Survival of Lactobacillus acidophilus La-5 Encapsulated Along with Spirulina platensis and the Application of this Capsule in Sour Cherry Juice as a Probiotic Drink

Belyani, Samira; Emtyazjoo, Mozhgan; Mirmoghtadaie, Leila; Hosseini, Seyede Marzieh

doi:10.30492/ijcce.2022.558995.5467

Survival of Lactobacillus acidophilus La-5 Encapsulated Along with Spirulina platensis and the Application of this Capsule in Sour Cherry Juice as a Probiotic Drink

Document Type : Research Article

Authors

¹ Department of Food Science and Technology, Faculty of Biological Sciences, North Tehran Branch, Islamic Azad University, Tehran, I.R. IRAN

² Department of Marine Science and Technology, Faculty of Marine Science and Technology, North Tehran Branch, Islamic Azad University, Tehran, I.R. IRAN

³ Department of Food Science and Technology, National Nutrition and Food Technology Research Institute, Faculty of Nutrition Sciences and Food Technology, Shahid Beheshti University of Medical Sciences, Tehran, I.R. IRAN

10.30492/ijcce.2022.558995.5467

Abstract

This study investigated the effects of the microencapsulation of Lactobacillus acidophilus La-5 along with Spirulina platensis on bacterial survival in sour cherry juice containing synbiotic capsules. S. platensis powder was used as a prebiotic and the microencapsulation of bacteria and S. platensis was conducted using the spray dryer method. S. platensis and bacteria were encapsulated in maltodextrin and cross-linked alginate. Bacterial survival, thermal tolerance, morphology, efficiency, and resistance under simulated gastric and intestinal conditions in sour cherry juice were examined. The results showed a decrease in probiotic bacterial death in sour cherry juice containing bacteria and algae encapsulated at 4°C on the 28th day of storage (7.9 ± 0.10) (Log CFU/mL) as well as an increase in temperature resistance in fruit juice containing bacteria capsules and S. platensis. The results of Scanning Electron Microscopy (SEM) analysis revealed that the capsules contained L. acidophilus La-5 and S. platensis with round shapes and had an average diameter of 12.80 ± 1.43 µm. The examination of bacterial encapsulation efficiency indicated that the highest and lowest values for bacteria encapsulated with Spirulina and bacteria capsules without Spirulina were 81.9% and 79.86%, respectively. In addition, organoleptic analysis of sour cherry juice at 4°C and at the end of storage duration in the refrigerator demonstrated the highest general acceptance (4.60 ± 0.10) for the juice, containing bacteria and Spirulina compared to other bacterial groups (p<0/05). L. acidophilus La-5 capsules containing Spirulina showed the largest viability during the 0-10 min period and 60-80°C temperature (p<0/05). Moreover, bacteria encapsulated with Spirulina exhibited the highest survival rate under simulated gastric and intestinal conditions over a 0-120 min incubation time. Overall, using S. platensis as a prebiotic can significantly stimulate the growth of L. acidophilus La-5 as a beneficial probiotic, which results in the production of healthier and more nutritious sour cherry juice.

Keywords

Main Subjects

Food Science & Technology

References

[1] Vejdani Nia M., Emtyazjoo M., Chamani M., Functional Quails Eggs using Enriched Spirulina during the Biosorption Process, Food Sci. Anim. Resour,42(1): 34-45 (2022).

[2] Ranjbar-Shamsi S., Sharifan A., Emtyazjoo M., Moslehishad M., The Chemical and Nutritional Properties of Processed Fruit Enriched with Algae, Journal of Food Quality, 2021 (2021).

[3] Alemzadeh I., Afarin M., Dehghan A., Sani M.A., Teimouri M., Seilani F., Abbasi P. and Vaziri A.S., Clinical Uses and Survival Study of Free and Encapsulated Probiotic Bacteria in Fruit Juices: A Review, Applied Food Biotechnology, 8(3): 161-180 (2021).

[4] Roberfroid M.B., Prebiotics and Probiotics: Are They Functional Foods?, Am. J. Clin. Nutr., 71(6): 1682S-1687S (2000).

[5] Williams N.T., Probiotics, American Journal of Health-System Pharmacy, 67(6): 449-458 (2010).

[6] Huy N.D., Phuong T.T.T., Kim T.L.T., Hoang V.N.Q., Quang L.N., Le Cong T., Dinh B.T., Chau A.N.T., Phuong L.T.T., Seung-Moon P., Assessment of Antioxidant and Antibacterial Activities of Lactobacillus farciminis HN11 as a Probiotic Candidate, Applied Food Biotechnology, 9(2): 103-112(2022).

[7] Zoghi A., Khosravi-Darani K., Sohrabvandi S., Attar H., Alavi S.A., Survival of Probiotics In Synbiotic Apple Juice During Refrigeration and Subsequent Exposure to Simulated Gastro-Intestinal Conditions, Iranian Journal of Chemistry and Chemical Engineering (IJCCE), 38(2): 159-170 (2019).

[8] Håkansson, Å., Bränning C., Molin G., Adawi D., Hagslätt M.L., Jeppsson B., Nyman M., Ahrne S., Blueberry husks and Probiotics Attenuate Colorectal Inflammation and Oncogenesis, and Liver Injuries in Rats Exposed to Cycling DSS-treatment, PLoS One, 7(3): e33510 (2012).

[9] Sarin S.K., Pande A., Schnabl B., Microbiome as a Therapeutic Target in Alcohol-Related Liver Disease, Journal of Hepatology, 70(2):260-272 (2019).

[10] Fang, H., Elina T., Heikki A., Seppo S., Modulation of Humoral Immune Response Through Probiotic Intake, FEMS Immunology & Medical Microbiology, 29(1): 47-52 (2000).

[11] Nanji A.A., Khettry U., Sadrzadeh S.H., Lactobacillus Feeding Reduces Endotoxemia and Severity of Experimental Alcoholic Liver (disease), Proceedings of the Society for Experimental Biology and Medicine, 205(3): 243-247(1994).

[12] Kligler B, Cohrssen A., Probiotics, American Family Physician, 78(9):1073-1078 (2008).

[13] Ahn, J.H., Kim Y.P., Seo E.M., Choi Y.K., Kim H.S., Antioxidant Effect of Natural Plant Extracts on the Microencapsulated High Oleic Sunflower Oil, Journal of Food Engineering, 84(2): 327-334(2008).

[14] Khoshtinat K., Barzegar M., Sahari M.A., Hamidi Z., Comparison of Antioxidant and Antibacterial Activities of Free And Encapsulated Garlic Oil with Beta-Cyclodextrin, Applied Food Biotechnology, 3(4): 254-268 (2016).

[15] Khoshtinat K., Barzegar M., Sahari M. A., Hamidi Z., Use of Encapsulated Garlic Oil in Low-Fat Salad Dressings: Physicochemical, Microbial and Sensory Properties, Applied Food Biotechnology, 9(2): 113-125 (2022).

[16] Dubey R., Microencapsulation Technology and Applications, Defence Science Journal, 59(1):82-95 (2009).

[17] Baygan A., Safaeian Sh., Shahinfar R., Khoshkhoo Zh., Encapsulation of Essential Oil of Ziziphoria clinopodioides Using Maltodextrin and Gum Arabic by Spray Drying Method, Iranian Journal of Food Science and Technology, 18(120): 263-281 (2022).

[18] Baygan A., Safaeian Sh., Shahinfar R., Khoshkhoo Zh., Comparing Antibacterial Properties of Ziziphora Clinopodioides Essential Oil in Free and Encapsulated States in Minced Beef Contaminated with Salmonella Typhimurium, Iranian Journal of Chemistry & Chemical Engineering (IJCCE), 42(2): - (2023) [in Press].

[19] Ruiz-Gonzalez N., Lopez-Malo A., Palou E., Ramirez-Corona N., Jimenez-Munguia M.T., Antimicrobial Activity and Physicochemical Characterization of Oregano, Thyme and Clove Leave Essential Oils, Nonencapsulated and Nanoencapsulated, Using Emulsification, Applied Food Biotechnology, 6(4): 237-246(2019).

[20] Karimi N., Ghanbarzadeh B., Hamishehkar H., Keyvani F., Pezeshki A., Gholian M.M., Phytosome and Liposome: the Beneficial Encapsulation Systems in Drug Delivery and Food Application, Applied Food Biotechnology, 2(3):17-27 (2015).

[21] Beikzadeh S., Shojaee-Aliabadi S., Dadkhodazade E., Sheidaei Z., Abedi A.S., Mirmoghtadaie L., Hosseini S.M., Comparison of Properties of Breads Enriched with Omega-3 Oil Encapsulated in β-Glucan and Saccharomyces Cerevisiae Yeast Cells, Applied Food Biotechnology, 7(1): 11-20 (2019).

[22] Tafreshi S.Y.H., Mirdamadi S., Survey Study of Lipid Effect on Nisin Nanoliposome Formation and Application in Pasteurized Milk as a Food Model, Applied Food Biotechnology, 2(2): 7-14 (2015).

[23] Goh C.H., Heng P.W.S., Chan L.W., Alginates as a Useful Natural Polymer for Microencapsulation and Therapeutic Applications, Carbohydrate Polymers, 88(1): 1-12 (2012).

[24] Yari M., Fooladi J., Motlagh M. A. K., Microencapsulation and Fermentation of Lactobacillus acidophilus LA-5 and Bifidobacterium BB-12, Applied Food Biotechnology, 2(4): 27-32 (2015).

[25] Mandal S., Puniya A., Singh K., Effect of Alginate Concentrations on Survival of Microencapsulated Lactobacillus casei NCDC-298, International Dairy Journal, 16(10): 1190-1195(2006).

[26] Krasaekoopt, W., Bhandari B., Deeth H., Evaluation of Encapsulation Techniques of Probiotics for Yoghurt, International Dairy Journal, 13(1): 3-13 (2003).

[27] Jafari S.M., Rabbani M., Emtyazjoo M., Piryaei F., Effect of dietary Spirulina platensis on Fatty Acid Composition of Rainbow Trout (Oncorhynchus mykiss) Fillet, Aquaculture International, 22(4): 1307-15 (2014).

[28] de Caire G.Z., Parada J.L., Zaccaro M.C., de Cano M.M.S, Effect of Spirulina platensis biomass on the growth of lactic acid bacteria in milk, World Journal of Microbiology and Biotechnology, 16(6): 563-565 (2000).

[29] İlter I., Akyıl S., Demirel Z., Koç M., Conk-Dalay M., Kaymak-Ertekin F., Optimization of Phycocyanin Extraction from Spirulina platensis Using Different Techniques, Journal of Food Composition and Analysis, 70: 78-88 (2018).

[30] Shabana E.F., Gabr M.A., Moussa H.R., El-Shaer E.A., Ismaiel M.M., Biochemical Composition and Antioxidant Activities of Arthrospira (Spirulina) platensis in Response to Gamma Irradiation, Food Chemistry, 214:550-555 (2017).

[31] Osanlou R., Emtyazjoo M., Banaei A., Hesarinejad M.A., Ashrafi F., Preparation of Solid Lipid Nanoparticles and Nanostructured Lipid Carriers Containing Zeaxanthin and Evaluation of Physicochemical Properties, Colloids and Surfaces A: Physicochemical and Engineering Aspects, 641: 128588 (2022).

[32 ] Marles R.J., Barrett M.L., Barnes J., Chavez M.L., Gardiner P., Ko R., Mahady G.B., Dog T.L., Sarma N.D., Giancaspro G.I., Sharaf M., United States Pharmacopeia Safety Evaluation of Spirulina, Critical Reviews in Food Science and Nutrition, 51(7): 593–604 (2011).

[33] Anvar A. A., Nowruzi B., Bioactive Properties of Spirulina: A Review, Microb. Bioact, 4(1): 134-142. (2021).

[34] Mukunda Vani M., Govardhana Rao D., Effective Diffusivity Coefficients for Degradation of Pectin in Guava (Psidium guajava L.) Pulps Using Immobilized Pectinase, Applied Food Biotechnology, 6 (2): 119-26 (2019).

[35] Abdollahi Aghdam S., Fotouhifar K.B., Introduction of Some Endophytic Fungi of Sour Cherry Trees (Prunus cerasus) in Iran, Rostaniha, 18(1): 77-94 (2017).

[36] Wallace T.C., Anthocyanins in Cardiovascular Disease, Adv. Nutr, 2(1): 1-7 (2011).

[37] Senthilkumar P., Shavrov V., Lega P., Subramani R., Resveratrol-Loaded β-Lactoglobulin Nanofibrils to Prevent Enzymatic Browning on Sliced Apple, Applied Food Biotechnology, 9(1): 9-16 (2022).

[38] Ştefănuţ M.N., Căta A., Pop R., Tănasie C., Boc D., Ienaşcu I., Ordodi V., Anti-hyperglycemic Effect of Bilberry, Blackberry and Mulberry Ultrasonic Extracts on Diabetic Rats, Plant Foods Hum Nut, 68(4): 378-384 (2013).

[39] Gyenis B., Szigeti J.F., Molnar N., Varga L., Use of Dried Microalgal Biomasses to Stimulate Acid Production and Growth of Lactobacillus plantarum and Enterococcus faecium in Milk, Acta Agraria Kaposváriensis, 9(2): 53-9(2005).

[40] Ásványi-Molnár N., Sipos-Kozma Z., Tóth Á., Ásványi B., Varga L., Development of Functional Dairy Food Enriched in Spirulina (Arthrospira platensis), Tejgazdaság, 69(2): 15-22(2009).

[41] Mousavi Z.E., Mousavi S.M., Razavi S.H., Emam-Djomeh Z., Kiani H.M., Fermentation of Pomegranate Juice by Probiotic Lactic Acid Bacteria, World J. Microbiol Biotechnol, 27(1): 123-128 (2011).

[42] Chaikham, P., Apichartsrangkoon A., Worametrachanon S., Supraditareporn W., Chokiatirote E., Van der Wiele T., Activities of Free and Encapsulated Lactobacillus acidophilus LA5 or Lactobacillus casei 01 in Processed Longan Juices on Exposure to Simulated Gastrointestinal Tract, Journal of the Science of Food and Agriculture, 93(9): 2229-2238 (2013).

[43] Strobel S.A., Allen K., Roberts C., Jimenez D., Scher H.B., Jeoh T., Industrially-Scalable Microencapsulation of Plant Beneficial Bacteria in Dry Cross-Linked Alginate Matrix, Industrial Biotechnology, 14(3):138-147 (2018).

[44] Azarkhavarani P.R., Ziaee E., Hosseini S.M.H., Effect of Encapsulation on the Stability and Survivability of Enterococcus Faecium in a Non-Dairy Probiotic Beverage, Food Science and Technology International, 25(3):233-242 (2019).

[45] Khalili N., Safi M., Ameri F., Investigation of the Color Stability of BCRA Ceramic Standards Using Univariate Statistical Methods, Journal of Color Science and Technology, 15(4): 243-254 (2022).

[46] Ahmadi A., Milani E., Madadlou A., Mortazavi S.A., Mokarram R.R., Salarbashi D., Synbiotic Yogurt-Ice Cream Produced Via Incorporation of Microencapsulated lactobacillus acidophilus (la-5) and Fructooligosaccharide, J. Food Sci. Technol., 51(8): 1568-1574 (2014).

[47] Zomorodi Sh., Survival of Free and microencapsulated Lactobacillus acidophilus and Bifidobacterium lactis in Doogh (a Yogurt Drink), Pharm Biomed Res, 5(1): 19-24 (2019).

[48] Ragavan M.L., Das N., Process Optimization for Microencapsulation of Probiotic Yeasts, Front. Biol, 13(3): 197-207 (2018).

[49] Brinques G.B., Ayub M.A.Z., Effect of Microencapsulation on Survival of Lactobacillus plantarum in Simulated Gastrointesti Nal Conditions, Refrigeration, and Yogurt, Journal of Food Engineering, 103(2): 123-128 (2011).

[50] Mokarram R.R., Mortazavi S.A., Najafi M.H., Shahidi F., The Influence of Multi Stage Alginate Coating on Survivability of Potential Probiotic Bacteria in Simulated Gastric and Intestinal Juice, Food Research International, 42(8): 1040-1045 (2009).

[51] Akalın A.S., Unal G., Dalay M.C., Influence of Spirulina platensis Biomass on Microbiological Viability in Traditional and Probiotic Yogurts During Refrigerated Storage, Ital. J. Food Sci, 21(3): 357-364(2009).

[52] Guldas M., Irkin R., Influence of Spirulina platensis Powder on the Microflora of Yoghurt and Acidophilus Milk, Mljekarstvo: Časopis za Unaprjeđenje Proizvodnje I Prerade Mlijeka, 60(4): 237-243 (2010).

[53] Beheshtipour H., Mortazavian A.M., Haratian P., Khosravi Darani K., Effects of Chlorella vulgaris and Arthrospira platensis Addition on Viability of Probiotic Bacteria In Yogurt and its Biochemical Properties, Eur. Food Res. Technol., 235(4): 719–728 (2012).

[54] Varga L., Szigeti J., Kovács R., Földes T., Buti S., Influence of a Spirulina platensis Biomass on the Microflora of Fermented ABT Milks During Storage (R1), J. Dairy Sci., 85(5): 1031-1038 (2002).

[55] Ozdemir G., Ulku Karabay N., Dalay M.C., Pazarbasi, B., Antibacterial Activity of Volatile Component and Various Extracts of Spirulina platensis, Phytotherapy Research: An International Journal Devoted to Pharmacological and Toxicological Evaluation of Natural Product Derivatives, 18(9):754-757(2004).

[56] Gupta S., Gupta C., Garg A.P., Prakash D., Prebiotic Efficiency of Blue Green Algae on Probiotics Microorganisms, J. Microbiol. Exp., 4(4): 00120 (2017).

[57] Sarabandi K., Gharehbeglou P., Jafari S.M., Spray-Drying Encapsulation of Protein Hydrolysates and Bioactive Peptides: Opportunities and Challenges, Drying Technology, 38(5-6): 577-595 (2020).

[58] Hansen L.T., Allan-Wojtas P.M., Jin Y.L., Paulson A.T., Survival of Ca-Alginate Microencapsulated Bifidobacterium spp. in Milk and Simulated Gastrointestinal Conditions, Food Microbiology, 19(1): 35-45 (2002).

[59] Praepanitchai O.A., Noomhorm A., Anal A.K., Survival and behavior of Encapsulated Probiotics (Lactobacillus plantarum) in Calcium-Alginate-Soy Protein Isolate-Based Hydrogel Beads in Different Processing Conditions (pH and temperature) and in Pasteurized Mango Juice, BioMed Research International, 2019 (2019).

[60] Ann E.Y., Kim Y., Oh S., Imm J.Y., Park D.J., Han K.S., Kim S.H., Microencapsulation of Lactobacillus acidophilus ATCC 43121 with Prebiotic Substrates Using a Hybridisation System, International Journal of Food Science & Technology, 42(4): 411-419 (2007).

[61] Fritzen-Freire C.B., Prudêncio E.S., Amboni R.D., Pinto S.S., Negrão-Murakami A.N., Murakami F.S., Microencapsulation of Bifidobacteria by Spray Drying in the Presence of Prebiotics, Food Research International, 45(1): 306-312(2012).

[62] Chávarri M., Marañón I., Ares R., Ibáñez F.C., Marzo F., del Carmen Villarán M., Microencapsulation of a Probiotic and Prebiotic in Alginate-Chitosan Capsules Improves Survival in Simulated Gastro-Intestinal Conditions, International Journal of Food Microbiology, 142(1-2): 185-189 (2010).

[63] Darjani P., Hosseini Nezhad M., Kadkhoddaee R., Milani E., Influence of Prebiotic and Coating Materials on Morphology and Survival of a Probiotic Strain of Lactobacillus casei Exposed to Simulated Gastrointestinal Conditions, LWT, 73: 162-167 (2016).

[64] Foroutan N.S., Tabandeh F., Khodabandeh M., Mojgani N., Maghsoudi A. and Moradi M., Isolation and Identification of an Indigenous Probiotic Lactobacillus Strain: Its Encapsulation with Natural Branched Polysaccharids to Improve Bacterial Viability, Applied Food Biotechnology, 4(3): 133- 142 (2017).