Effects of wild type lactic acid bacteria on histamine and tyramine formation in sucuk


Keywords:
histamine lactic acid bacteria sucuk tyramine
Y. N. DOĞAN
Ö. F. LENGER
M. DÜZ
I. DOĞAN
Z. GÜRLER
Abstract

Biogenic amines (BAs) are formed by the decarboxylation of amino acids in fermented products and accumulate in these products due to the fermentation conditions, the natural microflora of the product, and the diversity of amino acids. Although they are inhibited by the human body, they are a hazard to public health. Starter cultures used in fermented sucuk should not have amino acid decarboxylase properties. The aim of the present study was to determine proteolytic activity, histidine and tyrosine decarboxylase enzyme activities of Lactobacillus plantarum, Lactobacillus sake, and Lactobacillus curvatus species and to evaluate the level of BA in sucuk groups containing these lactic acid bacteria (LAB). It was determined that none of the LAB generated these activities. While histamine values were not statistically significant in the sucuk groups (P> 0.05), tyramine values showed statistically significant differences (P<0.05). The tyramine values of GI ( = 1.43 ± 0.75) and GIII ( = 2.73 ± 1.02) groups were lower than C ( = 8.97 ± 5.29) and GII ( = 7.58 ± 2.90) groups. According to the results of the study, L. plantarum or L. curvatus can provide more reliable fermented products with respect to tyramine formation. L. plantarum, L. sake, and L. curvatus could reduce histamine and tyramine formation in fermented sucuk.

Article Details
  • Section
  • Research Articles
Downloads
Download data is not yet available.
References
Benito MJ, Martın A, Aranda E, Perez-Nevado F, Ruiz-Moyano S, CordobaM(2007). Characterization and selection of autochthonous lactic acid bacteriaisolated from traditional Iberian dry-fermented salchichon and chorizo sausages. J Food Sci 72 (6): 193-201.
Bover-Cid S, Holzaphfel WH (1999). Improved screning procedure for biogenic amine production by lactic acid bacteria. Int J Food Microbiol 53:33-41.
Bover-Cid S, Izquierdo-Pulido M,Vidal-Carou MC (2001). Influence of hygienic quality of raw material on biogenic amine production during ripening and storage of dry fermented sausages.J Food Protect63: 1544- 1550.
Bover-Cid S, Izquierdo-Pulido M, Vidal-Carou MC (2000). Mixed starter cultures to control biogenic amine production in dry fermented sausages. J Food Protect63 (11): 1556-1562.
Bozkurt H,Erkmen O (2004). Effects of temperature, humidity and additives on the formation of biogenic amines in sucuk during ripening and storage periods. Food Sci Technol Int 10 (1): 21-28.
BuncicS, Paunovic LJ, Teodorovic V, Radisic D, Vojinovic G, Smiljanic D,Baltic M(1993). Effects of Glucono delta lactone and Lactobacillus plantarum on the production of histamine and tyramine in fermented sausages. Int J Food Microbiol 17: 303-309.
Choudhury N, Hansen W, Engesser D, Hammes WP, Holzapfel WH (1990). Formation of histamine and tyramine by lactic acid bacteria in decarboxylase medium. LettAppl Microbiol 11: 278-281.
Costantini A, Cersosimo M, PreteVD, Garcia-Moruno E (2006). Production of biogenic amines by lactic acid bacteria: screening by PCR, thin-layer chromatography, and high-performance liquid chromatography of strains isolated from wine and must. J Food Protect 69 (2):391-396.
Coton E, Coton M (2005). Multiplex PCR for colony direct detection of Gram positive histamine- and tyramine-producing bacteria.J Microbiol Meth 63: 296-304.
Dapkevicius MLE, Nout MR, Rombouts FM, Houben JH, Wymenga W (2000). Biogenic amine formation and degradation by potential fish silage starter microorganisms. Int JFood Microbiol57 (1-2): 107-114.
De Las Rivas B, Ruiz-Capillas C, Carrascosa AV, Curiel JA, Jiménez-Colmenero F, Muñoz R (2008). Biogenic amine production by Gram-positive bacteria isolated from Spanish dry-cured “chorizo” sausage treated with high pressure and kept in chilled storage. Meat Sci80(2): 272-277.
De Llano DG (1998). Biogenic amine production by wild lactococcal and leuconostoc strains. Lett Appl Microbiol 26(4): 270-274.
Demirel YN,Gürler Z (2016). Fermente Türk Sucuklarından İzole Edilen Lactobacillus plantarum, Lactobacillus sake, Lactobacillus curvatus ve Staphylococcus xylosus Suşlarının Starter Kültür Olarak Kullanılmasının Araştırılması. Doktora Tezi. Afyon Kocatepe Üniversitesi Sağlık Bilimleri Enstitüsü, Afyonkarahisar. (in Turkish)
Ekici K, Şekeroğlu R, Sancak YC, Noyan T (2004). A note on histamine levels in Turkish style fermented sausages. Meat Sci68:123-125.
Erkmen O, Bozkurt H (2004). Quality characteristics of retailed sucuk (Turkish dry-fermented sausage). Food TechnolBiotechnol42 (1):63-69.
Franciosi E, Settanni L, Cavazza A, Poznanski E (2009). Biodiversity and technological potential of wild lactic acid bacteria from raw cows’ milk. Int Dairy J19 (1): 3-11.
Gökalp HY, Kaya M, Zorba O (2004). Et ürünleri işleme mühendisliği. Atatürk Üniversitesi, Yayın No: 786 Ziraat Fak. Yayın No: 320, Erzurum.
Halász A, Barath A, Simon-Sarkadi L, Holzapfel W(1994). Biogenic amines and their production by microorganisms in food. Trends Food Sci Tech5 (2): 42-49.
Hammes WP, Knauf HJ (1994). Starters in the processing of meat products. Meat Sci36 (1-2): 155-168.
Kaban G, Kaya M (2007).Staphylococcus xylosus ve Lactobacillus plantarum suşlarının sucuğun duyusal özellikleri ve renk değerleri üzerine etkileri. Atatürk ÜniZiraat Fak Derg38 (1):83-89.
Köse S, Kaklıkkaya N, Koral S, Tufan B, Buruk KC, Aydın F (2011). Commercial test kits and the determination of histamine in traditional (ethnic) fish products-evaluation against an EU accepted HPLC method. Food Chem 125 (4): 1490-1497.
Landeta G, Curiel JA, Carrascosa AV, Muñoz R, De Las Rivas B (2013). Technological and safety properties of lactic acid bacteria isolated from Spanish dry-cured sausages. Meat Sci95 (2): 272-280.
Lee BH, Simard RE (1984). Evaluation of methods for detecting the production of H2S, volatile sulfides, and greening by lactobacilli. J Food Sci49 (4): 981-983.
Lehane L, Olley J (2000). Histamine fish poisoning revisited. Int J Food Microbiol 58 (1-2): 1-37.
Leroy F, Vuyst L (2004). Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food SciTechnol 15 (2): 67-78.
Leuschner RG, Hammes WP (1998). Tyramine degradation by micrococci during ripening of fermented sausage.Meat Sci49 (3): 289-296.
Lucas P, Landete J, Coton M, Coton E, Lonvaud-Funel A (2003). The tyrosine decarboxylase operon of Lactobacillus brevis IOEB 9809: characterization and conservation in tyramine-producing bacteria.
FEMS Microbiol Lett 229 (1): 65-71.
MaijalaR, Eerola S (1993). Contaminant lactic acid bacteria of dry sausages produce histamine and tyramine. Meat Sci35 (3): 387-395.
Maijala R (1993). Formation of histamine and tyramine by some lactic acid bacteria in MRS broth and modified decarboxylation agar.Letters Appl Microbiol17:40-43.
Maijala R (1994). Histamine and tryramine production by a Lactobacillus strain subjected to external pH decrease. J Food Protect57 (3):259-262.
Mangia NP, Trani A, Di Luccia A, Faccia M, Gambacorta G, Fancello F, Deiana P (2013). Effect of the use of autochthonous Lactobacillus curvatus, Lactobacillus plantarum and Staphylococcus xylosus strains on microbiological and biochemical properties of the Sardinian fermented sausage. Eur Food Res Technol236 (3): 557-566.
Marcobal A, De Las Rivas B, Moreno-Arribas MV, Muñoz R(2005). Multiplex PCR method for the simultaneous detection of histamine-, tyramine-,and putrescine-producing lactic acid bacteria in foods. J Food Protect 68 (4): 874-878.
Montel MC, Masson F, Talon R (1999). Comparison of biogenic amine content in traditional and industrial French dry sausages. Sci Aliment19 (2):247-254.
Öztürk İ (2013). Geleneksel fermente sucuklardan izole edilen mayaların tanımlanması, teknolojik ve fonksiyonel özelliklerinin belirlenmesi ve sucuk üretimine uygun izolatların seçilmesi. Doktora Tez. Erciyes Üniversitesi Fen Bilimleri Enstitüsü, Kayseri. (in Turkish)
Parente E, Martuscelli M, Gardini F, Grieco S, Crudele MA, Suzzi G (2001). Evolution of microbial populations and biogenic amine production in dry sausages produced in southern Italy. J Appl Microbiol 90:882-891.
Ruiz-Moyano S, Martin A, Benito MJ, Casquete R, Serradilla MJ, De Guía Córdoba M (2009). Safety and functional aspects of pre-selected lactobacilli for probiotic use in Iberian dry-fermented sausages. Meat Sci 83 (3): 460-467.
Shalaby AR (1996). Significance of biogenic amines to food safety and human health. Food Res Int29 (7): 675-690.
Silla-Santos MH (1998). Amino acid decarboxylase capability of microorganisms isolated in Spanish fermented meat products. Int J Food Microbiol 39: 227-230.
Silla-Santos MH (1996). Biogenic amines: Their Importance in Foods. IntJ Food Microbiol29: 213-231.
Sohrabvandi S, Mortazavian AM, Rezaei K(2012). Health-Related Aspects of Beer: A Review. Int J Food Prop 15: 350-373.
Straub BW, Kicherer M, Schilcher SM, Hammes WP(1995). The formation of biogenic amines by fermentation organisms. Z LebensUntersF201(1): 79-82.
Şenöz B, Işıklı N, Çoksöyler N (2000). Biogenic amines in Turkish sausages (Sucuks). J Food Sci65:764-767.
Ten Brink B, Damink C, Joosten HMLJ,Huisintveld JHJ (1990). Occurrence and formation of biologically active amines in foods. Int J Food Microbiol11: 73-84.
Vidal-Carou MC, Veciana-Nogues T, Latorre-Moratalla ML, Bover-Cid S(2007). Biogenic amines: risks and control. Handbook of fermented meat and poultry. Blackwell Publishing.
Villani F, Casaburi A, Pennacchia C, Filosa L, Russo F, Ercolini D (2007). Microbial ecology of the soppressata of Vallo di Diano, a traditional dry fermented sausage from southern Italy, and in vitro and in situ selection ofautochthonous starter cultures. Appl Environ Microbiol 73 (17): 5453-5463.
Most read articles by the same author(s)