The Effect of Inulin on Properties of Functional Fermented Milk Produced by Native Strains Isolated from Traditional Iranian Yogurt
Subject Areas : Microbiology
Faezeh shirkhan
1
,
Saeed Mirdamadi
2
,
mahta mirzaei
3
,
Behrouz Akbari-adergani
4
,
Nikoo Nasoohi
5
1 - Department of Food Science and Technology, Faculty of Pharmacy, Tehran Medical Sience, Islamic Azad,
Tehran, Iran.
2 - Professor, Department of Biotechnology, Iranian Research Organization for Science & Technology (IROST), Tehran, Iran, email: Mirdamadi@irost.ir
3 - Assistant professor, Department of Food Science and Technology, Shahr-e-Qods Branch, Islamic Azad University, Tehran, Iran
4 - Professor of food and drug laboratory research center, food and drug administration, ministry of health and medical education, Tehran, Iran
5 - Assistant Professor, Department of Biochemistry and Biophysics, Faculty of Advanced Science and Technology, Tehran Medical Sciences, Islamic Azad University, Tehran, Iran
Keywords: Inulin, Diabetes, Native strains, Fermented Milk, Functional foods, Storage time,
Abstract :
Introduction: The inclination to manufacture beneficial dairy products has increased in recent years, as consumers pay more attention to food products with adequate sensory qualities and health benefits. Materials and Methods: The current study looked first at the anti-diabetic efficacy of milk fermented by Lactobacillus delbrueckii, and Lactobacillus helveticus strains isolated from traditional yogurt as well as co-culture of two-strain based on the inhibitory activity of alpha-amylase and alpha-glucosidase enzymes for the production of functional fermented milk. Then, added 1% inulin as an appropriate and applied prebiotic to fermented milk resulting from the combination of two strains and evaluated physicochemical, anti-diabetic, anti-oxidant, proteolysis rate, and population of bacteria during 19 days at 4°C.Results: The results indicated that milk fermented with two-strain bacterial intercropping had stronger inhibitory activity on alpha-amylase (45%) and alpha-glucosidase (35%) than single strains of Lactobacillus delbrueckii and Lactobacillus helveticus (p<0.05). The addition of inulin increased the inhibitory activity of alpha-amylase (20%) and alpha-glucosidase (33%) at the end of fermentation, respectively. During storage at 4°C, the composition two bacterial strains and inuline significantly increased the population of bacteria, acidity and viscosity and significantly reduced the pH and proteolysis rate of fermented milk. However, there was a decrease in antioxidant and antidiabetic activities. Conclusion: The results revealed that both bacterial strains in combination with inulin have the capacity to produce functional food.
Astawan, M., Wresdiyati, T., Arief, I. I. & Septiawan, R. (2012). Production of synbiotic yogurt-like using indigenous lactic acid bacteria as functional food. Media Peternakan, 35(1), 9-14.
Ayyash, M., Al-Nuaimi, A. K., Al-Mahadin, S. & Liu, S. Q. (2018). 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.
Baba, A. S., Najarian, A., Shori, A. B., Lit, K. W. & Keng, G. A. (2014). Viability of Lactic Acid Bacteria, Antioxidant Activity and In Vitro Inhibition of Angiotensin-I-Converting Enzyme of Lycium barbarum Yogurt. Arabian Journal for Science and Engineering, 39 (7), 5355-5362.
Bedani, R., Rossi, E. A., Saad, S. M. I. (2013). Impact of inulin and okara on Lactobacillus acidophilus La-5 and Bifidobacterium animalis Bb-12 viability in a fermented soy product and probiotic survival under in vitro simulated gastrointestinal conditions. Food Microbiology, 34 (2), 382-389.
Boosjin, S. N., Noghani, V. F. & Hashemiravan, M. (2016). Characterization of probiotic fermented milk prepared by different inoculation size of mesophilic and thermophilic Lactic acid bacteria. Applied Food Biotechnology, 3(4), 276-282.
Chen, Y., Mi, Y., Li, Q., Dong, F. & Guo, Z. (2020). Synthesis of Schiff bases modified inulin derivatives for potential antifungal and antioxidant applications. International Journal of Biological Macromolecules, 143, 714-723.
Church, F. C., Swaisgood, H. E., Porter, D. H. & Catignani, G. L. (1983). Spectrophotometric Assay Using o-Phthaldialdehyde for Determination of Proteolysis in Milk and Isolated Milk Proteins. Journal of Aairy Science, 66(6), 1219-1227.
De Souza Oliveira, R. P., Perego, P., de Oliveira, M. N. & Converti, A. (2011). Effect of inulin as prebiotic and synbiotic interactions between probiotics to improve fermented milk firmness. Journal of Food Engineering, 107(1), 36-40.
Demain, A. L. & Solomon, N. A. (1986). Manual of Industrial Microbiology and Biotechnology. American Society for Microbiology, pp. 59-60.
Donkor, O. N., Henriksson, A., Vasiljevic, T. & Shah, N. P. (2006). Effect of acidification on the activity of probiotics in yoghurt during cold storage, International Dairy Journal, 16(10), 1181-1189.
Donkor, O. N., Nilmini, S. L. I., Stolic, P., Vasiljevic, T. & Shah, N. P. (2007). Survival and activity of selected probiotic organisms in set-type yoghurt during cold storage, International Dairy Journal, 17(6). 657–665.
Donkor, O.N., Henriksson, A., Vasiljevic, T. & Shah, N. P. (2005). Probiotic strains as starter cultures improve angiotensin-converting enzyme inhibitory activity in soy yogurt. Journal of Food Science, 70(8), 375-381.
Ehsani, J., Mohsenzadeh, M., Khomeiri, M., Ghasemnezhad, A. & Ebrahimi, S. (2020). A review of the most common prebiotic combinations, with an emphasis on inulin. Neyshabur University Medical Science, 8(4), 1-21 [In Persian].
El-Sayed, M. I., Awad, S. & Abou-Soliman, N. H. I. (2021). Improving the Antioxidant Properties of Fermented Camel Milk Using Some Strains of Lactobacillus. Food and Nutrition Sciences, 12 (4), 352-371.
Gargari, B. P., Dehghan, P., Aliasgharzadeh, A. & Jafar-Abadi, M. A. (2013). Effects of high performance inulin supplementation on glycemic control and antioxidant status in women with type 2 diabetes. Diabetes & Metabolism Journal, 37(2), 140-148.
Ghasab nezhad, M., Hojjati, M. & Jooyandeh, H. (2019). Effect of inulin on physico-chemical, microbial and sensory properties of the kefir produced of buffalo milk. Journal of Food Science and Technology, 16 (89), 357-367 [In Persian].
Guven, M., Yasar, K., Karaca, O. B. & Hayaloglu, A. A. (2005). The effect of inulin as a fat replacer on the quality of set-type low-fat yogurt manufacture. International Journal of Dairy Technology, 58(3), 180–184.
Habibi Najafi, M. B., Fatemizadeh, S. S. & Tavakoli, M. (2019). Release of Proteolysis Products with ACE-Inhibitory and Antioxidant Activities in Probiotic Yogurt Containing Different Levels of Fat and Prebiotics. International Journal of Peptide Research and Therapeutics, 25(1), 367-377.
Han, K., Cao, J., Wang, J., Chen, J., Yuan, K., Pang, F., Gu, S. & Huo, N. (2018). Effects of Lactobacillus helveticus Fermentation on the Ca2+ Release and Antioxidative Properties of Sheep Bone Hydrolysate. Korean Journal for Food Science of Animal Resources, 38 (6), 1144-1154.
Handaka, R., Wahyuni, E. & Taufiq, T. T. (2017). The quality of fermented milk produced using intestinal-origin lactic acid bacteria as starters. International Food Research Journal, 24(6), 2371–2376.
Kalyani Nair, K., Kharb, S. & Thompkinson, D. K. (2010). Inulin dietary fiber with functional and health attributes a review. Food Reviews Internationa, 26(2), 189-203.
Kwon, Y. I., Apostolidis, E. & Shetty, K. (2006). Anti-diabetes functionality of Kefir culture-Mediated fermented soymilk supplemented with Rhodiola extracts. Food Biotechnology, 20(1), 13-29.
Liao, S. M., Liang, G. E., Zhu, J., Lu, B. O., Peng, L.X., Wang, Q. Y., Wei, Y.T., Zhou, G. P. & Huang, R. B. (2019). Influence of Calcium Ions on the Thermal Characteristics of α-amylase from Thermophilic Anoxybacillus sp. GXS-BL. Protein and Peptide Letters, 26(2), 148-157.
Liu, J., Lu, J. F., Kan, J., Wen, X. Y. & Jin, C. H. (2014). Synthesis, characterization and in vitro anti-diabetic activity of catechin grafted inulin. International Journal of Biological Macromolecules, 64, 76-83.
Loghman, S., Moayedi, A., Mahmoudi, M. & Khomeiri, M. (2018). Evaluation of Proteolysis in milk fermented by proteolytic lactic acid bacteria and antibacterial activities of their peptide extract. Journal of Applied Microbiology, 4(2), 31-43 [In Persian].
Madhu, A. N., Amrutha, N. & Prapulla, S. G. (2012). Characterization and antioxidant property of probiotic and synbiotic yogurts. Probiotics and Antimicrobial Proteins, 4(2), 90-97.
Mashayekh, M., Taslimi, A., Ardeshir, H., Zohorian, G. & Abadi, A.R. (2009). Laboratory scale production of soy yogurt with strawberry Flavor. Iranian Journal of Science and Technology, 5(4), 1-9 [In Persian].
Mazloumi, S., Shekarforoush, S.S., Ebrahimnejad, H. & Sajedianfard, J. (2011). Effect of adding inulin on microbial and physicochemical properties of low fat probiotic yogurt, Iranian Journal of Veterinary Research, 12(2), 93–98.
Mirdamadi, S., Rajabi, A., Aziz Mohseni, F. & Momen B. (2007). Lactic acid production by Lactobacillus strains. Iranian Journal of Nutrition Sciences and Food Technology, 2(3), 57-64 [In Persian].
Mishra, S. & Mishra, H. N. (2018). Comparative study of the synbiotic effect of inulin and fructooligosaccharide with probiotics with regard to the various properties of fermented soy milk. Food Science and Technology International, 24(7), 564–575.
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Moslehishad, M., Ehsani, M. R., Salami, M., Mirdamadi, S., Ezzatpanah, H., Naslaji, A. N. & 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(2), 82-87.
Muganga, L., Liu, X., Tian, F., Zhao, J., Zhang, H. & Chen, W. (2015). Screening for lactic acid bacteria based on antihyperglycaemic and probiotic potential and application in synbiotic set yoghurt. Journal of Functional Foods, 16, 125-136.
Mukherjee, S., Pawar, N., Kulkarni, O., Nagarkar, B., Thopte, S., Bhujbal, A. & Pawar, P. (2011). Evaluation of free-radical quenching properties of standard Ayurvedic formulation Vayasthapana Rasayana, BMC Complement and Alternative Medicine, 11(1),1-6.
Nikmaram, P., Mousavi, S. M., Emam-Djomeh, Z., Kiani, H. & Razavi, S. H. (2015). Evaluation and prediction of metabolite production, antioxidant activities, and survival of Lactobacillus casei 431 in a pomegranate juice supplemented yogurt drink using support vector regression. Food Scienc and Biotechnology, 24(6), 2105-2112.
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Patil, P., Mandal, S., Tomar, S. K. &Anand, S. (2015). Food protein ‑ derived bioactive peptides in management of type 2 diabetes, European Journal of Nutrition, 54(6), 863-880.
Ramchandran, L. & Shah, N.P. (2009). Effect of EPS on the proteolytic and ACE-inhibitory activities and textural and rheological properties of low-fat yogurt during refrigerated storage. Journal of Dairy science, 92, 895–906.
Ramchandran, L. & Shah, N. P. (2010). Influence of addition of Raftiline HP® on the growth, proteolytic, ACE- and α-glucosidase inhibitory activities of selected lactic acid bacteria and Bifidobacterium. LWT-Food Science and Technology, 43(1), 146-152.
Rokhtabnak, N., Khaleghi, M. & Sasan, H. A. (2016). Isolation and identification of Lactobacillus bacteria with probiotic potential from traditional dairy in Kerman. Journal of Medical Microbiology, 10(1), 24-34 [In Persian].
Shahdadi, F. & Ezzati, R. (2020). Effect of Different Concentrations of Inulin and Whey on the Qualitative and Rheological Properties of Aloe vera Doogh Containing Microencapsulated probiotic bacteria. Food Science and Technology, 17(103), 15-31 [In Persian].
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_||_Astawan, M., Wresdiyati, T., Arief, I. I. & Septiawan, R. (2012). Production of synbiotic yogurt-like using indigenous lactic acid bacteria as functional food. Media Peternakan, 35(1), 9-14.
Ayyash, M., Al-Nuaimi, A. K., Al-Mahadin, S. & Liu, S. Q. (2018). 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.
Baba, A. S., Najarian, A., Shori, A. B., Lit, K. W. & Keng, G. A. (2014). Viability of Lactic Acid Bacteria, Antioxidant Activity and In Vitro Inhibition of Angiotensin-I-Converting Enzyme of Lycium barbarum Yogurt. Arabian Journal for Science and Engineering, 39 (7), 5355-5362.
Bedani, R., Rossi, E. A., Saad, S. M. I. (2013). Impact of inulin and okara on Lactobacillus acidophilus La-5 and Bifidobacterium animalis Bb-12 viability in a fermented soy product and probiotic survival under in vitro simulated gastrointestinal conditions. Food Microbiology, 34 (2), 382-389.
Boosjin, S. N., Noghani, V. F. & Hashemiravan, M. (2016). Characterization of probiotic fermented milk prepared by different inoculation size of mesophilic and thermophilic Lactic acid bacteria. Applied Food Biotechnology, 3(4), 276-282.
Chen, Y., Mi, Y., Li, Q., Dong, F. & Guo, Z. (2020). Synthesis of Schiff bases modified inulin derivatives for potential antifungal and antioxidant applications. International Journal of Biological Macromolecules, 143, 714-723.
Church, F. C., Swaisgood, H. E., Porter, D. H. & Catignani, G. L. (1983). Spectrophotometric Assay Using o-Phthaldialdehyde for Determination of Proteolysis in Milk and Isolated Milk Proteins. Journal of Aairy Science, 66(6), 1219-1227.
De Souza Oliveira, R. P., Perego, P., de Oliveira, M. N. & Converti, A. (2011). Effect of inulin as prebiotic and synbiotic interactions between probiotics to improve fermented milk firmness. Journal of Food Engineering, 107(1), 36-40.
Demain, A. L. & Solomon, N. A. (1986). Manual of Industrial Microbiology and Biotechnology. American Society for Microbiology, pp. 59-60.
Donkor, O. N., Henriksson, A., Vasiljevic, T. & Shah, N. P. (2006). Effect of acidification on the activity of probiotics in yoghurt during cold storage, International Dairy Journal, 16(10), 1181-1189.
Donkor, O. N., Nilmini, S. L. I., Stolic, P., Vasiljevic, T. & Shah, N. P. (2007). Survival and activity of selected probiotic organisms in set-type yoghurt during cold storage, International Dairy Journal, 17(6). 657–665.
Donkor, O.N., Henriksson, A., Vasiljevic, T. & Shah, N. P. (2005). Probiotic strains as starter cultures improve angiotensin-converting enzyme inhibitory activity in soy yogurt. Journal of Food Science, 70(8), 375-381.
Ehsani, J., Mohsenzadeh, M., Khomeiri, M., Ghasemnezhad, A. & Ebrahimi, S. (2020). A review of the most common prebiotic combinations, with an emphasis on inulin. Neyshabur University Medical Science, 8(4), 1-21 [In Persian].
El-Sayed, M. I., Awad, S. & Abou-Soliman, N. H. I. (2021). Improving the Antioxidant Properties of Fermented Camel Milk Using Some Strains of Lactobacillus. Food and Nutrition Sciences, 12 (4), 352-371.
Gargari, B. P., Dehghan, P., Aliasgharzadeh, A. & Jafar-Abadi, M. A. (2013). Effects of high performance inulin supplementation on glycemic control and antioxidant status in women with type 2 diabetes. Diabetes & Metabolism Journal, 37(2), 140-148.
Ghasab nezhad, M., Hojjati, M. & Jooyandeh, H. (2019). Effect of inulin on physico-chemical, microbial and sensory properties of the kefir produced of buffalo milk. Journal of Food Science and Technology, 16 (89), 357-367 [In Persian].
Guven, M., Yasar, K., Karaca, O. B. & Hayaloglu, A. A. (2005). The effect of inulin as a fat replacer on the quality of set-type low-fat yogurt manufacture. International Journal of Dairy Technology, 58(3), 180–184.
Habibi Najafi, M. B., Fatemizadeh, S. S. & Tavakoli, M. (2019). Release of Proteolysis Products with ACE-Inhibitory and Antioxidant Activities in Probiotic Yogurt Containing Different Levels of Fat and Prebiotics. International Journal of Peptide Research and Therapeutics, 25(1), 367-377.
Han, K., Cao, J., Wang, J., Chen, J., Yuan, K., Pang, F., Gu, S. & Huo, N. (2018). Effects of Lactobacillus helveticus Fermentation on the Ca2+ Release and Antioxidative Properties of Sheep Bone Hydrolysate. Korean Journal for Food Science of Animal Resources, 38 (6), 1144-1154.
Handaka, R., Wahyuni, E. & Taufiq, T. T. (2017). The quality of fermented milk produced using intestinal-origin lactic acid bacteria as starters. International Food Research Journal, 24(6), 2371–2376.
Kalyani Nair, K., Kharb, S. & Thompkinson, D. K. (2010). Inulin dietary fiber with functional and health attributes a review. Food Reviews Internationa, 26(2), 189-203.
Kwon, Y. I., Apostolidis, E. & Shetty, K. (2006). Anti-diabetes functionality of Kefir culture-Mediated fermented soymilk supplemented with Rhodiola extracts. Food Biotechnology, 20(1), 13-29.
Liao, S. M., Liang, G. E., Zhu, J., Lu, B. O., Peng, L.X., Wang, Q. Y., Wei, Y.T., Zhou, G. P. & Huang, R. B. (2019). Influence of Calcium Ions on the Thermal Characteristics of α-amylase from Thermophilic Anoxybacillus sp. GXS-BL. Protein and Peptide Letters, 26(2), 148-157.
Liu, J., Lu, J. F., Kan, J., Wen, X. Y. & Jin, C. H. (2014). Synthesis, characterization and in vitro anti-diabetic activity of catechin grafted inulin. International Journal of Biological Macromolecules, 64, 76-83.
Loghman, S., Moayedi, A., Mahmoudi, M. & Khomeiri, M. (2018). Evaluation of Proteolysis in milk fermented by proteolytic lactic acid bacteria and antibacterial activities of their peptide extract. Journal of Applied Microbiology, 4(2), 31-43 [In Persian].
Madhu, A. N., Amrutha, N. & Prapulla, S. G. (2012). Characterization and antioxidant property of probiotic and synbiotic yogurts. Probiotics and Antimicrobial Proteins, 4(2), 90-97.
Mashayekh, M., Taslimi, A., Ardeshir, H., Zohorian, G. & Abadi, A.R. (2009). Laboratory scale production of soy yogurt with strawberry Flavor. Iranian Journal of Science and Technology, 5(4), 1-9 [In Persian].
Mazloumi, S., Shekarforoush, S.S., Ebrahimnejad, H. & Sajedianfard, J. (2011). Effect of adding inulin on microbial and physicochemical properties of low fat probiotic yogurt, Iranian Journal of Veterinary Research, 12(2), 93–98.
Mirdamadi, S., Rajabi, A., Aziz Mohseni, F. & Momen B. (2007). Lactic acid production by Lactobacillus strains. Iranian Journal of Nutrition Sciences and Food Technology, 2(3), 57-64 [In Persian].
Mishra, S. & Mishra, H. N. (2018). Comparative study of the synbiotic effect of inulin and fructooligosaccharide with probiotics with regard to the various properties of fermented soy milk. Food Science and Technology International, 24(7), 564–575.
Moreno-Montoro, M., Olalla-Herrera, M., Rufián-Henares, J.Á., Martínez, R.G., Miralles, B., Bergillos, T., Navarro-Alarcón, M. & Jauregi, P. (2017). Antioxidant, ACE-inhibitory and antimicrobial activity of fermented goat milk: activity and physicochemical property relationship of the peptide components. Food & Function, 8(8), 2783-2791.
Moslehishad, M., Ehsani, M. R., Salami, M., Mirdamadi, S., Ezzatpanah, H., Naslaji, A. N. & 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(2), 82-87.
Muganga, L., Liu, X., Tian, F., Zhao, J., Zhang, H. & Chen, W. (2015). Screening for lactic acid bacteria based on antihyperglycaemic and probiotic potential and application in synbiotic set yoghurt. Journal of Functional Foods, 16, 125-136.
Mukherjee, S., Pawar, N., Kulkarni, O., Nagarkar, B., Thopte, S., Bhujbal, A. & Pawar, P. (2011). Evaluation of free-radical quenching properties of standard Ayurvedic formulation Vayasthapana Rasayana, BMC Complement and Alternative Medicine, 11(1),1-6.
Nikmaram, P., Mousavi, S. M., Emam-Djomeh, Z., Kiani, H. & Razavi, S. H. (2015). Evaluation and prediction of metabolite production, antioxidant activities, and survival of Lactobacillus casei 431 in a pomegranate juice supplemented yogurt drink using support vector regression. Food Scienc and Biotechnology, 24(6), 2105-2112.
Panwar, H., Calderwood, D., Grant, I. R., Grover, S. & Green, B. D. (2014). Lactobacillus strains isolated from infant faeces possess potent inhibitory activity against intestinal alpha and beta-glucosidases suggesting anti-diabetic potential. European Journal of Nutrition, 53(7(, 1465-1474.
Patil, P., Mandal, S., Tomar, S. K. &Anand, S. (2015). Food protein ‑ derived bioactive peptides in management of type 2 diabetes, European Journal of Nutrition, 54(6), 863-880.
Ramchandran, L. & Shah, N.P. (2009). Effect of EPS on the proteolytic and ACE-inhibitory activities and textural and rheological properties of low-fat yogurt during refrigerated storage. Journal of Dairy science, 92, 895–906.
Ramchandran, L. & Shah, N. P. (2010). Influence of addition of Raftiline HP® on the growth, proteolytic, ACE- and α-glucosidase inhibitory activities of selected lactic acid bacteria and Bifidobacterium. LWT-Food Science and Technology, 43(1), 146-152.
Rokhtabnak, N., Khaleghi, M. & Sasan, H. A. (2016). Isolation and identification of Lactobacillus bacteria with probiotic potential from traditional dairy in Kerman. Journal of Medical Microbiology, 10(1), 24-34 [In Persian].
Shahdadi, F. & Ezzati, R. (2020). Effect of Different Concentrations of Inulin and Whey on the Qualitative and Rheological Properties of Aloe vera Doogh Containing Microencapsulated probiotic bacteria. Food Science and Technology, 17(103), 15-31 [In Persian].
Shakerian, M., Hadi Razavi, S., Khodaiyan, F., Ziai, S. A., Saeid Yarmand, M. & Moayedi, A. (2014). Effect of different levels of fat and inulin on the microbial growth and metabolites in probiotic yogurt containing nonviable bacteria. International Journal of Food Science & Technology, 49(1), 261–268.
Shang, H. M., Zhou, H. Z., Yang, J. Y., Li, R., Song, H. & Wu, H. X. (2018). In vitro and in vivo antioxidant activities of inulin. PLoS ONE., 13(2), 1–12.
Simsek, S., Sánchez-Rivera, L., El, S. N., Karakaya, S. & Recio, I. (2017). Characterisation of in vitro gastrointestinal digests from low fat caprine kefir enriched with inulin. International Dairy Journal, 75, 68-74.
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