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Current Nutrition & Food Science

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ISSN (Print): 1573-4013
ISSN (Online): 2212-3881

Research Article

Isolation and Identification of Saccharomyces boulardii as a Probiotic Yeast and Investigation of its In vitro and In vivo Beneficial Applications

Author(s): Eman A. Helmy, Reda H. Abdel-Fadeel, Eman El-Husseiny Helal and Mohammed Yosri*

Volume 20, Issue 2, 2024

Published on: 19 May, 2023

Page: [210 - 219] Pages: 10

DOI: 10.2174/1573401319666230407143424

Price: $65

Abstract

Background: Yeasts are becoming increasingly popular as possible new resources to improve the nutritional value of food qualities like flavor, color, and vitamin content, as well as tools for preventing food spoiling due to their anti-microbial capabilities.

Objective: This study aims to test the role of isolated Saccharomyces boulardii as a promising probiotic as well as Jerusalem artichoke as a prebiotic in a feeding animal model to test their possible functions in regulating lipid profile and bacterial count in the faeces of tested animals.

Methods: For the isolation of yeast cultures on YM agar medium, five milk samples were randomly obtained from the Faculty of Agriculture at Al-Azhar University in Cairo, Egypt. S. boulardii was morphologically, physiologically, and molecularly identified and deposited in the gene bank; additionally, identification was confirmed using the BIOLOG system. For 30 days, researchers compared the roles of S. boulardii as a probiotic and Jerusalem artichoke as a prebiotic in controlling serum lipid profile and faeces microbial count in the tested animal groups.

Results: The acid and bile tolerance tests illustrate the promising ability of S. boulardii. Additionally, S. boulardii could survive on simulated stomach and intestinal fluids. An in vivo feeding test showed that rats fed S. boulardii grew and gained weight faster. Furthermore, eating S. boulardii causes a marked increase in HDL levels and a marked drop in LDL, cholesterol, and triglycerides. Rats that consumed Jerusalem artichokes and a probiotic strain had significantly lower numbers of coliforms and Staphylococcus sp. in their stools.

Conclusion: These results revealed the possible beneficial role of S. boulardii in overcoming hyperlipidemia, which should be applied on a large scale after verification of outcomes.

Graphical Abstract

[1]
Goodman C, Keating G, Georgousopoulou E, Hespe C, Levett K. Probiotics for the prevention of antibiotic-associated diarrhoea: A systematic review and meta-analysis. BMJ Open 2021; 11(8): e043054.
[http://dx.doi.org/10.1136/bmjopen-2020-043054] [PMID: 34385227]
[2]
Yadav MK, Kumari I, Singh B, Sharma KK, Tiwari SK. Probiotics, prebiotics and synbiotics: Safe options for next-generation therapeutics. Appl Microbiol Biotechnol 2022; 106(2): 505-21.
[http://dx.doi.org/10.1007/s00253-021-11646-8] [PMID: 35015145]
[3]
Tamang JP, Lama S. Probiotic properties of yeasts in traditional fermented foods and beverages. J Appl Microbiol 2022; 132(5): 3533-42.
[http://dx.doi.org/10.1111/jam.15467] [PMID: 35094453]
[4]
Durmaz S, Kurtoğlu T, Barbarus E, et al. Probiotic Saccharomyces boulardii alleviates lung injury by reduction of oxidative stress and cytokine response induced by Supraceliac aortic ischemiareperfusion injury in rats. Rev Bras Cir Cardiovasc 2020; 36(4): 515-21.
[http://dx.doi.org/10.21470/1678-9741-2020-0153] [PMID: 33355795]
[5]
Amorim JC, Piccoli RH, Duarte WF. Probiotic potential of yeasts isolated from pineapple and their use in the elaboration of potentially functional fermented beverages. Food Res Int 2018; 107: 518-27.
[http://dx.doi.org/10.1016/j.foodres.2018.02.054] [PMID: 29580515]
[6]
Menezes AGT, Ramos CL, Cenzi G, Melo DS, Dias DR, Schwan RF. Probiotic potential, antioxidant activity, and phytase production of indigenous yeasts isolated from indigenous fermented foods. Probiotics Antimicrob Proteins 2020; 12(1): 280-8.
[http://dx.doi.org/10.1007/s12602-019-9518-z] [PMID: 30685824]
[7]
Kalathinathan P, Kodiveri MG. Characterisation of a potential probiotic strain Paracoccus marcusii KGP and its application in whey bioremediation. Folia Microbiol 2021; 66(5): 819-30.
[http://dx.doi.org/10.1007/s12223-021-00886-w] [PMID: 34148171]
[8]
Ghazanfar M, Qubtia IA, Ahmed I, Hasa F, Anjum MI, Imran M. Effect of indigenously isolated Saccharomyces cerevisiae probiotics on milk production, nutrient digestibility, blood chemistry and fecal microbiota in lactating dairy cows. J Anim Plant Sci 2018; 28(2): 201.
[9]
Hameed A, Condò C, Tauseef I, et al. Isolation and characterization of a cholesterol-lowering bacteria from Bubalus bubalis raw milk. Fermentation 2022; 8(4): 163.
[http://dx.doi.org/10.3390/fermentation8040163]
[10]
Abid R, Waseem H, Ali J, et al. Probiotic yeast Saccharomyces: Back to nature to improve human health. J Fungi 2022; 8(5): 444.
[http://dx.doi.org/10.3390/jof8050444] [PMID: 35628700]
[11]
Boyajian JL, Ghebretatios M, Schaly S, Islam P, Prakash S. Microbiome and human aging: Probiotic and prebiotic potentials in longevity, skin health and cellular senescence. Nutrients 2021; 13(12): 4550.
[http://dx.doi.org/10.3390/nu13124550] [PMID: 34960102]
[12]
Hughes RL, Alvarado DA, Swanson KS, Holscher HD. The prebiotic potential of inulin-type fructans: A systematic review. Adv Nutr 2022; 13(2): 492-529.
[http://dx.doi.org/10.1093/advances/nmab119] [PMID: 34555168]
[13]
Trejo RIS, Alcántara QLE, Algara SP, Ruiz SMA, Grajales LA. Physicochemical properties, antioxidant capacity, prebiotic activity and anticancer potential in human cells of jackfruit (Artocarpus heterophyllus) seed flour. Molecules 2021; 26(16): 4854.
[http://dx.doi.org/10.3390/molecules26164854] [PMID: 34443442]
[14]
Ghorbani-Choboghlo H, Nikaein D, Khosravi AR, Rahmani R, Farahnejad Z. Effect of microencapsulation on Saccharomyces cerevisiae var. boulardii viability in the gastrointestinal tract and level of some blood biochemical factors in wistar rats. Iran J Microbiol 2019; 11(2): 160-5.
[http://dx.doi.org/10.18502/ijm.v11i2.1082] [PMID: 31341571]
[15]
Briand F, Sulpice T, Giammarinaro P, Roux X. Saccharomyces boulardii CNCM I-745 changes lipidemic profile and gut microbiota in a hamster hypercholesterolemic model. Benef Microbes 2019; 10(5): 555-67.
[http://dx.doi.org/10.3920/BM2018.0134] [PMID: 31090460]
[16]
Oh GM, Moon W, Seo KI, et al. Changes in the crohn’s disease activity index and safety of administering Saccharomyces Boulardii in Patients with Crohn’s Disease in clinical remission: A single hospital-based retrospective cohort study. Korean J Gastroenterol 2020; 76(6): 314-21.
[http://dx.doi.org/10.4166/kjg.2020.115] [PMID: 33250507]
[17]
Lazo-Vélez MA, Serna-Saldívar SO, Rosales-Medina MF, Tinoco-Alvear M, Briones-García M. Application of Saccharomyces cerevisiae var. boulardii in food processing: A review. J Appl Microbiol 2018; 125(4): 943-51.
[http://dx.doi.org/10.1111/jam.14037] [PMID: 29961970]
[18]
Sivananthan K, Petersen AM. Review of Saccharomyces boulardii as a treatment option in IBD. Immunopharmacol Immunotoxicol 2018; 40(6): 465-75.
[http://dx.doi.org/10.1080/08923973.2018.1469143] [PMID: 29771163]
[19]
Sharifi M, Futema M, Nair D, Humphries SE. Polygenic hypercholesterolemia and cardiovascular disease risk. Curr Cardiol Rep 2019; 21(6): 43.
[http://dx.doi.org/10.1007/s11886-019-1130-z] [PMID: 31011892]
[20]
D’Erasmo L, Di Costanzo A, Arca M. Autosomal recessive hypercholesterolemia. Curr Opin Lipidol 2020; 31(2): 56-61.
[http://dx.doi.org/10.1097/MOL.0000000000000664] [PMID: 32011344]
[21]
Barnett JA, Payne RW, Yarrow D, Eds. Yeasts: characterization and identification. Cambridge: Cambridge University Press 1990.
[22]
Suh SH, Paik IY, Jacobs K. Regulation of blood glucose homeostasis during prolonged exercise. Mol Cells 2007; 23(3): 272-9.
[PMID: 17646701]
[23]
Qvirist LA, De Filippo C, Strati F, et al. Isolation, identification and characterization of yeasts from fermented goat milk of the yaghnob valley in Tajikistan. Front Microbiol 2016; 7: 1690.
[http://dx.doi.org/10.3389/fmicb.2016.01690] [PMID: 27857705]
[24]
Geronikou A, Larsen N, Lillevang SK, Jespersen L. Occurrence and identification of yeasts in production of white-brined cheese. Microorganisms 2022; 10(6): 1079.
[http://dx.doi.org/10.3390/microorganisms10061079] [PMID: 35744597]
[25]
Kostas ET, White DA, Du C, Cook DJ. Selection of yeast strains for bioethanol production from UK seaweeds. J Appl Phycol 2016; 28(2): 1427-41.
[http://dx.doi.org/10.1007/s10811-015-0633-2] [PMID: 27057090]
[26]
Kostas ET, Cooper M, Shepherd BJ, Robinson JP. Identification of bio-oil compound utilizing yeasts through phenotypic microarray screening. Waste Biomass Valoriz 2019; 1-13. [Avaialble from:] https://link.springer.com/article/10.1007/s12649-019-00636-7
[http://dx.doi.org/10.1007/s12649-019-00636-7]
[27]
Boranbayeva T, Karahan AG, Tulemissova Z, Myktybayeva R, Özkaya S. Properties of a new probiotic candidate and lactobacterin-TK2 against diarrhea in calves. Probiotics Antimicrob Proteins 2020; 12(3): 918-28.
[http://dx.doi.org/10.1007/s12602-020-09649-4] [PMID: 32215859]
[28]
Al-Seraih A, Flahaut C, Krier F, Cudennec B, Drider D. Characterization of Candida famata isolated from poultry feces for possible probiotic applications. Probiotics Antimicrob Proteins 2015; 7(4): 233-41.
[http://dx.doi.org/10.1007/s12602-015-9201-y] [PMID: 26459296]
[29]
Fernández-Pacheco P, Pintado C, Pérez BA, Arévalo-Villena M. Potential probiotic strains of Saccharomyces and Non-Saccharomyces: Functional and biotechnological characteristics. J Fungi 2021; 7(3): 177.
[http://dx.doi.org/10.3390/jof7030177] [PMID: 33801543]
[30]
Yang R, Wang C, Ye H, et al. Effects of feeding hyperlipidemia rats with symbiotic oat based frozen yogurt on serum triglycerides and cholesterol. Food Sci Nutr 2019; 7(3): 1096-103.
[http://dx.doi.org/10.1002/fsn3.949] [PMID: 30918652]
[31]
Tanaka S, Madokoro S, Inaoka PT, Yamazaki T. Blood lipid profile changes in type 2 diabetic rats after tail suspension and reloading. Lipids Health Dis 2021; 20(1): 84.
[http://dx.doi.org/10.1186/s12944-021-01511-y] [PMID: 34334135]
[32]
Ebrahimi MN, Khaksari M, Sepehri G, Karam GA, Raji-amirhasani A, Azizian H. The effects of alone and combination tamoxifen, raloxifene and estrogen on lipid profile and atherogenic index of ovariectomized type 2 diabetic rats. Life Sci 2020; 263: 118573.
[http://dx.doi.org/10.1016/j.lfs.2020.118573] [PMID: 33058909]
[33]
Chettaoui R, Mayot G, De Almeida L, Di Martino P. Cranberry (Vaccinium macrocarpon) dietary supplementation and fecal microbiota of Wistar rats. AIMS Microbiol 2021; 7(2): 257-70.
[http://dx.doi.org/10.3934/microbiol.2021016] [PMID: 34250378]
[34]
Scholes AN, Pollock ED, Lewis JA. A wild yeast laboratory activity: From isolation to brewing. J Microbiol Biol Educ 2021; 22(2): e00186-21.
[http://dx.doi.org/10.1128/jmbe.00186-21] [PMID: 34594437]
[35]
Minamizuka T, Koshizaka M, Shoji M, et al. Low dose red yeast rice with monacolin K lowers LDL cholesterol and blood pressure in Japanese with mild dyslipidemia: A multicenter, randomized trial. Asia Pac J Clin Nutr 2021; 30(3): 424-35.
[http://dx.doi.org/10.6133/apjcn.202109_30(3).0009] [PMID: 34587702]
[36]
Zhang L, Zeng X, Guo D, Zou Y, Gan H, Huang X. Early use of probiotics might prevent antibiotic-associated diarrhea in elderly (>65 years): A systematic review and meta-analysis. BMC Geriatr 2022; 22(1): 562.
[http://dx.doi.org/10.1186/s12877-022-03257-3] [PMID: 35794520]
[37]
Bungau SG, Behl T, Singh A, et al. Targeting probiotics in rheumatoid arthritis. Nutrients 2021; 13(10): 3376.
[http://dx.doi.org/10.3390/nu13103376] [PMID: 34684377]
[38]
Socała K, Doboszewska U, Szopa A, et al. The role of microbiotagut-brain axis in neuropsychiatric and neurological disorders. Pharmacol Res 2021; 172: 105840.
[http://dx.doi.org/10.1016/j.phrs.2021.105840] [PMID: 34450312]
[39]
de Vos WM, Tilg H, Van Hul M, Cani PD. Gut microbiome and health: Mechanistic insights. Gut 2022; 71(5): 1020-32.
[http://dx.doi.org/10.1136/gutjnl-2021-326789] [PMID: 35105664]
[40]
Shakira G, Mirza IH, Latif A. Scope of common DNA based methods for the study of rumen bacterial population. Bangladesh J Anim Sci 2013; 41(2): 141-6.
[http://dx.doi.org/10.3329/bjas.v41i2.14134]
[41]
Tao D, Zhong T, Pang W. li X. Saccharomyces boulardii improves the behaviour and emotions of spastic cerebral palsy rats through the gut-brain axis pathway. BMC Neurosci 2021; 22(1): 76.
[http://dx.doi.org/10.1186/s12868-021-00679-4] [PMID: 34876019]
[42]
Zhao Y, Yang Y, Aruna et al. Saccharomyces boulardii combined with quadruple therapy for Helicobacter pylori eradication decreased the duration and severity of diarrhea: A multi-center prospective randomized controlled trial. Front Med (Lausanne) 2021; 8: 776955.
[http://dx.doi.org/10.3389/fmed.2021.776955] [PMID: 34869495]
[43]
Bohbot JM, Zhioua F,. Intérêt, de . Saccharomyces boulardii CNCM I-745 dans la prise en charge des infections vulvovaginales. The benefit of Saccharomyces boulardii CNCM I-745 in the management of vulvovaginal infections. Gynecol Obstet Fertil Senol 2021; 49(9): 716-23.
[http://dx.doi.org/10.1016/j.gofs.2021.04.008]
[44]
Pais P, Almeida V, Yılmaz M, Teixeira MC. Saccharomyces boulardii: What makes it tick as successful probiotic? J Fungi 2020; 6(2): 78.
[http://dx.doi.org/10.3390/jof6020078] [PMID: 32512834]
[45]
Hossain MN, Afrin S, Humayun S, Ahmed MM, Saha BK. Identification and growth characterization of a novel strain of saccharomyces boulardii isolated from soya paste. Front Nutr 2020; 7: 27.
[http://dx.doi.org/10.3389/fnut.2020.00027] [PMID: 32309286]
[46]
Suvarna S, Dsouza J, Ragavan ML, Das N. Potential probiotic characterization and effect of encapsulation of probiotic yeast strains on survival in simulated gastrointestinal tract condition. Food Sci Biotechnol 2018; 27(3): 745-53.
[http://dx.doi.org/10.1007/s10068-018-0310-8] [PMID: 30263800]
[47]
Romero-Luna HE, Hernández-Sánchez H, Ribas-Aparicio RM, Cauich-Sánchez PI, Dávila-Ortiz G. Evaluation of the probiotic potential of Saccharomyces cerevisiae Strain (C41) isolated from tibicos by in vitro studies. Probiotics Antimicrob Proteins 2019; 11(3): 794-800.
[http://dx.doi.org/10.1007/s12602-018-9471-2] [PMID: 30238220]
[48]
Ryan JJ, Hanes DA, Schafer MB, Mikolai J, Zwickey H. Effect of the probiotic saccharomyces boulardii on cholesterol and lipoprotein particles in hypercholesterolemic adults: A single-arm, openlabel pilot study. J Altern Complement Med 2015; 21(5): 288-93.
[http://dx.doi.org/10.1089/acm.2014.0063] [PMID: 25893960]
[49]
Sawicka B, Skiba D, Pszczółkowski P, Aslan I, Sharifi-Rad J, Krochmal-Marczak B. Jerusalem artichoke (Helianthus tuberosus L.) as a medicinal plant and its natural products. Cell Mol Biol 2020; 66(4): 160-77.
[http://dx.doi.org/10.14715/cmb/2020.66.4.20] [PMID: 32583794]
[50]
Soyturk M, Saygili SM, Baskin H, et al. Effectiveness of Saccharomyces boulardii in a rat model of colitis World J Gastroenterol 2012; 18(44): 6452-60.
[http://dx.doi.org/10.3748/wjg.v18.i44.6452]
[51]
Shao T, Yu Q, Zhu T, et al. Inulin from Jerusalem artichoke tubers alleviates hyperglycaemia in high-fat-diet-induced diabetes mice through the intestinal microflora improvement. Br J Nutr 2020; 123(3): 308-18.
[http://dx.doi.org/10.1017/S0007114519002332] [PMID: 31915077]
[52]
Khatana C, Saini NK, Chakrabarti S, et al. Mechanistic insights into the oxidized low-density lipoprotein-induced atherosclerosis. Oxid Med Cell Longev 2020; 2020: 5245308.
[http://dx.doi.org/10.1155/2020/5245308] [PMID: 33014272]
[53]
Green M, Arora K, Prakash S. Microbial medicine: Prebiotic and probiotic functional foods to target obesity and metabolic syndrome. Int J Mol Sci 2020; 21(8): 2890.
[http://dx.doi.org/10.3390/ijms21082890] [PMID: 32326175]
[54]
Pradhan AD, Paynter NP, Everett BM, et al. Rationale and design of the pemafibrate to reduce cardiovascular outcomes by reducing triglycerides in patients with diabetes (PROMINENT) study. Am Heart J 2018; 206: 80-93.
[http://dx.doi.org/10.1016/j.ahj.2018.09.011] [PMID: 30342298]
[55]
Kleessen B, Elsayed NAAE, Loehren U, Schroedl W, Krueger M. Jerusalem artichokes stimulate growth of broiler chickens and protect them against endotoxins and potential cecal pathogens. J Food Prot 2003; 66(11): 2171-5.
[http://dx.doi.org/10.4315/0362-028X-66.11.2171] [PMID: 14627303]
[56]
Pandey KR, Naik SR, Vakil BV. Probiotics, prebiotics and synbiotics- a review. J Food Sci Technol 2015; 52(12): 7577-87.
[http://dx.doi.org/10.1007/s13197-015-1921-1] [PMID: 26604335]
[57]
Molska M, Reguła J, Rudzińska M, Świeca M. Fatty acids profile, atherogenic and thrombogenic health lipid indices of lyophilized buckwheat sprouts modified with the addition of Saccharomyces cerevisiae var. boulardii. Acta Sci Pol Technol Aliment 2020; 19(4): 483-90.
[http://dx.doi.org/10.17306/J.AFS.0866] [PMID: 33179488]
[58]
Cangiano LR, Yohe TT, Steele MA, Renaud DL. Invited review: Strategic use of microbial-based probiotics and prebiotics in dairy calf rearing. Appl Anim Sci 2020; 36(5): 630-51.
[http://dx.doi.org/10.15232/aas.2020-02049]
[59]
Evdokimova SA, Nokhaeva VS, Karetkin BA, et al. A study on the synbiotic composition of bifidobacterium bifidum and fructans from arctium lappa roots and helianthus tuberosus tubers against staphylococcus aureus. Microorganisms 2021; 9(5): 930.
[http://dx.doi.org/10.3390/microorganisms9050930] [PMID: 33926121]

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