Efficacy of an Aromatic Vinegar in Reducing Psychrotrophic Bacteria and Biogenic Amines in Salmon Fillets (Salmo salar) Stored in Modified Atmosphere Packaging
Jessica Di Toro 1  
,   Raffaella Branciari 1  
,   Rossana Roila 1  
,   Serena Altissimi 2  
,   Haiyang Jiang 3  
,   Kang Zhou 3  
,   Simona Perucci 4  
,   Michela Codini 5  
,   David Ranucci 1  
More details
Hide details
Department of Veterinary Medicine, University of Perugia, Via San Constanzo 4, 06123 Perugia, Italy
Laboratorio Bromatologia, Istituto Zooprofilattico Sperimentale dell’Umbria e delle Marche “Togo Rosati”, Via G. Salvemini, 1, 06126 Perugia, Italy
College of Food Science, Sichuan Agricultural University, 46 Xinkang Rd, Ya’an, Sichuan, China
Freelance researcher, Italy
Department of Pharmaceutical Science, University of Perugia, Via San Costanzo 4, 06123 Perugia, Italy
Raffaella Branciari   

Department of Veterinary Medicine, University of Perugia, Italy
Submission date: 2019-06-27
Final revision date: 2019-09-18
Acceptance date: 2019-09-27
Online publication date: 2019-10-28
Publication date: 2019-11-18
Pol. J. Food Nutr. Sci. 2019;69(4):397–405
Salmon flesh spoilage can be greatly reduced through the use of preservation methods, using natural products combined with low temperature and packaging. Microbiological and physicochemical characteristics of fresh salmon fillets (Salmo salar), sprayed with an aromatic vinegar and stored in modified atmosphere packaging, were investigated. Fillets were kept at 4°C and sampled after 2 h and 3, 7 and 10 days. An untreated control group was used as well. Fish samples were analysed for microbiological (total viable count, Enterobacteriaceae, psychrotrophic microbial count, Pseudomonas spp.) and physicochemical (pH, colour, total volatile basic nitrogen, and biogenic amines) properties. Aromatic vinegar was found to beneficially contribute to the hygienic quality of the salmon, reducing microbial growth during storage and exerting a positive effect, mainly on psychrotrophic loads and Pseudomonas spp. The treatment had a positive effect on biogenic amine levels, showing lower values for histamine, putrescine, cadaverine, and tyramine.
Bakir, S., Devecioglu, D., Kayacan, S., Toydemir, G., Korbancioglu-Guler, F., Capanoglu, E. (2017). Investigating the antioxidant and antimicrobial activities of different vinegars. European Food Research and Technology, 243(12), 2083-2094.
Baranyi, J., Tamplin, M.L. (2004). ComBase: a common database on microbial responses to food environments. Journal of Food Protection, 67(9), 1967–1971.
Branciari, R., Ranucci, D., Urbani, E., Valiani, A., Trabalza-Marinucci, M., Dal Bosco, A., Franceschini, R. (2017). Freshwater fish burgers made from four different fish species as a valuable strategy appreciated by consumers for introducing EPA and DHA into a human diet. Journal of Aquatic Food Product Technology, 26(6), 686–694.
Briones, L.S., Reyes, J.E., Tabilo-Munizaga, G.E., Pérez-Won, M.O. (2010). Microbial shelf-life extension of chilled Coho salmon (Oncorhynchus kisutch) and abalone (Haliotis rufescens) by high hydrostatic pressure treatment. Food Control, 21(11), 1530–1535.
Chen, H., Chen, T., Giudici, P., Chen, F. (2016). Vinegar function on health: constituents, sources, and formation mechanisms. Comprehensive Reviews in Food Science and Food Safety, 15(6), 1124-1138.
Choulitoudi, E., Bravou, K., Bimpilas, A., Tsironi, T., Tsimogiannis, D., Taoukis, P., Oreopoulou, V. (2016). Antimicrobial and antioxidant activity of Satureja thymbra in gilthead seabream fillets edible coating. Food and Bioproducts Processing, 100, SI, 570–577.
Chytiri, S., Paleologos, E., Savvaidis, I., Kontominas, M.G. (2004). Relation of biogenic amines with microbial and sensory changes of whole and filleted freshwater rainbow trout (Onchorynchus mykiss) stored on ice. Journal of Food Protection, 67(5), 960–965.
CIE (1986). Commission International de 1’Eclairage. Publication No. 15.2: Colorimetry, 2nd ed., CIE Central Bureau, Wien, Austria.
Corbo, M.R., Bevilacqua, A., Campaniello, D., D’Amato, D., Speranza, B., Sinigaglia, M. (2009). Prolonging microbial shelf life of foods through the use of natural compounds and non-thermal approaches – a review. International Journal of Food Science and Technology, 44(2), 223–241.
Daglia, M. (2012). Polyphenols as antimicrobial agents. Current Opinion in Biotechnology, 23(2), 174–181.
Dalgaard, P. (2000). Fresh and lightly preserved seafood. In C. M. D. Man, & A. A. Jones (Eds.), Shelf-Life Evaluation of Foods (2nd ed.). Gaithersburg, MD: Aspen Publishers, pp. 110–139.
Emborg, J., Laursen, B.G., Rathjen, T., Dalgaard, P. (2002). Microbial spoilage and formation of biogenic amines in fresh and thawed modified atmosphere-packed salmon (Salmo salar) at 2°C. Journal of Applied Microbiology, 92(4), 790–799.
Erikson, U., Misimi, E. (2008). Atlantic salmon skin adn fillets color changes effected by perimortem handling stress, rigor mortis and ice storage. Journal of Food Science, 73(2), C50-C59.
European Commission (1995). 95/149/EC: Commission Decision of 8 March 1995 fixing the total volatile basic nitrogen (TVB-N) limit values for certain categories of fishery products and specifying the analysis methods to be used. Official Journal of the European Communities, L 097, 84–87.
FAO (2016). The state of world fisheries and aquaculture 2016. Contributing to food security and nutrition for all. Rome, Italy: Food and Agriculture Organization of the United Nations.
FDA (2011). Hazards and Controls Guidance Fourth Edition. Chapter 7: Scombrotoxin (Histamine) Formation in Fish and Fishery Products. Florida Sea Grant IFAS - Extension Bookstore University of Florida, Gainesville, FL, USA.
Fidalgo, L.G., Lemos, A. T., Delgadillo, I., Saraiva, J.A. (2018). Microbial and physicochemical evolution during hyperbaric storage at room temperature of fresh Atlantic salmon (Salmo salar). Innovative Food Science and Emerging Technologies, 45, 264–272.
Fernández, K., Aspe, E., Roeckel, M. (2009). Shelf-life extension on fillets of Atlantic salmon (Salmo salar) using natural additives, superchilling and modified atmosphere packaging. Food Control, 20(11), 1036–1042.
Fletcher, G.C., Summers, G., Corrigan, V., Cumarasamy, S., Dufour, J.P. (2002). Spoilage of king salmon (Oncorhynchus tshawytscha) fillets stored under different atmospheres. Journal of Food Science, 67(6), 2362–2374.
Giarratana, F., Muscolino, D., Beninati, C., Ziino, G., Giuffrida, A., Panebianco, A. (2016). Activity of R (+) limonene on the maximum growth rate of fish spoilage organisms and related effects on shelf-life prolongation of fresh gilthead sea bream fillets. International Journal of Food Microbiology, 237, 109–113.
Gimenez, B., Roncales, P., Beltran, J.A. (2005). The effects of natural antioxidant and lighting conditions on the quality of salmon (Salmo salar) fillets packaged in modified atmosphere. Journal of the Science of Food and Agriculture, 85(6), 1033-1040.
Gram, L., Dalgaard, P. (2002). Fish spoilage bacteria – problems and solutions. Current Opinion in Biotechnology, 13(3), 262–266.
Hu, Y., Huang, Z., Chen, X. (2014). Histamine-producing bacteria in blue scad (Decapterus maruadsi) and their abilities to produce histamine and other biogenic amines. World Journal of Microbiology and Biotechnology, 30(8), 2213–2221.
Huang, Z., Liu, X., Jia, S., Zhang, L., Luo, Y. (2018). The effect of essential oils on microbial composition and quality of grass carp (Ctenopharyngodon idellus) fillets during chilled storage. International Journal of Food Microbiology, 266, 52–59.
ICMSF (1986). Microorganisms in foods 2: sampling for microbiological analysis: principles and specific applications. Oxford: Blackwell Scientific Publications, pp. 127–278.
ISO standard 17410:2001. Microbiology of food and animal feeding stuffs. Horizontal method for the enumeration of psychrotrophic microorganisms. Geneva, Switzerland: International Organization for Standardization.
ISO standard 4833-1:2013. Microbiology of the food chain. Horizontal method for the enumeration of microorganisms. Part 1: colony count at 30 degrees C by the pour plate technique. Geneva, Switzerland: International Organization for Standardization.
ISO standard 6579-1:2017. Microbiology of the food chain. Horizontal method for the detection, enumeration and serotyping of Salmonella. Part 1: detection of Salmonella spp. Geneva, Switzerland: International Organization for Standardization.
ISO standard 11290-1:2017. Microbiology of the food chain. horizontal method for the detection and enumeration of Listeria monocytogenes and of Listeria spp. Part 1: detection method. Geneva, Switzerland: International Organization for Standardization.
ISO standard 21528-2:2017. Microbiology of the food chain. Horizontal method for the detection and enumeration of Enterobacteriaceae. Part 2: colony-count technique. Geneva, Switzerland: International Organization for Standardization.
Kim, M.K., Mah, J.H., Hwang, H.J. (2009). Biogenic amine formation and bacterial contribution in fish, squid and shellfish. Food Chemistry, 116(1), 87–95.
Koutsoumanis, K. (2001). Predictive modeling of the shelf life of fish under nonisothermal conditions. Applied and Environmental Microbiology, 67(4), 1821-1829.
Koutsoumanis, K., Nychas, G.J.E. (2000). Application of a systematic experimental procedure to develop a microbial model for rapid fish shelf life predictions. International Journal of Food Microbiology, 60(2-3), SI, 171-184.
Kundukad, B., Schussman, M., Yang, K., Seviour, T., Yang, L., Rice, S.A., Kielleberg, S., Doyle, P.S. (2017). Mechanistic action of weak acid drugs on biofilms. Scientific Reports, 7, art. no. 4783.
Leisner, J.J., Gram, L. (2014). Spoilage of fish. In Butt and Tortorello (Eds.), Encyclopedia of Food Microbiology 2nd Ed. Academic Press, London, UK, pp. 813–820.
Lerfall, J., Bendiksen, E.Å., Olsen, J.V., Morrice, D., Østerlie, M. (2016). A comparative study of organic- versus conventional farmed Atlantic salmon. I. Pigment and lipid content and composition, and carotenoid stability in ice-stored fillets. Aquaculture, 451, 170–177.
Lingham, T., Besong, S., Ozbay, G., Lee, J.L. (2012). Antimicrobial activity of vinegar on bacterial species isolated from retail and local channel catfish (Ictalurus punctatus). Food Processing and Technology, S11-001 [http://dx.doi.org/10.4172/2157...].
Machado, M.M., dos Santos Montagner, G.F.F., Boligon, A., Athayde, M.L., da Rocha, M.I.U.M., Lera, J.P.B., Belló, C., da Cruz, I.B.M. (2011). Determination of polyphenol contents and antioxidant capacity of no-alcoholic red grape products (Vitis labrusca) from conventional and organic crops. Quimica Nova, 34(5), 798–803.
Medina, E., Romero, C., Brenes, M., de Castro, A. (2007). Antimicrobial activity of olive oil, vinegar, and various beverages against foodborne pathogens. Journal of Food Protection, 70(5), 1194–1199.
Mexis, S.F., Chouliara, E., Kontominas, M.G. (2009). Combined effect of an oxygen absorber and oregano essential oil on shelf life extension of rainbow trout fillets stored at 4oC. Food Microbiology, 26(6), 598-605.
Miks-Krajnik, M., Yoon, Y.J., Ukuku, D.O., Yuk, H.G. (2016). Volatile chemical spoilage indexes of raw Atlantic salmon (Salmo salar) stored under aerobic condition in relation to microbiological and sensory shelf lives. Food Microbiology, 53, 182–191.
Miraglia, D., Esposto, S., Branciari, R., Urbani, S., Servili, M., Perucci, S., Ranucci D. (2016). Effect of a phenolic extract from olive vegetation water on fresh salmon steak quality during storage. Italian Journal of Food Safety, 5, 224-228.
Miraglia, D., Ranucci, D., Trabalza-Marinucci, M., Acuti, G., Forte, C., Codini, M., Roila, R., Branciari, R. (2017). Microbiological, chemical-physical and sensory characteristics of Fabriano salami from pigs fed Oregano vulgaris extract. Italian Journal of Food Safety, 6, 203-207.
Ozogul, F., Oztekin, R., Kulawik, P. (2017). Biogenic amine formation and microbiological quality of anchovy (Engraulis encrasicolus) treated with lavender and lemon balm ethanol extracts. Journal of Food Science, 82(5),1278–1284.
Pearson, D. (1991). Chapter 13. Flesh foods. In D. Pearson (Ed.), The Chemical Analysis of Food. Churchill, New York, London, pp. 510-512.
Pons-Sànchez-Cascado, S., Veciana-Nogués, M.T., Bover-Cid, S., Mariné-Font, A., Vidal-Carou, M.C. (2006). Use of volatile and non-volatile amines to evaluate the freshness of anchovies stored in ice. Journal of the Science of Food and Agriculture, 86(5), 699–705.
Rashidinejad, A., Birch, E.J., Sun-Waterhouse, D., Everett, D.W. (2013). Effects of catechin on the phenolic content and antioxidant properties of low-fat cheese. International Journal of Food Science and Technology, 48(12), 2448–2455.
Regulation (EC) No 1019/2013 of 23 October 2013 amending Annex I to Regulation (EC) No 2073/2005 as regards histamine in fishery products. Official Journal of the European Union, L282, 24 October 2013, 46-47.
Sallam, K.I. (2007). Chemical, sensory and shelf life evaluation of sliced salmon treated with salts of organic acids. Food Chemistry, 101(2), 592–600.
Santos, M.H.S. (1996). Biogenic amines: their importance in foods. International Journal of Food Microbiology, 29(2-3), 213–231.
Sivertsvik, M., Rosnes, J.T., Kleiberg, G.H. (2003). Effect of modified atmosphere packaging and superchilled storage on the microbial and sensory quality of Atlantic salmon (Salmo salar) fillets. Journal of Food Science, 68(4), 1467–1472.
Tacon, A.G.J., Metian, M. (2013). Fish matters: importance of aquatic foods in human nutrition and global food supply. Reviews in Fisheries Science, 21(1), 22–38.
Van Immerseel, F., Russell, J.B., Flythe, M.D., Gantois, I., Timbermont, L., Pasmans, F., Haesebrouck, F., Ducatelle, R. (2006). The use of organic acids to combat Salmonella in poultry: a mechanistic explanation of the efficacy. Avian Pathology, 35(3), 182-188.
Wang, Z., Hu, S., Gao, Y., Ye, C., Wang, H. (2017a). Effect of collagen-lysozyme coating on fresh-salmon fillets preservation. LWT - Food Science and Technology, 75, 59–64.
Wang, H., Liu, X., Zhang, Y., Lu, H., Xu, Q., Shi, C., Luo, Y. (2017b). Spoilage potential of three different bacteria isolated from spoiled grass carp (Ctenopharyngodon idellus) fillets during storage at 4°C. LWT - Food Science and Technology, 81, 10–17.
Wunderlichová, L., Buňková, L., Koutný, M., Jančová, P., Buňka, F. (2014). Formation, degradation, and detoxification of putrescine by foodborne bacteria: a review. Comprehensive Reviews in Food Science and Food Safety, 13(5), 1012–1030.
Yagnik, D., Serafin, V., Shah, A. J. (2018). Antimicrobial activity of apple cider vinegar against Escherichia coli, Staphylococcus aureus and Candida albicans; downregulating cytokine and microbial protein expression. Scientific Reports, 8, art. no. 1732.
Zaragozá, P., Fernández-Segovia, I., Fuentes, A., Vivancosa, J.L., Ros-Lisa, J.V., Barat, J. M., Martínez-Mánez, R. (2014). Monitorization of Atlantic salmon (Salmo salar) spoilage using an optoelectronic nose. Sensors and Actuators B: Chemical, 195, 478–485.
Zhai, H., Yang, X., Li, L., Xia, G., Cen, J., Huang, H., Hao, S. (2012). Biogenic amines in commercial fish and fish products sold in southern China. Food Control, 25(1), 303–308.
The impacts of salt with Chinese liquor on the inhibition of microbial spoilage and quality attributes of grass carp ( Ctenopharyngodon idellus ) fillets stored at 4°C
Dan Hu, Yanshun Xu, Dawei Yu, Wenshui Xia, Qixing Jiang
Journal of Food Processing and Preservation