EFFECT OF ENCAPSULATED STARTER CULTURE INCLUSION AND HEAT TREATMENT ON BIOGENIC AMINES CONTENT OF SUCUK

In this study, the effect of encapsulated starter culture (Lactobacillus plantarum plus Staphylococcus xylosus) inclusion on biogenic amines (BAs) content of sucuk was investigated comparatively in heat treated (at ~70 °C for 20 min) and fermented sucuks. The highest contents of histamine, which is known as the most toxic BA, were observed in the fermented samples including nonencapsulated (103.6 mg/kg) and encapsulated (102.3 mg/kg) starter cultures, while the lowest values were detected in the heat treated sucuks (p < .05), including non-encapsulated (24.2 mg/kg) and encapsulated (21.4 mg/kg) starter cultures, at the end of 45 days of storage. Based on the principal component analysis of the microbiological count and BAs content of the samples, the heat treated and encapsulated starter culture included sucuks discriminated themselves from control groups and non-encapsulated encapsulated starter culture included samples with lower histamine and tyramine contents as well as their microbiological loads.

PDF

___

Ansorena, D., Montel, M., Rokka, M., Talon, R., Eerola, S., Rizzo, A., Demeyer, D. (2002). Analysis of biogenic amines in northern and southern European sausages and role of flora in amine production. Meat Science, 61, 141-147. https://doi.org/10.1016/S0309-1740(01)00174-7

Bardócz, S. (1995). Polyamines in food and their consequences for food quality and human health. Trends in Food Science and Technology, 6, 341-346. https://doi.org/10.1016/S0924-2244(00)89169-4

Bilenler, T., Karabulut, I., Candogan, K. (2017). Effects of encapsulated starter cultures on microbial and physicochemical properties of traditionally produced and heat treated sausages (sucuks). LWT -Food Science and Technology, 75, 425- 433. https://doi.org/10.1016/j.lwt.2016.09.003

Bover-Cid, S., Izquierdo-Pulido, M., Vidal-Carou, M.C. (1999). Effect of proteolytic starter cultures of Staphylococcus spp. on biogenic amine formation during the ripening of dry fermented sausages. International Journal of Food Microbiology, 46, 95-104. https://doi.org/10.1016/S0168-1605(98)00170-6

Bover-Cid, S., Izquierdo-Pulido, M., Vidal-Carou, M.C. (2000). Mixed starter cultures to control biogenic amine production in dry fermented sausages. Journal of Food Protection, 63, 1556-1562. https://doi.org/10.4315/0362-028X-63.11.1556 PMid:11079700

Bover-Cid, S., Miguélez-Arrizado, M.J., Becker, B., Holzapfel, W.H., Vidal-Carou, M.C. (2008). Amino acid decarboxylation by Lactobacillus curvatus CTC273 affected by the pH and glucose availability. Food Microbiology, 25, 269- 277. https://doi.org/10.1016/j.fm.2007.10.013 PMid:18206769

Bozkurt, H., Erkmen, O. (2002). Effects of starter cultures and additives on the quality of Turkish style sausage (sucuk). Meat Science, 61, 149-156. https://doi.org/10.1016/S0309-1740(01)00176-0

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 Science and Technology International, 10, 21-28. https://doi.org/10.1177/1082013204041992

Corbo, M.R., Bevilacqua, A., Speranza, B., Di Maggio, B., Gallo, M., Sinigaglia, M. (2016). Use of alginate beads as carriers for lactic acid bacteria in a structured system and preliminary validation in a meat product. Meat Science, 111, 198-203. https://doi.org/10.1016/j.meatsci.2015.10.005 PMid:26476507

Dalmış, Ü., Soyer, A. (2008). Effect of processing methods and starter culture (Staphylococcus xylosus and Pediococcus pentosaceus) on proteolytic changes in Turkish sausages (sucuk) during ripening and storage. Meat Science, 80, 345- 354. https://doi.org/10.1016/j.meatsci.2007.12.022 PMid:22063339

De Prisco, A., Mauriello, G. (2016). Probiotication of foods: A focus on microencapsulation tool. Trends in Food Science and Technology, 48, 27-39. https://doi.org/10.1016/j.tifs.2015.11.009

Eerola, S., Hinkkanen, R., Lindfors, E., Hirvi, T. (1993). Liquid chromatographic determination of biogenic amines in dry sausages. Journal of AOAC International, 76, 575-577.

Ercoşkun, H., Tağı, Ş., Ertaş, A.H. (2010). The effect of different fermentation intervals on the quality characteristics of heat-treated and traditional sucuks. Meat Science, 85, 174- 181. https://doi.org/10.1016/j.meatsci.2009.12.022 PMid:20374882

Galgano, F., Favati, F., Bonadio, M., Lorusso, V., Romano, P. (2009). Role of biogenic amines as index of freshness in beef meat packed with different biopolymeric materials. Food Research International, 42, 1147-1152. https://doi.org/10.1016/j.foodres.2009.05.012

Gardini, F., Özogul, Y., Suzzi, G., Tabanelli, G., Özogul, F. (2016). Technological factors affecting biogenic amine content in foods: a review. Frontiers in Microbiology, 7, 1218. https://doi.org/10.3389/fmicb.2016.01218 PMid:27570519 PMCid:PMC4982241

Gençcelep, H., Kaban, G., Kaya, M. (2007). Effects of starter cultures and nitrite levels on formation of biogenic amines in sucuk. Meat Science, 77, 424-430. https://doi.org/10.1016/j.meatsci.2007.04.018 PMid:22061796

Gençcelep, H., Kaban, G., Aksu, M.İ., Öz, F., Kaya, M. (2008). Determination of biogenic amines in sucuk. Food Control, 19, 868-872. https://doi.org/10.1016/j.foodcont.2007.08.013

Hernández-Jover, T., Izquierdo-Pulido, M., VecianaNogués, M. T., Mariné-Font, A., Vidal-Carou, M. C. (1997). Biogenic amine and polyamine contents in meat and meat products. Journal of Agricultural and Food Chemistry, 45, 2098-2102. https://doi.org/10.1021/jf960790p

Jairath, G., Singh, P. K., Dabur, R. S., Rani, M., Chaudhari, M. (2015). Biogenic amines in meat and meat products and its public health significance: a review. Journal of Food Science and Technology, 52, 6835-6846. https://doi.org/10.1007/s13197-015-1860-x

Kaban, G., Kaya, M. (2009). Effects of Lactobacillus plantarum and Staphylococcus xylosus on the quality characteristics of dry fermented sausage "Sucuk". Journal of Food Science, 74, 58-63. https://doi.org/10.1111/j.1750-3841.2008.01014.x PMid:19200122

Kailasapathy, K. (2002). Microencapsulation of probiotic bacteria: technology and potential applications. Current Issues in Intestinal Microbiology, 3, 39-48.

Kaniou, I., Samouris, G., Mouratidou, T., Eleftheriadou, A., Zantopoulos, N. (2001). Determination of biogenic amines in fresh unpacked and vacuum-packed beef during storage at 4°C. Food Chemistry, 74, 515-519. https://doi.org/10.1016/S0308-8146(01)00172-8

Kurt, Ş., Zorba, Ö. (2009). The effects of ripening period, nitrite level and heat treatment on biogenic amine formation of "sucuk" - a Turkish dry fermented sausage. Meat Science, 82, 179-184. https://doi.org/10.1016/j.meatsci.2009.01.008 PMid:20416765

Kurt, Ş., Zorba, Ö. (2010). Biogenic amine formation in Turkish dry fermented sausage (sucuk) as affected by nisin and nitrite. Journal of the Science of Food and Agriculture, 90, 2669-2674. https://doi.org/10.1002/jsfa.4138 PMid:20740550

Latorre-Moratalla, M.L., Bover-Cid, S., Talon, R., Garriga, M., Zanardi, E., Ianieri, A., Vidal-Carou, M.C. (2010). Strategies to reduce biogenic amine accumulation in traditional sausage manufacturing. LWT-Food Science and Technology, 43, 20-25. https://doi.org/10.1016/j.lwt.2009.06.018

Leroy, F., Verluyten, J., De Vuyst, L. (2006). Functional meat starter cultures for improved sausage fermentation. International Journal of Food Microbiology, 106, 270-285. https://doi.org/10.1016/j.ijfoodmicro.2005.06.027 PMid:16213053

Martín, M.J., Lara-Villoslada, F., Ruiz, M.A., Morales, M.E. (2015). Microencapsulation of bacteria: a review of different technologies and their impact on the probiotic effects. Innovative Food Science and Emerging Technologies, 27, 15- 25. https://doi.org/10.1016/j.ifset.2014.09.010

Papavergou, E.J. (2011). Biogenic amine levels in dry fermented sausages produced and sold in Greece. Procedia Food Science, 1, 1126-1131. https://doi.org/10.1016/j.profoo.2011.09.168

Rabie, M.A., Peres, C., Malcata, F.X. (2014). Evolution of amino acids and biogenic amines throughout storage in sausages made of horse, beef and turkey meats. Meat Science, 96, 82-87. https://doi.org/10.1016/j.meatsci.2013.05.042 PMid:23896140

Ravyts, F., Vuyst, L. De, Leroy, F. (2012). Bacterial diversity and functionalities in food fermentations. Engineering in Life Sciences, 12, 356-367. https://doi.org/10.1002/elsc.201100119

Ruiz-Capillas, C., Jiménez-Colmenero, F. (2004). Biogenic amines in meat and meat products. Critical Reviews in Food Science and Nutrition, 44, 489-499. https://doi.org/10.1080/10408690490489341

Ruiz-Capillas, C., Jiménez Colmenero, F., Carrascosa, A.V., Muñoz, R. (2007). Biogenic amine production in Spanish dry-cured "chorizo" sausage treated with high-pressure and kept in chilled storage. Meat Science, 77, 365-371.

https://doi.org/10.1016/j.meatsci.2007.03.027 PMid:22061789

Santos, M.H.S. (1998). Amino acid decarboxylase capability of microorganizms isolated in Spain fermented meat product. International Journal of Food Microbiology, 29, 227-230. https://doi.org/10.1016/S0168-1605(97)00129-3 Scientific Opinion on risk based control of biogenic amine formation in fermented foods (2011). EFSA Journal, 9, 2393. https://doi.org/10.2903/j.efsa.2011.2393

Soyer, A., Ertaş, A.H., Üzümcüoğlu, Ü. (2005). Effect of processing conditions on the quality of naturally fermented Turkish sausages (sucuks). Meat Science, 69, 135-141. https://doi.org/10.1016/j.meatsci.2004.06.015 PMid:22062649

Sultana, K., Godward, G., Reynolds, N., Arumugaswamy, R., Peiris, P., Kailasapathy, K. (2000). Encapsulation of probiotic bacteria with alginate-starch and evaluation of survival in simulated gastrointestinal conditions and in yoghurt. International Journal of Food Microbiology, 62, 47-55. https://doi.org/10.1016/S0168-1605(00)00380-9

Sun, X., Zhou, K., Gong, Y., Zhang, N., Yang, M., Qing, D., Yang, Y. (2016). Determination of biogenic amines in Sichuanstyle spontaneously fermented sausages. Food Analytical Methods, 9, 2299-2307. https://doi.org/10.1007/s12161-016-0417-6

Suzzi, G., Gardini, F. (2003). Biogenic amines in dry fermented sausages: a review. International Journal of Food Microbiology, 88, 41-54. https://doi.org/10.1016/S0168-1605(03)00080-1

Tabanelli, G., Coloretti, F., Chiavari, C., Grazia, L., Lanciotti, R., Gardini, F. (2012). Effects of starter cultures and fermentation climate on the properties of two types of typical Italian dry fermented sausages produced under industrial conditions. Food Control, 26, 416-426. https://doi.org/10.1016/j.foodcont.2012.01.049