Abstract
This study addresses the application of native, multiple strain starter cultures for standardization of game meat sausages production. The designed starter cultures consisting of two indigenous Lactobacillus sakei and one Leuconostoc mesenteroides strains. These strains were used in both, the encapsulated and non-encapsulated form, in the game meat dough, individually or in combination, with eight treatments in total. Microbiological and physicochemical characteristics of the sausages were monitored throughout the manufacturing process, while sensory properties, biogenic amine content, and volatile compounds were evaluated in the final products. As revealed by rep-PCR, native starter cultures, encapsulated or non-encapsulated, had survived the whole sausage production process; however, to varying degrees. The application of indigenous decarboxylase negative Lb. sakei strains significantly (P < 0.05) reduced tyramine content, rapidly decreased pH and promoted the number reduction of Enterobacteriaceae and elimination of E. coli, L. monocytogenes and coliforms in ready-to-eat products. A total of 84 volatile compounds were identified by SPME–GC–MS in the eight treatment batches of game meat sausages, with only minor differences between the treatments. No significant differences in sensory traits (P > 0.05) between tested treatments were found, although treatment with the Lb. sakei strains received the highest scores for the sensory traits including cross-section, odour, hardness, aroma, and overall acceptability. Combination of multi-strain Lb. sakei starter cultures resulted in growth prevention of undesirable microbiota, reduction of tyramine content and increased the acceptability parameters of full-ripened sausages, which make them good candidates for industrial as well as artisanal application.
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References
Abd El-Salam MH, El-Shibiny S (2015) Preparation and properties of milk proteins-based encapsulated probiotics: a review. Dairy Sci Techol 95:393–412. https://doi.org/10.1007/s13594-015-0223-8
Adams RP (2007) Identification of essential oil components by gas chromatography/mass spectrometry, 4th edn. Allured Publishing Corporation, Carol Stream
Ammor MS, Mayo B (2007) Selection criteria for lactic acid bacteria to be used as functional starter cultures in dry sausage production: an update. Meat Sci 76:138–146. https://doi.org/10.1016/j.meatsci.2006.10.022
Danilović B, Joković N, Petrović L, Veljović K, Tolinački M, Savić D (2011) The characterisation of lactic acid bacteria during the fermentation of an artisan Serbian sausage (Petrovská Klobása). Meat Sci 88:668–674. https://doi.org/10.1016/j.meatsci.2011.02.026
De Prisco A, van Valenberg HJ, Fogliano V, Mauriello G (2017) Microencapsulated starter culture during yoghurt manufacturing, effect on technological features. Food Bioproc Technol 10:1767–1777. https://doi.org/10.1007/s11947-017-1946-8
Di Cello F, Bevivino A, Chiarini L, Fani R, Paffetti D, Tabacchioni S, Dalmastri C (1997) Biodiversity of a Burkholderia cepacia population isolated from the maize rhizosphere at different plant growth stages. Appl Environ Microb 63:4485–4493
Domig KJ, Kiss H, Petricevic L, Viernstein H, Unger F, Kneifel W (2014) Strategies for the evaluation and selection of potential vaginal probiotics from human sources: an exemplary study. Benef Microbes 5:263–272. https://doi.org/10.3920/BM2013.0069
Eerola S, Hinkkanen R, Lindfors E, Hirvi T (1993) Liquid chromatographic determination of biogenic amines in dry sausages. J AOAC Int 76:575–577
Elias M, Potes ME, Roseiro LC, Santos C, Gomes A, Agulheiro-Santos AC (2014) The effect of starter cultures on the portuguese traditional sausage “Paio do Alentejo” in terms of its sensory and textural characteristics and polycyclic aromatic hydrocarbons profile. J Food Res 3:45–56. https://doi.org/10.5539/jfr.v3n3p45
Frece J, Kovačević D, Kazazić S, Mrvcić J, Vahčić N, Ježek D, Hruškar M, Babić I, Markov K (2014) Comparison of sensory properties, shelf-life and microbiological safety of industrial sausages produced with autochthonous and commercial starter cultures. Food Technol Biotechnol 52:307–316
García C, Rendueles M, Díaz M (2019) Liquid-phase food fermentations with microbial consortia involving lactic acid bacteria: a review. Food Res Int 119:207–220. https://doi.org/10.1016/j.foodres.2019.01.043
Hartemink R, Domenech VR, Rombouts FM (1997) LAMVAB—A new selective medium for the isolation of lactobacilli from faeces. J Microbiol Methods 29:77–84. https://doi.org/10.1016/S0167-7012(97)00025-0
Heidebach T, Först P, Kulozik U (2012) Microencapsulation of probiotic cells for food applications. Crit Rev Food Sci Nutr 52:291–311. https://doi.org/10.1080/10408398.2010.499801
HPA (2009) Guidelines for assessing the microbiological safety of ready-to-eat foods placed on the market. Health Protection Agency, London
ISO 11290-1:1996/Amd 1 (2004) Microbiology of food and animal feeding stuffs—horizontal method for the detection and enumeration of Listeria monocytogenes—part 1: detection method—amendment 1: modification of the isolation media and the haemolysis test, and inclusion of precision data. International Organization for Standardization, Geneva
ISO 6579:2002/Amd 1 (2007) Microbiology of food and animal feeding stuffs—horizontal method for the detection of Salmonella spp.—Amendment 1: annex D: detection of Salmonella spp. in animal faeces and in environmental samples from the primary production stage. International Organization for Standardization, Geneva
ISO 4832 (2006) Microbiology of food and animal feeding stuffs—horizontal method for the enumeration of coliforms—colony-count technique. International Organization for Standardization, Geneva
ISO 21527-2 (2008) Microbiology of food and animal feeding stuffs—horizontal method for the enumeration of yeasts and moulds—part 2: colony count technique in products with water activity less than or equal to 0.95. International Organization for Standardization, Geneva
ISO 21528-2 (2004) Microbiology of food and animal feeding stuffs—horizontal methods for the detection and enumeration of Enterobacteriaceae—part 2: colony-count method. International Organization for Standardization, Geneva
Kavitake D, Kandasamy S, Devi PB, Shetty PH (2018) Recent developments on encapsulation of lactic acid bacteria as potential starter culture in fermented foods—a review. Food Biosci 21:34–44. https://doi.org/10.1016/j.fbio.2017.11.003
Khosravi Zanjani MA, Tarzi BG, Sharifan A, Mohammadi N (2014) Microencapsulation of probiotics by calcium alginate-gelatinized starch with chitosan coating and evaluation of survival in simulated human gastro-intestinal condition. Iran J Pharm Res 13:843–852
Kos I, Zgomba Maksimovic A, Zunabovic-Pichler M, Mayrhofer S, Domig KJ, Mrkonjic Fuka M (2019) The influence of meat batter and sausage diameter on microbiota and sensory traits of artisanal wild boar meat sausages. Food Technol Biotechnol 57:378–387. https://doi.org/10.17113/ftb.57.03.19.6197
Kozačinski L, Zdolec N, Hadžiosmanović M, Cvrtila Ž, Filipović I, Majić T (2006) Microbial flora of the Croatian traditionally fermented sausage. Arch Lebensmittelhyg 57:141–147
Lorenzo JM, Carballo J, Franco D (2013) Effect of the inclusion of chestnut in the finishing diet on volatile compounds of dry-cured ham from celta pig breed. J Integr Agric 12:2002–2012. https://doi.org/10.1016/S2095-3119(13)60638-3
Lorenzo JM, Gómez M, Purriños L, Fonseca S (2016) Effect of commercial starter cultures on volatile compound profile and sensory characteristics of dry-cured foal sausage. J Sci Food Agric 96(4):1194–1201. https://doi.org/10.1002/jsfa.7203
Lücke FK (2000) Utilization of microbes to process and preserve meat. Meat Sci 56:105–115. https://doi.org/10.1016/S0309-1740(00)00029-2
Mrkonjic Fuka M, Tanuwidjaja I, Zgomba Maksimovic A, Zunabovic-Pichler M, Kublik S, Hulak N, Domig KJ, Schloter M (2020) Bacterial diversity of naturally fermented game meat sausages: sources of new starter cultures. LWT Food Sci Technol 118:108782. https://doi.org/10.1016/j.lwt.2019.108782
Olivares A, Navarro JL, Flores M (2015) Characterization of volatile compounds responsible for the aroma in naturally fermented sausages by gas chromatography-olfactometry. Food Sci Technol Int 21:110–123. https://doi.org/10.1177/1082013213515500
Oliveira M, Ferreira V, Magalhães R, Teixeira P (2018) Biocontrol strategies for Mediterranean-style fermented sausages. Food Res Int 103:438–449. https://doi.org/10.1016/j.foodres.2017.10.048
Palavecino Prpich NZ, Castro MP, Cayré ME, Garro OA, Vignolo GM (2015) Autochthonous starter culture selection to keep traditions in the manufacture of dry sausages alive. Ann Microbiol 65:1709–1719. https://doi.org/10.1007/s13213-014-1010-0
Petričević S, Marušić Radovčić N, Lukić K, Listeš E, Medić H (2018) Differentiation of dry-cured hams from different processing methods by means of volatile compounds, physico-chemical and sensory analysis. Meat Sci 137:217–227. https://doi.org/10.1016/j.meatsci.2017.12.001
Pham AJ, Schilling MW, Mikel WB, Williams JB, Martin JM, Coggins PC (2008) Relationships between sensory descriptors, consumer acceptability and volatile flavor compounds of American dry-cured ham. Meat Sci 80:728–737. https://doi.org/10.1016/j.meatsci.2008.03.015
Román S, Sánchez-Siles LM, Siegrist M (2017) The importance of food naturalness for consumers: results of a systematic review. Trends Food Sci Technol 67:44–57. https://doi.org/10.1016/j.tifs.2017.06.010
Vinceković M, Jalšenjak N, Topolovec-Pintarić S, Dermić E, Bujan M, Jurić S (2016) Encapsulation of biological and chemical agents for plant nutrition and protection: chitosan/alginate microcapsules loaded with copper cations and Trichoderma viride. J Agric Food Chem 64:8073–8083. https://doi.org/10.1021/acs.jafc.6b02879
Zagorec M, Champomier-Vergès MC (2017) Lactobacillus sakei: a starter for sausage fermentation, a protective culture for meat products. Microorganisms 5:56. https://doi.org/10.3390/microorganisms5030056
Žgomba Maksimović A, Zunabovic-Pichler M, Kos I, Mayrhofer S, Hulak N, Domig KJ, Mrkonjić Fuka M (2018) Microbiological hazards and potential of spontaneously fermented game meat sausages: a focus on lactic acid bacteria diversity. LWT Food Sci Technol 89:418–426. https://doi.org/10.1016/j.lwt.2017.11.017
Acknowledgements
We thank Melita Bačić and Mateja Pećina for technical assistance with samples manipulation.
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This work was supported by the Croatian Science Foundation (miCROgame UIP-11-20136640).
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Mrkonjic Fuka, M., Zgomba Maksimovic, A., Hulak, N. et al. The survival rate and efficiency of non-encapsulated and encapsulated native starter cultures to improve the quality of artisanal game meat sausages. J Food Sci Technol 58, 710–719 (2021). https://doi.org/10.1007/s13197-020-04587-z
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DOI: https://doi.org/10.1007/s13197-020-04587-z