In vitro gastrointestinal resistance of Lacticaseibacillus rhamnosus GG in passion fruit drinks added with whey

Authors

DOI:

https://doi.org/10.33448/rsd-v11i16.37763

Keywords:

Functional food; Dairy co-product; Tropical fruit; Probiotic; In vitro assay.

Abstract

Foods containing whey in their formulation are widespread in different parts of the world. Thus, the objective of this work was to evaluate the in vitro simulated gastrointestinal resistance of Lacticaseibacillus rhamnosus GG (LGG) in passion fruit drinks added with whey. Beverages with 6% and 11% whey powder were prepared, added with passion fruit pulp and probiotic, and they were evaluated for microbiological characteristics, LGG viability throughout the shelf life, LGG resistance to gastrointestinal conditions simulated in vitro and physicochemical characteristics. The beverages showed satisfactory microbiological quality and the probiotic remained viable throughout the storage period, with count values higher than 7.91 Log CFU/mL. After the in vitro simulation of the gastrointestinal tract, it was found that LGG showed greater resistance when conveyed in the beverage that contained 6% of whey, which may be due to lower saturation in the medium, when compared to the formulation that contained 11%. The physicochemical quality of the drinks was adequate, with consistent results both in terms of formulation and storage time. Therefore, the beverages developed have potential for commercial use and diversification of the food line containing whey and probiotics.

References

Andrews, M. H., Wang, H., Jacobson, A., Ge, B., Zhang, G., & Hammack, T. S. (2021). Manual Analítico Bacteriológico (BAM). https://www.fda.gov/food/laboratory-methods-food/bacteriological-analytical-manual-bam.

AOAC (2016). Association of Official Analytical Chemists. Official methods of analysis of the Association of Official Analytical Chemists. (20a.ed.), v.2.

Bedani, R., Rossi, E. A., & Saad, S. M. I. (2013). Impact of inulin and okara on Lactobacillus acidophilus La-5 and Bifidobacterium animals Bb-12 viability in a fermented soy product and probiotic survival under in vitro simulated gastrointestinal conditions. Food Microbiology. 34, 382-389. https://doi:10.1016/j.fm.2013.01.012.

Beuchat, I. R., & Cousin, M. A. (2201). Years and molds. In: Downes, F. P.; Ito, K. (ed.). Compendium of Methods for the Microbiological Examination of Foods, (4a.ed.): American Public Health Association-APHA, chapter 20, p. 209-215.

Brasil. (1999). Agência Nacional de Vigilância Sanitária. Portaria n.º 398, de 30 de abril de 1999. Regulamento Técnico que estabelece as diretrizes básicas para análise e comprovação de propriedades funcionais e ou de saúde alegadas em rotulagem de alimentos. DF: Brasília, Diário Oficial da União.

Brasil. (2003). Ministério da Agricultura Pecuária e Abastecimento. Instrução normativa nº 12, de 4 de setembro de 2003. Aprova o Regulamento Técnico para Fixação dos Padrões de Identidade e Qualidade Gerais para Suco Tropical; os Padrões de Identidade e Qualidade dos Sucos Tropicais de Abacaxi, Acerola, Cajá, Caju, Goiaba, Graviola, Mamão, Manga, Mangaba, Maracujá e Pitanga; e os Padrões de Identidade e Qualidade dos Néctares de Abacaxi, Acerola, Cajá, Caju, Goiaba, Graviola, Mamão, Manga, Maracujá, Pêssego e Pitanga. Diário Oficial da União, Brasília.

Brasil. (2006). Ministério da Agricultura, Pecuária e Abastecimento. Secretaria de Defesa Agropecuária. Instrução Normativa n.º 68, de 12 de dezembro de 2006. Métodos Analíticos Físico-Químicos para Controle de Leite e Produtos Lácteos. Ministério da Agricultura. Brasília, DF: Diário Oficial da União.

Brasil. (2013). Ministério da Agricultura, Pecuária e Abastecimento. Instrução Normativa n°19, de 19 de Junho de 2013. Estabelece a complementação dos padrões de identidade e qualidade para as bebidas. Brasília, DF: Diário Oficial da União.

Campos, R. C. A. B., Martins, E. M. F., Pires, B. A., Peluzio, M. C. G., Campos, da R. A. N., Ramos, A. M., Júnior, B. R. C. L., Martins, A. D. O., Silva, R. R. S., & Martins, M. L. (2019). In vitro and in vivo resistance of Lactobacillus rhamnosus GG carried by a mixed pineapple (Ananas comosus L. Merril) and jussara (Euterpe edulis Martius) juice to the gastrointestinal tract. Food Research International, 116, 1247-1257. https://doi: 10.1016/j.foodres.2018.10.012.

Champagne, C. P., Gomes, da C. A., & Daga, M. (2018). Strategies to improve the functionality of probiotics in supplements and foods. Current Opinion in Food Science. 22, 160-166. https://doi.org/10.1016/j.cofs.2018.04.008.

Fonseca, H. C., Melo, D. de S., Ramos, C. L., Menezes, A. G. T., Dias, D. R., & Schwan, R. F. (2021). Sensory and flavor-aroma profiles of passion fruit juice fermented by potentially probiotic Lactiplantibacillus plantarum CCMA 0743 strain. Food Research International, 152, 1-30. https://doi.org/10.1016/j.foodres.2021.110710

Furtado, L. L., Martins, M. L., Ramos, A. M., da Silva, R. R., Junior, B. R. D. C. L., & Martins, E. M. F. (2019). Viability of probiotic bacteria in tropical mango juice and the resistance of the strains to gastrointestinal conditions simulated in vitro. Semina: Ciências Agrárias, 40, 149-162. 10.5433/1679-0359.2019v40n1p149.

Goldin, B. R., Gorbach, S. L., Saxelin, M., Barakat, S., Gualtieri, L., & Salminen, S. (1992). Survival of Lactobacillus species (strain GG) in human gastrointestinal tract. Digestive diseases and sciences. 37, 121-128. https://doi.org/10.1007/BF01308354.

IBGE. (2020). Produção Agrícola Municipal. Available at: https://sidra.ibge.gov.br/tabela/5457#resultado.

Karim, A., & Aider, M. (2022). Production of prebiotic lactulose through isomerisation of lactose as a part of integrated approach through whey and whey permeate complete valorisation: A review. International Dairy Journal. 126, 1-14. https://doi.org/10.1016/j.idairyj.2021.105249.

Khalili, L., Alipour, B., Jafar-Abadi, M. A., Faraji, I., Hassanalilou, T., Abbasi, M., Vaghef-Mehrabany, E., & Sani, M. A. (2019). The effects of Lactobacillus casei on glycemic response, serum Sirtuin1 and Fetuin-A levels in patients with type 2 diabetes mellitus: a randomized controlled trial. Iranian Biomedical Journal, 23, 68. https://doi.org/10.29252/.23.1.68.

Kim, S., Huang, E., Park, S., Holzapfel, W., & Lim, S. D. (2018). Physiological characteristics and anti-obesity effect of Lactobacillus plantarum K10. Korean Journal for food Science Animal Resources, 38, 554-569. https://doi.org/10.5851/kosfa.2018.38.3.554.

Kornacki, J. L., & Johnson, J. L. (2001). Enterobacteriaceae, coliforms, and Escherichia coli as quality and safety indicators. In: Downes, F. P., Ito, K. (ed.). In: Compendium of methods for the microbiological examination of foods. 4.ed. Washington: American Public Health Association – APHA, p. 69-82.

Lee, E., Jung, S. R., Lee, S. Y., Lee, N. K., Paik, H. D., & Lim, S. I. (2018). Lactobacillus plantarum strain Ln4 attenuates diet-induced obesity, insulin resistance, and changes in hepatic mRNA levels associated with glucose and lipid metabolism. Nutrients, 10, 1-15. https://doi.org/10.3390/nu10050643.

Liu, W. C., Yang, M. C., Wu, Y. Y., Chen, P. H., Hsu, C. M., & Chen, C.M. (2018). Lactobacillus plantarum reverse diabetes-induced Fmo3 and ICAM expression in mice through enteric dysbiosis-related c-Jun NH2-terminal kinase pathways. Plos One, 13, 1-23. https://doi.org/10.1371/journal.pone.0196511.

Madureira, A. R., Amorim, M., Gomes, A. M., Pintado, M. E., & Malcata, F. X. (2011). Protective effect of whey cheese matrix on probiotic strains exposed to simulated gastrointestinal conditions. Food Research International, 44, 465-470. https://doi.org/10.1016/j.foodres.2010.09.010.

Milkpoint. (2021). Whey protein: como o produto do soro do leite foi de descarte poluente a um ingrediente caro. https://www.milkpoint.com.br/noticias-e-mercado/giro-noticias/como-o-whey-protein-foi-de-descarte-poluente-a-um-ingrediente-caro-227613/.

Miranda, J. S., Pereira, C. V. A. C., Andrade, M. E., Vargas, S. O. E., Oliveira, M. M., Lima, D. C. N., Júnior, B. R, C. L., Ferreira, D. R., & Martins, M. L. (2022). Impact of adding milk whey, probiotic and prebiotic in passion fruit drinks. Brazilian Journal of Development, 8, 30484-30504. https://doi.org/10.34117/bjdv8n4-500

Mehra, R., Kumar, H., Kumar, N., Ranvir, S., Jana, A., Buttar, H. S., Telessy, I. G., Awuchi, C., Okpala, C. O., Korzeniowska, M., & Guiné, R. P. F. (2021). Whey proteins processing and emergent derivatives: An insight perspective from constituents, bioactivities, functionalities to therapeutic applications. Journal of Functional Foods, 87, 1-17. https://doi.org/10.1016/j.jff.2021.104760.

Moreira, R. M., Martins, M. L., Júnior, B. R. D. C. L., Martins, E. M. F., Ramos, A. M., Cristianini, M., Campos, A. N. R., Stringheta, P. C., Silva, R.O., Canuto, J. W., Oliveira, D. C., & Pereira, D. C. S. (2017). Development of a juçara and Ubá mango juice mixture with added Lactobacillus rhamnosus GG processed by high pressure. LWT, 77, 259-268. https://doi.org/10.1016/j.lwt.2016.11.049.

Pimentel, T. C., Gomes, L. I. O., Lourdes, E. C. M., Costa, G. N., Dias, D. R., Schwan, R. F., & Magnani, M. (2021). Understanding the potential of fruits, flowers, and ethnic beverages as valuable sources of techno-functional and probiotics strains: Current scenario and main challenges. Trends in Food Science e Technology, 114, 25-59. https://doi:10.1016/j.tifs.2021.05.024.

Rasika, D. M. D., Vidanarachchi, J. K., Rocha, R. S., Balthazar, C. F., Cruz, A. G., Chaminda, A. S. S., & Ranadheera, C. S. (2021). Plant-based milk substitutes as emerging probiotic carriers. Current Opinion in Food Science, 38, 8-20. https://doi.org/10.1016/j.cofs.2020.10.025.

Richter, R. L., & Vedamuthu, E. R. (2001). Milk and milk products. In: Downes, F. P., & Ito, K. (Eds.). Compendium of Methods for the Microbiological Examination of Foods. (4a. ed.): American Public Health Association – APHA, p.483-505.

Routy, B., Lechatelier, E., Derosa, L., Duong, C. O. M., Alou, M. T., Daillere, R., Fluckiger, A., Messaoudene, M., Rauber, C., Roberti, M. P., Fidelle, M., Flament, C., Poirier-Colame, V., Opolon, P., Klein, C., Iribarren., K, Mondragón, L., Jacquelot, N., Qu, B., Ferrere, G., Clemenson, C., Mezquita, L., Masip, J. R., Naltet, C., Brosseau, S., Kaderbhai, C., Richard, C., Rizvi, H., Levenez, F., Galleron, N., Quinquis, B., Pons, N., Ryffel, B., Minard-Colin, V., Gonin, P., Soria, J. C., Deutsch, E., Loriot, Y., Ghiringhelli, F., Zalcman, G., Goldwasser, F., Escudier, B., Helmann, M. D., Eggermont, A., Raoult, D., Albiges, L., Kroemer, G., & Zitvogel, L. (2018). Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science, 359, 91-97. https://doi.org/10.1126/science. aan3706.

Rosa, L. P., Barros, L. de S., Souza, R. S. de., Pereira, D. H., & Cruz, L. C. C. 2020. Análise da bebida láctea de cupuaçu. Pesquisa, Sociedade e Desenvolvimento, 9, 1-11. http://dx.doi.org/10.33448/rsd-v9i10.9441.

Rudzki, L., Ostrowska, L., Pawlak, D., Matus, A., Pawlak, K., Waszkiewicz, N., & Szulc, A. (2019). Probiotic Lactobacillus plantarum 299v decreases kynurenine concentration and improves cognitive functions in patients with major depression: A double-blind, randomized, placebo-controlled study. Psychoneuroendocrinology, 100, 213-222. https://doi: 10.1016/j.psyneuen.2018.10.010.

Sanders, M. E., Merenstein, D. J., Reid, G., Gibson, G. R., & Rastall, R. A. (2019). Probiotics and prebiotics in intestinal health and disease: from biology to the clinic. Nature Reviews Gastroenterology e Hepatology, 16, 605- 616. https://doi.org/10.1038/s41575-019-0199-6.

Siedlecka, K. K., Daca, A., Fic, M., Wetering, T. V de., Folwarski, M., & Makarewicz, W. (2020). Therapeutic methods of gut microbiota modification in colorectal cancer management – fecal microbiota transplantation, prebiotics, probiotics, and synbiotics. Gut Microbes, 11, 1518-1530. https://doi.org/10.1080/19490976.2020.1764309.

Soldi, S., Tagliacarneb, S. C., Valsecchic, C., Pernad, S., Rondanellie, M., Zivianif, L., Millerif, S., Annonig, A., & Castellazzib, A. (2019). Effect of a multistrain probiotic (Lactoflorene® Plus) on inflammatory parameters and microbiota composition in subjects with stress-related symptoms. Neurobiology of Stress, 10, 100-138. https://doi.org/10.1016/j.ynstr.2018.11.001.

Succi, M., Tremonte, P., Reale, A., Sorrentino, E., Grazia, L., Pacifico, S., & Coppola, R. (2005). Bile salt and acid tolerance of Lactobacillus rhamnosus strains isolated from Parmigiano Reggiano cheese. FEMS microbiology letters, 244, 129-137. https://doi.org/10.1016/j.femsle.2005.01.037

Swanson, K. M. J., Petran, R. L., & Hanlin, J. H. (2001). Culture methods for enumeration of microorganisms. Compendium of methods for the microbiological examination of foods, (4th ed.) American Public Health Association, Washington, DC, 53-62.

TIBCO Software Inc. (2017). Statistica. Version 13. Global Leader in Integration and Analytics Software.

World Gastroenterology Organisation - WGO. (2017). Diretrizes Mundiais da Organização Mundial de Gastroenterologia. Probióticos e prebióticos, 35 https://www.worldgastroenterology.org/UserFiles/file/guidelines/probiotics-and-prebiotics-portuguese-2017.pdf.

Wu, C. A., Lin, F. H., Lee, Y. T., Ku, M. S., & Lue, K. H. (2019). Effect of Lactobacillus rhamnosus GG immunopathologic changes in chronic mouse asthma model. Journal of Microbiology, Immunology and Infection, 52, 911-919. https://doi.org/10.1016/j.jmii.2019.03.002.

Zhang, S., Guo, T., Xin, Y., Qin, L., & Kong, J. (2021). Biotechnological production of d-tagatose from lactose using metabolically engineering Lactiplantibacillus plantarum. LWT, 142, 2-9.110995. https://doi.org/10.1016/j.lwt.2021.110995.

Published

01/12/2022

How to Cite

EMILIANO, G. dos S. .; CUNHA, R. A. .; RODRIGUES, C. H. G. .; CALSAVARA, J. F. V. .; LEANDRO, S. P. .; ANTUNES, D. J. de P. .; CAMPOS, R. C. de A. B. .; MARTINS, . E. M. F. .; MARTINS, M. L. . In vitro gastrointestinal resistance of Lacticaseibacillus rhamnosus GG in passion fruit drinks added with whey. Research, Society and Development, [S. l.], v. 11, n. 16, p. e105111637763, 2022. DOI: 10.33448/rsd-v11i16.37763. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/37763. Acesso em: 23 apr. 2024.

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Section

Health Sciences