The development of novel probiotic fermented plant milk alternative from flaxseed oil cake using Lactobacillus rhamnosus GG acting as a preservative agent against pathogenic bacteria during short-term refrigerated storage
DOI:
https://doi.org/10.9755/ejfa.2021.v33.i4.2679Abstract
This study is aimed at investigating the suitability of flaxseed oil cake plant milk alternative (FOCM) to produce an innovative probiotic drink using Lactobacillus rhamnosus GG (LGG). Three variants of beverage were prepared: without supplementation, supplemented with 1% of glucose and supplemented with 1% of fructose. The viability of LGG, levels of polyphenolics, flavonoids and antioxidant activity were analysed. Moreover, color, viscosity and titratable acidity measurements were performed. Fermented beverages were artificially contaminated with pathogenic bacteria, and preservative effect of LGG was evaluated. The fermentation improved antioxidant activity, polyphenolics and flavonoids content, whereas viscosity of the samples decreased. During storage at 6°C for 48 hours the viability of LGG in all the samples was over the recommended probiotic minimum level (>106 CFU/mL). Supplementation with sugars significantly enhanced acidification of FOCM. Acidification was linked with preservative effect of LGG against pathogenic microflora. A significant reduction of Gram-negative pathogens was observed, whereas moderate activity was noted against Gram-positive bacteria. Due to the functional and biochemical characteristics conferred to the fermented beverages, the use of LGG showed adequate potential for industrial application. There is a potential for these products to be used where non-dairy alternatives for probiotic consumption are desired.
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References
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Kocková, M., M. Dilongová, E. Hybenová and L. Valík. 2013. Evaluation of cereals and pseudocereals suitability for the development of new probiotic foods. J. Chem. Article ID414303: 8 p.
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Łopusiewicz, Ł., E. Drozłowska, A. Tarnowiecka-Kuca, A. Bartkowiak, K. Mazurkiewicz-Zapałowicz and P. Salachna. 2020b. Biotransformation of Flaxseed Oil Cake into Bioactive Camembert-Analogue Using Lactic Acid Bacteria, Penicillium camemberti and Geotrichum candidum. Microorganisms. 8: 1266.
Lorusso, A., R. Coda, M. Montemurro and C. G. Rizzello. 2018. Use of Selected Lactic Acid Bacteria and Quinoa Flour for Manufacturing Novel Yogurt-Like Beverages. Foods 7(4): 51.
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Mauro, C. S. I., K. Guergoletto and S. Garcia. 2016. Development of Blueberry and Carrot Juice Blend Fermented by Lactobacillus reuteri LR92. Beverages 2(4):37.
Meurman, J. H., H. Antila, A. Korhonen and S. Salminen. 1995. Effect of Lactobacillus rhamnosus strain GG (ATCC 53103) on the growth of Streptococcus sobrinus in vitro. Eur. J. Oral. Sci. 103(4): 253–258.
Minervini, F., J. Missaoui, G. Celano, M. Calasso, L. Achour, D. Saidane, M. Gobbetti, and M. De Angelis. 2020. Use of Autochthonous Lactobacilli to Increase the Safety of Zgougou. Microorganisms. 8(1): 29.
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Ranadheera, C., J. Vidanarachchi, R. Rocha, A. Cruz and S. Ajlouni. 2017. Probiotic Delivery through Fermentation: Dairy vs. Non-Dairy Beverages. Fermentation 3, 67.
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Servin, A. L. 2004. Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol. Rev. 28(4): 405–440.
Sireswar, S., G. Dey, K. Dey and K. Kundu. 2017. Evaluation of Probiotic L. rhamnosus GG as a Protective Culture in Sea Buckthorn-Based Beverage. Beverages, 3(4): 48.
Sireswar, S., I. Ghosh, K. Dey, L. Behera, M. Reza, S. S. Das and G. Dey. 2019. Evaluation of probiotic-beverage matrix interaction for efficient control of Enterobacter aerogenes and Staphylococcus aureus. J. Food Prot. 82(4): 669–676.
Sun, J., X. L. Hu, G. W. Le and Y. H. Shi. 2010. Lactobacilli prevent hydroxy radical production and inhibit Escherichia coli and Enterococcus growth in system mimicking colon fermentation. Lett. Appl. Microbiol. 50(3): 264–269.
Sun, J., H. Chen, Y. Qiao, G. Liu, C. Leng, Y. Zhang, L. Xuepeng and Z. Feng. 2019. The nutrient requirements of Lactobacillus rhamnosus GG and their application to fermented milk. J. Dairy Sci. 102(7): 5971–5978.
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Tayo, B. A. and S. Akpeji. 2016. Probiotic viability, physicochemical and sensory properties of probiotic pineapple juice. Fermentation. 2(4).
Tong, T., Y.-J. Liu, J. Kang, C.-M. Zhang and S.-G. Kang. 2019. Antioxidant Activity and Main Chemical Components of a Novel Fermented Tea. Molecules 24(16): 2917.
Tsafrakidou, P., A.-M. Michaelidou and C.G. Biliaderis. 2020. Fermented Cereal-based Products: Nutritional Aspects, Possible Impact on Gut Microbiota and Health Implications. Foods 9, 734.
Valík, L., A. Medved’ová and D. Liptáková. 2008. Characterization of the growth of Lactobacillus rhamnosus GG in milk at suboptimal temperatures. J. Food Nutr. Res. 47(2): 60–67.
Valero-Cases, E., D. Cerdá-Bernad, J.-J. Pastor and M.-J. Frutos. 2020. Non-Dairy Fermented Beverages as Potential Carriers to Ensure Probiotics, Prebiotics, and Bioactive Compounds Arrival to the Gut and Their Health Benefits. Nutrients 12, 1666.
Vesterlund, S., K. Salminen and S. Salminen. 2012. Water activity in dry foods containing live probiotic bacteria should be carefully considered: A case study with Lactobacillus rhamnosus GG in flaxseed. Int. J. Food Microbiol. 157(2): 319–321.
Westerik, N., R. Kort, W. Sybesma and G. Reid. 2018. Lactobacillus rhamnosus probiotic food as a tool for empowerment across the value chain in Africa. Front. Microbiol. 9(2018): 1–6.
Williams, M. and S. Hekmat. 2017. Lactobacillus rhamnosus GR-1 in Fermented Rice Pudding Supplemented with Short Chain Inulin, Long Chain Inulin, and Oat as a Novel Functional Food. Fermentation. 3(4). 55.
Yan, F. and D. B. Polk. 2012. Lactobacillus rhamnosus GG: An Updated Strategy to Use Microbial Products to Promote Health. Funct. Food Rev. 4(2): 77–84.
Zhang, Y., L. Zhang, M. Du, H. Yi, C. Guo, Y. Tuo, X. Han, Y. Li, L. Zhang and L. Yang. 2011. Antimicrobial activity against Shigella sonnei and probiotic properties of wild lactobacilli from fermented food. Microbiol. Res. 167(1): 27–31.
Alegre, I., I. Viñas, J. Usall, M. Anguera and M. Abadias. 2011. Microbiological and physicochemical quality of fresh-cut apple enriched with the probiotic strain Lactobacillus rhamnosus GG. Food Microbiol. 28(1): 59–66.
Atalar, I. 2019. Functional kefir production from high pressure homogenized hazelnut milk. LWT 107: 256–263.
Balejko, E., E. Kucharska and A. Bartkowiak. 2009. Influence of Lactobacillus rhamnosus GG metabolites on immunological processes in vitro. Cent. Eur. J. Immunol. 34(3): 147–153.
Bartkiene, E., V. Lele, M. Ruzauskas, K. J. Domig, V. Starkute, P. Zavistanaviciute, V. Bartkevics, I. Pugajeva, D. Klupsaite, G. Juodeikiene, R. Mickiene and J. M. Rocha. 2020. Lactic Acid Bacteria Isolation from Spontaneous Sourdough and Their Characterization Including Antimicrobial and Antifungal Properties Evaluation. Microorganisms 8(1) 64: 1-20.
Bernat, N., M. Cháfer, A. Chiralt and C. González-Martínez. 2014. Hazelnut milk fermentation using probiotic Lactobacillus rhamnosus GG and inulin. Int. J. Food Sci. 49(12): 2553–2562.
Castellano, P., M. Pérez Ibarreche, M. Blanco Massani, C. Fontana and G. Vignolo. 2017. Strategies for Pathogen Biocontrol Using Lactic Acid Bacteria and Their Metabolites: A Focus on Meat Ecosystems and Industrial Environments. Microorganisms 5(3): 38.
De Keersmaecker, S. C. J., T. L. A. Verhoeven, J. Desair, K. Marchal, J. Vanderleyden and I. Nagy. 2006. Strong antimicrobial activity of Lactobacillus rhamnosus GG against Salmonella typhimurium is due to accumulation of lactic acid. FEMS Microbiol. Lett. 259(1): 89–96.
Dueñas, M. and I. García-Estévez. 2020. Agricultural and Food Waste: Analysis, Characterization and Extraction of Bioactive Compounds and Their Possible Utilization. Foods 9, 817.
Erkkilä, S., M. Venlinen, S. Hielm, E. Petj, E. Puolanne and T. Mattila-Sandholm. 2000. Survival of Escherichia coli 0157:H7 in dry sausage fermented by probiotic lactic acid bacteria. J. Sci. Food Agr. 80(14): 2101–2104.
FAO/WHO. 2006. Working Group Report on Drafting Guidelines for the Evaluation of Probiotics in Food. London, Ontario, Canada. 30 April—1 May 2002. In: Probiotics in food. Health and nutritional properties and guidelines for evaluation. World Health Organization. Food and Agriculture Organization of the United Nations. Rome. 2006: 46.
Fayol-Messaoudi, D., N.C. Berger, M.-H. Coconnier-Polter, V. Liévin-Le Moal and A. L. Servin. 2005. pH-, Lactic Acid-, and Non-Lactic Acid-Dependent Activities of Probiotic Lactobacilli against. Appl. Environ. Microbiol. 71(10): 6008–6013.
Hadinezhad, M., C. Duc, N. F. Han and F. Hosseinian. 2013. Flaxseed Soluble Dietary Fibre Enhances Lactic Acid Bacterial Survival and Growth in Kefir and Possesses High Antioxidant Capacity. J. Food Res. 2(5): 152–163.
Hedberg, M., P. Hasslöf, I. Sjöström, S. Twetman and C. Stecksén-Blicks. 2008. Sugar fermentation in probiotic bacteria - An in vitro study. Oral Microbiol. Immunol. 23(6): 482–485.
Horwitz, W. 2000. Official methods of analysis of AOAC International (17th ed.). Gaithersburg Md.: AOAC International.
Iglesias, M. B., G. Echeverría, I. Viñas, M.L. López and M. Abadias. 2018. Biopreservation of fresh-cut pear using Lactobacillus rhamnosus GG and effect on quality and volatile compounds. LWT 87: 581–588.
Jia, R., H. Chen, H. Chen, and W. Ding. 2016. Effects of fermentation with Lactobacillus rhamnosus GG on product quality and fatty acids of goat milk yogurt. J. Dairy Sci. 99(1): 221–227.
Johnson-Henry, K. C., K. A. Donato, G. Shen-Tu, M. Gordanpour and P. M. Sherman. 2008. Lactobacillus rhamnosus strain GG prevents enterohemorrhagic Escherichia coli O157:H7-induced changes in epithelial barrier function. Infect Immun. 76(4): 1340-1348.
Kandylis, P., K. Pissaridi, A. Bekatorou, M. Kanellaki and A. A. Koutinas. 2016. Dairy and non-dairy probiotic beverages. Curr. Opin. Food Sci. 7: 58–63.
Kehinde, B.A., A. Panghal, M.K. Garg, P. Sharma and N. Chhikara. 2020. Chapter Four - Vegetable milk as probiotic and prebiotic foods. Adv. Food Nutr. Res. 94: 115-160.
Kocková, M., M. Dilongová, E. Hybenová and L. Valík. 2013. Evaluation of cereals and pseudocereals suitability for the development of new probiotic foods. J. Chem. Article ID414303: 8 p.
Kwiatkowski, P., Ł. Łopusiewicz, M. Kostek, E. Drozłowska, A. Pruss, B. Wojciuk, M. Sienkiewicz, H. Zielińska-Bliźniewska and B. Dołęgowska. 2019. The Antibacterial Activity of Lavender Essential Oil Alone and In Combination with Octenidine Dihydrochloride against MRSA Strains. Molecules 25(1): 95.
Łopusiewicz, Ł., E. Drozłowska, P. Siedlecka, M. Mężyńska. A. Bartkowiak, M. Sienkiewicz, H. Zielińska-Bliźniewska and P. Kwiatkowski. 2019. Development, characterization, and bioactivity of non-dairy kefir-like fermented beverage based on flaxseed oil cake. Foods. 8(11): 544.
Łopusiewicz, Ł., E. Drozłowska, P. Siedlecka, M. Mężyńska and A. Bartkowiak. 2020a. Preparation and characterization of novel flaxseed oil cake yogurt-like plant milk fortified with inulin. J. Food Nutr. Res. 59(1): 61–70.
Łopusiewicz, Ł., E. Drozłowska, A. Tarnowiecka-Kuca, A. Bartkowiak, K. Mazurkiewicz-Zapałowicz and P. Salachna. 2020b. Biotransformation of Flaxseed Oil Cake into Bioactive Camembert-Analogue Using Lactic Acid Bacteria, Penicillium camemberti and Geotrichum candidum. Microorganisms. 8: 1266.
Lorusso, A., R. Coda, M. Montemurro and C. G. Rizzello. 2018. Use of Selected Lactic Acid Bacteria and Quinoa Flour for Manufacturing Novel Yogurt-Like Beverages. Foods 7(4): 51.
Makras, L., V. Triantafyllou, D. Fayol-Messaoudi, T. Adriany, G. Zoumpopoulou, E. Tsakalidou, A. Servin and L. De Vuyst. 2006. Kinetic analysis of the antibacterial activity of probiotic lactobacilli towards Salmonella enterica serovar Typhimurium reveals a role for lactic acid and other inhibitory compounds. Res. Microbiol. 157(3): 241–247.
Mauro, C. S. I., K. Guergoletto and S. Garcia. 2016. Development of Blueberry and Carrot Juice Blend Fermented by Lactobacillus reuteri LR92. Beverages 2(4):37.
Meurman, J. H., H. Antila, A. Korhonen and S. Salminen. 1995. Effect of Lactobacillus rhamnosus strain GG (ATCC 53103) on the growth of Streptococcus sobrinus in vitro. Eur. J. Oral. Sci. 103(4): 253–258.
Minervini, F., J. Missaoui, G. Celano, M. Calasso, L. Achour, D. Saidane, M. Gobbetti, and M. De Angelis. 2020. Use of Autochthonous Lactobacilli to Increase the Safety of Zgougou. Microorganisms. 8(1): 29.
Moreira, R. M., M.L. Martins, B. R. C. Leite, E. M. F. Martins, A. M. Ramos, M. Cristianini, A. N. R. Campos, P. C. Stringheta, V. R. O. Silva, J. W. Canuto, D. C. Oliveira and D. C. S. Pereira. 2017. Development of a juçara and Ubá mango juice mixture with added Lactobacillus rhamnosus GG processed by high pressure. LWT 77: 259–268.
Mpofu, A., A. R. Linnemann, M. J. R. Nout, M. H. Zwietering, E. J. Smid and H. M. W. den Besten. 2016. Inactivation of bacterial pathogens in yoba mutandabota, a dairy product fermented with the probiotic Lactobacillus rhamnosus yoba. Int. J. Food Microbiol. 217: 42–48.
Nazhand, A., E.B. Souto, M. Lucarini, S.B. Souto, A. Durazzo and A. Santini. 2020. Ready to Use Therapeutical Beverages: Focus on Functional Beverages Containing Probiotics, Prebiotics and Synbiotics. Beverages 6, 26.
Ranadheera, C., J. Vidanarachchi, R. Rocha, A. Cruz and S. Ajlouni. 2017. Probiotic Delivery through Fermentation: Dairy vs. Non-Dairy Beverages. Fermentation 3, 67.
Ricci, A., V. Bernini, A. Maoloni, M. Cirlini, G. Galaverna, E. Neviani and C. Lazzi. 2019. Vegetable by-product lacto-fermentation as a new source of antimicrobial compounds. Microorganisms 7(12).
Santos, D. C. dos, J. G. de Oliveira Filho, A. C. A. Santana, B. S. M. de Freitas, F. G. Silva, K. P. Takeuchi and M. B. Egea. 2019. Optimization of soymilk fermentation with kefir and the addition of inulin: Physicochemical, sensory and technological characteristics. LWT. 104: 30–37.
Servin, A. L. 2004. Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol. Rev. 28(4): 405–440.
Sireswar, S., G. Dey, K. Dey and K. Kundu. 2017. Evaluation of Probiotic L. rhamnosus GG as a Protective Culture in Sea Buckthorn-Based Beverage. Beverages, 3(4): 48.
Sireswar, S., I. Ghosh, K. Dey, L. Behera, M. Reza, S. S. Das and G. Dey. 2019. Evaluation of probiotic-beverage matrix interaction for efficient control of Enterobacter aerogenes and Staphylococcus aureus. J. Food Prot. 82(4): 669–676.
Sun, J., X. L. Hu, G. W. Le and Y. H. Shi. 2010. Lactobacilli prevent hydroxy radical production and inhibit Escherichia coli and Enterococcus growth in system mimicking colon fermentation. Lett. Appl. Microbiol. 50(3): 264–269.
Sun, J., H. Chen, Y. Qiao, G. Liu, C. Leng, Y. Zhang, L. Xuepeng and Z. Feng. 2019. The nutrient requirements of Lactobacillus rhamnosus GG and their application to fermented milk. J. Dairy Sci. 102(7): 5971–5978.
Szparaga, A., S. Tabor, S. Kocira, E. Czerwińska, M. Kuboń, B. Płóciennik and P. Findura. 2019. Survivability of probiotic bacteria in model systems of non-fermented and fermented coconut and hemp milks. Sustainability 11(21): 1–19.
Tayo, B. A. and S. Akpeji. 2016. Probiotic viability, physicochemical and sensory properties of probiotic pineapple juice. Fermentation. 2(4).
Tong, T., Y.-J. Liu, J. Kang, C.-M. Zhang and S.-G. Kang. 2019. Antioxidant Activity and Main Chemical Components of a Novel Fermented Tea. Molecules 24(16): 2917.
Tsafrakidou, P., A.-M. Michaelidou and C.G. Biliaderis. 2020. Fermented Cereal-based Products: Nutritional Aspects, Possible Impact on Gut Microbiota and Health Implications. Foods 9, 734.
Valík, L., A. Medved’ová and D. Liptáková. 2008. Characterization of the growth of Lactobacillus rhamnosus GG in milk at suboptimal temperatures. J. Food Nutr. Res. 47(2): 60–67.
Valero-Cases, E., D. Cerdá-Bernad, J.-J. Pastor and M.-J. Frutos. 2020. Non-Dairy Fermented Beverages as Potential Carriers to Ensure Probiotics, Prebiotics, and Bioactive Compounds Arrival to the Gut and Their Health Benefits. Nutrients 12, 1666.
Vesterlund, S., K. Salminen and S. Salminen. 2012. Water activity in dry foods containing live probiotic bacteria should be carefully considered: A case study with Lactobacillus rhamnosus GG in flaxseed. Int. J. Food Microbiol. 157(2): 319–321.
Westerik, N., R. Kort, W. Sybesma and G. Reid. 2018. Lactobacillus rhamnosus probiotic food as a tool for empowerment across the value chain in Africa. Front. Microbiol. 9(2018): 1–6.
Williams, M. and S. Hekmat. 2017. Lactobacillus rhamnosus GR-1 in Fermented Rice Pudding Supplemented with Short Chain Inulin, Long Chain Inulin, and Oat as a Novel Functional Food. Fermentation. 3(4). 55.
Yan, F. and D. B. Polk. 2012. Lactobacillus rhamnosus GG: An Updated Strategy to Use Microbial Products to Promote Health. Funct. Food Rev. 4(2): 77–84.
Zhang, Y., L. Zhang, M. Du, H. Yi, C. Guo, Y. Tuo, X. Han, Y. Li, L. Zhang and L. Yang. 2011. Antimicrobial activity against Shigella sonnei and probiotic properties of wild lactobacilli from fermented food. Microbiol. Res. 167(1): 27–31.
Published
2021-05-21
How to Cite
Łopusiewicz, Łukasz, E. Drozłowska, P. Trocer, M. Kostek, A. Bartkowiak, and P. Kwiatkowski. “The Development of Novel Probiotic Fermented Plant Milk Alternative from Flaxseed Oil Cake Using Lactobacillus Rhamnosus GG Acting As a Preservative Agent Against Pathogenic Bacteria During Short-Term Refrigerated Storage”. Emirates Journal of Food and Agriculture, vol. 33, no. 4, May 2021, pp. 266-7, doi:10.9755/ejfa.2021.v33.i4.2679.
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Research Article
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