Comparative Application of Different Strategies of Bacteriocins Produced by Carnobacterium maltaromaticium MMF-32 for Inhibition of Listeria monocytogenes ATCC 19114 in Cold-Smoked Haddock

Authors

  • Ngozi Izuchukwu Institute of Aquaculture, School of Natural Sciences, University of Stirling, Stirling, FK9 4LA, UK

Keywords:

Anti-listerial activity, Biogenic amines, Biopreservation, Carnobacterium, Cold-smoked haddock, Sensory analysis.

Abstract

Cold-smoked haddock fillets (undyed) treated with bacteriocin producing C. maltaromaticum MMF-32, C. piscicola A9b bac? (a non-producer of bacteriocin) and supernatant, supernatant concentrated with (NH4)2SO4 and semi-purified bacteriocin of C. maltaromaticum MMF-32 were challenged with L. monocytogenes ATCC 19114 (up to 2.2 x 103 CFU g-1).  Following treatment, samples were kept at 4 °C for 10 days.L. monocytogenes ATCC 19114, total bacterial and carnobacterium counts were determined along with changes in total volatile base nitrogen (TVBN) and biogenic amine production as well as texture, color and odor. The anti-listerial effect of C. maltaromaticum MMF-32 and C. piscicola A9b bac? did not work on the cold smoked haddock, this is because there were few Carnobacterium cells in the samples that were inoculated with 4 x 106 CFU g?1, than the control i.e untreated fish samples and sample having only L. monocytogenes ATCC 19114. C. maltaromaticum MMF-32 did not show any spoiling capacity from the odour. All treated samples produced cadavarine. There is marked spoilage odour observed in samples treated with MRS supernatant and ammonium sulphate precipitated supernatant. During the period of storage, TVB-N treated samples exceeded the limit of 35 mg N 100 g-1. The use of bacteriocins for inactivation of listeria cells, semi-purified bacteriocin showed a statistically significant reduction in L. monocytogenes ATCC 19114 growth on day 7. Although the study on anti-listerial effects of C. maltaromaticum MMF-32 was not successful, this organism did have a positive effect on retention of firmness and sensory perception in cold smoked haddock.

References

[1] A. Campos, P. Castro, S. P. Aubourg, and J. B. Velázquez, “Use of Natural Preservatives in Seafood”, in Novel technologies in Food Science, Integrating Food Science and Engineering Knowledge Into Food Chain, ed. McElhatton, A. and Sobral, P. J. A, Springer Science+Business Media, 2012, pp. 325-360.
[2] P. Calo-Mata, S. Arlindo, K. Boehme, T. de Miguel, A. Pascola, and J. Barros-Velazquez, “Current applications and future trends of lactic acid bacteria and their bacteriocins for the biopreservation of aquatic food products”. Food Bioprocess Technology, vol. 1 (1), pp. 43–63, Mar. 2008.
[3] S. Alzamora, J. Welti-Chanes, and S. Guerrero, “Rational use of novel technologies: A comparative analysis of the performance of several new food preservation technologies for microbial inactivation”, in Novel technologies in food science, integrating food science and engineering knowledge into the food chain, ed. McElhatton, A. and Sobral, P. J. A. Springer Science+Business Media, LLC, 2012.
[4] P. K. Ben Embarek, “Presence, detection and growth of Listeria monocytogenes in seafood: a review”. International Journal Food Microbiology, vol. 23 (1), pp. 17-34, Sept. 1994.
[5] L. Rorvik, B. Aase, T. Alvestad, and D. Caugant, “Molecular epidemiological survey of Listeria monocytogenes in seafood and seafood-processing plants”, Applied and Environmental Microbiology, vol. 66 (11), pp. 4779-89, Nov. 2000.
[6] J. Kuzmanovi?, R. Ašanin, M. Balti?, D. Miši?, M. Dimitrijevi?, M. Stojanovi?, N. Ašanin, and I. Kova?evi?, “Presence of Listeria spp. in fish samples, fish products and seafood products”, Acta Veterinaria (Beograd), vol. 61 (2-3), pp. 193-203, 2011.
[7] H. Hof, T. Nichterlein, and M. Kretschmar, “When are Listeria in foods a health risk?” Trends in Food Science and Technology vol. 5 (6), pp. 185-190, Jun. 1994.
[8] U. Nufer, R. Stephan, and T. Tasara, “Growth characteristics of Listeria monocytogenes, Listeria welshimeri and Listeria innocua strains in broth cultures and a sliced bologna-type product at 4 and 7°C”, Food Microbiology, vol. 24 (5), pp. 444-451, Aug. 2007.
[9] M. Uyttendaele, P. Busschaert, A. Valero, A. H. Geeraerd, A. Vermeulen, L. Jacxsens, K. K. Goh, A. De Loy, J. F. Van Impe, and F. Devlieghere, “Prevalence and challenge tests of Listeria monocytogenes in Belgian produced and related mayonnaise-based deli-salads, cooked meat products and smoked fish between 2005 and 2007”, International Journal of Food Microbiology, vol. 133 (1-2), pp. 94-104, Jul. 2009.
[10] S. Pao, M. R. Ettinger, M. F. Khalid, A. O. Reid, and B. L. Nerrie, “Microbial quality of raw aquacultured fish fillets procured from Internet and local retail markets”, Journal of Food Protection, vol. 71 (8), pp. 1544–1549, Aug. 2008.
[11] T. Gelbí?ová, and R. Karpíšková, “Occurrence and Characteristics of Listeria monocytogenes in ready-to-eat food from retail market in the Czech Republic”, Czech Journal of Food Science, vol. 27 (2), pp. S2-3-S2-7, 2009.
[12] M. Cheroutre-Vialette, I. Lebert, M. Hebraud, J. C. Labadie and A. Lebert, “Effects of pH or aw stress on growth of Listeria monocytogenes”, International Journal of Food Microbiology, vol. 42 (1-2), pp. 71–77, Jun. 1998.
[13] W. J. Dorsa, D. L. Marshall, M. W. Moody and C. R. Hackney, “Low temperature growth and thermal inactivation of Listeria monocytogenes in precooked crawfish tail meat”, Journal of Food Protection, vol. 56 (2), pp. 106-109, Feb. 1993.
[14] A. Galvez, H. Abriouel, N. Benomar, and R. Lucas, “Microbial antagonists to food-borne pathogens and biocontrol”, Current Opinion in Biotechnology, vol. 21 (2), pp. 142-148, Apr. 2010.
[15] P. Garcia, L. Rodriguez, A. Rodriguez, and B. Martinez, “Food biopreservation: Promising strategies using bacteriocin, bacteriophage and endolysins”, Trends in Food Science and Technology, pp. 373-382, Aug. 2010.
[16] S. Rodgers, “Preserving non-fermented refrigerated foods with microbial cultures—a review”, Trends in Food Science and Technology, vol. 12 (8), pp. 276–284, Aug. 2001.
[17] L. De Vuyst, and E. J. Vandamme, “Antimicrobial potential of lactic acid bacteria”, in Bacteriocin of Lactic acid Bacteria, L. De Vuyst, and E. J. Vandamme, Ed., London: Blackie, 1994, pp. 91-142.
[18] B. Collins, P. Cotter, Hill and R. Paul Ross, “Application of Lactic Acid Bacteria – Produced Bacteriocins”, in Biotechnology of Lactic Novel Applications, F. Mozzi, R. Raya and G. M. Vignolo, Blackwell Publishing, 2010, pp. 89-109.
[19] A. Brillet, M.-F. Pilet, H. Prevost, M. Cardinal, and F. Leroi, “Effect of inoculation of Carnobacterium divergens V41, a biopreservative strain against Listeria monocytogenes risk, on the microbiological, chemical and sensory quality of cold-smoked salmon”, International Journal of Food Microbiology, vol. 104 (3), pp. 309–324, Oct. 2005.
[20] A. L. Pinto, M. Fernandes, C. Pinto, H. Albano, F. Castilho, P. Teixeira and P. A. Gibbs, “Characterization of anti-Listeria bacteriocins isolated from shellfish: potential antimicrobials to control non-fermented seafood”, International Journal of Food Microbiology, vol. 129 (1), pp. 50-58, Jan. 2009.
[21] F. Leroi, “Occurrence and role of lactic acid bacteria in seafood products”, Food Microbiology, vol. 27 (6), pp. 698-709, Sept. 2010.
[22] P. Rattanachaikunsopon and P. Phumkhachorn, “Lactic acid bacteria: their antimicrobial compounds and their uses in food production”, Annals of Biological Research, vol. 1 (4), pp. 218-228, 2010.
[23] F. Leroi, J. J. Joffraud, F. Chevalier and M. Cardinal, “Study of the microbial ecology of cold-smoked salmon during storage at 8 °C”, International Journal of Food Microbiology, vol. 39 (1-2), pp. 111– 121, Jan. 1998.
[24] D. Drider, G. Firmland, Y. Héchard, L. M. McMullen and H. Prévost, “The continuing story of class IIa bacteriocins”, Microbiology and Molecular Biology Reviews, vol. 70 (2), pp. 564–582, Jun. 2006.
[25] V. Stohr, J. J. Joffraud, M. Cardinal and F. Leroi, “Spoilage potential and sensory profile associated with bacteria isolated from cold-smoked salmon”, Food Research International, vol. 34 (9), pp. 797- 806, Nov. 2001.
[26] M. E. Stiles, “Biopreservation by lactic acid bacteria”, Antonie Van Leeuwenhoek, vol. 70 (2-4), pp. 331–345, Oct. 1996.
[27] L. Nilsson, L. Gram, and H. H. Huss, “Growth control of Listeria monocytogenes on cold-smoked salmon using a competitive lactic acid bacteria flora”, Journal of Food Protection, vol. 62 (4), pp. 336–342, Apr. 1999.
[28] K. Yamazaki, M. Suzuki, Y. Kawai, N. Inoue and T. J. Montville, “Inhibition of Listeria monocytogenes in cold-smoked salmon by Carnobacterium piscicola CS526 isolated from frozen Surimi”, Journal of Food Protection, vol. 66 (8), pp. 1420– 1425, Aug. 2003.
[29] I. Tahiri, M. Desbiens, R. Benech, E. Kleadr, C. Lacroix and I. Fliss, “Comparison of different application strategies of divergicin M35 for inactivation of Listeria monocytogenes in cold-smoked wild salmon” Food Microbiology, vol. 26 (8), pp. 783-793, Dec. 2009.
[30] L. Nilsson, Y. Y. Ng, J. N. Christiansen, B. L. Jorgensen, D. Grotinum and L. Gram, “The contribution of bacteriocin to inhibition of Listeria monocytogenes by Carnobacterium piscicola strains in cold smoked salmon systems”, Journal of Applied Microbiology, vol. 96 (1), pp. 133-143, Jan. 2004.
[31] J.-J. Lia, Y.-D. Liu, F.-W. Wang, G.-H. Ma and Z.-G. Su, “Hydrophobic interaction chromatography correctly refolding proteins assisted by glycerol and urea gradients” Journal of Chromatography A, vol. 1061 (20), pp. 193-199, Dec. 2004.
[32] P. K. Smith, R. I. Krohn, G. T. Hermanson, A. K. Mallia, F. H. Gartner, M. D. Provenzano, E. K. Fujimoto, N. M. Goeke, B. J. Olson, and D. C. Klenk, “Measurement of protein using bicinchoninic acid” Analytical Biochemistry, vol. 150 (1), pp. 76-85, Oct. 1985.
[33] L. Truelstrup Hansen, T. Gill and H. H. Huss, “Effects of salt and storage temperature on chemical, microbiological and sensory changes in cold-smoked salmon” Food Research International, vol. 28 (2), pp. 123-130, 1995.
[34] M. A. Wasney, R. A. Holley and D. S. Jayas, “Cresol red thallium acetate sucrose inulin (CTSI) agar for the selective recovery of Carnobacterium spp.”, International Journal of Food Microbiology, vol. 64 (1-2), pp. 167–174, Feb. 2001.
[35] P. Malle and M. Vallé, “Assay of biogenic amines involved in fish decomposition”, Journal of AOAC International, vol. 79 (1), pp. 43-49, Jan.-Feb. 1996.
[36] J. P. Gouygou, C. Sinquin and P. Durand, “High Pressure Liquid Chromatography determination of histamine in fish,” Journal of Food Science, vol. 52 (4), pp 925-927, Jul. 1987.
[37] J. P. Gouygou, C. Martin, C. Sinquin and P. Durand “Determination of biogenic amines in fish”, Océanis, vol. 15, pp. 599-604, 1989.
[38] J. L. Corbin, B. H. Marsh and G. A. Peters, “An improved method for analysis of polyamines in plant tissue by precolumn derivatization with o-phthaldehyde and separation by High Performance Liquid Chromatography”, Plant Physiology, vol. 90, pp. 434-439, Jan. 1989.
[39] M. A. Cichy, D.L. Stegmeier, H. Veening and H. D. Becker, “High performance liquid chromatographic separation of biogenic polyamines using 2-(1-pyrenyl) ethyl chloroformate as a new fluorogenic derivatizing reagent”, Journal of Chromatography, vol. 613 (1), pp. 15-21, Mar. 1993.
[40] G. Taibi and M. R. Schiavo, “Simple high performance Liquid chromatographic assay for polyamines and their monoacetyl derivatives”, Journal of Chromatography, vol. 614 (1), pp. 153-158, Apr. 1993.
[41] J. Kirschbaum and B. Luckas, “Pre-column derivatization of biogenic amines and amino acids with 9-fluorenylmethyl chloroformate and heptylamine”, Journal of Chromatography A, 661 (1-2), pp. 193-199, Feb. 1994.
[42] M. Marcé, D. S. Brown, T. Capell, X. Figueras and A. F. Tiburcio, “Rapid High Performance Liquid Chromatographic method for the quantitation of polyamines as their dansyl derivatives: application to plant and animal tissues”, Journal of Chromatography B, 666 (2), pp. 329-335, Apr. 1995.
[43] J. S. Park, C. H. Lee, E. Y. Kwon, H. J. Lee and Kim and S. H. Kim, “Monitoring the contents of biogenic amines in fish and fish products consumed in Korea”, Food Control, vol. 21 (9), pp. 1219–1226, Sept. 2010.
[44] L. Franzetti, M. Scarpellini, D. Mora and A. Galli, “Carnobacterium spp. in seafood packaged in modified atmosphere”, Annual Microbiology, vol. 53, pp. 189–198, 2003.
[45] K. Rudi, T. Maugesten, S. E. Hannevik and H. Nissen, “Explorative multivariate analyses of 16S rDNA gene data from microbial communities in modified-atmosphere-packed salmon and coalfish”, Applied and Environmental Microbiology, vol. 70 (8), pp. 5010-5018, Aug. 2004.
[46] J. Emborg, B. G. Laursen, T. Rahtjen and P. Dalsgaard, “Microbial spoilage and formation of biogenic amines in fresh and thawed modified atmosphere-packed salmon (Salmo salar) at 2 °C”, Journal of Applied Microbiology, vol. 92, pp. 790–799, 2002.
[47] J. Emborg, B. G. Laursen, and P. Dalgaard, “Significant histamine formation in tuna (Thunnus albacares) at 2 °C – effect of vacuum- and modified atmosphere-packaging on psychrotolerant bacteria”, International Journal of Food Microbiology, vol. 101 (3), pp. 263–279, Jun. 2005.
[48] R. L. Buchanan and L. K. Bagi, “Microbial competition: effect of culture conditions on the suppression of Listeria monocytogenes Scott A by Carnobacterium piscicola”, Journal of Food Protection, vol. 60 (3), pp. 254–261, 1997.
[49] P. P. Vijayakumar and P. M. Muriana, “A microplate growth inhibition assay for screening bacteriocins against Listeria monocytogenes to differentiate their mode-of-action”, Biomolecules, vol. 5 (2), pp. 1178-1194, Jun. 2015.
[50] C. A. Campos, Ó. Rodríguez, P. Calo-Mata, M. Prado and J. Barros-Vela´zquez, “Preliminary characterization of bacteriocins from Lactococcus lactis, Enterococcus faecium and Enterococcus mundtii strains isolated from turbot (Psetta maxima)”, Food Research International, vol. 39 (3), pp. 356–364, 2006.
[51] A. G. Ponce, M. R. Moreira, C. E. del Valle and S. I. Roura, “Preliminary characterization of bacteriocin-like substances from lactic acid bacteria isolated from organic leafy vegetables”, Swiss Society of Food Science and Technology, vol. 41 (3), pp. 432-441, Apr. 2008.
[52] T. Katla, K. Naterstad, M. Vancanneyt, J. Swings and L. Axelsson, “Differences in susceptibility of Listeria monocytogenes strains to sakacin P, sakacin A, pediocin PA-1, and nisin”, Applied and Environmental Microbiology, vol. 69 (8), pp. 4431–4437, Aug. 2003.
[53] A. Brillet, M.-F. Pilet, H. Prevost, A. Bouttefroy, and F. Leroi, “Biodiversity of Listeria monocytogenes sensitivity to bacteriocin-producing Carnobacterium strains and application in sterile cold-smoked salmon”, Journal of Applied Microbiology, vol. 97 (5), pp. 1029–1037, Aug. 2004.
[54] A. Brillet, M.-F., Pilet, H., Prevost, M. Cardinal and F. Leroi, “Effect of inoculation of Carnobacterium divergens V41, a biopreservative strain against Listeria monocytogenes risk, on the microbiological, chemical and sensory quality of cold-smoked salmon”, International Journal of Food Microbiology, vol. 104 (3), pp. 309–324, Oct. 2005.
[55] J. J. Joffraud, F. Leroi, C. Roy and J. L. Berdagué, “Characterization of volatile compounds produced by bacteria isolated from the spoilage flora of cold-smoked salmon”, International Journal of Food Microbiology, 66 (3), pp.175–184, Jun. 2001.
[56] M. Ando, “Correspondence of collagen to the softening of meat during refrigeration”, in Extracellular matrix of fish and shellfish, Sato, K., Sakaguchi, M. and Bremner, H. A. Eds. Trivandrum, India: Research Signpost, 1999, pp. 69–79.
[57] I. Mitchie, “Causes of downgrading in the salmon farming industry”, in Farmed fish quality, Kestin, S. C. and Warris, P. D. Eds. Oxford: Fishing New Books, 2001, pp. 129–136.
[58] A. Koteng, “Markedsundersøkelse norsk laks”, Bergen, Norway: Fiskerinaeringens Landsforening FHL, 1992, pp. 165.
[59] T. Mørkøre and O. Einen, “Relating sensory and instrumental texture analyses of Atlantic salmon”, Journal of Food Science: Sensory and Nutritive Qualities of Food, 68 (4), pp. 1492-14967, May. 2003.
[60] S. Jittinandana, P. B. Kenney, S. D. Slider and R. A. Kiser, “Effect of brine concentration and brining time on quality of smoked rainbow trout filets”, Journal of Food Science, 67 (6), pp. 2095–2099, Aug. 2002.
[61] M. Morzel, G. F. Fitzgerald and E. K. Arendt, “Fermentation of salmon fillets with a variety of lactic acid bacteria”, Food Research International, 30, pp. 777–785, 1997.
[62] S. Samsun, M. E. Erdem and N. Samsun, “The determination of meal yield and chemical composition of whiting (Merlangius merlangus euxinus Nordmann, 1840)”, Journal of Science and Engineering F?rat University, vol. 18 (2), pp. 165–170, 2006.
[63] T. Katla, T. Møretrø, I. M. Aasen, A. Holck, L. Axelsson and K. Naterstad, “Inhibition of Listeria monocytogenes in cold smoked salmon by addition of sakacin P and/or live Lactobacillus sakei cultures”, Food Microbiology, vol. 18 (4), pp. 431–439, Aug. 2001.
[64] F. Duffes, C. Corre, F. Leroi, X. Dousset and P. Boyaval, “Inhibition of Listeria monocytogenes by in situ produced and semi-purified bacteriocins of Carnobacterium spp. on vacuum-packed, refrigerated cold-smoked salmon”, Journal of Food Protection, vol. 62 (12), pp. 1394-1403, Dec. 1999.
[65] M., Vaz-Velho, S. Todorov, J. Ribeiro, and P. Gibbs, “Growth control of Listeria innocua 2030c during processing and storage of cold-smoked salmon-trout by Carnobacterium divergens V41 culture and supernatant”, Food Control, vol. 16 (6), pp. 541–549, Jul. 2005.
[66] M. I. Aasen, S. Markussen, T. Møretrø, T. Katla, L. Axelsson and K. Naterstad, “Interactions of the bacteriocin sakacin P and nisin with food constituents”, International Journal of Food Microbiology, vol. 87 (1-2), pp. 35-43, Oct. 2003.
[67] I. F. Nes, H. Holo, G. Fimland, H. H. Hauge and J. Nissen-Meyer, “Unmodified peptide-bacteriocins (class II) produced by lactic acid bacteria” in peptide antibiotics, discovery, modes of action and applications, C. J. Dutton, M. A. Haxell, H. A. I. McArthur and R. G. Wax, Eds. New York: Marcel Dekker, 2002, pp. 81–115.
[68] A. D. Crandall and T. J. Montville, "Nisin resistance in Listeria monocytogenes ATCC 700302 is a complex phenotype”, Applied and Environmental Microbiology, vol. 64(1), pp. 231–237, Jan. 1998.
[69] L. Nilsson, Y. Chen, M. L. Chikindas, H. H. Huss, L. Gram and T. J. Montville, “Carbon dioxide and nisin acts synergistically on Listeria monocytogenes”, Applied and Environmental Microbiology, vol. 66 (2), pp. 769–774, Feb. 2000.
[70] B. A. M. Banja, “Shelf life trial on cod (Gadus morhua L.) and haddock (Melanogrammus aeglefinus L.) stored on ice around 0 °C”, Fisheries Department, Department of State for Presidential Affairs, Fisheries and Natural Resources, Gambia, pp. 1-29, 2002.
[71] G. Olafsdottir, H. L. Lauzon, E. Martinsdottir and K. Kristbergsson, “Influence of storage temperature on microbial spoilage characteristics of haddock fillets (Melanogrammus aeglefinus) evaluated by multivariate quality prediction”, International Journal of Food Microbiology, vol. 111 (2), pp. 112–125, Sept. 2006.
[72] L. Gram, “Microbiological spoilage of fish and seafood products”, in Compendium of Microbiological spoilage of foods and beverages, Food Microbiology and Food Safety, W. H. Sperber, and M. P. Doyle, Eds. New York, NY. Springer Science and Business Media, 2009, pp. 87-119.
[73] L. Gram and P. Dalsgaard, “Fish spoilage bacteria – problems and solutions”, Current Opinion in Biotechnology, vol. 13 (3), pp. 262–266, Jun. 2002.
[74] F. Leroi, J. J. Joffraud, F. Chevalier and M. Cardinal, “Study of the microbial ecology of cold-smoked salmon during storage at 8 °C”, International Journal of Food Microbiology, vol. 39 (1-2), pp. 111– 121, Jan. 1998.
[75] L. Truelstrup Hansen and H. H. Huss, “Comparison of the microflora isolated from spoiled cold-smoked salmon from three smokehouses”, Food Research International, vol. 31 (10), pp. 703– 711, Dec. 1998.
[76] U. Lyhs, J. Björkroth and H. Korkeala, “Characterisation of lactic acid bacteria from spoiled vacuum-packaged, cold smoked rainbow trout using ribotyping”, International Journal of Food Microbiology, vol. 52 (1-2), pp. 77– 84, Nov. 1999.
[77] L. V. Jorgensen, P. Dalsgaard and H. H. Huss, “Multiple compound quality index for coldsmoked salmon (Salmo salar) developed by multivariate regression of biogenic amine and pH”, Journal of Agricultural and Food Chemistry, vol. 48 (6), pp. 2448–2453, Jun. 2000a.
[78] L. V. Jorgensen, H. H. Huss and P. Dalsgaard, “The effect of biogenic amine production by single bacterial cultures and metabiosis on cold-smoked salmon”, Journal of Applied Microbiology, vol. 89, pp. 920–934, Dec. 2000b.
[79] S. L. Taylor, “Histamine food poisoning: toxicology and clinical aspects”, Critical Reviews in Toxicology 17 (2), 91–128, 1986.
[80] B. Ten Brink, C. Damink, H. M. Joosten, and J. H. Huis in’t Veld, “Occurrence and formation of biologically active amines in foods”, International Journal of Food Microbiology, vol. 11 (1), pp. 73– 84, Aug. 1990.
[81] P. Russo, G. Spano, M. P. Arena, V. Capozzi, F. Grieco and L. Beneduece, “Are consumers aware of the risks related to biogenic amines in food?”, Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology, vol. 2, pp. 1087-1095, 2010.
[82] European Union, 1995. 95/149/EC: commission decision of 08 March 1995 “fixing the total volatile basic nitrogen (TVB-N) limit values for certain categories of fishery products and specifying the analysis method to be used”, Official Journal L 097, 0084–0087, 29/04/1995.
[83] J. Oehlenschläger, “Suitability of ammonia-N, dimethylamine-N, trimethylamine-N, trimethylamine oxide-N and total volatile basic nitrogenas freshness indicators in seafoods”, in Methods to Determine the Freshness of Fish in Research and Industry, G. Olafsdottir, J. Luten, P. Dalgaard, M. Careche, V. Verrez-Bagnis, E. Martinsdottir and K. Heia, Eds. International Institute of Refrigeration, Paris, pp. 92–99, 1998.
[84] S. Baixas-Nogueras, S. Bover-Cid, M. T. Veciana-Nogues, and M. C. Vidal-Carou, “Suitability of volatile amines as freshness indexes for iced Mediterranean Hake”, Journal of Food Science, vol. 68, pp. 1607–1610, 2003.
[85] E. S. Sant’Anna and R. C. O. Torres, “Growth of Pediococcus acidilactici on sugar cane blackstrap molasses”, Review of Microbiology, vol. 29 (3), pp. 202-207, Sept. 1998.

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2017-12-30

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Izuchukwu, N. (2017). Comparative Application of Different Strategies of Bacteriocins Produced by Carnobacterium maltaromaticium MMF-32 for Inhibition of Listeria monocytogenes ATCC 19114 in Cold-Smoked Haddock. American Scientific Research Journal for Engineering, Technology, and Sciences, 38(2), 311–340. Retrieved from https://www.asrjetsjournal.org/index.php/American_Scientific_Journal/article/view/3679

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