Effect of different starter cultures on the biogenic amines production as a critical control point in fresh fermented sausages


The selection of critical control points is one of the most important steps in the design of a hazard analysis and critical control points system. In this study, the influence of starter culture inoculation on biogenic amine accumulation in fresh fermented sausage as critical control point was studied. The effect of three starter culture Lactobacillus plantarum plus Bifidobacterium lactis, L. plantarum plus Bifidobacterium bifidum or L. plantarum plus B. lactis and B. bifidum on amines production were investigated. Tyramine (TY), Cadaverine (CA), Putrescine (PU), Histamine (HIS) and Tryptamine (TR) contents increased during the fermentation and storage stage, and TY was the prevailing amine in the final product. Sausages produced by fermentation with starters, as compared to natural fermentation (control), had a lower amount of biogenic amine. A great reduction in biogenic amine content was achieved when Bifidobacterium sp. were inoculated, also levels of species of Enterobacteriaceae and Pseudomonas decreased, while lactic acid bacteria counts increased during fermentation and storage.

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  1. 1.

    Ahmad C, Natascha P, Wei C, Hao Z (2008) Antimicrobial proteinaceous compounds obtained from bifidobacteria: from production to their application. Int J Food Microbiol 125:215–222

    Article  Google Scholar 

  2. 2.

    Amal AG (2005) Effect of Bifidobacterium lactis containing starter culture on organoleptic quality and production of biogenic amine in fresh fermented sausages. J Food Sci 33:15–27

    Google Scholar 

  3. 3.

    Armengol MN, Vilalta EB, Sancho J (1994) Evolución de la flora microbiana del fuet de la comarca de Osona. Aliment Nov: 29–32

  4. 4.

    AOAC (1984) Official Method Analysis Association of Official Analytical Chemists. Washington, DC

  5. 5.

    Bover-Cid S, Hugas M, Izquierdo-Pulido M, Vidal-Carou C (2000) Reduction of biogenic amine formation using a negative amino acid-decarboxylase starter culture for fermentation of fuet sausages. J Food Prot 63:237–243

    CAS  Google Scholar 

  6. 6.

    Bover-Cid S, Izquierdo-Pulido M, Vidal-Carou MC (2001) Effect of the interaction between a low tyramine-producing Lactobacillus and proteolytic staphylococci on biogenic amine production during ripening and storage of dry sausages. Inter J Food Microbiol 65:113–123

    Article  CAS  Google Scholar 

  7. 7.

    Bover-Cid S, Miguelez-Arrizado MJ, Becker B, Holzapfel WH, Vidal-Carou MC (2008) Amino acid decarboxylation by Lactobacillus curvatus CTC273 affected by the pH and glucose availability. J Food Microbiol 25:269–277

    Article  CAS  Google Scholar 

  8. 8.

    Bover-Cid SM, Izquierdo-Pulido M, Vidal Carou C (1999) Effect of proteolytic starter cultures of Staphylococcus ssp. On biogenic amine formation during the ripening of dry fermented sausages. Int J Food Microbiol 46:95

    Article  CAS  Google Scholar 

  9. 9.

    Bover-Cid SM, Schoppen S, Izquierdo-Pulido M, Vidal Carou MC (1999) Relationship between biogenic amine contents and the size of dry fermented sausages. Meat Sci 51:305

    Article  CAS  Google Scholar 

  10. 10.

    Brink BJT, Damink C, Joosten HMLJ, Huis-in’t Veld JHJ (1990) Occurence and formation of biologically active amines in foods. Int J Food Microbiol 11:73–84

    Article  Google Scholar 

  11. 11.

    Leroy F, Verluyten J, De Vuyst L (2006) Functional meat starter cultures for improved sausage fermentation. Int J Food Microbiol 106(3):270–285

    Article  Google Scholar 

  12. 12.

    Chiu-Chu H, Hsien-Feng Kung, Chung-Saint L, Deng-Fwu H, Yung-Hsiang T (2011) Bacteriological quality and histamine forming bacteria associated with fish meats and environments in HACCP and non-HACCP fish processing factories. Food Cont 22(10):1657–1662

    Article  Google Scholar 

  13. 13.

    Collado MC, Hernández M, Sanz Y (2005) Production of bacteriocin-like compounds by human fecal Bifidobacterium strains. J Food Prot 68:1034–1040

    CAS  Google Scholar 

  14. 14.

    Demeyer DI, Vandekerchhove P, Moemans R (1979) Compounds determining pH in dry sausage. Meat Sci 3:161

    Article  CAS  Google Scholar 

  15. 15.

    El-Adawy TA, Mansour EH, Khalil AH (1996) Effect of nigella sativa seed oil on the storage stability of sausage. Conference and exhibition the food special, Suez Canal University, Ismailia

  16. 16.

    El-Deep SH (1987) Studies on the quality of Egyptian sausage as determined by certain chemical and microbial changes. Ph. D. Thesis, Faculty of Agriculture, Ain Shams University

  17. 17.

    Comi G, Urso R, Iacumin L, Rantsiou K, Cattaneo P, Cantoni C, Cocolin L (2005) Characterisation of naturally fermented sausages produced in the North East of Italy. Meat Sci 69:381–392

    Article  Google Scholar 

  18. 18.

    Mogensen G, Salminen S, O’Brien J, Ouwehand A, Hozapfel W, Short C, Fonden R, Miller GD, Donohue D, Playne M, Crittenden R, Bianchi Salvadori B, Zink R (2002) Food microorganisms: health benefits a safety evaluation of certain food components. Bull IDF 377:4–9

    Google Scholar 

  19. 19.

    Hammes WP, Hatter D (1998) What is known about the effect of probiotics in meat products? Fleis 78:301–306

    Google Scholar 

  20. 20.

    Hernandez-Jover T, Izquierdo-pulido M, Veciana-Nogues M, Marine-Font A, Vidal-Carou M (1997) Biogenic amine and polyamine contents in meat and meat products. J Agri Food Chem 45:2098

    Article  CAS  Google Scholar 

  21. 21.

    Huff-Lonergan E, Lonergan SM (2005) Mechanisms of water-holding capacity of meat: the role of postmortem biochemical and structural changes. Meat Sci 71:194–204

    Article  CAS  Google Scholar 

  22. 22.

    Kang KH, Shin HJ, Park YH, Lee TS (1989) Studies on the antibacterial substances produced by lactic acid bacteria: purification and some properties of antibacterial substance ‘Bifilong’ produced by B. longum. Korean Dairy Sci 1:204–216

    Google Scholar 

  23. 23.

    Kebary KM (1995) Production, partial purification and stability of antimicrobial substances produced by Bifidobacterium bifidum. Egypt J Dairy Sci 23:151

    CAS  Google Scholar 

  24. 24.

    Kim CR, Hearnsberger JO, Vickery AP, White CH, Marshall DL (1995) Sodium acetate and bifidobacteria increase shelf-life of refrigerated catfish fillets. J Food Sci 60:25

    Article  CAS  Google Scholar 

  25. 25.

    Ogier JC, Serror P (2008) Safety assessment of dairy microorganisms: the Enterococcus genus. Int J Food Microbiol 126(3):291–301

    Article  CAS  Google Scholar 

  26. 26.

    Križek M, Vácha F, Vorlová L, Lukášová J, Cupáková S (2004) Biogenic amines in vacuum-packed and non-vacuum-packed flesh of carp (Cyprinus carpio) stored at different temperatures. Food Chem 88:185–191

    Article  Google Scholar 

  27. 27.

    Latorre-Moratalla ML, Veciana-Nogués T, Bover-Cid S, Garriga M, Aymerich T, Zanardi E, Ianieri A, Fraqueza MJ, Patarata L, Drosinos EH, Laukova A, Talon R, Vidal-Carou MC (2008) Biogenic amines in traditional fermented sausages produced in selected European countries. Food Chem 107:912–921

    Article  CAS  Google Scholar 

  28. 28.

    Marques AP, Leitao MC, San Ramao MV (2008) Biogenic amines in wines: influence of oenological factors. Food Chem 1072:853–860

    Article  Google Scholar 

  29. 29.

    Mc-Cabe B (1986) Dietary tyramine and other pressor amines in MAOI regimens. A review. J Amer Diet Assoc 86:1059

    CAS  Google Scholar 

  30. 30.

    Muhammad Z, Fatimah A, Bakar SJ, Jamilah B (2011) Novel starter cultures to inhibit biogenic amines accumulation during fish sauce fermentation. Int J Food Microbiol 145:84–91

    Article  Google Scholar 

  31. 31.

    Penas E, Frias J, Sidro B, Vidal-Valverde C (2010) Impact of fermentation conditions and refrigerated storage on microbial quality and biogenic amine content of sauerkraut. Food Chem 123:143–150

    Article  CAS  Google Scholar 

  32. 32.

    Ruiz-Capillas C, Jiménez-Colmenero F (2004) Biogenic amines in meat and meat products. Crit Rev Food Sci Nut 44:489–499

    Article  CAS  Google Scholar 

  33. 33.

    Santiago R, Alberto M, María JB, Alejandro H, Rocio C, María C (2011) Application of Lactobacillus fermentium HL57 and Pediococcus acidilactici SP979 as potential probiotics in the manufacture of traditional Iberian dry fermented sausages. Food Microbiol 28:839–847

    Article  Google Scholar 

  34. 34.

    Silla-Santos MH (1996) Biogenic amines: their importance in food. Int J Food Microbiol 29:213–231

    Article  CAS  Google Scholar 

  35. 35.

    Giraffa G (2003) Functionality of enterococci in dairy products. Int J Food Microbiol 88:215–222

    Article  CAS  Google Scholar 

  36. 36.

    Yanshun X, Wenshui X, Fang Y, Jin MK, Xiaohua N (2010) Effect of fermentation temperature on the microbial and physicochemical properties of silver carp sausages inoculated with Pediococcus pentosaceus. Food Chem 118:512–518

    Article  Google Scholar 

  37. 37.

    Zaika LL, Zell TE, Smith JL (1976) The role of nitrite and nitrate in Lebanon bologna. Fermented sausage. J Food Sci 41:1457

    Article  CAS  Google Scholar 

  38. 38.

    Sullivan O’ (2004) Isolated bifidobacteria that produce siderophores which inhibit growth of Lactococcus lactis. US patent No. 6,746,672 B2

  39. 39.

    Hoyos AB (1999) Reduced incidence of necrotizing enterocolitis associated with enteral administration of Lactobacillus acidophilus and Bifidobacterium infantis to neonates in an intensive care unit. Int J Infec Dis 3:197–202

    Article  CAS  Google Scholar 

  40. 40.

    Yamashita M, Sakaue M, Iwata M, Sugino H, Murooka Y (1993) Purification and characterization of monoamine oxidase from Klebsiella aerogenes. J Ferment Bioeng 76:289–295

    Article  CAS  Google Scholar 

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Correspondence to Gehad Sallah Saeed Eldeep.

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Mokhtar, S., Mostafa, G., Taha, R. et al. Effect of different starter cultures on the biogenic amines production as a critical control point in fresh fermented sausages. Eur Food Res Technol 235, 527–535 (2012). https://doi.org/10.1007/s00217-012-1777-9

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  • Critical control point
  • Hazard analysis
  • Sausage
  • Biogenic amine
  • Starter culture