. 61: 74-77 (1996)
Wong TW, Cheng CW, Hsieh ZJ, Liang JY. Effects of blue or violet light on the inactivation of Staphylococcus aureus by riboflavin-5′-phosphate photolysis. Journal of Photochemistry and Photobiology B: Biology. 173: 672-680 (2017)
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This work was supported by Guangdong Province Science and Technology Plan Project (International Science and Technology Cooperation Field) (Grant No. 2020A0505100049).
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Kim, MJ., Da Jeong, M., Zheng, Q. et al. Antimicrobial activity of 405 nm light-emitting diode (LED) in the presence of riboflavin against Listeria monocytogenes on the surface of smoked salmon. Food Sci Biotechnol 30, 609–618 (2021). https://doi.org/10.1007/s10068-021-00895-y
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DOI: https://doi.org/10.1007/s10068-021-00895-y