Response of microencapsulated Lactobacillus casei to in-vitro conditions that simulate the gastrointestinal environment and inhibitory potential on Staphylococcus aureus
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Keywords

Foodborne Diseases
Lactobacillales
Lactobacillus casei
Prebiotics
Probiotics
Staphylococcus aureus

How to Cite

Cerón-Córdoba, J.-F., Bolaños-Bolaños, J. C., & Jurado Gámez, H. (2024). Response of microencapsulated Lactobacillus casei to in-vitro conditions that simulate the gastrointestinal environment and inhibitory potential on Staphylococcus aureus . Médicas UIS, 37(2), 9–22. https://doi.org/10.18273/revmed.v37n2-2024001

Abstract

Introduction: from a microbiological point of view, Staphylococcus aureus is one of the main contaminants causing foodborne illnesses, with symptoms such as nausea, vomiting, diarrhea, abdominal cramps, joint or back pain and fatigue. Bacterial resistance of pathogenic bacteria has recently been found to be a public health problem. An alternative is the use of microencapsulated probiotics for the inhibition of pathogenic microorganisms such as Lactobacillus casei. Objective: evaluate microencapsulated Lactobacillus casei ATCC 393® under in-vitro conditions simulating the gastrointestinal environment and the inhibitory potential on Staphylococcus aureus ATCC BAA 1708®. Materials and methods: reconstitution, seeding and adjustment of the inoculum; antibiogram of the two bacterial strains; fermentation kinetics of Lactobacillus casei; identification of peptides, amino acids and lactic acid of the supernatant; resistance of Lactobacillus casei to different temperatures (37 °C and 45 °C); microencapsulation of Lactobacillus casei; study, characterization and exposure to simulated gastrointestinal conditions of the microencapsulate after 90 days of storage and production of Exopolysaccharides. Results: the results indicate inhibitory action of the Lactobacillus casei strain against pathogenic bacteria; exponential phase at 15 hours (MRS culture medium) and 18 hours (PRO culture medium); results of the microencapsulation study and analysis: viability 100 %; efficiency 84,64 %; humidity 4,0 %; solubility 99,8 %; wettability 2 min with 22 seconds; water activity 0,617 and particle size between 2,10 µm and 5,28 µm. Conclusion: it was concluded that the microencapsulated Lactobacillus casei showed inhibitory properties against the pathogenic strain.

https://doi.org/10.18273/revmed.v37n2-2024001
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References

Koohestani M, Moradi M, Tajik H, Badali A. Effects of cell-free supernatant of Lactobacillus acidophilus LA5 and Lactobacillus casei 431 against planktonic form and biofilm of Staphylococcus aureus. Vet Res Forum. 2018;9(4):301-306.

Mendonca A, Thomas-Popo E, Gordon A. Microbiological considerations in food safety and quality systems implementation. In: Lakhan R, Mondal S, editors. Food Safety and Human Health. London: Elsevier; 2020. p. 185-260.

Munera G. Encapsulación de antimicrobianos naturales en sistemas nano y microestructurados: técnicas y aplicaciones en tecnología de alimentos [tesis]. Valencia: Universitat Politécnica de Valencia; 2020.

Zheng Y, Gracia A, Hu L. Predicting Foodborne Disease Outbreaks with Food Safety Certifications: Econometric and Machine Learning Analyses. J Food Prot. 2023;86(9):100136.

Osorio MB, Rizo-Tello VZ, Sánchez EM, Prieto-Alvarado F, Gómez LC. Foodborne illness outbreak in a special population. Cali, Colombia 2021. IJEPH. 2021;4(2):1-8.

Long J, Du G, Chen J, Xie C, Xu J, Yuan J. Bacteria and poisonous plants/fungi were the primary causative hazards of foodborne disease outbreaks: A five-year survey from Guangzhou, Guangdong. Int J Food Microbiol. 2023;400:110264.

Stewart GC. Staphylococcal Food Poisoning. Foodborne Diseases. 2017;367–380.

Taylor MH, Zhu MJ. Control of Listeria monocytogenes in low-moisture foods. Trends Food Sci Technol. 2021;116:802-814.

Khamis MA, Mousa MM, Helmy NM. Methicillin-Resistant Staphylococcus aureus (MRSA) in some meat products. Alex J Vet Sci. 2021;70(1):96-105.

De Andrade JB, Alexandre MA, da Silva CR, de Sousa R, Aires do Nascimento FBS, Serpa Sampaio L, et al. A mechanistic approach to the in-vitro resistance modulating effects of fluoxetine against meticillin resistant Staphylococcus aureus strains. Microb Pathog. 2019;127:335-340.

Torres G, Vargas K, Reyes-Vélez J, Jiménez N, Blanchard A, Olivera-Angel M. High genetic diversity and zoonotic potential of Staphylococcus aureus strains recovered from bovine intramammary infections in Colombians dairy herds. Comp Immunol Microbiol Infect Dis. 2023;93(52):101940.

Torres G, Vargas K, Sánchez-Jiménez M, Reyes-Velez J, Olivera-Angel M. Genotypic and phenotypic characterization of biofilm production by Staphylococcus aureus strains isolated from bovine intramammary infections in Colombian dairy farms. Heliyon. 2019;5(10):e02535.

Roldán-Perez S, Gómez-Rodriguez SL, Sepúlveda-Valencia JU, Ruiz-Villadiego OS, Márquez-Fernandez ME, Montoya-Campuzano OI, et al. Assessment of probiotic properties of lactic acid bacteria isolated from an artisanal Colombian cheese. Heliyon. 2023;9(11):e21558.

El-Enshasy HA, Yang ST. Probiotics, the Natural Microbiota in Living Organisms. 1st ed. Boca Raton. CRC Press; 2021.

Salazar-Salazar Z, Hurtado-Ayala L, Perez-Morales E, Alcántara-Jurado L, Landeros-Sánchez B, Brito-Perea M. Pruebas de susceptibilidad a bacteriocinas producidas por BAL en bacterias resistentes a antibióticos. Rev Mex Ciencias Farm. 2017;48(1):7–17.

Saidi N, Saderi H, Owlia P, Soleimani M. Anti-Biofilm Potential of Lactobacillus casei and Lactobacillus rhamnosus Cell-Free Supernatant Extracts against Staphylococcus aureus. Adv Biomed Res. 2023;12(1):50.

Chen W. Lactic Acid Bacteria Bioengineering and Industrial Applications: Bioengineering and Industrial Applications. Singapore: Springer; 2019.

González-Ferrero C. Microencapsulation of Probiotics in Soybean Protein Particles Obtained From a Food By-Product. Universidad de Navarra; 2019.

Hutkins R. Microbiology and Technology of Fermented Food. 2nd Edition. Hoboken, NJ, USA: John Wiley & Sons, Inc; 2019.

Rodrigues FJ, Cedran MF, Bicas JL, Sato HH. Encapsulated probiotic cells: Relevant techniques, natural sources as encapsulating materials and food applications – A narrative review. Food Res Int. 2020;137:109682.

González E, Gómez-Caravaca AM, Giménez B, Cebrián R, Maqueda M, Parada J, et al. Role of maltodextrin and inulin as encapsulating agents on the protection of oleuropein during in vitro gastrointestinal digestion. Food Chem. 2020;310:125976.

Fonseca HC, de Sousa-Melo D, Ramos CL, Dias DR, Schwan RF. Probiotic Properties of Lactobacilli and Their Ability to Inhibit the Adhesion of Enteropathogenic Bacteria to Caco-2 and HT-29 Cells. Probiotics Antimicrob Proteins. 2021;13(1):102-112.

Jurado-Gámez H, Calpa-Yama F, Chaspuengal-Tulcán A. DETERMINACIÓN IN VITRO DE LA ACCIÓN PROBIÓTICA DE Lactobacillus plantarum SOBRE Yersinia pseudotuberculosis AISLADA DE Cavia porcellus. Rev Med Vet Zoot. 2014;61(3):241–257.

Tagg JR, McGiven AR. Assay System for Bacteriocins. Appl Microbiol. 1971;21(5):943.

Jurado-Gámez H, Ramírez C, Aguirre D. Cinética de fermentación de Lactobacillus plantarum en un medio de cultivo enriquecido como potencial probiótico. Revista Veterinaria Y Zootecnia. 2013; 7(2):37–53.

Bauer AW, Kirby W, Sherris CJ, Turck M. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol. 1966;45(4):493–496.

Sánchez EP, Nuñez D, Cruz RO, Torres MA, Herrera E. Simulación y Conteo de Unidades Formadoras de Colonias. Rev electrónica Comput Informática, Biomédica y Electrónica. 2017;6(1):97–111.

Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. Colorimetric Method for Determination of Sugars and Related Substances. Anal Chem. 1956;28(3):350–356.

Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. PROTEIN MEASUREMENT WITH THE FOLIN PHENOL REAGENT. J Biol Chem. 1951;193(1):265–275.

Cai Y, Puangpen S, Premsuda S, Benno Y. Classification and characterization of lactic acid bacteria isolated from the intestines of common carp and freshwater prawns. J Gen Appl Microbiol. 1999;45(4):177–184.

Montes-Ramírez LM. Efecto de la microencapsulación con agentes prebióticos sobre la viabilidad de microorganismos probióticos (Lactobacillus casei ATCC 393 y Lactobacillus rhamnosus ATCC 9469). Universidad Nacional de Colombia. 2013.

Rodríguez-Barona S, Giraldo GI, Montes LM. Encapsulación de Alimentos Probióticos mediante Liofilización en Presencia de Prebioticos. Inf tecnológica. 2016;27(6):135–144.

Gonzales-Cuello R, Perez-Mendoza J, Morón-Alcazar L. Efecto de la Microencapsulación sobre la Viabilidad de Lactobacillus delbrueckii sometido a Jugos Gástricos Simulados. Inf tecnológica. 2015;26(5):11–16

Cruz Pacheco K, Madrigal Mendoza GA, Valencia G, Páramo Durán E. VIABILIDAD DE LACTOBACILLUS DELBRUECKII LIBRE E INMOVILIZADO BAJO CONDICIONES GASTROINTESTINALES SIMULADAS IN VITRO. 2009;1–22.

Cruz Ramos R. ESTUDIO DE LA SUPERVIVENCIA DE BACTERIAS PROBIÓTICAS MICROENCAPSULADAS BAJO CONDICIONES GASTROINTESTINALES SIMULADAS EN UN SISTEMA DINÁMICO. Instituto Tecnológico de Tuxtla Gutiérrez; 2015.

Maciel-Paulo E, Pinho-Vasconcelos M, Santiago-Oliveira I, de Jesús-Affe HM, Nascimento R, de Melo IS, et al. An alternative method for screening lactic acid bacteria for the production of exopolysaccharides with rapid confirmation. ACS Food Sci Technol. 2012;32(4):710-714.

Guimarães DP, Costa FAA, Rodrigues MI, Maugeri F. Optimization of dextran syntesis and acidic hydrolisis by surface response analysis. Braz. J. Chem. Eng. 1999;16(2):129-139.

Serna-Jimenez AJ. Elaboración De Jugos De Fruta Con Adición De Bacterias Ácido Lácticas Con Potencial Probiótico [tesis]. Chía: Universidad de la Sabana; 2012.

Hayes MA. The use of Giemsa stain for tissue sections. Med Bull (Ann Arbor). 1951;17(6):206-207.

Flores-Tixicuro JM, País-Chanfrau JM, Sánchez-de-Céspedes IS, Lara-Fiallos MV, Núñez-Pérez J. Optimización estadística de un bioproceso de ácido láctico a partir de lactosuero. Ciencia Latina Revista Científica Multidisciplinar. 2021:5(3);3259-3274.

Rai R, Bai JA. Beneficial Microbes in Fermented and Functional Foods. Beneficial Microbes in Fermented and Functional Foods. Boca Raton: CRC Press; 2014.

Erginkaya Z, Turhan EU, Tatli D. Determination of antibiotic resistance of lactic acid bacteria isolated from traditional Turkish fermented dairy products. Iran J Vet Res. 2018;19(1):56.

Sánchez L, Omura M, Lucas A, Pérez T, Ferreira C de L. Cepas de Lactobacillus spp. con capacidades probióticas aisladas del tracto intestinal de terneros neonatos. Rev Salud Anim. 2015;37(2):94-104.

Flórez AB, Mayo B. Antibiotic resistance-susceptibility profiles of Streptococcus thermophilus isolated from raw milk and genome analysis of the genetic basis of acquired resistances. Front Microbiol. 2017;8:1-12.

Guo H, Pan L, Li L, Lu J, Kwok L, Menghe B, et al. Characterization of Antibiotic Resistance Genes from Lactobacillus Isolated from Traditional Dairy Products. J Food Sci. 2017;82(3):724-730.

May-Torruco AL, Corona-Cruz AI, Jiménez ALL, González-Cortés N, Jiménez-Vera R. Sensibilidad y Resistencia a Antibióticos de Cepas Probióticas Empleadas en Productos Comerciales. ESJ. 2020;16(18):43-60.

Acosta-Nieves IP, Roenes-Gale GJ. Staphylococcus aureus procedentes de quesos costeños de Valledupar; susceptibilidad a antibióticos y perfil plasmídico. Rev Méd Risaralda. 2019;25(1):10-14.

Schulte RH, Munson E. Staphylococcus aureus Resistance Patterns in Wisconsin: 2018 Surveillance of Wisconsin Organisms for Trends in Antimicrobial Resistance and Epidemiology (SWOTARE). Clin Med Res. 2019;17(3-4):72-81.

Gao L, Zhu H, Chen Y, Yang Y. Antibacterial pathway of cefquinome against Staphylococcus aureus based on label-free quantitative proteomics analysis. J Microbiol. 2021;59(12):1112-1124.

Jurado-Gámez H, Guzmán-Insuasty M, Jarrín-Jarrín V. Determinación de la cinética, pruebas de crecimiento y efecto de inhibición in vitro de Lactobacillus lactis en Staphylococcus aureus, Staphylococcus epidermidis, Streptococcus agalactiae y Escherichia coli. Rev. Med. Vet. Zoot. 2015;62(2):40-56.

Rajkovic A, Smigic N, Devlieghere F. Contemporary strategies in combating microbial contamination in food chain. Int J Food Microbiol. 2010;141(supplement):S29-S42.

Chen L, Song Z, Tan SY, Zhang H, Yuk HG. Application of Bacteriocins Produced from Lactic Acid Bacteria for Microbiological Food Safety. Curr. Top. Lact. Acid Bact. Probiotics. 2020;6(1):1-8.

Alizadeh-Behbahani B, Noshad M, Falah F. Inhibition of Escherichia coli adhesion to human intestinal Caco-2 cells by probiotic candidate Lactobacillus plantarum strain L15. Microb Pathog. 2019;136:103677.

Jurado-Gámez H, Martínez-Benavides J, Romero-Benavides DA, Morillo-Garcés JA, Orbes-Villacorte AE, Mesías-Pantoja LN. Cinética de fermentación, pruebas de desafío in vitro y efecto de inhibición de Lactobacillus gasseri ATCC 19992. Rev. Med. Vet. Zoot. 2016;63(2):95-112.

Sinsajoa-Tepud M, Jurado-Gamez H, Narváez-Rodríguez M. Evaluación de Lactobacillus plantarum microencapsulado y su viabilidad bajo condiciones gastrointestinales simuladas e inhibición frente a Escherichia coli O157:H7. Rev la Fac Med Vet y Zootec. 2019; 66(3):231–244.

Vera-Mejía R, Sánchez-Miranda L, Zambrano-Gavilares P, Rodriguez-Perdomo Y. Obtención de un candidato a probiótico de Lactobacillus plantarum 22 LMC a partir de un medio de cultivo natural con materias primas agroindustriales. Rev Salud Anim. 2021;43(3):e03.

González BA, Domínguez-Espinosa R, Alcocer BR. USE OF Aloe vera JUICE AS SUBSTRATE FOR GROWTH OF Lactobacillus plantarum and L. casei. Cienc y Tecnol Aliment. 2007;6(2):152–157.

James M, Velastegui E, Cruz MA. Evaluación de las condiciones de cultivo de Lactobacillus acidophilus y Lactobacillus casei a nivel de laboratorio, con inulina como fuente de carbono. Bionatura. 2017;2(1):235-240.

Fajardo-Argoti C, Jurado-Gámez H, Parra-Suescun, J. Viabilidad de Lactobacillus plantarum microencapsulado bajo condiciones gastrointestinales simuladas e inhibición sobre Escherichia coli O157:H7. Rev. UDCA. Actual. Divulg. Cient. 2021;24(1): e1733.

Jurado-Gámez HA, Romero-Benavides DA, Morillo-Garces JA. INHIBICIÓN DE Lactobacillus gasseri SOBRE Yersinia pseudotuberculosis BAJO CONDICIONES IN VITRO. Rev. Med. Vet. Zoot. 2016;63(2):95-112.

Fang Wu Wu JW. CARACTERIZACIÓN DE BACTERIAS ÁCIDO LÁCTICAS (BAL) AISLADAS DE ENSILADOS DE PIÑA COMO MICROORGANISMOS CON POTENCIAL PROBIÓTICO Y DETERMINACIÓN DE SU APLICABILIDAD COMO CULTIVO BIOPROTECTOR EN LECHE AGRIA. Costa Rica. Universidad de Costa Rica. 2020

Kanauchi M. Lactic Acid Bacteria: Methods and Protocols. New York: Humana Press; 2019. p.194.

Vallejo M, Ledesma P, Anselmino L, Marguet E. Efecto de las condiciones de crecimiento y composición del medio de cultivo sobre la producción de bacteriocina de Enterococcus mundtii Tw56. Rev. Colomb. Biote. 2014;16(2):174-179.

Rosales-Bravo H, Vázquez-Martínezb J, Morales-Torres HC, Olalde-Portuga V. Evaluación de propiedades tecno-funcionales de cepas probióticas comerciales del género Lactobacillus. Rev. Int. Investig. innov. tecnol. 2020;8(45):1-19.

Ceron-Cordoba JF, Jurado-Gámez H, Bolaños-Bolaños JC. Aplicación de un probiótico (Lactobacillus Reuteri ATCC 53608) microencapsulado en una bebida tipo sorbete a base de pulpa de fruta (banano y mango) como alimento funcional y su aplicación en la industria alimentaria. Aglala. 2021;12(2):249–263.

Paim DRSF, Costa SDO, Walter EHM, Tonon RV. Microencapsulation of probiotic jussara (Euterpe edulis M.) juice by spray drying. Lwt. 2016;74:21–25.

Brodkorb A, Egger L, Alminger M, Alvito P, Assunção R, Ballance S, et al. INFOGEST static in vitro simulation of gastrointestinal food digestion. Nat Protoc. 2019;14(4):991–1014.

Sultana M, Chan ES, Janarthanan P, Choo WS. Functional orange juice with Lactobacillus casei and tocotrienol-enriched flaxseed oil co-encapsulation: Physicochemical properties, probiotic viability, oxidative stability, and sensorial acceptability. Lwt. 2023;188:115388.

Korcz E, Varga L. Exopolysaccharides from lactic acid bacteria: Techno-functional application in the food industry. Vol. 110, Trends in Food Science and Technology. 2021;(110):375–384.

Mora-Villalobos JA, Montero-Zamora J, Barboza N, Rojas-Garbanzo C, Usaga J, Redondo-Solano M, et al. Multi-Product Lactic Acid Bacteria Fermentations: A Review. Fermentation. 2020;6(23):21.

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