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Review: Functional Properties of Kefir

Zeynep B. Guzel-Seydim , Tugba Kok-Tas , Annel K. Greene & Atif C. Seydim
a a a b a

Department of Food Engineering, Sleyman Demirel University, nr, Isparta, 32260, Turkey
b

Department of Animal & Veterinary Sciences, Clemson University, Clemson, SC, 29634-0328, USA Published online: 03 Mar 2011.

To cite this article: Zeynep B. Guzel-Seydim , Tugba Kok-Tas , Annel K. Greene & Atif C. Seydim (2011): Review: Functional Properties of Kefir, Critical Reviews in Food Science and Nutrition, 51:3, 261-268 To link to this article: http://dx.doi.org/10.1080/10408390903579029

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Critical Reviews in Food Science and Nutrition, 51:261268 (2011) Copyright C Taylor and Francis Group, LLC ISSN: 1040-8398 print / 1549-7852 online DOI: 10.1080/10408390903579029

Review: Functional Properties of Kefir

1 , TUGBA KOK-TAS1 , ANNEL K. GREENE2 ZEYNEP B. GUZEL-SEYDIM 1 C. SEYDIM and ATIF
1 2

n Department of Food Engineering, S uleyman Demirel University, C u ur, Isparta, 32260, Turkey Department of Animal & Veterinary Sciences, Clemson University, Clemson, SC, 29634-0328, USA

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Ker is a unique cultured dairy product due to combined lactic acid and alcoholic fermentation of lactose in milk. Ker is produced by microbial activity of ker grains which have a relatively stable and specic balance of lactic acid bacteria and yeast. Due to the claimed health benets of ker which include reduction of lactose intolerance symptoms, stimulation of the immune system, lowering cholesterol, and antimutagenic and anticarcinogenic properties, ker has become an important functional dairy food and consequently, research on ker has increased in the past decade. In the following review, recent studies on the functional properties of ker are reviewed. Keywords fermented milk, health, probiotic, anticarcinogenic

INTRODUCTION: HEALTH BENEFITS OF FERMENTED DAIRY PRODUCTS Nobel Laureate (1908) Elie Metchnikoff pioneered research suggesting that fermented milk has a benecial value and reported this in his theory of longevity (Amer and Lammerding, 1983). In vitro and in vivo studies on the functional properties of fermented dairy products are ongoing, leading to further understanding of the complexities of the product and the effect of the product on human health. Probiotics are live microorganisms that provide positive health effects. Previous studies have indicated that fermented dairy products can cause probiotic effects such as improvement in digestive system health, serum cholesterol reduction, improvement in lactose tolerance, improved immune function, control of irritable bowel symptoms, as well as anticarcinogenic properties. Some of the most prevalent benecial probiotic microorganisms have been identied as Bidobacteria species, Lactobacillus acidophilus, Lactobacillus plantarum, Lactobacillus reuteri, Lactobacillus rhamnosus, Lactobacillus salivarius, and Saccharomyces boulardii (Parvez et al., 2006; Shah, 2007). Ker made from ker grains provides natural probiotics mainly Lactobacillus acidophilus, Bidobacterium bidum, many lactic acid bacteria, and yeast in high numbers
Address correspondence to Zeynep B. Guzel-Seydim, Department of Food n Enginnering, S uleyman Demirel University, C u ur, Isparta, 32260, Turkey. Tel.: +90 (246) 211 1681; Fax: +90 (246) 237 1255. E-mail: zeyneps@sdu.edu.tr

(Kok-Tas, 2010) while people are seeking to develop functional fermented dairy products. Parvez et al. (2006) also reported that probiotic microorganisms are most commonly consumed in the form of fermented dairy products. Bioactive peptides and proteins from fermented dairy foods also provide important health benets such as stimulating effects on lymphocyte proliferation and immunoglobulin production, hypertension reduction, and increased absorption of intestinal calcium (M oller et al., 2008). The antimutagenic activity of fermented milk has been reported in various microbial and mammalian cell systems (Hosono et al., 1986a; 1986b; 1990; Bodana and Rao, 1990; Renner and Munzner, 1991; Hosoda et al., 1992; Nadathur et al., 1995; 1996; Guzel-Seydim et al., 2006). Pool-Zobel et al. (1993) determined that lactic acid bacteria have a high capacity for binding mutagens. Stidl et al. (2008) conducted a study on the ability of lactic acid bacteria to reduce heterocyclic amines formed during cooking of meat. The team noted overall reductions in heterocyclic aromatic amine concentration by Lactobacillus helveticus, Streptococcus thermophilus, Lactobacillus delbrueckii subsp. bulgaricus, Bidobacterium longum, Lactobacillus casei, Lactobacillus acidophilus, Lactobacillus plantarum, and Lactobacillus ker were 83, 68, 59, 44, 42, 20, 10, and 9%, respectively. Nadathur et al. (1995) used the Ames test with S. typhimurium TA100 to study the antimutagenicity of acetone-extracted yogurt against different mutagenic chemicals. Their results indicated that fermented milk samples had an

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antimutagenic effect against 2,3-dimethyl-4-aminobiphenyl (DMAB) and against direct acting N-methyl-N-nitro-Nnitrosoguanidine (MNNG), which is one of the most potent mutagenic chemicals known. Consumption of fermented milk inhibited growth of certain types of tumors in several animalbased studies (Reddy et al., 1973; Ayebo et al., 1981; Cevikbas et al., 1994; McIntosh et al., 1995; de Moreno de LeBlanc et al. 2006).

KEFIR AND KEFIR GRAINS: DESCRIPTION AND MICROBIAL FLORA Ker grains were rst described by the tribes in the Northern Caucasus mountain region in Russia (Seydim, 2001). Ker is produced by fermentative activity of ker grains which contain a diverse range of inherent lactic acid bacteria, yeast, and sometimes acetic acid bacteria in a polysaccharide matrix of semi-hard granules. When ker grains are added to milk and incubated for approximately 22 h at 25 C, microorganisms in the grains continue to proliferate in milk with the production of the lactic acid and other avor compounds causing physicochemical changes (Guzel-Seydim et al., 2000a). The resultant product, ker, is a self-carbonated, refreshing fermented milk drink which has a unique avor due to a mixture of lactic acid, carbon dioxide, acetaldehyde, acetoin, slight alcohol, and other fermentation avor products (Guzel-Seydim et al., 2000b). One feature of ker that differs from other fermented milk products is that ker grains are recovered after fermentation. The biomass of ker grains slowly increases during the process of ker fermentation (Guzel-Seydim et al., 2000a; Gorsek and Tramsek, 2007). The microora of ker are summarized in Table 1.

in ker than in yogurt or milk. In addition to being anticarcinogenic, CLA have hypocholesterolemic and anti-atherogenic effects which would protect against atherogenesis, the formation of atheromas (plaques) in arteries (Ha et al., 1987; Miller et al., 1995; Ip et al., 1994). Liu et al. (2005) reported that milk and soymilk ker samples signicantly reduced the N-methylN-nitro-N-nitrosoguanidine (MNNG) and 4-nitroquinoline-Noxide (NQNO) mutagenesis in Ames test. The inhibition rates of milk ker and soy milk ker against NQNO mutagen were 89.3% and 68.8%, respectively. 1,1-diphenyl-2-picryl-hydrazyl (DPPH) radical scavenging activities of milk ker and soy milk ker signicantly increased at the end of the fermentation (Liu et al. 2005). Animal Tests Shiomi et al. (1982) reported anti-tumor effects from a watersoluble polysaccharide (approximate molecular weight 1,000 kDa) isolated from ker grains. Whether administered orally or intraperitoneally, the polysaccharide inhibited the growth of Ehrlich carcinoma and Sarcoma 180 compared to control mice receiving no ker derived polysaccharide (Shiomi et al., 1982; Murofushi et al., 1983). In a number of other studies, the exopolysaccharide keran exhibited antimicrobial and antitumor activity (Maeda et al., 2004; Medrano et al., 2008; Rodrigues et al., 2005; Vinderola et al., 2006). In a study on induced breast cancer in mice, de Moreno de LeBlanc et al. (2006) reported that mice receiving 2 days cyclical feeding with both ker and cell-free fraction of ker during 27 days had a reduced tumor growth and increased the IgA(+) cells. The results of this study proved the importance of nonmicrobial components released during milk fermentation. Tumors are classied as carcinomas or sarcomas. Sarcoma tumors are derived from supportive or connective tissues such as bone, fat, and cartilage (Kuby, 1994). Sarcoma 180 is one of the transplantable, non-metastasizing, connective tissue tumors of the mouse. Liu et al. (2002) experimented that mice were fed with reconstituted milk, milk ker, soy milk, or soy milk ker beginning one week after sarcoma 180 tumor cells had been inoculated under the abdominal skin. At day 30, the positive control, milk, milk ker, soy milk, and soy milk ker groups had tumor sizes of 1,631 753, 2,115 901, 574 335, 1,017 770, and 475 292 mm3 , respectively. Consequently, oral administration of kers generated from milk or soy milk resulted in signicant inhibition of tumor growth. Soy contains a signicant content of genistein which is an isoavone belonging to the class of phytoestrogens. Genistein has promising health attributes such as inhibition of cancer cells and improving the bone health (Cederrotha and Nef, 2009; Taylor et al., 2009). The concentrations of genistein in soy milk and soy milk ker were approximately 47 and 50 g/g, respectively. However, it was concluded that the tumor inhibiting the effect of soy milk ker was not associated with the isoavone content of soy milk. Furthermore, IgA levels in the small intestine wall were also increased.

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FUNCTIONAL PROPERTIES OF KEFIR The functional properties of ker are discussed in detail below and a schematic diagram is presented of in Fig. 1.

ANTIMUTAGENIC AND ANTICARCINOGENIC PROPERTIES OF KEFIR Cell In Vitro Tests Guzel-Seydim et al. (2006) compared the antimutagenic activities of milk, yogurt, and ker samples using the Ames test. Ker extract signicantly decreased methyl methanosulfate, sodium azide, and aatoxin B1 induced mutagenicity whereas yogurt extract and milk decreased the mutagenicity to lesser degrees. Guzel-Seydim et al. (2006) determined that three isomers of CLA ([c9,t11], [t10,c12], and [t9,t11]), as well as butyric, palmitic, palmitoleic, oleic acids were in higher concentrations

FUNCTIONAL PROPERTIES OF KEFIR

Table 1 Microora species reported in ker and ker grains Koreleva 1991; Pintado et al., 1996; Takizawa et al., 1994; Kandler and Kunath, 1983; Santos et al., 2003; Angulo et al., 1993; Garrote et al., 2001; Mobili et al., 2008; Fujisawa et al., 1988; Santos et al., 2003; Wang et al., 2008; Vinderola et al., 2007 Takizawa et al., 1994 Takizawa et al., 1994; Garrote et al., 2001 Ottogalli et al., 1973; Simova et al., 2002; Santos et al., 2003; Angulo et al., 1993; Mobili et al., 2008 Garrote et al., 2001; Santos et al., 2003 Koreleva 1991; Lin et al., 1999; Simova et al., 2005; Valasaki et al., 2007 Ottogalli et al., 1973; Santos et al., 2003; Angulo et al., 1993 Koreleva 1991; Simova et al., 2002; Santos et al., 2003 Koreleva 1991; Angulo et al., 1993. Simova et al., 2002; Ergullu and Ucuncu, 1983; Karag ozl u, 1990 Santos et al., 2003 Yoshida and Toyoshima, 1994 Angulo et al., 1993

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Lactobacilli Lactobacillus ker Lactobacillus keranofaciens Lactobacillus kergranum Lactobacillus paraker Lactobacillus brevis Lactobacillus plantarum Lactobacillus helveticus Lactobacillus acidophilus Lactobacillus delbrueckii Lactobacillus rhamnosus Lactobacillus casei Lactobacillus paracasei Lactobacillus fructivorans, Lactobacillus hilgardii Lactobacillus fermentum, Lactobacillus viridescens, Lactobacillus gasseri Lactobacillus fermentum, L. mesenteroides, L. crispatus Lactococci Lactococcus lactis subsp. lactis

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Garbers et al., 2004 Ergullu and Ucuncu, 1983; Koreleva 1991; Pintado et al., 1996; Yuksekdag et al., 2004; Dousset and Caillet 1993; Ottogalli et al., 1973; Simova et al., 2002; Yoshida and Toyoshima, 1994; Garrote et al., 2001; Angulo et al., 1993; Kojic et al., 2007; Mainville et al., 2005 Garrote et al., 2001 Mainville et al., 2005 Yuksekdag et al., 2004; Simova et al., 2002; Ergullu and Ucuncu, 1983; Karag ozl u, 1990 Yuksekdag et al., 2004 Koreleva, 1991; Lin et al., 1999; Ottogalli et al., 1973; Garrote et al., 2001 Garrote et al., 2001 Ottogalli et al., 1973 Koreleva, 1991; Rosi, 1978; Angulo et al. 1993; Rohm et al., 1992 Rosi and Rossi, 1978; Engel et al., 1986 Angulo et al., 1993; Marshall, 1993; Engel et al., 1986; Berruga and Sanjose, 1997 Latorre Garcia et al., 2007 Latorre Garcia et al., 2007 Latorre Garcia et al., 2007 Latorre Garcia et al., 2007 Latorre Garcia et al., 2007 Wang et al., 2008; Berruga and Sanjose, 1997 Wang et al., 2008 Wang et al., 2008 Iwasawa et al., 1982 Angulo et al., 1993; Engel et al., 1986 Angulo et al., 1993

Lc. lactis subsp. lactis biovar. diacetylactis Lc. lactis subsp. cremoris Streptococci Streptococcus thermophilus Streptococcus cremoris, Streptococcus faecalis Streptococcus durans Leuconostoc mesenteroides Acetic Acid Bacteria Acetobacter sp. Acetobacter pasteurianus Acetobacter aceti Yeast Saccharomyces cerevisiae Saccharomyces delbruecki Candida ker Kluyveromyces lactis, Issatchenkia orientalis Saccaromyces unisporus Saccharomyces exiguus Saccharomyces humaticus Kluyveromyces marxianus Saccharomyces turicensis Pichia fermentas Torulopsis holmii Candida holmii Torulospora delbrueckii, Candida friedricchi, Candida albicans

However, Hlastan-Ribi c et al. (2005) studied that the Wistar rats with colorectal epithelial tumors were fed with ker made from 1.1% fat milk and 3.5% fat milk. No protective effect from ker was observed in this study. The protective effects of ker and Vitamin C in mice against toxicity of azoxymethane was studied by Sozmen et al. (2005). It was reported that azoxymethane causes severe liver lesions in mice and ker ad-

ministration reduced the severity of these lesions (Sozmen et al., 2005). Cenesiz et al. (2008) concluded that ker had an antioxidative effect in mice with colonic abnormal crypt formation induced by azoxymethane. Malondialdehyde and nitric oxide levels were increased in liver, stomach, spleen, and colon in the azoxymethane group while the kerazoxymethane group had lower increases of these compounds present in the organs.

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Figure 1

Schematic diagram of functional properties of ker.

EFFECT OF KEFIR ON CHOLESTEROL Cell In Vitro Tests Positive effects on cholesterol metabolism have been reported due to yogurt consumption and several hypotheses have been proposed regarding the possible mechanism of action (Kiessling et al., 2002; Xiao et al., 2003; Guven et al., 2003). Vujicic et al. (1992) reported that ker grains from different origins could assimilate and reduce cholesterol up to 62% in milk incubated at 20 C for 24 h or up to 84% for ker incubated and stored at 10 C for 48 h. Yoon et al. (1998) reported that cholesterol assimilation was strain dependent and L. acidophilus CU 673 isolated from ker displayed the highest cholesterol assimilation activity with 68.8% reduction. The same research team also reported that L. plantarum and L. paracasei and some Bidobacterium strains exhibited cholesterol assimilation activity. In one reported clinical study, St-Onge et al. (2002) noted that ker consumption in thirteen hypocholesterolemic men did not decrease plasma lipid concentration.

dase was reported in the ker-supplemented group which would suggest improvement in protein digestion. Ker supplementation did not affect body weights, body growth index, and organ weight. The levels of triacylglycerol, cholesterol, and HDL cholesterol slightly increased in the ker supplemented group. Liu et al. (2006) reported that milk ker and soy milk ker lowered serum triacylglycerol and total cholesterol concentrations in hamsters. Guven et al. (2003) reported that malonyldialdehyde levels of plasma in mice fed with ker and yogurt decreased, which indicated fermented dairy products had a protective effect against lipid peroxidation. These conicting results with ker may be due to the difference in ker grains used in the experimental study. Yoshida et al. (2005) reported that cell wall substances of Kluyveromyces marxianus YIT 8292 such as mannan and -glucan resulted in hypocholesterolemic activity in rats.

ACE Inhibitory Activity Angiotension converting enzyme (ACE) inhibitory activity was detected in ker made from caprine milk. This activity was due to the formation of low molecular weight peptides released from the major milk protein casein (Quiros et al., 2005). Sixteen peptides were identied in the fractions collected by reversephase HPLC. Two of those peptides (PYVRYL and LVYPFTGPPN) had ACE inhibitory activity. Maeda et al. (2004) reported that the consumption of keran signicantly reduced

Animal Tests Urdaneta et al. (2007) analyzed the effect of ker on intestinal enzymatic activity, sugar uptake, and body weight. Twenty female Wistar rats were fed with standard- and ker-supplemented diets for 22 days. Increased activity of the intestinal dipepti-

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blood pressure. ACE activities in the serum and thoracic aorta of SHRSP/Hos rats were signicantly reduced in all of the keranfed groups. Lower levels of total cholesterol, LDL-cholesterol, and triglycerides in the serum were also observed.

ANTIMICROBIAL PROPERTIES Cell In Vitro Tests Ker has an antibacterial effect against many pathogenic organisms due to the inherent formation of organic acids, hydrogen peroxide, acetaldehyde, carbon dioxide, and bacteriocins (Powell et al., 2007). For example, 3.5 kDa bacteriocin was identied from Lactobacillus plantarum ST8KF in ker (Powell et al., 2007). The antibacterial effect of ker produced from a freezedried commercial starter culture (PROBAT KC3, Danisco, Denmark) was determined against Staphylococcus aureus (ATCC 29213), Bacillus cereus (ATCC 11778), Salmonella enteritidis (ATCC 13076), Listeria monocytogenes (ATCC 7644), and Escherichia coli (ATCC 8739) and compared with ampicillin and gentamycin (Ulusoy et al., 2007). The antimicrobial effect was determined after 24 h and 48 h fermentations and during 7 day cold storage. Zones of inhibition formed by the antibiotics and the ker samples were similar for each pathogen; for example, the inhibition zone (in diameter) for E. coli was 19.5 mm, 18.6 mm, 20.2 mm, and 20.8 mm for 24 h fermented ker, 48 h fermented ker, ampicillin, and gentamycin, respectively. Antimicrobial activity of ker was as effective as ampicillin and gentamycin while neither the length of fermentation nor the duration of cold storage signicantly affected the antimicrobial activity (Ulusoy et al., 2007). Santos et al. (2003) studied the probiotic properties of Lactobacillus spp. isolated from ker. The team used Caco-2 cells as a model for human enterocytes. The strains of Lactobacillus spp. were tested for adhesion ability to Caco-2 cell, resistance to pH 2.5 and bile acids, antimicrobial prole activity, and inhibition of S. typhimurium. It was determined that L. acidophilus CYC 10051 and L. keranofaciens CYC 10058 had strong probiotic properties.

researchers also noted that mitochondrial dehydrogenase activity in cell toxicity tests was higher in the presence of keran. Scanning electron microscopy indicated that keran imparted a protective effect against structural cell damages by B. cereus. Rodrigues et al. (2005) conducted an animal study using Wistar rats with induced skin lessions and inoculated with 0.1 mL of Staphylacoccus aureus to determine the cicatrizing effects of ker. In the study, NaCl as negative control group, neomycin clostebol emulsion as positive control, or ker gel were applied topically to the wounds. Seven days of continuous treatment with the 70% ker gel caused improved wound healing better than even the application of positive control neomycinclostebol emulsion.

STIMULATION OF THE IMMUNE SYSTEM Animal Tests It was reported in a number of animal studies that dietary lactobacilli stimulated the immune system (Perdigon et al. 1986; 1987; 1988). Thoreux and Schmucker (2001) reported that ker consumption increased the specic intestinal mucosal immune response against cholera toxin in young adult rats. However, the same effect was not observed in senescent rats. Ker consumption in BALB/c female mice modulated the intestinal mucosal immune response because IgA+ and IgG+ cells were increased after feeding with ker regardless of the fact that the ker contained different doses of viable or heat-inactivated bacteria. In a study by Vinderola et al. (2005), the importance of ker dose and cell viability to obtain an intestinal mucosal immune response in the mouse gut was investigated. Ker increased the phagocytic activity of peritoneal and pulmonary macrophages. In a second study, these same authors investigated the immunomodulating capacity of keran produced by the ker microora L. keranofaciens. The oral administration of keran (100 mg/kg) for 7 days resulted in improved gut mucosal response with an increased number of IgA+ cells and caused a concurrent increase in small intestine IL-4, IL-6, IL-10+, and IL-6+ cells.

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Animal Tests Marquina et al. (2002) reported that the consumption of ker increased the population of lactic acid bacteria and decreased the population of Enterobacteriaceae and Clostridia in the mucosa of mice bowel. Kakisu et al. (2007) reported that the introduction of 5% ker grains can prevent the growth of Bacillus cereus while 1% ker grains did not produce a similar effect. Medrano et al. (2008) reported that keran protected against Bacillus cereus B 10502 damage to Caco-2 cells when introduced in the concentration range from 300 to 1000 mg/l. The study revealed that keran was capable of signicantly protecting cultured enterocytes from activity of B. cereus B10502 supernatants. The

LACTOSE INTOLERANCE EFFECT Animal and Human Trials A signicant proportion of the global population is lactose intolerant, due to insufcient intestinal -galactosidase activity (Alm, 1982). The enzyme -galactosidase degrades lactose into the monosaccharides glucose and galactose. Without galactosidase activity, intact lactose is carried into the intestinal tract where coliform bacteria digest it and produce carbon dioxide which can cause discomfort and gastrointestinal symptoms (Alm, 1982). During lactic acid fermentation, a signicant amount of lactose is utilized and the overall concentration of

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lactose decreases. De Viese et al. (1992) investigated the effect of ker consumption on lactose digestion. In animal trials, the team reported that mean postprandial plasma galactose peak was improved by 30% through the consumption of ker. Hertzler and Clancy (2003) conducted a human trial to determine the effect of keran on lactose digestion in adults with lactose maldigestion. Ker consumption reduced the severity of atulence by 71%. CONCLUSION Ker is a distinctive fermented dairy product due to the unique, multi-species natural ker grains used as the starter culture during the product manufacture. The microbiological and chemical composition of ker provide a complex probiotic effect due to the inherent lactic acid bacteria and yeast. The metabolic substances produced during fermentation have proven neutraceutical activities. Such positive health properties lend credence to the view that ker is a valuable food and warrants further laboratory and clinical study. REFERENCES
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