Abstract

Propionic-acid bacteria and bifidobacteria are widely used in food industry. Therefore, it is important to determine their biochemical activity and their aroma producing potential. In this study, the effect of the use of propionibacteria and bifidobacteria as starter cultures on the sensory characteristics of raw smoked sausages has been studied. The sausages were prepared with starter culture consisted of Propionibacterium shermanii KM-186 and Bifidobacterium longum B379M and compared with the sausages with a commercial starter culture Bitec LS-25. The results have shown, that the sausages containing starter culture of propionic-acid and bifidobacteria, obtained better sensory scores, better quality characteristics compared to the sausages made with commercial starter culture. The analysis of volatile compounds has shown, that the addition of starter culture, containing propionic-acid bacteria and bifidobacteria leads to formation of additional compounds, including lactones, phenols, and terpenes. During sensory evaluation, experts noticed the presence of mild creamy note in experimental sample. It can be the result of lactones formation by propionic-acid bacteria and bifidobacteria. In addition, it was shown that the addition of propionic-acid bacteria and bifidobacteria reduces nitrite amount in sausages in several times (11 times approximately compared to commercial starter culture) due to nitroreductase activity of these bacterial strains.

Keywords

Raw smoked sausages, propionic-acid bacteria, bifidobacteria, starter cultures, volatile compounds, flavor, sausages

REFERENCES

1. Hui Y.H., Nip W.-K., Rogers R.W., and Young O.A. Meat Science and Applications. New York: Marcel Dekker, 2001. n. p.
2. Lücke F.K. Fermented sausages. In: Wood B.J.B. (ed.) Microbiology of fermented foods. London: Elsevier Applied Science, 1985, vol. 2, p. 41.
3. Incze K. Raw fermented and dried meat products. Fleischwirtschaft, 1992, vol. 72, pp. 58-62.
4. Berdagué J.L., Monteil P., Montel M.C., and Talon R. Effects of Starter Cultures on the Formation of Flavour Compounds in Dry Sausage. Meat Science, 1993, vol. 35, no. 3, pp. 275-287. DOI: 10.1016/0309-1740(93)90033-E.
5. Nieto-Lozano J.C., Reguera-Useros J.I., Peláez-Martínez M.C., and Hardisson de la Torre A. Bacteriocinogenic activity from starter cultures used in Spanish meat industry. Meat Science, 2002, vol. 62, no. 2, pp. 237-243. DOI: http://doi.org/10.1016/S0309-1740(01)00252-2.
6. Tabanelli G., Coloretti F., Chiavari C., et al. 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, 2012, vol. 26, no. 2, pp. 416-426. DOI: http://doi.org/10.1016/j.foodcont.2012.01.049.
7. Park H.S., Reinbold G.W., Hammond E.G., and Clark W.S. Growth of propionibacteria at low temperatures. Journal of Dairy Science, 1967, vol. 50, no. 4, pp. 589-591. DOI: 10.3168/jds.S0022-0302(67)87474-5.
8. Fernández-López J., Viuda-Martos M., Sendra E., et al. Orange fibre as potential functional ingredient for dry-cured-sausage. European Food Research Technology, 2007, vol. 226, pp. 1-6. DOI: 10.1007/s00217-006-0501-z.
9. Casquete R., Benito M.J., Martin A., et al. Use of Autochthonous Pediococcus acidilactici and Staphylococcus vitulus Starter Cultures in the Production of “Chorizo” in 2 Different Traditional Industries. Food Science, 2012, vol. 71, pp. 70-79.
10. Vorobjeva L.I. Propionibacteria. Springer Netherlands Publ., 1999, 281 p. DOI: 10.1007/978-94-017-2803-4.
11. Hettinga D.H. ande Reinbold G.W. The propionic acid bacteria. A review. Journal of Milk and Food Technology, 1972, vol. 35, pp. 295-301, pp. 358-372, pp. 436-447.
12. Frohlich-Wyder M.T. and Bachmann H.P. Cheeses with propionic acid fermentation. In: Fox PF., McSweeney P.L.H., Cogan T.M., and Guinee T.P. (eds). Cheese chemistry, physics and microbiology, vol. 1. General aspects. London: Elsevier Publ., 2004, pp. 141-156.
13. Boyaval P., Deborde C., Corre C., Blanco C., and Begue E. Stress and osmoprotection in propionibacteria. Lait, 1999, vol. 79, pp. 59-69.
14. Langsrud T. and Reinbold G.W. Flavour development and microbiology of Swiss cheese. A review. II Starters, manufacturing process and procedure. Journal of Milk and Food Technology, 1973, vol. 11, pp. 531-542.
15. Richoux R., Faivre E., and Kerjean J.R. Effet de la teneur en NaCl sur la fermentation du lactate par Propionibacterium freudenreichii dans des minifromages a` pate cuite. Lait, 1998, vol. 78, pp. 319-331.
16. Field M.F. and Lichstein H.C. Factors affecting the growth of propionibacteria. Journal of Bacteriology, 1957, vol. 73, no. 1, pp. 96-99.
17. Kurtz F.E., Hupfer J.A., Corbin E.A., Hargrove R.F., and Walter H.E. Interrelationships between pH, populations of Propionibacterium shermanii, levels of free fatty acids, and the flavour ratings of Swiss cheeses. Journal of Dairy Science, 1959, vol. 42, no. 6, pp. 1008-1019. DOI: 10.3168/jds.S0022-0302(59)90684-8.
18. Thierry A., Deutsch M.S., Falentin H., et al. New insights into physiology and metabolism of Propionibacterium freudenreichii. International Journal of Food Microbiology, 2011, vol. 149, no. 1, pp. 19-27. DOI: http://doi.org/10.1016/j.ijfoodmicro.2011.04.026.
19. Thierry A., Falentin H., Deutsch S.M., and Jan G. Propionibacterium. spp. In: Fuquay J.W., Fox P.F., McSweeney P.L.H. Encyclopedia of Dairy Sciences. 2nd edn. Academic Press, 2011, pp. 403-411.
20. Dupuis C., Corre C., and Boyaval P. Proteinase activity of dairy Propionibacterium. Applied Microbiology and Biotechnology, 1995, vol. 42, no. 5, pp. 750-755. DOI: 10.1007/BF00171957.
21. Searles M.A., Argyle P.J., Chandan R.C., and Gordon J.F. Lipolytic and proteolytic activities of lactic cultures. XXVIII International Dairy Congress. Australia, Sydney, 1970, vol. 1, p. 111.
22. El-Soda M, Ziada N., and Ezzat N. The intracellular peptidehydrolase system of Propionibacterium. Microbios., 1992, vol. 72, pp. 65-74.
23. Sahlström S., Espinoza C., Langsrud R., and Sørhaug T. Cell wall membrane and intracellular peptidase activities of Propionibacterium shermanii, Journal of Dairy Science, 1989, vol. 72, no. 2, pp. 342-350. DOI: https://doi.org/10.3168/jds.S0022-0302(89)79115-3.
24. Langsrud T., Sorhaug T., and Vegarud G.E. Protein degradation and amino acid metabolism by propionibacteria. Le Lait, 1975, vol. 75, pp. 325-330.
25. Perez Chaia A., Pesce de Ruiz Hoigado A., and Oliver G. Peptide hydrolases of propionibacteria: effect of pH and temperature. Journal of Food Protection, 1990, vol. 53, no. 3, pp. 237-240. DOI: http://dx.doi.org/10.4315/0362-028X-53.3.237.
26. Panon G. Purification and characterization of a proline aminopeptidase from Propionibacterium shermanii ATCC 13673. Lait, 1990, vol. 70, pp. 439-452.
27. Thierry A., Maillard M.B., Bonnarme P., and Roussel E. The addition of Propionibacterium freudenreichii to Raclette cheese induces biochemical changes and enhances flavour development. Journal of Agricultural and Food Chemistry, 2005, vol. 53, no. 10, pp. 4157-4165. DOI: 10.1021/jf0481195.
28. Thierry A., Maillard M.B., Hervé C., et al. Varied volatile compounds are produced by Propionibacterium freudenreichii in Emmental cheese. Food Chemistry, 2004, vol. 87, no. 3, pp. 439-446. DOI: https://doi.org/10.1016/j.foodchem.2003.12.018.
29. Holkoa I., Hraběa J., Šalakováb A., and Radac V. The substitution of a traditional starter culture in mutton fermented sausages by Lactobacillus acidophilus and Bifidobacterium animalis. Meat Science, 2013, no. 3, vol. 94, pp. 275-279. DOI: https://doi.org/10.1016/j.meatsci.2013.03.005.
30. Rouhi M., Sohrabvandi S., Mortazavian A.M. Probiotic Fermented Sausage: Viability of Probiotic Microorganisms and Sensory Characteristics. Critical Reviews in Food Science and Nutrition, 2013, vol. 53, no. 4, pp. 331-348. DOI: http://dx.doi.org/10.1080/10408398.2010.531407.
31. Picard C., Fioramonti J., Francois A., et al. Review article: bifidobacteria as probiotic agents - physiological effects and clinical benefits. Alimentary Pharmacology & Therapeutics, 2005, vol. 22, no. 6, pp. 495-512.
32. Ashraf R. and Shah N.P. Immune system stimulation by probiotic microorganisms. Critical Reviews in Food Science and Nutrition, 2014, vol. 54, no. 7, pp. 938-956. DOI: http://dx.doi.org/10.1080/10408398.2011.619671.
33. Misharina T.A., Terenina M.B., Krikunova N.I., et al. The influence of starter cultures on the formation of volatile compounds in dry smoked sausages. Applied Biochemistry and Microbiology, 2008, vol. 44, no. 5, pp. 545-550. DOI: 10.1134/S0003683808050165.
34. Vorobjeva L.I., Khodjaev E.Yu., and Vorobjeva N.V. Propionic acid bacteria as probiotics. Microbial Ecology in Health and Disease, 2008, vol. 20, no. 2, pp.109-112.
35. Swart R., Riedel K.H., and Britz T. Optimized standard conditions for determination of nitrate reduction in propionibacteria. Lait, 1998, no. 78, pp. 217-226.
36. Grill J.-P., Crociani J. and Ballongue J. Effect of bifidobacteria on nitrites and nitrosamines. Letters in Applied Microbiology, 1995, vol. 20, no. 5, pp. 328-330. DOI: 10.1111/j.1472-765X.1995.tb00456.x.
37. Sobko T., Reinders C.I., Jansson E.A., et al. Gastrointestinal bacteria generate nitric oxide from nitrate and nitrite. Nitric Oxide Biology and Chemistry, 2005, vol. 4, pp. 272-278.