Microbiological, biochemical, and functional aspects of sugary kefir fermentation - A review

Food Microbiology

Volumn 66, Issue , 2017, Pages 86-95

  Fiorda, Fernanda Assumpção ^a   de Melo Pereira, Gilberto Vinicius ^a   Thomaz Soccol, Vanete ^a   Rakshit, Sudip Kumar ^b   Pagnoncelli, Maria Giovana Binder ^c   Vandenberghe, Luciana Porto de Souza ^a   Soccol, Carlos Ricardo ^a  

^a FEDERAL UNIVERSITY OF PARANÁ   (Brazil)

^b LAKEHEAD UNIVERSITY   (Canada)

^c UNIVERSIDADE TECNOLÓGICA FEDERAL DO PARANÁ   (Brazil)

Author keywords

Functional products; Lactic acid bacteria; Microbial symbiosis; Probiotic; Sugary kefir

Indexed keywords

KEFIR;

ANALYSIS; ANIMAL; BUDDING YEAST; FERMENTATION; FOOD HANDLING; FUNCTIONAL FOOD; HUMAN; LACTOBACILLALES; METABOLISM; MICROBIOLOGY;

ANIMALS; FERMENTATION; FOOD HANDLING; FUNCTIONAL FOOD; HUMANS; KEFIR; LACTOBACILLALES; SACCHAROMYCETALES;

EID: 85018477243     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2017.04.004     Document Type: Review

References (87)

1. Alsayadi, M.S., Jawfi, Y.A., Belarbi, M., Sabri, F.Z., Antioxidant potency of water kefir. J. Microbiol. Biotechnol. Food Sci. 2 (2013), 2444–2447.
2. Arneborg, N., Siegumfeldt, H., Andersen, G.H., Nissen, P., Daria, V.R., Rodrigo, P.J., Glu ¨ckstad, J., Interactive optical trapping shows that confinement is a determinant of growth in a mixed yeast culture. FEMS Microbiol. Lett. 245 (2005), 155–159.
3. Beijerinck, M.W., 1889. Sur le kefir. Archives Neerlandaies des Sciences Exactes et Naturelles, Haarlem, 23, 248–258.
4. Bensmira, M., Nsabimana, C., Jiang, B., Effects of fermentation conditions and homogenization pressure on the rheological properties of kefir. LWT-Food Sci. Technol. 43 (2010), 1180–1184.
5. Bernardi, T.L., Pereira, G.V.M., Cardoso, P.G., Dias, E.S., Schwan, R.F., Saccharomyces cerevisiae strains associated with the production of cachaça: identification and characterization by traditional and molecular methods (PCR, PFGE and mtDNA-RFLP). World J. Microbiol. Biotechnol. 24 (2008), 2705–2712.
6. Blaiotta, G., Capua, M.D., Romano, A., Coppola, R., Aponte, M., Optimization of water curing for the preservation of chestnuts (Castanea sativa Mill.) and evaluation of microbial dynamics during process. Food Microbiol. 42 (2014), 47–55.
7. Cetinkaya, F., Elal-Mus, T., Determination of microbiological and chemical char- acteristics of kefir consumed in Bursa. Ankara Üniversitesi Veteriner Fakültesi Dergisi (Vet. J. Ankara Univ.) 59 (2012), 217–221.
8. Chen, H.C., Wang, S.Y., Chen, M.J., Microbiological study of lactic acid bacteria in kefir grains by culture-dependent and culture-independent methods. Food Microbiol. 25 (2008), 492–501.
9. Corona, O., Randazzo, W., Miceli, A., Guarcello, R., Francesca, N., Erten, H., Moschetti, G., Settanni, L., Characterization of kefir-like beverages produced from vegetable juices. LWT - Food Sci. Technol. 66 (2016), 572–581.
10. Daker, W.D., Stacey, M., Investigation of a polysaccharide produced from sucrose by beta- bacterium vermiforme (ward-meyer). Biochem. J. 36 (1938), 1946–1948.
11. Davidovic, S.Z., Miljkovic, M.G., Antonovic, D.G., Rajilic-Stojanovic, M.D., Dimitrijevic-Brankovic, S.I., Water Kefir grain as a source of potent dextran producing lactic acid bacteria. Hemijska Industrija 69 (2015), 595–604.
12. De Oliveira Leite, A.M., Miguel, M.A.L., Peixoto, R.S., Rosado, A.S., Silva, J.T., Paschoalin, V.M.F., Microbiological, technological and therapeutic properties of kefir: a natural probiotic beverage. Braz. J. Microbiol. 44 (2013), 341–349.
13. Dhaliwal, S.S., Oberoia, S.H., Sandhua, S.K., Nandab, D., Kumarb, D., Uppalc, S.K., Enhanced ethanol production from sugarcane juice by galactose adaptation of a newly isolated thermotolerant strain of Pichia kudriavzevii. Bioresour. Technol. 102 (2011), 5968–5975.
14. Diniz, R.O., Garla, L.K., Carvalho, J.C.T., Schneedorf, J.M., Study of anti-inflammatory activity of tibetan mushroom, a symbiotic culture of bacteria and fungi encapsulated into a polysaccharide matrix. Pharmacol. Res. 47 (2003), 49–52.
15. Diosma, G., Romanin, D.E., Rey-Burusco, M.F., Londero, A., Garrote, G.L., Yeasts from kefir grains: isolation, identification, and probiotic characterization. World J. Microbiol. Biotechnol. 30 (2014), 43–53.
16. Farnworth, E.R., Kefir – a complex probiotic. Food Sci. Technol. Bull. Funct. Foods 2 (2005), 1–17.
17. Fiorda, F.A., De Melo Pereira, G.V., Thomaz-Soccol, V., Medeiros, A.P., Rakshit, S.K., Soccol, C.R., Development of kefir-based probiotic beverages with DNA protection and antioxidant activities using soybean hydrolyzed extract, colostrum and honey. LWT - Food Sci. Technol., 86, 2016 690–607.
18. Fiorda, F.A., De Melo Pereira, G.V., Thomaz-Soccol, V., Rakshit, S.K., Soccol, C.R., Evaluation of a potentially probiotic non-dairy beverage developed with honey and kefir grains: fermentation kinetics and storage study. Food Sci. Technol. Int., 2016, 10.1177/1082013216646491 online before print, April 26, 2016.
19. Fleet, G.H., Yeast interactions and wine flavour. Int. J. Food Microbiol. 86 (2003), 11–22.
20. Fleet, G.H., Yeasts in foods and beverages: impact on product quality and safety. Curr. Opin. Biotechnol. 18 (2007), 170–175.
21. Fuente-Salcido, N.M., Castañeda-Ramírez, J.C., García-Almendárez, B.E., Bideshi, D.K., Salcedo-Hernández, R., Barboza-Corona, J.E., Isolation and characterization of bacteriocinogenic lactic bacteria from M- Tuba and Tepache, two traditional fermented beverages in México. Food Sci. Nutr. 3 (2015), 434–442.
22. Galli, A., Fiori, E., Franzetti, L., Pagani, M.A., Ottogalli, G., Microbiological and chemical composition of sugar kefir grains. Ann. Microbilogy Enzimology 45 (1995), 85–95.
23. Garofalo, C., Osimani, A., Milanović, V., Aquilanti, L., De Filippis, F., Stellato, G., Di Mauro, S., Turchetti, B., Buzzini, P., Ercolini, D., Clementi, F., Bacteria and yeast microbiota in milk kefir grains from different Italian regions. Food Microbiol. 49 (2015), 123–133.
24. Garrote, G.L., Abraham, A.G., De Antoni, G.L., Preservation of kefir grains, a comparative study. LWT-Food Sci. Technol. 30 (1997), 77–84.
25. Garrote, G.L., Abraham, A.G., De Antoni, G.L., Chemical and microbiological characterisation of kefir grains. J. Dairy Res. 68 (2001), 639–652.
26. Gaware, V., Kotade, K., Dolas, R., Dhamak, K., Somwanshi, S., Nikam, V., Khadse, A., Kashid, V., The magic of kefir: a review. Pharmacology 1 (2011), 376–386 online.
27. Gemechu, T., Review on lactic acid bacteria function in milk fermentation and preservation. Afr. J. Food Sci. 9 (2015), 170–175.
28. Golowczyc, M.A., Mobili, P., Garrote, G.L., Abraham, A.G., Antoni, G.L., Protective action of Lactobacillus kefir carrying S-layer protein against Salmonella enterica serovar Enteritidis. Int. J. Food Microbiol. 118 (2007), 264–273.
29. Golowczyc, M.A., Silva, J., Texeira, P., Antoni, G. l., Abraham, A.G., Cellular injuries of spray-dried Lactobacillus spp. isolated from kefir and their impact on probiotic properties. Int. J. Food Microbiol. 144 (2011), 556–560.
30. Grønnevik, H., Falstad, M., Narvhus, J.A., Microbiological and chemical properties of Norwegian kefir during storage. Int. Dairy J. 21 (2011), 601–606.
31. Guerra, M.J., Mujica, M.V., Physical and chemical properties of granulated cane sugar “panelas”. Food Sci. Technol. (Campinas) 30 (2010), 250–257.
32. Gulitz, A., Stadie, J., Wenning, M., Ehrmann, M.A., Vogel, R.F., The microbial diversity of water kefir. Int. J. Food Microbiol. 151 (2011), 284–288.
33. Gulitz, A., Stadie, J., Ehrmann, M.A., Ludwig, W., Vogel, R.F., Comparative phylobiomic analysis of the bacterial community of water kefir by 16S rRNA gene amplicon sequencing and ARDRA analysis. J. Appl. Microbiol. 114 (2013), 1082–1091.
34. Guzel-Seydim, Z., Seydim, A.C., Greene, A.K., Organic acids and volatile flavor components evolved during refrigerated storage of kefir. J. Dairy Sci. 83 (2000), 275–277.
35. Hsieh, H., Wang, S., Chen, T., Huang, Y., Chen, M., Effects of cow's and goat's milk as fermentation media on the microbial ecology of sugary kefir grains. Int. J. Food Microbiol. 157 (2012), 73–81.
36. Ikram-Ul-Haq, Ali, S., Kinetics of invertase production by Saccharomyces cerevisiae in batch cultures. Pak. J. Bot. 39 (2007), 907–912.
37. Jianzhonga, Z., Xiaolia, L., Hanhub, J., Mingsheng, D., Analysis of the microflora in Tibetan kefir grains using denaturing gradient gel electrophoresis. Food Microbiol. 26 (2009), 770–775.
38. Kabak, B., Dobson, A.D.W., An introduction to the traditional fermented foods and beverages of Turkey. Crit. Rev. Food Sci. Nutr. 51 (2011), 248–260.
39. Kesmen, Z., Kacmaz, N., Determination of lactic microflora of kefir grains and kefir beverage by using culture-dependent and culture-independent methods. J. Food Sci. 76 (2011), 276–283.
40. Koutinas, A.A., Athanasiadis, I., Bekatorou, A., Iconomopoulou, M., Blekas, G., Kefir yeast technology: scale-up in SCP production using milk whey. Biotechnol. Bioeng. 89 (2005), 788–796.
41. Laureys, D., De Vuyst, L., Microbial species diversity, community dynamics, and metabolite kinetics of water kefir fermentation. Appl. Environ. Microbiol. 80 (2014), 2564–2572.
42. Laureys, D., Cnockaert, M., De Vuyst, L., Vandamme, P., Bifidobacterium aquikefiri sp. nov., isolated from water kefir. Int. J. Syst. Evol. Microbiol. 66 (2016), 1281–1286.
43. Li, S.S., Cheng, C., Li, Z., Chen, J.Y., Yan, B., Han, B.Z., Reeves, M., Yeast species associated with wine grapes in China. Int. J. Food Microbiol. 138 (2010), 85–90.
44. Lin, S., Yang, B., Chen, F., Jiang, G., Li, Q., Duan, X., Jiang, Y., Enhanced DPPH radical scavenging activity and DNA protection effect of litchi pericarp extract by Aspergillus awamori bioconversion. Chem. Central J., 6, 2012, 108.
45. Liu, J., Wang, S., Chen, M., Yueh, S., Lin, C., The anti-allergenic properties of milk kefir and soymilk kefir and their beneficial effects on the intestinal microflora. J. Sci. Food Agric. 86 (2006), 2527–2533.
46. Lopitz-Otsoa, A., Rementeria, F., Elguezabal, N.R., Garaizar, J., Kefir: a symbiotic yeasts-bacteria community with alleged healthy capabilities. Revista Iberoamericana de Micologia 2 (2006), 67–74.
47. Lutz, M.L., Recherches biologiques sur la constitution du Tibi. Bulletin trimestriel de la Société mycologique de France 15 (1899), 68–72.
48. Magalhães, K.T., De Melo Pereira, G.V., Dias, D.R., Schwan, R.F., Microbial communities and chemical changes during fermentation of sugary Brazilian kefir. World J. Microbiol. Biotechnol. 33 (2010), 1–10.
49. Magalhães, K.T., De Melo Pereira, G.V., Campos, C.R., Dragone, G., Schwan, R.F., Brazilian kefir: structure, microbial communities and chemical composition. Braz. J. Microbiol. 42 (2011), 693–702.
50. Magalhaes, K.T., Dragone, G., de Melo Pereira, G.V., Oliveira, J.M., Comparative study of the biochemical changes and volatile compound formations during the production of novel whey-based kefir beverages and traditional milk kefir. Food Chem. 126 (2011), 249–253.
51. Marsh, A.J., O'Sullivan, O., Hill, C., Ross, R.P., Cotter, P.D., Sequence- based analysis of the microbial composition of water kefir from multiple sources. FEMS Microbiol. Lett. 348 (2013), 79–85.
52. Miguel, M.G.C.P., Cardoso, P.G., Magalhães, K.T., Schwan, R.F., Profile of microbial communities present in tibico (sugary kefir) grains from different Brazilian states. World J. Microbiol. Biotechnol. 27 (2011), 1875–1884.
53. Mistry, V.V., Fermented liquid milk products. Hui, Y.H., Meunier-Goddik, L., Hansen, Ö.S., Josephsen, J., Nip, W., Stanfield, P.S., Toldra, F., (eds.) Handbook of Food and Beverage Fermentation Technology, 2004, Marcel Dekker, New York, 939–957.
54. Moinas, M., Horisberger, M., Bauer, H., The structural organization of the Tibi grain as revealed by light, scanning and transmission microscopy. Archives Microbiol. 128 (1980), 157–161.
55. Moreira, M.E.C., Santos, M.H., Zolini, G.P.P., Wouters, A.T.B., Carvalho, J.C.T., Schneedorf, J.M., Anti-inflammatory and cicatrizing activities of a carbohydrate fraction isolated from sugary kefir. J. Medicial Food 11 (2008), 356–361.
56. Moreno-Terrazas, R., Reyes-Morales, H., Huerta-Ochoa, S., Guerrero-Legarreta, I., Vernon-Carter, E.J., Consumer awareness of the main sensory attributes of tepache, a traditional fermented fruit beverage. Food Sci. Technol. Int. 7 (2001), 411–415.
57. Morrissey, W.F., Davenport, B., Querol, A., Dobson, A.D.W., The role of indigenous yeasts in traditional Irish cider fermentations. J. Appl. Microbiol. 97 (2004), 647–655.
58. Mousavi, Z.E., Mousavi, S.M., Razavi, S.H., Emam-Djomeh, Z., Kiani, H., Fermentation of pomegranate juice by probiotic lactic acid bactéria. World J. Microbiol. Biotechnol. 27 (2011), 123–128.
59. Nova, M.X., Schuler, A.R., Brasileiro, B.T., Morais, M.A., Yeast species involved in artisanal cachaça fermentation in three stills with different technological levels in Pernambuco. Braz. Food Microbiol. 26 (2009), 460–466.
60. Otles, S., Cagindi, O., Kefir: a probiotic dairy-composition, nutritional and therapeutic aspects. Food Eng. Dep. 2 (2003), 54–59.
61. Paramithiotis, S., Gioulatos, S., Tsakalidou, E., Kalantzopoulus, G., Interactions between Saccharomyces cerevisiae and lactic acid bacteria in sourdough. Process Biochem. 41 (2006), 2429–2433.
62. Peres, C.M., Peres, C., Hernández-Mendoza, A., Malcata, F.X., Review on fermented plant materials as carriers and sources of potentially probiotic lactic acid bacteria - with an emphasis on table olives. Trends Food Sci. Technol. 26 (2012), 31–42.
63. Pidoux, M., The microbial flora of sugary kefir grain (the gingerbeer plant): biosynthesis of the grain fromlactobacillus hilgardii producing a polysaccharide gel. MIRCEN J. Appl. Microbiol. Biotechnol. 5 (1989), 223–238.
64. Prado, F.C., Parada, J.L., Pandey, A., Soccol, C.R., Trends in non-dairy probiotic beverages. Food Res. Int. 41 (2008), 111–123.
65. Prado, F.C., De Dea Linder, J., Inaba, J., Thomaz-Soccol, V., Brar, S.K., Soccol, C.R., Development and evaluation of a fermented coconut water beverage with potential health benefits. J. Funcional Foods 12 (2015), 489–497.
66. Prado, M.R., Blandón, M.L., Vandenberghe, L.P.S., Rodrigues, C.C., Guillermo, R., Thomaz-Soccol, V.T., Soccol, C.R., Milk kefir: composition, microbial cultures, biological activities, and related products. Front. Microbiol. 6 (2015), 1–12.
67. Puerari, C., Magalhães, K.T., Schwan, R.F., New cocoa pulp-based kefir beverages: microbiological, chemical composition and sensory analysis. Food Res. Int. 48 (2012), 634–640.
68. Randazzo, W., Corona, O., Guarcello, R., Francesca, N., Germana, M.A., Erten, H., Moschetti, G., Settanni, L., Development of new non-dairy beverages from Mediterranean fruit juices fermented with water kefir microorganisms. Food Microbiol. 54 (2016), 40–51.
69. Rodrigues, K.L., Caputo, L.R.G., Carvalho, J.C.T., Evangelista, J., Schneedorf, J.M., Antimicrobial and healing activity of kefir and kefiran extract. Int. J. Antimicrob. Agents 25 (2005), 404–408.
70. Rodrigues, K.L., Araújo, T.H., Schneedorf, J.M., Ferreira, C.S., Moraes, G.O.I., Coimbra, R.S., Rodrigues, M.R., A novel beer fermented by kefir enhances anti-inflammatory and anti-ulcerogenic activities found isolated in its constituents. J. Funct. Foods 21 (2016), 58–69.
71. Rubio, M.T., Lappe, P., Wacher, C., Ulloa, M., Microbial and biochemical studies of the fermentation of sugary solutions inoculated with tibi grains. Revista Latinoamericana de Microbiología 35 (1993), 19–31.
72. Sabir, F., Beyatli, Y., Cokmus, C., Darilmaz, D.O., Assessment of potential probiotic properties of Lactobacillus spp., Lactococcus spp., and Pediococcus spp. strains isolated from kefir. J. Food Sci. 75 (2010), 568–573.
73. Sarikkha, P., Nitisoravut, R., Poljungreed, I., Boonyarattanakalin, S., Identification of bacteria and yeast communities in a Thai sugary kefir by polymerase chain reaction-denaturing gradient gel electrophoresis (PCR-DGGE) analyses. J. Industrial Technol. 11 (2015), 25–39.
74. Sarkar, S., Potential of kefir as a dietetic beverage – a review. Br. J. Nutr. 109 (2007), 280–290.
75. Schneedorf, J.M., Kefir D'Aqua and its probiotic properties. Rigobelo, E.C., (eds.) Probiotic in Animals, 2012, Intech, Croatia, 53–76.
76. Schrezenmeir, J., De Vrese, M., Probiotics, prebiotics, and synbiotics — approaching a definition. Am. J. Clin. Nutr. 77 (2001), 361–364.
77. Schwan, R.F., De Melo Pereira, G.V.M., Fleet, G.H., Microbial activities during cocoa fermentation. Schwan, R.F., Fleet, G.H., (eds.) Cocoa and Coffee Fermentations, 2014, CRC Press, Boca Raton, 130–184.
78. Simova, E., Beshkova, D., Angelov, A., Hristozova, T., Frengova, G., Spasov, Z., Lactic acid bacteria and yeasts in kefir grains and kefir made from them. J. Industrial Microbiol. Biotechnol. 28 (2002), 1–6.
79. Soccol, C.R., Vandenberghe, L.P.S., Spier, M.R., Medeiros, A.B.P., Yamaguishi, C.T., Lindner, J.D.D., Thomaz-Soccol, V., The potential of probiotics: a review. Food Technol. Biotechnol. 48 (2010), 413–434.
80. Vayssier, Y., Le kéfir: analyse qualitative et quantitative. Revue Laitière français 361 (1978), 3–75.
81. Waldherr, F.W., Doll, V.M., Meissner, D., Vogel, R.F., Identification and characterization of a glucan-producing enzyme from Lactobacillus hilgardii TMW 1.828 involved in granule formation of water kefir. Food Microbiol. 27 (2010), 672–678.
82. Wang, S.Y., Chen, H.C., Liu, J.R., Cin, Y.C., Chen, M.J., Identification of yeasts and evaluation of their distribution in Taiwanese kefir and viili starters. J. Dairy Sci. 91 (2008), 3798–3805.
83. Ward, H.M., The ginger-beer plant, and the organisms composing it: a contribution to the study of fermentation-yeasts and bacteria. Philosophical Trans. R. Soc. Lond. 183 (1892), 125–197.
84. Witthuhn, R.C., Schoeman, T., Britz, T.J., Characterisation of the microbial population at different stages of Kefir production and Kefir grain mass cultivation. Int. Dairy J. 15 (2005), 383–389.
85. Yildiz, F., Development and manufacture of yogurt and other functional dairy products. Ustunol, Z., (eds.) International Journal of Dairy Technology, 2010, CRC Press, Boca Raton, 300–301.
86. Yuksekdag, Z.N., Beyatli, Y., Aslim, B., Determination of some characteristics coccoid forms of lactic acid bacteria isolated from Turkish kefirs with natural probiotic. LWT – Food Sci. Technol. 37 (2004), 663–667.
87. Zanirati, S.B.F., Abatemarco, M. Jr., Sandes, S.H.C., Nicoli, J.R., Nunes, A.C., Neumann, E., Selection of lactic acid bacteria from Brazilian kefir grains for potential use as starter or probiotic cultures. Anaerobe 32 (2015), 70–76.