PROBIOTIC YOGHURT MANUFACTURED WITH TIGER-NUT EXTRACT (CYPERUS ESCULENTUS) AS A FUNCTIONAL DAIRY FOOD

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1 El-Shenawy et al, Journal of Agricultural Research and Natural Resources, 1(2): 20-31, September 2012 Available online at Science Park Journals Review PROBIOTIC YOGHURT MANUFACTURED WITH TIGER-NUT EXTRACT (CYPERUS ESCULENTUS) AS A FUNCTIONAL DAIRY FOOD M. El-Shenawy*, M. Abd El-Aziz, W.I. El-kholy, M.T. Fouad Dairy Science Dept., National Research Centre, Dokki, Cairo 12311, Egypt. Accepted 23 August 2012 ABSTRACT: Tiger-nut (cyperus esculentus) has nutritional and health benefits. A probiotic yoghurt fortified with tiger-nut extract (TNE) was manufactured using the conventional yoghurt starter together with Bifidobacterium bifidum as a probiotic bacterial strain. Tiger-nut extract was prepared and added at a concentration of, 20, and 30% to Buffalo's skim milk. The chemical, rheological and sensory properties of the final product, as well as, the viability of the LAB were evaluated during of storage at refrigeration temperature. The (LAB) strains have showed relatively higher counts in yoghurt fortified with TNE than the corresponding control. No changes in post acidification of yoghurt treatments were observed. Yoghurt containing % TNE have showed the highest apparent viscosity and the lowest whey syneresis, however the product containing 30% have showed the lowest apparent viscosity and highest whey syneresis. No significant differences were observed in sensory properties among yoghurt containing or 20% TNE and control. The results indicated that, addition of or 20% TNE could serve as a good fortification for manufacturing of nutritional and therapeutic yoghurt since it will not influence the chemical and sensory properties, instead it will improve the rheological properties of the final product. Keywords: Tiger-nut extract, Probiotic yoghurt, Functional dairy food. Introduction Yoghurt in human nutrition is based not only on the nutritive effect of milk but also on its beneficial effect on intestinal micro flora, prophylactic and health effects (Marshall, 1984 and Buttriss, 1997). Yoghurt can be presented in large varieties ranging from set or stirred yoghurt, plain, partly skimmed or skimmed to sweetened and flavored forms (Imele & Atemnkeng, 2001). The probiotic bacteria used in commercial products are mainly members of the genera lactobacillus and bifidobacterium (Heller, 2001). Bifidobacteria are recognized currently as promoting the health of humans. Their potential beneficial roles in human intestines have been reported. Bifidobacteria exhibits antagonistic effects towards enteropathogenic bacteria (Saleh & El-sayed, 2004 and kebary et al., 200), reduces the risk of diarrhea, enhances immune function, reduces cholesterol levels, reduces the risk of eczema, relieves lactose intolerance symptoms and exhibits antitumorigenic activity (Marteau et al, 2001, Calder & Kew, 2002, Wright et al., 2002, and Ibrahim et al., 200). Because of these health benefits, efforts have been devoted to incorporate bifidobactria into dairy products. Cyperus esculentus (Tiger nut in English, Habelaziz in Arabic and Chufa in Spanish) has long been recognized for its health benefits as *Correspondence: m_elshenawy@hotmail.com Tel: they are rich in fiber, protein, natural sugars, minerals such as phosphorous and potassium and in vitamins such as E and C. They have a high content of soluble glucose and oleic acid, along with high energy content (starch, fats, sugars and proteins (Mason, 2008). Zhang (1996) reported that the oil of the yellow nut-sedge tuber was found to contain 18% saturated (palmitic acid and stearic acid) and 82% unsaturated (olieic acid and linoleic acid) fatty acids. The nut was found to be ideal for children, elder persons and sportsman (Martinez, 2003). In Egypt, it is widely eaten as soaked tubers and is used, like in China, as a liver tonic, to heal stomach pain, mouth and gum ulcers, promote normal menstruation, enhance production of breast milk in nursing mothers and in folk medicine it used as a colon evacuator and cleaner. These numerous nutritional advantages, health benefits and therapeutic advantages associated with tigernut makes it more attractive for fortification of milk used in manufacture of dairy products. Therefore, this work has been done to evaluate the effect of incorporation of probiotic lactic acid bacterial starters together with tiger-nuts extract, to buffalo's skim milk, on the chemical, rheological and sensory properties of yoghurt manufactured from buffalo s skim milk when stored at refrigerator temperature for. Study of the viability of the used bacterial strains, during this storage time, was another goal of the study

2 Table 1. Gross composition of yoghurt supplemented with different level of Tiger-nut extract. Gross composition Treatments Total solids Total protein Fat Carbohydrates Ash (%) C T T T C, control probiotic yoghurt made without Tiger-nut extract; T 1, probiotic yoghurt supplemented with % Tiger-nut extract; T 2, probiotic yoghurt supplemented with 20 % Tiger-nut extract; T 3, probiotic yoghurt supplemented with 30 % Tiger-nut extract. MATERIALS AND METHODS buffalo s skim milk and sweet cream (~ 40.0% fat) were obtained from the farm of Fac. Agric., Cairo Univ., Egypt. Skim milk powder (low heat), made in the USA was purchased from the local market at Cairo, Egypt. Tiger-Nut (cyperus esculentus) was purchased from Al Azhar market, Cairo, Egypt. Strains of Streptococcus thermophilus and Lactobacillus bulgaricus were obtained from stock cultures of Dairy Microbiology Lab., National Research Centre, Dokki-Cairo, Egypt. Strain of Bifidobacterium bifidum was obtained from Chr. Hansen s Lab., A/S Copenhagen- Denmark. Preparation of the Tiger-nut extract Tiger-nut extract was prepared by sorting out all unwanted objects and other rotten nuts, washed and rinsed in distilled water and soaked overnight to soften the fiber. The water was changed 2-3 times to avoid bad smell. Nine-hundred grams of tiger-nuts were added to two liters of warm water and blended several times. The mash was then sieved twice with a neat cloth to separate the extract. It was further strained to obtain a fine consistency. The filtered extract was heated at 90 C for 1 minutes, cooled to 4 C and refrigerated for further processes. Starter activation Bifidobacterium bifidum was activated by three successive transfers in modified MRS (Venting & Mistry, 1993), followed by three successive transfers in sterile % reconstituted skim milk powder and incubated at 37 C under anaerobic conditions. Lactobacillus bulgaricus and Streptococcus thermophilus were activated individually by three successive transfers in sterile % reconstituted skim milk powder..

3 El-Shenawy et al. 22 Preparation of yoghurt Tiger-nut extract was added to Buffalo's skim milk at a concentration of 0,, 20, and 30%. All mixtures were heated to 60 C and adjusted to have the similar total solids (~1.0%) and milk fat (~3.2%) contents using skim milk powder and sweet cream (Table 1). Heating was raised to 90 C, held for min and followed by cooling to 4 C. This was followed by inoculation with 1.0% w/v of S. thermophilus, L. bulgaricus, and B. bifidum. The inoculated mixtures were mixed thoroughly, dispensed in 0 ml polystyrene cups and incubated at 42 C until a uniform coagulation was formed (Barrantes et al., 1994). The produced yoghurt treatments were analyzed when fresh, and after 3, 7 and of storage at 4±2 C. The yogurt manufacturing was done three times. Bacteriological analysis Yoghurt samples were diluted and subsequently plated in duplicate onto selective media. MRS medium was used to enumerate L. bulgaricus (De Man et al., 1990) and the plates were incubated at 37 C for 48 h. S. thermophilus was enumerated on M17 agar after aerobic incubation at 37C for 48 h (Terzaghi & sandine, 197). B. bifidum was determined according to (Blanchett et al., (1996) using modified MRS agar supplemented with 0.0% L-cysteine-HCl and the plates were incubated at 37 C for 48 h under anaerobic conditions. Coliforms group were enumerated according to Harrigan & McCance (1996), using Violet Red Bile Agar medium; incubated at 37 C for 24 h. Moulds and yeasts were determined using Malt Extract Agar medium and the plates were incubated at 30 C for days. Chemical analysis Total solids, fat, total nitrogen (TN), water soluble nitrogen (WSN) and ash content were determined according to methods described in AOAC (2007). Protein content was calculated by multiplying the percentage of total nitrogen by The ph was measured using a digital ph meter (HANNA, instrument, Italy). Acetaldehyde and diacetyl of the yoghurt samples were measured using Shimadzu spectrophotometer (240 UV Vis, Japan) as described by Less & Jago (1970). Whey syneresis An amount of 0 g. of the yoghurt sample was placed into centrifuge tube and centrifuged for 20 min at 1290 xg (Sigma Laborzentri Fugen, 2 K1, Germany) as described by Aguilera and Kessler (1989). The weight fraction of the supernatant liquid was used as index of whey syneresis. Apparent viscosity Yoghurt samples were gently stirred times in clockwise direction with a plastic spoon prior to viscosity measurements. Apparent viscosity was measured at 7 o C using a Brookfield digital viscometer (Model DV-II, Spindle-0, Canada). The sample was subjected to shear rates ranging from 3 to 0 S -1 for upward curve. Viscosity was expressed as Pascal (Pa.s). Sensory properties evaluation Yoghurt samples were evaluated for their sensory properties (appearance, body & texture, flavor) on a -point hedonic scale ( excellent, 1 unacceptable) performed by expert judges selected from staff member of Dairy Science Department, National Research Center, Egypt (Mohebbi & Ghoddusi, 2008). Yoghurt samples were presented in three-digit coded white plastic containers and tasted 1 minutes after leaving refrigerator.

4 23 C T1 T2 T3 Streptococcus thermophilus 9 Logcfu/g) Storage period (Days) C T1 T2 T3 Lactobacillus delbrueck ii spp bulgarius 9 Logcfu/g) Storage period (Days) C T1 T2 T3 Bifidiobacterium bifidum 9 Logcfu/g) Storage period (Days) Fig (1). The count of S. thermophilus, L. delbrueckii sub sp. bulgaricus and Bifidobactrium bifidum during storage of control yoghurt and yoghurts supplemented with different levels of Tiger-nut extract at 4±2 C for. C, control probiotic yoghurt made without Tiger-nut extract; T 1, probiotic yoghurt supplemented with % Tiger-nut extract; T 2, probiotic yoghurt supplemented with 20 % Tiger-nut extract; T 3, probiotic yoghurt supplemented with 30 % Tiger-nut extract.

5 El-Shenawy et al. 24 Statistical analysis Data were expressed as means ±SE. Statistical analysis was performed using the GLM procedure with software SAS (2004). Analysis of variance (ANOVA) and Duncan's multiple comparison procedure were used to compare the means. A probability of P< 0.0 was used to establish statistical significance. Microbiological properties Figure 1 demonstrates the changes in counts (log cfu/g) of the yoghurt starters including S. thermophilus, L. bulgaricus and B. bifidum during refrigerated storage of the control and treatments made with different levels of tiger-nut extract. In general, there was no significant difference (P > 0.0), in the counts of S. thermophilus, L. bulgaricus and Bifidobactrium bifidum, in the control and all yoghurt treatments even though these counts were numerically higher in all treatments than in the control. This increase in counts of lactic acid bacteria may be due to the presence of some growth promoter, such as salts, free amino acids, or vitamins present in Tiger-nut extract (Mason, 2008). During storage time, a slight increase (P > 0.0) was detected in the counts of these microorganisms at day 3 and remained stable until day. Thereafter, a significant decrease (P < 0.0) in count of S. thermophilus at day 7 and in counts of L. bulgaricus and Bifidobactrium bifidum at day was observed. This reduction in counts may be attributed to the high acidity, resulted from the presence of lactic and acetic acids, which decline the viable microorganisms till the end of storage period (Hamann & Marth, 1984 and Dave & Shah, 1997). The Japanese Fermented Milk and Lactic Acid Bacteria Beverages Association (26, 27) reported that a minimum of 6 7 viable cfu/gm should be present in food product in order to meet the requirements of probiotic food to have health promoting effects. Our current results demonstrated that the counts of the numbers of Bifidobacterium bifidum remained more than seven log cycles/g, in all treatments, until the end of storage period which is in agreement of the requirements of the former Japanese the Japanese Beverages Association (Olvieira et al., 2002). A similar observation was mad by Zhao (2006). Moulds, yeasts and coliforms bacteria were not detected in all treatments either when fresh or during refrigerated storage which reflects the good hygienic conditions during manufacture and storage, as well as, the bactericidal effect of the used starter and probiotic bacteria. Similar findings were obtained by Atalla (2006).

6 2 Table (2). Changes in ph, acetaldehyde and diacetyl during storage of plain control yoghurt and yoghurts supplemented with different levels of Tiger-nut extract stored at 4 ±2 C for. Biochemical properties Treatments Storage period ph Acetaldehyde (µmol/0g) Diacetyl (µmol/0g) C.08 a ± a ±0..00 a ± a ± cde ± de ± e ± e ± c ± c ± bc ± bc ±1.20 T b ± b ± bc ± b ± ab ± abc ± bcd ± de ± c ± c ± c ± bc ±1.23 T dc ± d ± dc ± d ± a ± a ± abc ± cde ± bc ± bc ± bc ± ab ±1.24 T d ± d ± d ± d ± abc ± bcd ± cde ± cde ± bc ± abc ± ab ± a ± 1.16 Means with the same letters are not significantly differences (p<0.0). C, control probiotic yoghurt made without Tiger-nut extract; T 1, probiotic yoghurt supplemented with % Tiger-nut extract; T 2, probiotic yoghurt supplemented with 20% Tiger-nut extract; T 3, probiotic yoghurt supplemented with 30% Tiger-nut extract. Chemical properties As shown in Table 2, all probiotic yoghurt samples showed a significant (P < 0.0) decrease in the ph at day 3 and 7, after which the decreases were not significant (P > 0.0) for the rest of the storage period. ph decreased (p < 0.0) at the same rate within all yoghurt samples during storage. Similar changes in the ph during storage of yoghurt were obtained by Ozer et al., 200 and Ramchandran & Shah, There was no significant difference (P > 0.0) in the ph of the control and all treatments (T1, T 2 and T 3 ). Thus, supplementation with Tiger-nut extract did not influence (P > 0.0) either on the fermentation process or on the final ph of yoghurt. Acetaldehydes together with Daicetyl are the major aroma compounds (Gilliland, 198 and Beshkova et al., 1998). Both T 1 and T 2 treatments showed a significant (P < 0.0) increase in the acetaldehyde content compared with the control at fresh, day 3 and day 7 of storage after which the increase was not significant (P > 0.0). Acetaldehyde content of T 3 sample was also higher than that of control, but the differences were not significant (P > 0.0). A gradual decrease in the concentration of acetaldehyde was observed until day, the increase being significant (P < 0.0) only at day

7 El-Shenawy et al. 26 in T 1 and T 2 samples. No significant change in the concentration of diacetyl between all yoghurt samples was observed until day 3. Thereafter, a gradual increase in the concentration of diacetyl was observed until day, which was more pronounced in T 3 (P < 0.0). Gilliland (198) reported that, in mixed cultures diacetyl production is enhanced by the rapid drop in ph associated with the growth of Streptococci. The results of acetaldehyde and diacetyl content during storage are in agreement with Vahcic and Hruskar (2000), in which acetaldehyde and ethanol were found to decrease at temperature levels of 4, 20, and 37 C during 2 day of storage. Our obtained levels of acetaldehyde and diacetyl may explained by the high level of Tiger-nut extract which may reduce acetaldehyde to ethanol and thus enhance the production of diacetyl. 40 C T1 T2 T3 Syneresis (g/0g) Storage period (Days) Fig (2). Whey syneresis during storage of control yoghurt and yoghurts supplemented with different levels of Tiger-nut extract at 4±2 C for. C, Plain control probiotic yoghurt; T 1, probiotic yoghurt supplemented with % Tiger-nut extract; T 2, probiotic yoghurt supplemented with 20 % Tiger-nut extract; T 3, probiotic yoghurt supplemented with 30 % Tiger-nut extract. Rheological properties Figure 2 exhibits the whey syneresis during storage time of the control and the different treatments. On day 1, whey syneresis was significantly (P < 0.0) lower in T 1 and T 2 than in the control however in T 3 It was significantly higher than in the control (P 0.0). There was no difference in the amount of whey syneresis resulted in T 1 and T 2 even if whey syneresis was numerically higher in T 2 than in T 1. Its appears that supplementation with low level of Tiger-nut extract may contain some polysaccharides which enhance the water holding capacity, while supplementation with the high level impaired the yoghurt structure, thereby increased whey syneresis. Folkenberg et al. (2006) observed that syneresis was more pronounced in EPS containing yoghurts. They have suggested that yoghurts should have a structure with medium size pores containing polysaccharides to provide a stable structure with minimum syneresis. A gradual decrease in the whey syneresis of all yoghurt samples was observed until day, the decrease being significant (P<0.0) only at day 3 in control and

8 27 T 3 sample. A similar observation during storage was made by Doleyres et al. (200) in yoghurts prepared using EPS-producing cultures. At lower temperatures, bonds between gel particles are either stronger or their numbers are greater which helps in holding water and prevents whey syneresis (Walstra et al., 1999 and Doleyres et al., 200). Viscosity (Pa.s) C 1% 2% 3% Shear rate (S -1 ) Viscosity (Pa.s) C 1% 2% 3% Shear rate (S -1 ) 3 C 1% 2% 3% Viscosity (Pa.s) Shear rate (S -1 )

9 El-Shenawy et al. 28 Visco sity (Pa.s) C 1% 2% 3% Shear rate (S -1 ) Fig (3). Apparent viscosity during storage of control yoghurt and yoghurts supplemented with different levels of Tiger-nut extract at 4 ±2 C for. C, Plain control probiotic yoghurt; T 1, probiotic yoghurt supplemented with % Tiger-nut extract; T 2, probiotic yoghurt supplemented with 20% Tiger-nut extract; T 3, probiotic yoghurt supplemented with 30% Tiger-nut extract The results of yoghurt viscosity containing Tiger-nut extract during cold storage at different shear rate are shown in Fig 3. The apparent viscosity of T 1 (on increasing shear rate, corresponding to the downward curve) was higher than that of the control and T 2, the difference being not significant (P < 0.0) throughout the storage period. However, the apparent viscosity was lower in T 3 than in control yoghurt, T 1 and T 2, the difference being significant (P<0.0) only at fresh and day. This is confirmed by the higher (P < 0.0) whey syneresis (Fig 2) of T 3 as compared to other yoghurt samples. These results could be attributed to either the lower protein content in T 3 (Table 1) or the higher level of Tiger-nut extract which decrease intermolecular bonds between micelles of casein. A gradual increase in the apparent viscosity of all yoghurt samples was observed until day, the increase being significant (P < 0.0) only at day 3 in T 3 and day 7 in T1, T2 and control yoghurt. Walstra et al (1999) reported that during storage, the bonds between the particles of the gel became stronger or their numbers are greater. Presumably, this is because the particles are more swollen and are thereby connected to each other over a larger area.

10 29 Table (3). Sensory properties during storage of control yoghurt and yoghurt supplemented with different levels of Tiger-nut extract stored at 4 ±2 C for. Treatments C Storage period Sensory properties Appearance Body & Texture 4.37 a ± a ± ab ± a ± abc ± ab ± abc ± ab ±0.23 Flavor 4.2 a ± a ± ab ± ab ±0.16 T abc ± ab ± abc ± abc ± ab ± ab ± ab ± ab ± ab ± ab ± ab ± ab ±0.13 T abc ± abc ± abc ± bc ± ab ± ab ± ab ± ab ± ab ± ab ± ab ± ab ±0.19 T abc ± abc ± abc ± ab ± ab ± ab ± ab ± ab ± b ± c ± b ± b ±0.26 Means with the same letters are not significantly differences (p<0.0). C, control plain probiotic yoghurt; T 1, probiotic yoghurt supplemented with % Tiger-nut extract; T 2, probiotic yoghurt supplemented with 20% Tiger-nut extract; T 3, probiotic yoghurt supplemented with 30% Tigernut extract. Sensory properties As shown in Table 3, there was no significant difference in the score of sensory properties (appearance, body & texture and flavor) in T 1 and T 2 compared with control at different storage period. In T 3, the score of sensory properties was lower than those in control, the difference being significant (P<0.0) only at day in appearance and body & texture, and at day 7 and in flavor. Presence of starch and pectin in yoghurt were found to induce a significant decrease of aroma compounds In conclusion, these results indicated that, addition of or 20% TNE could serve as a good fortification for manufacturing of nutritional and in the headspace Decourcelle et al. (2004) and Lubbers et al. (2004). Probiotic yoghurt made with high level of Tiger-nut extract (T 3) characterized with weak body (gelatinous body) and sweet flavor, which may impair the pleasant acid flavor. Slight decrease in sensory properties was observed during cold storage. Similar observations by Zhao (2006) and Routray and Mishra (2011), were found that the storage time had a negative impact on the flavor score of yoghurt. Thus, sensory quality decreased with duration and was closely related to changes in the contents of aroma compounds. therapeutic yoghurt since it will not influence the chemical and sensory properties, instead it will improve the rheological properties of the final product.

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