Improving the Antioxidant Properties of Fermented Camel Milk Using Some Strains of <i>Lactobacillus</i> — Oak Academic Publishing
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Improving the Antioxidant Properties of Fermented Camel Milk Using Some Strains of <i>Lactobacillus</i>
Department of Dairy Technology Research, Food Technology Research Institute, ARC, Giza, Egypt
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Dairy Microorganisms and Cheese Research Laboratory (DMCR), Department of Dairy Science and Technology, Faculty of Agriculture, Alexandria University, Alexandria, Egypt
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Animal Breeding Department, Animal and Poultry Production Division, Desert Research Centre, Matariya, Cairo, Egypt
1 Department of Dairy Technology Research, Food Technology Research Institute, ARC, Giza, Egypt
2 Dairy Microorganisms and Cheese Research Laboratory (DMCR), Department of Dairy Science and Technology, Faculty of Agriculture, Alexandria University, Alexandria, Egypt
3 Animal Breeding Department, Animal and Poultry Production Division, Desert Research Centre, Matariya, Cairo, Egypt
This study aimed at improving the antioxidant capacity of fermented camel milk using some single strains of <i> Lactobacillus </i> ( <i> Lb. helveticus </i> B-734 , <i> Lb. casei </i> subsp. <i> casei </i> B-1922, <i> Lb. paracasei </i> subsp. <i> paracasei </i> B-4560, <i> Lb. rhamnosus </i> B-1445 or <i> Lb. rhamnosus </i> B-442), as well as evaluating the acceptability of the final products. The acidity, proteolysis degree, antioxidant activity, viscosity and organoleptic properties of fermented milk were assessed during 14 days of storage at 4 ° C. Total phenolic content (TPC), DPPH radical scavenging activity, Ferrous ion chelating ability (FCA) and Ferric reducing antioxidant power (FRAP) assays were used to determine the antioxidant activity of fermented milks. The results indicated that fermented milks differed significantly (P < 0.05) in all studied parameters due to the type of starter culture used. During storage period, samples containing <i> Lb. helveticus </i> had the highest proteolysis degree, while samples with commercial starter culture (control) showed the lowest degree of proteolysis. Fermented milks containing <i> Lactobacillus </i> strains showed higher DPPH radical scavenging activity compared to those samples containing commercial starter culture. By the end of storage, there was a significant improvement (P < 0.05) in scavenging activity for all fermented milk samples. Regarding FCA, at the beginning of storage fermented milks containing <i> Lb. paracasei </i> , <i> Lb. rhamnosus </i> B-442 or commercial starter culture had the highest FCA values, while <i> Lb. rhamnosus </i> B-1445 samples recorded the highest value at the end of storage. <i> Lb. helveticus </i> samples had the highest TPC and FRAP values (P < 0.05) throughout the storage. There was a high significant correlation (P < 0.0001) between the proteolysis degree and the values of FRAP and TPC. Samples containing <i> Lb. rhamnosus </i> B-442, <i> Lb. rhamnosus </i> B-1445 or commercial starter culture received the highest taste and overall acceptability scores while <i> Lb. helveticus </i> samples were the lowest. It is recommended to use <i> Lb. rhamnosus </i> B-442 and <i> Lb. rhamnosus </i> B-1445 for producing fermented camel milk with high antioxidant activity and acceptability.
Salami, M., Yousefi, R., Ehsani, M.R., Razavi, S.H., Chobert, J.M., Haertl, T., et al. (2009) Enzymatic Digestion and Antioxidant Activity of the Native and Molten Globule States of Camel β-Lactalbumin: Possible Significance for Use in Infant Formula. International Dairy Journal, 19, 518-523. https://doi.org/10.1016/j.idairyj.2009.02.007
Bai, Y. and Zhao, D. (2015) The Acid-Base Buffering Properties of Alxa Bactrian Camel Milk. Small Ruminant Research, 123, 287-292. https://doi.org/10.1016/j.smallrumres.2014.10.011
Quan, S., Tsuda, H. and Miyamoto, T. (2008) Angiotensin I-Converting Enzyme Inhibitory Peptides in Skim Milk Fermented with Lactobacillus helveticus 130B4 from Camel Milk in Inner Mongolia, China. Journal of the Science of Food and Agriculture, 88, 2688-2692. https://doi.org/10.1002/jsfa.3394
Badkook, M.M. (2013) Fermented Camel Milk Reduces Inflammation in Rats Fed a High-Fat Diet. International Journal of Health Sciences and Research, 3, 7-17.
Solanki, D. and Hati, S. (2018) Fermented Camel Milk: A Review on Its Bio-Functional Properties. Emirates Journal of Food and Agriculture, 30, 268-274. https://doi.org/10.9755/ejfa.2018.v30.i4.1661
Berhe, T., Seifu, E., Ipsen, R., Kurtu, M.Y. and BechHansen, E. (2017) Processing Challenges and Opportunities of Camel Dairy Products. International Journal of Food Science, 2017, Article ID: 9061757. https://doi.org/10.1155/2017/9061757
Donkor, O.N., Henriksson, A., Singh, T.K., Vasiljevic, T. and Shah, N.P. (2007) ACE-Inhibitory Activity of Probiotic Yoghurt. International Dairy Journal, 17, 1321-1331. https://doi.org/10.1016/j.idairyj.2007.02.009
El-Sayed, M.I., Awad, S., Wahba, A., El Attar, A., Yousef, M.I. and Zedan, M. (2016) In Vivo Anti-Diabetic and Biological Activities of Milk Protein and Milk Protein Hydrolyaste. Advances in Dairy Research, 4, Article ID: 1000154.
Awad, S., El-Sayed, M.I., Wahba, A., El Attar, A., Yousef, M.I. and Zedan, M. (2016) Antioxidant Activity of Milk Protein Hydrolyaste in Alloxan-Induced Diabetic Rats. Journal of Dairy Science, 99, 8499-8510. https://doi.org/10.3168/jds.2015-10626
El-Sayed, M. and Awad, S. (2019) Milk Bioactive Peptides: Antioxidant, Antimicrobial and Anti-Diabetic Activities. Advances in Biochemistry, 7, 22-33. https://doi.org/10.11648/j.ab.20190701.15
Jrad, Z., Girardet, J.M., Adt, I., Oulahal, N., Degraeve, P., Khorchani, T. and El Hatm, H. (2014) Antioxidant Activity of Camel Milk Casein before and after in Vitro Simulated Enzymatic Digestion. Mljekarstvo, 64, 287-294. https://doi.org/10.15567/mljekarstvo.2014.0408
Lactobacillus<
/i>
Phelan, M., Aherne, A., FitzGerald, R.J. and O’Brien, N.M. (2009) Casein-Derived Bioactive Peptides: Biological Effects, Industrial Uses, Safety Aspects and Regulatory Status. International Dairy Journal, 19, 643-654. https://doi.org/10.1016/j.idairyj.2009.06.001
Pimentel, F.B., Cermeño, M., Kleekayai, T., Harnedy, P., et al. (2020) Effect of in Vitro Simulated Gastrointestinal Digestion on the Antioxidant Activity of the Red Seaweed Porphyra dioica. Food Research International, 136, Article ID: 109309. https://doi.org/10.1016/j.foodres.2020.109309
Zhou, D., Zhu, B., Lu, Q., Wu, H., Li, D., Yang, J., et al. (2012) In Vitro Antioxidant Activity of Enzymatic Hydrolysates Prepared from Abalone (Haliotis discus hannai Ino) Viscera. Food and Bioproducts Processing, 90, 148-154. https://doi.org/10.1016/j.fbp.2011.02.002
Savijoki, K., Ingmer, H. and Varmanen, P. (2006) Proteolytic Systems of Lactic Acid Bacteria. Applied Microbiology and Biotechnology, 71, 394-406. https://doi.org/10.1007/s00253-006-0427-1
Kunji, E.R.S., Mierau, I., Hagting, A., Poolman, B. and Konings, N. (1996) The Proteolytic System of Lactic Acid Bacteria. Antonie Leeuwenhoek, 70, 187-221. https://doi.org/10.1007/BF00395933
Bahobail, A.S., Ali, A.A. and Alyan, A.A. (2014) Effect of Fermentation Process on the Improvement of Nutrition Value of Camel Milk. International Journal of Multidisciplinary and Current Research, 2, 78-82.
Moslehishad, M., Ehsani, M.R., Salami, M., Mirdamadi, S., Ezzatpanah, H., Naslaji, A.N. and Moosavi-Movahedi, A.A. (2013) The Comparative Assessment of ACE-Inhibitory and Antioxidant Activities of Peptide Fractions Obtained from Fermented Camel and Bovine Milk by Lactobacillus rhamnosus PTCC 1637. International Dairy Journal, 29, 82-87. https://doi.org/10.1016/j.idairyj.2012.10.015
Ayyash, M., Al-Nuaimi, A.K., Al-Mahadin, S. and Liu, S.Q. (2017) In Vitro Investigation of Anticancer and ACE-Inhibiting Activity, α-Amylase and α-Glucosidase Inhibition, and Antioxidant Activity of Camel Milk Fermented with Camel Milk Probiotic: A Comparative Study with Fermented Bovine Milk. Food Chemistry, 239, 588-597. https://doi.org/10.1016/j.foodchem.2017.06.149
Kansci, G., Genot, C., Meynier, A., Gaucheron, F. and Chobert, J.M. (2004) B-Caseinophosphopeptide (f1-25) Confers on β-Casein Tryptic Hydrolysate an Antioxidant Activity during Iron/Ascorbate-Induced Oxidation of Liposomes. Lait, 84, 449-462. https://doi.org/10.1051/lait:2004019
Moslehishad, M., Mirdamadi, S., Ehsani, M.R., Ezzatpanah, H. and Moosavimovahed, A.A. (2013) The Proteolytic Activity of Selected Lactic Acid Bacteria in Fermenting Cow’s and Camel’s Milk and the Resultant Sensory Characteristics of the Products. International Journal of Dairy Technology, 66, 279-285. https://doi.org/10.1111/1471-0307.12017
Salami, M., Moosavi-Movahedi, A.A., Moosavi-Movahe-di, F., Ehsani, M.R., Yousefi, R., Fahadi, M., Niasari-Nasl-aji, A., Saboury, A.A., Chobert, J.M. and Haertlé, T. (2011) Biological Activity of Camel Milk Casein Following Enzymatic Digestion. Journal of Dairy Research, 78, 471-487. https://doi.org/10.1017/S0022029911000628
Tamime, A.Y. and Robinson, R.K. (2007) Tamime and Robinson’s Yoghurt: Science and Technology. 3rd Edition, Woodhead Publishing Limited, Cambridge, 11-118.
AOAC (2005) Official Methods of Analysis of the Association Analytical Chemists. 18th Edition, Association of Official Analytical Chemistry, Gaithersburg.
Shori, A.B. and Baba, A.S. (2013) Antioxidant Activity and Inhibition of Key Enzymes Linked to Type-2 Diabetes and Hypertension by Azadirachta indica-Yogurt. Journal of Saudi Chemical Society, 17, 295-301. https://doi.org/10.1016/j.jscs.2011.04.006
Folkertsma, B. and Fox, P.F. (1992) Use of the Cd-Ninhydrin Reagent to Assess Proteolysis in Cheese during Ripening. Journal of Dairy Research, 59, 217-224. https://doi.org/10.1017/S0022029900030466
Laemmli, U.K. (1970) Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4. Nature, 277, 680-685. https://doi.org/10.1038/227680a0
Abirami, A., Nagarani, G. and Siddhuraju, P. (2014) In Vitro Antioxidant, Antidiabetic, Cholinesterase and Tyrosinase Inhibitory Potential of Fresh Juice from Citrus hystrix and C. maxima Fruits. Food Science and Human Wellness, 3, 16-25. https://doi.org/10.1016/j.fshw.2014.02.001
Lim, Y.Y. and Quah, E.P.L. (2007) Antioxidant Properties of Different Cultivars of Portulaca oleracea. Food Chemistry, 103, 734-740. https://doi.org/10.1016/j.foodchem.2006.09.025
Chan, E.W.C., Lim, Y.Y. and Chew, Y.L. (2007) Antioxidant Activity of Camellia sinensis Leaves and Tea from a Lowland Plantation in Malaysia. Food Chemistry, 102, 1214-1222. https://doi.org/10.1016/j.foodchem.2006.07.009
Oyaizu, M. (1986) Studies on Products of Browning Reaction: Antioxidative Activities of Products of Browning Reaction Prepared from Glucosamine. Japan Journal of Nutrition, 44, 307-315. https://doi.org/10.5264/eiyogakuzashi.44.307
Papadimitriou, C.G., Mastrojiannaki, A.V., Silva, A.V., Gomes, A.M., Malcata, F.X. and Alichanidis, E. (2007) Identification of Peptides in Traditional and Probiotic Sheep Milk Yoghurt with Angiotensin I-Converting Enzyme (ACE)-Inhibitory Activity. Food Chemistry, 105, 647-656. https://doi.org/10.1016/j.foodchem.2007.04.028
Al-Sheraji, S.H., Ismail, A., Manap, M.Y., Mustafa, S., Yusof, R.M. and Hassan, F.A. (2013) Prebiotics as Functional Foods: A Review. Journal of Functional Foods, 5, 1542-1553. https://doi.org/10.1016/j.jff.2013.08.009
Shori, A.B. (2013) Antioxidant Activity and Viability of Lactic Acid Bacteria in Soybean-Yogurt Made from Cow and Camel Milk. Journal of Taibah University for Science, 7, 202-208. https://doi.org/10.1016/j.jtusci.2013.06.003
De-Oliveira, M.N. (2014) Fermented Milks and Yogurt (in Fermented Milks). In: Batt, C. and Batt, C.A., Eds., Encyclopedia of Food Microbiology, 2nd Edition, Academic Press, London, 908-922. https://doi.org/10.1016/B978-0-12-384730-0.00121-X
Sasaki, M., Bosman, B.W. and Tan, P.S.T. (1995) Comparison of Proteolytic Activities in Various Lactobacilli. Journal of Dairy Research, 62, 601-610. https://doi.org/10.1017/S0022029900031332
Griffiths, M.W. and Tellez, A.M. (2013) Lactobacillus helveticus: The Proteolytic System. Frontiers in Microbiology, 4, 1-9. https://doi.org/10.3389/fmicb.2013.00030
El-Zahar, K., Sitohy, M., Dalgalarrondo, M., Choiset, Y., Métro, F., et al. (2004) Purification and Physicochemical Characterization of Ovine β-Lactoglobulin and α-Lactalbumin. Nahrung/Food, 48, 177-183. https://doi.org/10.1002/food.200300447
Li, S., Tang, S., He, Q., Hu, J. and Zheng, J. (2019) Changes in Proteolysis in Fermented Milk Produced by Streptococcus thermophilus in Co-Culture with Lactobacillus plantarum or Bifidobacterium animalis subsp. lactis during Refrigerated Storage. Molecules, 24, 3699. https://doi.org/10.3390/molecules24203699
Ainsworth, E.A. and Gillespie, K.M. (2007) Estimation of Total Phenolic Content and Other Oxidation Substrates in Plant Tissues Using Folin-Ciocalteu Reagent. Nature Protocols, 2, 875-877. https://doi.org/10.1038/nprot.2007.102
Virtanen, T., Pihlanto, A., Akkanen, S. and Korhonen, H. (2007) Development of Antioxidant Activity in Milk Whey during Fermentation with Lactic Acid Bacteria. Journal of Applied Microbiology, 102, 106-115. https://doi.org/10.1111/j.1365-2672.2006.03072.x
Alemán, A., Giménez, B., Pérez-Santin, E., Gómez-Guillén, M. and Montero, P. (2011) Contribution of Leu and Hyp Residues to Antioxidant and ACE-Inhibitory Activities of Peptide Sequences Isolated from Squid Gelatin Hydrolysate. Food Chemistry, 125, 334-341. https://doi.org/10.1016/j.foodchem.2010.08.058
Namdari, A. and Nejati, F. (2016) Development of Antioxidant Activity during Milk Fermentation by Wild Isolates of Lactobacillus helveticus. Applied Food Biotechnology, 3, 178-186.
Yilmaz-Ersan, L., Ozcan, T., Akpinar-Bayizit, A. and Sahin, S. (2016) The Antioxidative Capacity of Kefir Produced from Goat Milk. International Journal of Chemical Engineering and Applications, 7, 22-26. https://doi.org/10.7763/IJCEA.2016.V7.535
Barac, M., Vucic, T., Zilic, S., Pesic, M., Sokovic, M., Petrovic, J., Kostic, A., Ignjatovic, I.S. and Milincic, D. (2019) The Effect of in Vitro Digestion on Antioxidant, ACE-Inhibitory and Antimicrobial Potentials of Traditional Serbian White-Brined Cheeses. Foods, 8, 94. https://doi.org/10.3390/foods8030094
Abd El-Fattah, A., Sakr, S., El-Dieb, S.M. and Elkashef, H. (2017) Biological Activities of Lactobacilli Relevant to Cardiovascular Health in Skim Milk. Food Science and Biotechnology, 26, 1613-1623. https://doi.org/10.1007/s10068-017-0219-7
Abou-Soliman, N.H.I. (2020) The Impact of Using Some Adjunct Cultures on the Quality of Fermented Camel Milk Fortified with Iron. Journal of Food and Dairy Science, Mansoura University, 11, 251-257. https://doi.org/10.21608/jfds.2020.118364
Walters, M.E., Esfandi, R. and Tsopmo, A. (2018) Potential of Food Hydrolyzed Proteins and Peptides to Chelate Iron or Calcium and Enhance Their Absorption. Foods, 7, 172. https://doi.org/10.3390/foods7100172
Zhang, T., Li, Y., Miao, M. and Jiang, B. (2011) Purification and Characterisation of a New Antioxidant Peptide from Chickpea (Cicer arietium L.) Protein Hydrolysates. Food Chemistry, 128, 28-33. https://doi.org/10.1016/j.foodchem.2011.02.072
Zhu, K.X., Su, C.Y., Guo, X.N., Peng, W. and Zhou, H.M. (2011) Influence of Ultrasound during Wheat Gluten Hydrolysis on the Antioxidant Activities of the Resulting Hydrolysate. International Journal of Food Science and Technology, 46, 1053-1059. https://doi.org/10.1111/j.1365-2621.2011.02585.x
Putri, Y.D., Setianim, N.A. and Warya, S. (2020) The Effect of Temperature, Incubation and Storage Time on Lactic Acid Content, pH and Viscosity of Goat Milk Kefir. Current Research on Biosciences and Biotechnology, 2, 101-104. https://doi.org/10.5614/crbb.2020.2.1/HPMQ5042
Fguiri, I., Ziadi, M., Abassi, M., Arroum, S. and Khorchani, T. (2012) Suitability of Camel Milk to Transformation in Leben by Lactic Starter. African Journal of Microbiology Research, 6, 7185-7192.
Kavas, N. (2016) Yoghurt Production from Camel (Camelus dramedarius) Milk Fortified with Samphire Molasses and Different Colloids. Mljekarstvo, 66, 34-47. https://doi.org/10.9734/BJAST/2016/23683
Buffa, M., Morais, J., Jiménez-Belenguer, A., Hernández-Giménez, E. and Guamis, B. (2005) Technological Characterization of Lactic Acid Bacteria Isolated from Raw Ewes’ Milk for Cheese Making. Milchwissenschaft, 61, 404-407.
Amani, E., Eskandari, M.H. and Shekarforoush, S. (2017) The Effect of Proteolytic Activity of Starter Cultures on Technologically Important Properties of Yogurt. Food Science & Nutrition, 5, 525-537. https://doi.org/10.1002/fsn3.427