EFFECT OF MIXED STARTER CULTURES ON BIOGENIC AMINE FORMATION DURING THE RIPENING OF TUNISIAN DRY FERMENTED CAMEL MEAT SAUSAGE

Main Article Content

S. EL ADAB
W. BEN WADDA
A. TEKIKI
O. BEN MOUSSA
M. BOULARES
S. SADOK
M. HASSOUNA

Keywords

biogenic amine, fermented sausages, starter cultures, quality, ripening

Abstract

The effect of mixed starter cultures on biogenic amine production was examined during the ripening process of dry camel meat sausage. Changes in pH, moisture content, proteolysis, microbial counts and lipid oxidation were also studied. The combination of three amine-negative bacteria, resulted in a drastic reduction of biogenic amine production. The highest total free amino acid concentration was observed in batches manufactured with mixed starter cultures. The bactericidal properties of L. sakei improved the hygienic quality of sausages by decreasing the number of Enterobacteriaceae. Inoculation of sausages with a mixture of strains, significantly delayed lipid oxidation and enhanced sensory characteristics.

Abstract 109 | pdf Downloads 52

References

Ahn J., Grün I. and Fernando L. 2002. Antioxidant properties of natural plant extracts containing polyphenolic compounds in cooked ground beef. J. Food Sci. 67:1364-1369.

Baka A.M., Papavergou E.J., Pragalaki T., Bloukas J.G. and Kotzekidou P. 2011. Effect of selected autochthonous starter cultures on processing and quality characteristics of Greek fermented sausages. Food Sci. Technol. 44:54-61.

Boulares M., Mankai M., Sadok S. and Hassouna M. 2017. Anti-Listerial inhibitory lactic acid bacteria in fresh farmed sea bass (Dicentrarchus labrax) fillets during storage at 4 °C under vacuum-packed conditions. J. Food Safety. 37:1-14.

Bourne M.C. 1978. Texture profile analysis. Food Technol. 32: 72.

Bover-Cid S., Izquierdo-Pulido M. and Vidal-Carou M.C. 1999. Effect of proteolytic starter cultures of Staphylococcus spp. on the biogenic amine formation during the ripening of dry fermented sausages. Inter. J. Food Microbiol. 46: 95-104.

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

Bover-Cid S., Izquierdo-Pulido M. and Carmen Vidal-Carou M. 2001. Changes in biogenic amine and polyamine contents in slightly fermented sausages manufactured with and without sugar. Meat Sci. 57: 215-221.

Bozkurt H. and Erkmen O. 2002. Effects of starter cultures and additives on the quality of Turkish style sausage (Sucuk). Meat Sci. 61:149-156.

Bozkurt H. and Bayram M. 2006. Colour and textural attributes of sucuk during ripening. Meat Sci. 73:344-350.

Chang M. and Chang H.C. 2012. Development of a screening method for biogenic amine producing Bacillus spp.Inter. J. Food Microbiol. 153:269-274.

Ciuciu S., Vizireanu A.M., Alexe C., Franco P. and Carballo J. 2014. Effect of the use of selected starter cultures on some quality, safety and sensorial properties of Dacia sausage, a traditional Romanian dry-sausage variety. Food Control. 35:123-131.

Dalla Santa O.R., Macedo R.E.F., Dalla Santa H.S., Zanette C.M., Freitas R.J.S. and Terra N.N. 2014. Use of starter cultures isolated from native microbiota of artisanal sausage in the production of Italian sausage. Food Sci. Technol. Campinas. 34:780-786.

Domínguez R., Munekata P.E., Agregán R. and Lorenzo J.M. 2016. Effect of commercial starter cultures on free amino acid, biogenic amine and free fatty acid contents in dry cured foal sausage. LWT-Food Sci. Technol. 71:47-53.

Durlu-Özkaya F., Ayhan K. and Vural N. 2001. Biogenic amines produced by Enterobacteriaceae isolated from meat products. Meat Sci. 58:163-166.

El Adab S. and Hassouna M. 2016. Proteolysis, lipolysis and sensory characteristics of a Tunisian dry fermented poultry meat sausage with oregano and thyme essential oils. J. Food Safety. 36:19-32.

Essid I. and Hassouna M. 2013. Effect of inoculation of selected Staphylococcus xylosus and Lactobacillus plantarum strains on biochemical, microbiological and textural characteristics of a Tunisian dry fermented sausage. Food Control. 32:707-714.

Folch J., Lees M. and Sloane-Stanley G. 1957. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226:497-509.

Fonseca S., Cachaldora A., Gŏmez M., Franco I. and Carballo J. 2013.nEffect of different autochthonous starter cultures on the volatile compounds profile and sensory properties of Galician chorizo, traditional Spanish dry fermented sausage. Food Control. 33:6-14.

Gençcelep H., Kaban G. and Kaya M. 2007. Effect of starter cultures and nitrite levels on formation of biogenic amines in sucuk. Meat Sci. 77:424-430.

Genot C. 1996. Some factors influencing TBA test. Report of diet-ox project (AIRIII-CT-92-1577).

Gonzalez-Fernandez C., Santos E.M., Jaime I. and Rovira J. 2003. Influence of starter cultures and sugar concentrations on biogenic amine contents in chorizo dry sausage. Food Microbiol. 20:275-284.

Gonzalez-Fernandez C., Santos E.M., Rovira J. and Jaime I. 2006. The effect of sugar concentration and starter culture on instrumental and sensory textural properties of chorizo-Spanish dry cured sausage. Meat Sci. 74:467-475.

Hamoen J.R., Vollebregt H.M. and Van der Sman R.G.M. 2013. Prediction of the time evolution of pH in meat. Food Chem. 141:2363-2372.

Herández-Jover T., Izquierdo-Pulido M., Veciana-Nogue ́s M.T., Marine-Font A. and Vidal-Carou M.C. 1997. Effect of starter cultures on biogenic amine formation during fermented sausage production. J. Food Protect. 60:825-830.

Hu Y., Xia W. and Liu X. 2007. Changes in biogenic amines in fermented silver carp sausages inoculated with mixed starter cultures. Food Chem. 104:188-195.

Huges M.C., Kerry J.P., Arendt E.K., Kenneally P.M., Mcsweeney P.L.H. and Oneill E.E. 2002. Characterization of proteolysis during the ripening of semi-dry fermented sausages. Meat Sci. 62:205-216.

ISO. 1973. Meat and meat products –determination of moisture, ISO 1442-1973 (E).

Jin G., Zhang J., Yu X., ZhangY., Lei Y. and Wang J. 2010. Lipolysis and lipid oxidation in bacon during curing and drying-ripening. Food Chem. 123:465-471.

Kadim I., Mahgoub O. and Purchas R. 2008. A review of the growth, and of the carcass and meat quality characteristics of the one-humped camel (Camelus dromedaries). Meat Sci. 80:555-569.

Kargozari M., Moini S., Basti A.A., Emam-Djomeh Z., Ghasemlou M., Martin I.R., Carbonell-Barrachina A.A. and Szumny A. 2014. Development of Turkish dry-fermented sausage (sucuk) reformulated with camel meat and hump fat and evaluation of physicochemical, textural, fatty acid and volatile compound profiles during ripening. LWT -Food Sci. Technol. 59:849-858.

Kayaardi S. and Gök V. 2003. Effect of replacing beef fat with olive oil on quality characteristics of Turkish soudjouk (sucuk). Meat Sci. 66:249-257.

Komprda T., Sladkova P. and Dohnal V. 2009. Biogenic amine content in dry fermented sausages as influenced by a producer, spice mix, starter culture, sausage diameter and time of ripening. Meat Sci. 83:534-542.

Latorre-Moratalla M.L., Bover-Cid S., Talon R., Garriga M., Aymerich T., Zanardi E., Ianieri A., Fraqueza M.J., Elias M., Drosinos E.H., Lauková A. and Vidal-Carou M.C. 2010. Distribution of aminogenic activity among potential autochthonous starter cultures. J. Food Protect.73:524-525.

Latorre-Moratalla M.L., Bover-Cid S., Bosch-Fusté J. and Vidal-Carou M.C. 2012. Influence of technological conditions of sausage fermentation on the aminogenic activity of L. curvatusCTC273. Food Microbiol. 29:43-48.

Lee Y.C., Kung H.F., Huang C.Y., Huang T.C. and Tsai Y.H. 2016. Reduction of histamine and biogenic amines during salted fish fermentation by Bacillus polymyxa as a starter culture. J. Food Drug Anal. 24:1-7.

Liaros N.G., Katsanidis E. and Bloukas J.G. 2009. Effect of ripening time under vacuum and packaging film permeability on processing and quality characteristics of low fermented sausages. Meat Sci. 83:589-598.

Lorenzo J.M., Martínez S., Franco I. and Carballo J. 2007. Biogenic amine content during the manufacture of dry-cured lacon, a Spanish traditional meat product: effect of some additives. Meat Sci. 77:287-293.

Lorenzo J.M., Eduardo P., Munekata S. and Dominguez R. 2017. Role of autochthonous starter cultures in the reduction of biogenic amines in traditional meat products. Curr.Opin. Food Sci.14:61-65.

Lu S., Xu X., Zhou G., Zhu Z., Meng Y. and Sun Y. 2010. Effect of starter cultures on microbial ecosystem and biogenic amines in fermented sausage. Food Control. 21:444-449.

Lu S., Ji H., Wang Q., Li B., Li K. and Xu C. 2014. The effects of starter cultures and plant extracts on the biogenic amine accumulation in traditional Chinese smoked horsemeat sausages. Food Control. 5:869-875.

Marine-Font A., Vidal-Carou C., Izquierdo-Pulido M., Veciana-Nogue ́s T. and Hernandez-Jover T. 1995.Les amines biogènes dans les aliments, leur signification, leur analyse. Annal. Fals. Exp. Chim. 88:119-140.

Masson F, Talon R. and Montel M. 1996. Histamine and tyramine production by bacteria from meat products. Inter. J. Food Microbiol. 32:199-207.

Mejri L., Ziadi A., El Adab S., Boulares M., Essid I. and Hassouna M. 2017. Effect of commercial starter cultures on physicochemical, microbiological and textural characteristics of a traditional dry fermented sausage reformulated with camel meat and hump fat. J. Food Meas. Charact. 11:758-767.

Nie X., Zhang Q. and Lin S. 2014. Biogenic amine accumulation in silver carp sausage inoculated with Lactobacillus plantarum plus Saccharomyces cerevisiae.Food Chem. 153:432-436.

Olivares A., Navarro J.L., Salvador A. and Flores M. 2010. Sensory acceptability of slow fermented sausages based on fat content and ripening time. Meat Sci. 86:251-257.

Perez-Alvarez J.A., Sayes-Barbare M.E., Fernandez-Lopez J. and Aranda-Catala V. 1999. Physicochemical characteristics of Spanish type dry-cured sausage. Food Res. Inter. 32:599-607.

Qinxiu S., Qian C., Fangfei L., Dongmei Z. and Baohua K. 2016. Biogenic amine inhibition and quality protection of Harbin dry sausages by inoculation with Staphylococcus xylosus and Lactobacillus plantarum. Food Control. 68:358-366.

Rabie M., Simon-Sarkadi L., Siliha H., El-seedy S. and El Badawy A.A. 2009. Changes in free amino acids and biogenic amines of Egyptian salted-fermented fish (Feseekh) during ripening and storage. Food Chem. 115:635-638.

Ravyts F., Steen L., Goemaere O., Paelinck H., De Vuyst L. and Leroy F. 2010. The application of staphylococci with flavor generating potential is affected by acidification in fermented dry sausages. Food Microbiol. 27:945-954.

Renes E., Diezhandino I., Fernandez D., Ferrazza R., Tornadijo M. and Fresno J. 2014. Effect of autochthonous starter cultures on the biogenic amine content of ewe's milk cheese throughout ripening. Food Microbiol. 44:271-277.

Rubio B., Martínez B., García-Cachán M.D., Rovira J. and Jaime I. Effect of the packaging method and the storage time on lipid oxidation and colour stability on dry fermented sausage salchichón manufactured with raw material with a high level of mono and polyunsaturated fatty acids. Meat Sci. 80:1182-1187.

Straub B.W., Kicherer M., Schilcher S.M. and Hammes W.P. 1995. The formation of biogenic amines by fermentation organisms.Z. Lebensm. Unters. For. 201:79-82.

Suzzi G. and Gardini F. 2003. Biogenic amines in dry fermented sausages: a review. Inter. J. Food Microbiol. 88:41-54.

Talon R. and Leroy S. 2011. Diversity and safety hazards of bacteria involved in meat fermentation. Meat Sci. 89:303-309.

Zhao L., JinY., Ma C., Song H., Li H., Wang Z. and Xiao S. 2011. Physico-chemical characteristics and free fatty acid composition of dry fermented mutton sausages as affected by the use of various combinations of starter cultures and spices. Meat Sci. 88:761-766.