Kefir: a comprehensive overview of microbiological, physicochemical, and health-promoting properties
DOI:
https://doi.org/10.5327/fst.00420%20Palavras-chave:
antimicrobial, antineoplastic, antidiabetic, antimutagenic, intestinal, fermented milk, probioticsResumo
Kefir is a naturally carbonated and mildly acidic milk beverage fermented by grains that consist of bacteria and yeast living in a symbiotic relationship. Its unique flavor arises from a blend of lactic acid, ethanol, carbon dioxide, and other compounds produced by the microorganisms within the kefir grains. The microorganisms in kefir are a complex microbial population that varies by geographical region. Kefir is widely acknowledged for its probiotic content, with reported health benefits that include modulation of intestinal microflora, immune system stimulation, and antimicrobial, antineoplastic, hypocholesterolemic, antidiabetic, and antimutagenic effects. It also exhibits β-galactosidase activity and benefits lipid and blood pressure levels. This review focuses on the microbiological aspects, composition, and production of milk kefir, highlighting how its biological properties correlate with the health benefits associated with its consumption.
Downloads
Referências
Aghlara, A., Mustafa, S., Manap, Y. A., & Mohamad, R. (2009). Characterization of headspace volatile flavour compounds formed during kefir production: Application of solid phase microextraction. International Journal of Food Properties, 12(4), 808-818. https://doi.org/10.1080/10942910802073189
Ahmed, A., Ismaiel, M., Mohamed, F., Ayman, G. K., & Naggar, E. L. (2011). Milk kefir: Ultrastructure, antimicrobial activity and efficacy on aflatoxin B1 production by Aspergillus flavus. Current Microbiology, 62(5), 1602-1609. https://doi.org/10.1007/s00284-011-9901-9
Ahmed, Z., Wang, Y., Ahmad, A., Khan, S. T., Nisa, M., Ahmad, H., & Afreen, A. (2013). Kefir and health: A contemporary perspective. Food Science and Nutrition, 53(5), 422-434. https://doi.org/10.1080/10408398.2010.540360
Alm, L. (1982). Effect of fermentation on lactose, glucose, and galactose content in milk and suitability of fermented milk products for lactose-intolerant individuals. Journal of Dairy Science, 65(3), 346-352. https://doi.org/10.3168/jds.S0022-0302(82)82198-X
Azizi, N. F., Kumar, M. R., Yeap, S. K., Abdullah, J. O., Khalid, M., Omar, A. R., Osman, M. A., Mortadza, S. A. S., & Alitheen, N. B. (2021). Kefir and its biological activities. Foods, 10(6), 1-20.
Begley, M., Hill, C., & Cormac, G. M. (2006). Bile salt hydrolase activity in probiotics. Applied and Environmental Microbiology, 72(3), 1729-1738. https://doi.org/10.1128/AEM.72.3.1729-1738.2006
Beshkova, D. M., Simova, E. D., Frengova, G. I., Simov, Z. I., & Dimitrov, Z. H. P. (2003). Production of volatile aroma compounds by kefir starter cultures. International Dairy Journal, 13(6), 529-535.
Brashears, M., Gilliland, S. E., & Buck, L. M. (1998). Bile salt deconjugation and cholesterol removal from media by Lactobacillus casei. Journal of Dairy Science, 81(8), 2103-2110. https://doi.org/10.3168/jds.s0022-0302(98)75785-6
Brasil (2007). Ministério da Agricultura, Pecuária e Abastecimento. Instrução Normativa Nº 46, de 23 de outubro de 2007. Regulamento Técnico de Identidade e Qualidade de Leites Fermentados. Diário Oficial da União.
Cenesiz, S., Yaman, H., Ozcan, A., Kart, A., & Karademir, G. (2008). Effects of kefir as a probiotic on serum cholesterol, total lipid, aspartate aminotransferase and alanine aminotransferase activities in broiler chicks. Medycyna Weterynaryjna, 64(2), 168-170.
Chen, C., Hing, M. C., & Kubow, S. (2007). Kefir extracts suppress in vitro proliferation of estrogen-dependent human breast cancer cells but not normal mammary epithelial cells. Journal of Medicinal Food, 10(3), 416-422. https://doi.org/10.1089/jmf.2006.236
Chen, H. S., Wang, S. Y., & Chen, M. J. (2008). Microbiological study of lactic acid bacteria in kefir grains by cultured-dependent and cultured-independent methods. Food Microbiology, 25(3), 492-501. https://doi.org/10.1016/j.fm.2008.01.003
Codex Alimentarius International Food Standards (2003). Codex Standard for Fermented Milks (Codex Stan CXS 243-2003). Codex Alimentarius Commission. Retrieved from https://www.fao.org/fao-who-codexalimentarius
Czamanski, R. T., Greco, D. P., & Wiest, J. M. (2004). Evaluation of antibiotic activity in filtrates of traditional kefir. Higiene Alimentar, 18(1), 75-77.
De Vrese, M., Keller, B., & Barth, C. A. (1992). Enhancement of intestinal hydrolysis of lactose by microbial β-galactosidase (EC 3.2.1.23) of kefir. British Journal of Nutrition, 67(1), 67-75. https://doi.org/10.1079/bjn19920009
De Vrese, M., Stegelmann, A., Richter, B., Fenselau, S., Laue, C., & Schrezenmeir, J. (2001). Probiotics-compensation for lactase insufficiency. American Journal of Clinical Nutrition, 73(2 Suppl.), 421S-429S. https://doi.org/10.1093/ajcn/73.2.421s
Dertli, A., & Çon, A. H. (2017). Microbial diversity of traditional kefir grains and their role on kefir aroma. Food Science and Technology, 85(Part A), 151-157. https://doi.org/10.1016/j.lwt.2017.07.017
Duitschaever, C. L., Kemp, N., & Emmons, D. (1987). Pure culture formulation and procedure for the production of kefir. Milchwissenschaft, 42(2), 80-82.
Farnworth, E. R. (2005). Kefir: a complex probiotic. Food Science and Technology Bulletin: Functional Foods, 2(1), 1-17.
Gao, J., Gu, F., Abdella, N. H., Ruan, H., & He, G. (2012). Investigation on culturable microflora in Tibetan kefir grains from different areas of China. Journal of Food Science, 77(7), 425-433. https://doi.org/10.1111/j.1750-3841.2012.02805.x
Gao, J., Gu, F., Ruan, H., Chen, Q., He, J., & He, G. (2013). Induction of apoptosis of gastric cancer cells SGC7901 in vitro by a cell-free fraction of Tibetan kefir. International Dairy Journal, 30(1), 14-18. https://doi.org/10.1016/j.idairyj.2012.11.011
Garofalo, C., Osimani, A., Milanović, V., Aquilanti, L., De Filippis, F., Stellato, G., Di Mauro, S., Turchetti, B., Buzzini, P., Ercolini, D., & Clementi, F. (2015). Bacteria and yeast microbiota in milk kefir grains from different Italian regions. Food Microbiology, 49, 123-133. https://doi.org/10.1016/j.fm.2015.01.017
Garrote, G. L., Abraham, A. G., & De Antoni, G. L. (2001). Chemical and microbiological characterization of kefir grains. Journal of Dairy Research, 68(4), 639-652. https://doi.org/10.1017/s0022029901005210
Guzel-Seydim, Z. B., Seydim, A. C., Greene, A. K., & Bodine, A. B. (2000). Determination of organic acids and volatile flavor substances in kefir during fermentation. Journal of Food Composition and Analysis, 13(1), 35-43. https://doi.org/10.1006/jfca.1999.0842
Hertzler, S. R., & Clancy, S. M. (2003). Kefir improves lactose digestion and tolerance in adults with lactose maldigestion. Journal of the American Dietetic Association, 153(5), 582-587. https://doi.org/10.1053/jada.2003.50111
Heyman, M. (2000). Effect of lactic acid bacteria on diarrheal diseases. Journal of the American College of Nutrition, 19(2 Suppl.), 137-146. https://doi.org/10.1080/07315724.2000.10718084
Irigoyen, A., Arana, I., Castiella, M., & Torre, P. (2005). Microbiology, physicochemical and sensory characteristics of kefir during storage. Food Chemistry, 90(4), 613-620. https://doi.org/10.1016/j.foodchem.2004.04.021
John, S. M., & Deeseenthum, S. (2015). Properties and benefits of kefir: A review. Songklanakarin Journal of Science and Technology, 37(3), 275-282.
Kemp, N. (1984). Kefir, the champagne of cultured dairy products. Cultured Dairy Products Journal, 19(3), 29-30.
Khoury, N., El-Hayek, S., Tarras, O., El-Sabban, M., El-Sibai, M., & Rizk, S. (2014). Kefir exhibits anti-proliferative and pro-apoptotic effects on colon adenocarcinoma cells with no significant effects on cell migration and invasion. International Journal of Oncology, 45(5), 2117-2127. https://doi.org/10.3892/ijo.2014.2635
Kim, D. H., Jeong, C. H., Cheng, W. N., Kwon, H. C., Kim, D. H., Seo, K. H., Choi, Y., & Han, S. G. (2021). Effects of kefir on doxorubicin-induced multidrug resistance in human colorectal cancer cells. Journal of Functional Foods, 78, 104371. https://doi.org/10.1016/j.jff.2021.104371
Kondyli, E., Katsiari, M. C., Masouras, T., & Voutsinas, L. P. (2002). Free fatty acids and volatile compounds of low-fat feta-type cheese made with a commercial adjunct culture. Food Chemistry, 79(2), 199-205. https://doi.org/10.1016/S0308-8146(02)00132-2
Koroleva, N. S. (1991). Therapeutic properties of fermented milks. In: R. K. Robinson (Ed.), Elsevier Applied Sciences Publishers (pp. 157-159). Elsevier.
Korsak, N., Taminiau, B., Leclercq, M., Nezer, C., Crevecoeur, S., Ferauche, C., Detry, E., Delcenserie, V., & Daube, G. (2015). Short communication: Evaluation of the microbiota of kefir samples using metagenetic analysis targeting the 16S and 26S ribosomal DNA fragments. Journal of Dairy Science, 98(6), 3684-3689. https://doi.org/10.3168/jds.2014-9065
Kwon, C. S., Park, M. Y., Cho, J. S., Choi, S. T., & Chang, D. S. (2003). Identification of effective microorganisms from kefir fermented milk. Food Science and Biotechnology, 12(5), 476-479.
Labayen, I., Forga, L., Gonzalez, A., Lenoir-Wijnkoop, I., & Martinez, J. A. (2001). Relationship between lactose digestion, gastrointestinal transit time and symptoms in lactose malabsorbers after dairy consumption. Alimentary Pharmacology and Therapeutics, 15(4), 543-549. https://doi.org/10.1046/j.1365-2036.2001.00952.x
Linossier, J. P., & Dousset, X. (1994). Stimulation de la croissance et du métabolisme de Lactobacillus kefir par Candida kefir. Microbiologie Aliments Nutrition, 12, 341-351.
Liu, J. R., Chen, M. J., & Lin, C. W. (2002a). Characterization of polysaccharide and volatile compounds produced by kefir grains grown in soymilk. Food Chemistry and Toxicology, 67(1), 104-108. https://doi.org/10.1111/j.1365-2621.2002.tb11367.x
Liu, J. R., Wang, S. Y., Chen, M. J., Chen, H. L., Yueh, P. Y., & Lin, C. W. (2006). Hypocholesterolaemic effects of milk kefir and soymilk-kefir in cholesterol-fed hamsters. British Journal of Nutrition, 95(5), 939-946. https://doi.org/10.1079/bjn20061752
Liu, J. R., Wang, S. Y., Lin, Y. Y., & Lin, C. W. (2002b). Antitumor activity of milk kefir and soy milk kefir in tumor-bearing mice. Nutrition and Cancer, 44(2), 183-187. https://doi.org/10.1207/s15327914nc4402_10
Maeda, H., Zhu, X., Omura, K., Suzuki, S., & Kitamura, S. (2004). Effects of an exopolysaccharide (kefiran) on lipids, blood pressure, blood glucose, and constipation. BioFactors, 22(1-4), 197-200. https://doi.org/10.1002/biof.5520220141
Magalhães, K. T., Pereira, G. V. M., Campos, C. R., Dragone, G., & Schwan, R. F. (2011). Brazilian kefir: Structure, microbial communities and chemical composition. Brazilian Journal of Microbiology, 42(2), 693-702. https://doi.org/10.1590/S1517-83822011000200034
Marteau, P., Gerhardt, M. F., Myara, A., Bouvier, E., Trivin, F., & Rambaud, J. C. (1995). Metabolism of bile salts by alimentary bacteria during transit in the human small intestine. Microbial Ecology in Health and Disease, 8(4), 151-157. https://doi.org/10.3109/08910609509140093
Mauriello, G., Moio, L., Moschetti, G., Piombino, P., Addeo, F., & Coppola, S. (2001). Characterization of lactic acid bacteria strains on the basis of neutral volatile compounds produced in whey. Journal of Applied Microbiology, 90(6), 928-942. https://doi.org/10.1046/j.1365-2672.2001.01327.x
Medrano, M., Perez, P. F., & Abraham, A. G. (2008). Kefiran antagonizes cytopathic effects of Bacillus cereus extracellular factors. International Journal of Food Microbiology, 122(1-2), 1-7. https://doi.org/10.1016/j.ijfoodmicro.2007.11.046
Montes, R. G., Bayless, T. M., Saavedra, J. M., & Perman, J. A. (1995). Effect of milks inoculated with Lactobacillus acidophilus or a yogurt starter culture in lactose-maldigesting children. Journal of Dairy Science, 78(8), 1657-1664. https://doi.org/10.3168/jds.s0022-0302(95)76790-x
Ott, A., Germond, J. E., & Chaintreau, A. (2002). Origin of acetaldehyde production by Streptococcus thermophilus. Applied and Environment Microbiology, 68(11), 5656-5662.
Parvez, S., Malik, K. A., Ah Kang, S., & Kim, H.-Y. (2006). Probiotics and their fermented food products are beneficial for health. Journal of Applied Microbiology, 100(6), 1171-1185. https://doi.org/10.1111/j.1365-2672.2006.02963.x
Paucean, A., & Carmen, S. (2008). Probiotic activity of mixed cultures of kefir’s lactobacilli and non-lactose fermenting yeasts. Bulletin UASVM, 65(2).
Pelletier, X., Laure-Boussuge, S., & Donazzolo, Y. (2001). Hydrogen excretion upon ingestion of dairy products in lactose-intolerant male subjects: Importance of the live flora. European Journal of Clinical Nutrition, 55(6), 509-512. https://doi.org/10.1038/sj.ejcn.1601169
Plaza-Diaz, J., Ruiz-Ojeda, F. J., Gil-Campos, M., & Gil, A. (2019). Mechanisms of action of probiotics. Advances in Nutrition, 10(Suppl. 1), 49-66. https://doi.org/10.1093/advances/nmy063
Pringsulaka, O., Rueangyotchathana, K., & Suwannasai, N. (2015). In vitro screening of lactic acid bacteria for multi-strain probiotics. Livestock Science, 174, 66-73. https://doi.org/10.1016/j.livsci.2015.01.016
Rattray, F. P., & Connell, M. J. (2011). Encyclopedia of Dairy Sciences (2ª ed). Fukay, J. W.
Rea, M. C., Lennartsson, T., & Dillon, P. (1996). Irish kefir-like grains: Their structure, microbial composition, and fermentation kinetics. Journal of Applied Bacteriology, 81(1), 83-94. https://doi.org/10.1111/j.1365-2672.1996.tb03286.x
Reid, G., Jass, J., Sebulsky, M. T., & McCormick, J. K. (2003). Potential uses of probiotics in clinical practice. Clinical Microbiological Reviews, 16(4), 658-672. https://doi.org/10.1128/cmr.16.4.658-672.2003
Reynier, M. O., Montet, J. C., Gerolami, A., Marteau, C., Crotte, C., Montet, A. M., & Mathieu, S. (1981). Comparative effects of cholic, chenodeoxycholic, and ursodeoxycholic acids on micellar solubilization and intestinal absorption of cholesterol. Journal of Lipid Research, 22(3), 467-473.
Roberts, M., Yarunin, S., & Danone. (2000). Moves into Russian kefir market. New Nutrition Business, 6(3), 22-24.
Rodrigues, K. L., Caputo, L. R. G., Carvalho, J. C. T., Evangelista, J., & Schneedorf, J. M. (2005). Antimicrobial and healing activity of kefir and kefiran extract. International Journal of Antimicrobial Agents, 25(5), 404-408. https://doi.org/10.1016/j.ijantimicag.2004.09.020
Santos, A., Sanmauro, M., Sanchez, A., Torres, J. M., & Marquina, D. (2003). The antimicrobial properties of different strains of Lactobacillus spp. isolated from kefir. Systematic and Applied Microbiology, 26(3), 434-437. https://doi.org/10.1078/072320203322497464
Schwan, R. F., Magalhães-Guedes, K. T., & Dias, D. R. (2015). Kefir - Grains and beverages: A review. Scientia Agraria Paranaensis, 14(1), 1-9. https://doi.org/10.18188/sap.v14i1.11137
Semih, O. E., & Cagindi, C. (2003). Kefir: A probiotic dairy - Composition, nutritional and therapeutic aspects. Pakistan Journal of Nutrition, 2(2), 54-59. https://doi.org/10.3923/pjn.2003.54.59
Sen, M. (2019). Role of probiotics in health and disease - A review. International Journal of Advancement in Life Sciences Research, 2(2), 1-11.
Sharifi, M., Moridnia, A., Mortazavi, D., Salehi, M., Bagheri, M., & Sheikhi, A. (2017). Kefir: A powerful probiotic with anticancer properties. Medical Oncology, 34(11), 183. https://doi.org/10.1007/s12032-017-1044-9
Tamai, Y., Yoshimitsu, N., Watanabe, Y., Kuwabara, Y., & Nagai, S. (1996). Effects of milk fermented by culturing with various lactic acid bacteria and a yeast on serum cholesterol level in rats. Journal of Fermentation and Bioenergy, 81, 181-182.
Thakur, K., Zhang, J. G., Wei, Z. J., Kumar, N., Tomar, S. K., & Pophaly, S. D. (2017). Nutraceuticals and innovative food products for healthy living and preventive care. Medical Information Science Reference.
Tripathi, M. K., & Giri, S. K. (2014). Probiotic functional foods: Survival of probiotics during processing and storage. Journal of Functional Foods, 9, 225-241.
Vinderola, C. G., Duarte, J., Thangavel, D., Perdigón, G., Farnworth, E., & Matar, C. (2005). Remote-site stimulation and duration of the immune response by kefir. European Journal of Inflammation, 3(2), 63-73.
Vinderola, C. G., Perdigón, G., Duarte, J., Farnworth, E., & Matar, C. (2006). Effects of the oral administration of the products derived from milk fermentation by kefir microflora on immune stimulation. Journal of Dairy Research, 73(4), 472-479. https://doi.org/10.1017/s002202990600197x
Wang, H., Wang, C., & Guo, M. (2020). Autogenic successions of bacteria and fungi in kefir grains from different origins when sub-cultured in goat milk. Food Research International, 138(Part B), 109784. https://doi.org/10.1016/j.foodres.2020.109784
Wang, S. Y., Chen, K. N., Lo, Y. M., Chiang, M. L., Chen, H. C., Liu, J. R., & Chen, M. J. (2012). Investigation of microorganisms involved in biosynthesis of the kefir grain. Food Microbiology, 32(2), 274-285. https://doi.org/10.1016/j.fm.2012.07.001
Weschenfelder, S. (2009). Caracterização de kefir tradicional quanto à composição físico-química, sensorialidade e atividade anti-Escherichia coli (Dissertação de mestrado, Universidade Federal do Rio Grande do Sul).
Witthuhn, R. C., Schoeman, T., & Britz, T. J. (2005). Characterisation of the microbial population at different stages of kefir production and kefir grain mass cultivation. International Dairy Journal, 15(4), 383-389. https://doi.org/10.1016/j.idairyj.2004.07.016
Wszolek, M., Tamime, A. Y., Muir, D. D., & Barclayb, M. N. I. (2001). Properties of kefir made in Scotland and Poland using bovine, caprine and ovine milk with different starter cultures. LWT - Food Science and Technology, 34(4), 251-261. https://doi.org/10.1006/fstl.2001.0773
Wyder, M. T., Meile, L., & Teuber, M. (1999). Description of Saccharomyces turicensis sp. nov., a new species from kefir. Systematic and Applied Microbiology, 22(3), 420-425. https://doi.org/10.1016/S0723-2020(99)80051-4
Yang, X. J., Fan, M. T., Shi, J. L., & Dang, B. (2007). Isolation and identification of preponderant flora in Tibetan kefir. China Brewing, 171, 52-55.
Yerlikaya, O. (2018). Probiotic potential and biochemical and technological properties of Lactococcus lactis ssp. lactis strains isolated from raw milk and kefir grains. Journal of Dairy Science, 102(1), 124-134. https://doi.org/10.3168/jds.2018-14983
Yilmaz-Ersan, L., Ozcan, T., Akpinar-Bayizit, A., & Sahin, S. (2018). Comparison of antioxidant capacity of cow and ewe milk kefirs. Journal of Dairy Science, 101(5), 3788-3798. https://doi.org/10.3168/jds.2017-13871
Yuksekdag, Z. N., Beyatli, Y., & Aslim, B. (2004a). Determination of some characteristics coccoid forms of lactic acid bacteria isolated from Turkish kefirs with natural probiotic. LWT - Food Science and Technology, 37(6), 663-667. https://doi.org/10.1016/j.lwt.2004.02.004
Yuksekdag, Z. N., Beyath, Y., & Aslim, B. (2004b). Metabolic activities of Lactobacillus spp. strains isolated from kefir. Nahrung / Food, 48(3), 218-220. https://doi.org/10.1002/food.200300414
Zanarati, D. F., Abatemarco, M., de Cicco Sandes, S. H., Nicoli, J. R., Nunes, Á. C., & Neumann, E. (2015). Selection of lactic acid bacteria from Brazilian kefir grains for potential use as starter or probiotic cultures. Anaerobe, 32, 70-76. https://doi.org/10.1016/j.anaerobe.2014.12.007
