Effects of Lactococcus lactis (L. lactis) subsp. lactis Supernatant on the Shelf Life of Vacuum-packaged Oncorhynchus mykiss Fillets

مجله پژوهشهای علوم و صنایع غذایی ایران

Article 2, Volume 19, Issue 6 - Serial Number 84, January and February 2024, Pages 111-124   

Document Type: Research Article-en

DOI: 10.22067/ifstrj.2023.83834.1274

Authors

Asad Abbaspour Anbi^{* 1}; Masoud Seidgar¹; Masoud Neyriz Nagadehi²

¹National Artemia Research Center, Iranian Fisheries Science Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Urmia, Iran

²Department of Food Hygiene and Quality Control, Urmia Branch, Islamic Azad University, Urmia, Iran

Abstract

The present investigation was done to study the effects of Lactococcus lactis (L. lactis) subsp. lactis on the shelf life of the vacuum-packaged Oncorhynchus mykiss. Fish fillets were prepared and divided into 5 different treatment groups including control (distilled water), 2% and 4% supernatant, and 10⁶ CFU/g L. lactis subspecies lactis. The pH, Thiobarbituric Acid Reactive Substances (TBARS), Total volatile Nitrogen (TVN), and Peroxide Value (PV) of the fillets were determined on days 0, 5, 10, and 15 while maintained at 4˚C. Protein expression and destruction were analyzed using the SDS-PAGE. The organoleptic assessment was done using five expert sensory panelists. Contents of TBARS, TVN, pH, and PV were increased throughout the storage period (P <0.05). An increase in the concentration of supernatant caused a significant decrease in the content of TBARS, TVN, pH, and PV (P <0.05). The highest and lowest contents of TBARS, TVN, pH and PV on 15^th day were belonged to the control (3.367±0.04 mg MDA/kg) and pure bacteria (0.70±0.02 mg MDA/kg), control (87.20±6.40 mg/100g) and 4% supernatant (40.79±0.61 mg/100g), pure bacteria (6.23±0.04) and 4% supernatant (5.44±0.07) and control (12.22±0.01 meq/kg) and 4% supernatant (3.08±0.06 meq/kg) groups, respectively. Protein destruction was lower in the fillet samples treated with pure bacteria and 4% supernatant. The highest scores of the odor, flavor, texture, and color were obtained for fillets treated with 4% supernatant, pure bacteria, pure bacteria, and 4% supernatant and pure bacteria, respectively. The results revealed that treating O. mykiss fillets with 4% supernatant and 10⁶ CFU/g of pure L. lactis subsp. lactis can extend the shelf life of O. mykiss fillets.

Keywords

Fish; L. lactis subsp. lactis; Oncorhynchus mykiss; Shelf life; Vacuum package

References

1. Abbaspour, A.A., Rasavilar, V., Neyriz Naghadehi, M., Asadpour Osalou, Y.A. (2019). Study of the effect of incorporation of Lactococcus lactis on the shelf life of rainbow trout fillet in glacial condition. Journal of Food Microbiology, 6(4), 45-58. (In Persian)
2. Abbaspour Anbi, A., Razavilar, V., Neyriz Naghadehi, M., Seidgar, M., Nekuiefard, A., & Asadpour Osalou, Y.A. (2018). The effects of lactococcus lactis lactis and its supernatant on some bacteriological and sensory values in rainbow trout (Oncorhynchus mykiss) fillets. Microbiology Research, 9, 7431, 19-25. https://doi.org/10.4081/mr.2018.7431
3. Ammor, S., Tauveron, G., Dufour, E., & Chevallier, I. (2006). Antibacterial activity of lactic acid bacteria against spoilage and pathogenic bacteria isolated from the same meat small-scale facility 1-Screening and characterization of the antibacterial compounds. Food Control, 454–461. https://doi.org/10.1016/j.foodcont.2005.02.006
4. Adilla, S.N, Utami, R., Nursiwi, A., & Nurhartadi, E.( 2016). The effect of nisin from Lactococcus lactis subsp. lactis on refrigerated patin fillet quality. In: International Conference On Food Science and Engineering. vol 193. IOP Publishing, https://doi.org/1088/1757-899X/193/1/012014
5. Alak, G. (2010). Microbiological and chemical properties of modified atmosphere and vacuum. Kafk Üniver Vet Fak Dergisi, 16, S73-S80. https://doi.org/10.9775/kvfd.2009.1475
6. Benjakul, S., Seymour, T.A., Morrissey, M.T., & An, H.(2006). Physicochemical changes in Pacific whiting muscle proteins during iced storage. Journal Food Science, 62, 729-33. https://doi.org/10.1111/j.1365-2621.1997.tb15445.x
7. Bogdanović, T., Šimat, V., Frka Roić, A., & Marković, K. (2012). Development and application of quality index method scheme in a shelf life study of wild and fish farm affected bogue (Boops boops, L.). Journal Food Science, 77, 99-106. https://doi.org/10.1111/j.1750-3841.2011.02545.x
8. Boulares, M., Mankai, M., Belaam, Z., & Hassouna, M. (2013). Effect of inoculation of lactic acid bacteria on the proteolytic activity of psychrotrophic Gram-negative bacteria in fresh farmed sea bass (Dicentrarchus labrax) fillets during storage at 4° C under vacuum-packed conditions. Annal Microbiology, 63, 1493-500. https://doi.org/10.1007/s13213-013-0613-1
9. Chanarat, S., Benjakul, S., & Xiong, Y.I. (2014). Physicochemical changes of myosin and gelling properties of washed tilapia mince as influenced by oxidative stress and microbial transglutaminase. Journal Food Science Technology, 52, 3824–36.
10. Chanarat, S., Benjakul, S., & Xiong, Y.I. (2014). Physicochemical changes of myosin and gelling properties of washed tilapia mince as influenced by oxidative stress and microbial transglutaminase. Journal Food Science Technology, 52, 3824–36.
11. Chowdhury, S., Raychaudhuri, U., Nath, S., & Dora, K. (2016). Shelf life of lactic acid bacteria inoculated vacuum packed Tenualosa Elisha (Hamilton, 1822) at low temperature. Indian Journal of Fisheries, 63, 156-61. https://doi.org/10.21077/ijf.2016.63.1.27811-25
12. Chytiri, S., Chouliara, I., Savvaidis, I., Kontominas, M.(2004). Microbiological, chemical, and sensory assessment of iced whole and filleted aquacultured rainbow trout. Food Microbiol, 21: 157-65. https://doi.org/10.1016/S0740-0020(03)00059-5
13. (1999). Guidelines for the sensory evaluation of fish and shellfish in laboratories. CAC/GL 311999: 1-32.
14. DeWitt, C.A.M., & Oliveira, A. (2016). Modified atmosphere systems and shelf life extension of fish and fishery products. Foods, 5, 48.  https://doi.org/10.3390/foods5030048
15. Erkan, N., Özden, Ö., & Inuğur, M. (2007). The effects of modified atmosphere and vacuum packaging on quality of chub mackerel. International Journal of Food Science & Technology, 42, 1297-304. https://doi.org/10.1111/j.1365-2621.2006.01325.x
16. Fijan, S. (2014). Microorganisms with claimed probiotic properties: an overview of recent literature. International Journal of Environmental Research and Public Health, 11, 4745–4767. https://doi.org/10.3390/ijerph110504745
17. Fuentes-Amaya, L.F., Munyard, S., Fernandez‐Piquer, J., & Howieson, J. (2015). Sensory, microbiological and chemical changes in vacuum‐packaged blue spotted Emperor (Lethrinus), Saddletail Snapper (Lutjanus malabaricus), Crimson Snapper (Lutjanus erythropterus), Barramundi (Lates calcarifer) and Atlantic Salmon (Salmo salar) Fillets Stored at 4° C. Food Science Nutrient, 4, 479-89. https://doi.org/10.1002/fsn3.309
18. Gelman, A., Glatman, L., Drabkin, V., & Harpaz, S. (2001). Effects of storage temperature and preservative treatment on the shelf life of the pond-raised freshwater fish, silver perch (Bidyanus biryanis). Journal of Food Protection, 64, 1584-91. https://doi.org/10.4315/0362-028x-64.10.1584
19. Giuffrida, A., Giarratana, F., Valenti, D., Muscolino, D., Parisi, R., Parco, A., Marotta, S., Ziino, G., & Panebianco, A. (2017). A new approach to predict the fish fillet shelf-life in the presence of natural preservative agents. Italian Journal Food Safety, 6, 6768.
20. Goussault, B., & Leveau, B. (2006). A guide to packaging technology for seafood value-addition. Eurofish, Copenhagen, 1-20.
21. Greene, B.E., & Cumuze, T.H. (1981). Relationship between TBA numbers and inexperienced panelists' assessments of oxidized flavor in cooked beef. Journal Food Science, 47, 52-8. https://doi.org/10.1111/j.1365-2621.1982.tb11025.x
22. Ibrahim, S., & Desouky, S.G. (2009). Effect of antimicrobial metabolites produced by lactic acid bacteria (Lab) on quality aspects of frozen tilapia (Oreochromis niloticus) fillets. World Journal of Fish and Marine Sciences, 1, 40-5.
23. Krishnamoorthi, R., Srinivas, M., Mahalingam, P.U., Malaikozhundan, B., Suganya, P., & Gurushankar, K. (2022) Antimicrobial, anti-biofilm, antioxidant and cytotoxic effects of bacteriocin by Lactococcus lactis strain CH3 isolated from fermented dairy products—An in vitro and silico approach. International Journal of Biological Macromolecules, 220, 291-306. https://doi.org/10.1016/j.ijbiomac.2022.08.087
24. Kilinc, B., & Cakli, S. (2004). Chemical, microbiological, and sensory changes in thawed fillets of sardine (Sardina pilchardus) during marination. Food Chemistry, 88, 275–80. https://doi.org/10.1016/j.foodchem.2004.01.044
25. Lakshmanan, P. (2000). Fish spoilage and quality assessment. Central Institute of Fisheries Technology and Society of Fisheries Technology, Cochin, India.
26. Larsen, R., Eilertsen, K.E, & Elvevoll, E.O. (2011). Health benefits of marine foods and ingredients. Biotechnology Advances, 29, 508-18. https://doi.org/10.1016/j.biotechadv.2011.05.017
27. Malle, P., & Poumeyrol, M. (1989). A new chemical criterion for the quality control of fish: trimethylamine/total volatile basic nitrogen (%). Journal of Food Protection, 52, 419-23. https://doi.org/10.4315/0362-028X-52.6.419
28. Nath, S., Chowdhury, S., & Dora, K. (2014). Effect of lactic acid bacteria application on shelf life and safety of fish fillet at 6±1 c. International Journal of Advanced Research, 2, 201-7.
29. Ndaw, A., Faid, M., Bouseta, A., & Zinedine, A. (2008). Effect of controlled lactic acid bacteria fermentation on the microbiological and chemical quality of Moroccan sardines (Sardina pilchardus). International Journal of Agriculture and Biology, 10, 21-7. https://doi.org/10.1556/AMicr.55.2008.3.2
30. Özpolat, E., Patır, B., Guran, H., & Gul, M. (2014). Effect of vacuum-packing method on the shelf–life of Capoeta umbrella sausages. Iranian Journal of Fisheries Sciences, 13, 178-84. https://doi.org/20.1001.1.15622916.2014.13.1.15.5
31. Pavlićević, N., Đorđević, V., Dimitrijević, M., Bošković, M., Marković, R., & Baltić, M.Ž. (2013). Lactic acid bacteria: Effect on the quality and safety of fishery products. In: 6^th International Conference Water and Fish, Faculty of Agriculture, Belgrade-Zemun (Serbia), p 436-42
32. Julie, A.A.A. & Nacional, L.M. (2007). Effect of lactic, acetic, and citric acids on quality changes of refrigerated green mussel, Perna viridis (Linnaeus, 1758). Songklanakarin Journal of Science and Technology, 29, 171-179. https://doi.org/10.12944/crnfsj.6.3.29
33. Rahmatipoor, R., Roomiani, L., & Askary Sary, A. (2017). Effect of different packaging on the shelf life of silver carp (Hypophthalmichthys molitrix) fillets stored at 4 ºC. Iranian Journal of Aquatic Animal Health, 3, 22-35. https://doi.org/10.29252/ijaah.3.2.22
34. Sałański, P.,  Kowalczyk, M., & Bardowski, J.K. (2022). Health-promoting nature of Lactococcus lactisIBB109 and Lactococcus lactis IBB417 strains exhibiting proliferation inhibition and stimulation of interleukin-18 expression in Colorectal cancer cells, Frontiers in Microbiology, 13, 1-13. https://doi.org/10.3389/fmicb.2022.822912
35. Salih, A., Smith, D., Price, J., & Dawson, L. (1987). Modified extraction 2-thiobarbituric acid method for measuring lipid oxidation in poultry. Poultry Science, 66, 1483-8. https://doi.org/10.3382/ps.0661483
36. Sallam, K.I., Ahmed, A.M., Elgazzar, M.M., & Eldaly, E.A. (2007). Chemical quality and sensory attributes of marinated Pacific saury (Cololabis saira) during vacuum-packaged storage at 4^o Food Chemistry, 102, 1061-70. https://doi.org/10.1016/j.foodchem.2006.06.044
37. Sarika, A., Lipton, A., Aishwarya, M., & Dhivya, R. (2012). Isolation of a bacteriocin-producing Lactococcus lactis and application of its bacteriocin to manage spoilage bacteria in high-value marine fish under different storage temperatures. Applied Biochemistry and Biotechnology, 167, 1280-9. https://doi.org/10.1128/aem.55.8.1901-1906.1989
38. Schillinger, U., & Lücke, F.K. (1989). Antibacterial activity of Lactobacillus sake isolated from meat. Applied and Environmental Microbiology, 55, 1901-6. https://doi.org/10.1128/aem.55.8.1901-1906.1989
39. Sen, M., & Temelli, S. (2003). Microbiological and chemical qualities of marinated anchovy prepared with different vegetable additives and sauce. Review Médicine Véterinary, 154, 703-8.
40. Shamloofar, M., Hoseini, E., Kamali, A., Motalebi Moghanjoghi, A., & Poorgholm, R. (2015). Antibacterial activities of nisin encapsulated in zein and modified atmosphere packaging on rainbow trout (Oncorhynchus mykiss) fillet during chilled storage 4 C. Iranian Journal of Fisheries Sciences, 14, 369-81.
41. Shon, J., & Chin, K. (2008). Effect of whey protein coating on quality attributes of low‐fat, aerobically packaged sausage during refrigerated storage. Journal Food Sciences, 73, 469-475. https://doi.org/10.1111/j.1750-3841.2008.00829.x
42. Soltanian, S., Behnam, S., Rezai, M., Safari, R., & Anvari, M. (2011). Nisin is a preservative for rainbow trout (Oncorhynchus mykis). Online Journal of Veterinary Research, 15, 354-65.
43. Sudalayandi, K. (2011). Efficacy of lactic acid bacteria in the reduction of trimethylamine-nitrogen and related spoilage derivatives of fresh Indian mackerel fish chunks. African Journal of Biotechnology, 10, 42-7.
44. Tufail, M., Hussain, S., Malik, F., Mirza, T., Parveen, G., Shafaat, S., Wajid, A., Mahmood, R., Channa, R.A., & Sadiq, A. (2011). Isolation and evaluation of antibacterial activity of bacteriocin produced by Lactobacillus bulgaricus from yogurt. African Journal of Microbiology Research, 5, 3842-7. https://doi.org/10.5897/AJMR11.846