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Publication Date: 2014-06-20
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Fernández Villa, K. J., Chanci Echeverri, I. C., Wilches López, L., & Cardona Arias, J. A. (2014). Characterization of metabolites of lactic acid bacteria and inhibitory effect of bacteriocins on pathogenic microorganisms in foods: A systematic literature review, 2008-2012. Biosalud, 13(1), 45–61. Retrieved from https://revistasojs.ucaldas.edu.co/index.php/biosalud/article/view/4687
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Abstract
Introduction: Lactic acid bacteria are widely used in the food industry in order to preserve food and improve food sensory properties; its metabolites can inhibit the growth of Salmonella, Listeria monocytogenes, Escherichia coli and Staphylococcus aureus. Objective: To characterize the studies about microbial growth inhibiting metabolites and to describe the inhibitory effect of lactic acid bacteria bacteriocins in pathogenic microorganisms in food. Method: A systematic literature review with original articles published in Science Direct, PubMed and SCOPUS. The terms bacteriocins, lactic acid, hydrogen peroxide, citric acid, food, bacteriocin, Salmonella spp., Staphylococcus aureus, Listeria monocytogenes, Escherichia coli were used in the search. Results: One hundred-twenty-five studies about inhibitors metabolites were found, from which only 31 were carried out on food. Regarding bacteriocins and the type of microorganism inhibited, 114 studies were obtained, from which 50 worked with bactericins produced by acid lactic bacteria. The most common metabolites were bacteriocins. The most studied microorganism is Staphylococcus aureus and Staphylococcus aureus. The most frequently studied products are dairy and meat. Conclusion: The bacteriocins are the most studied metabolites to inhibit the growth of pathogenic microorganisms in food matrices; these might be relevant to reduce the foodborne illness.
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References
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Concha-Meyer A, Schöbitz R, Brito C, Fuentes R. Lactic acid bacteria in an alginate film inhibit Listeria monocytogenes growth on smoked salmon. Food Control. 2011; 22 (3-4): 485-9.
Vásquez S, Suarez H, Zapata S. Utilización de sustancias antimicrobianas producidas por Bacterias ácido Lácticas en la conservación de la carne. Rev Chil Nutr. 2009; 36 (1): 64-71.
Suarez H, De Francisco A, Beira L. Influencia de bacteriocinas producicas por Lactobacillus plantarum LPBM10 sobre la vida útil de filetes del híbrido de cachama Piaractus brachypomus x Colossoma macropomum empacado al vacio. Vitae 2008; 15 (1): 32-40.
Gueimonde M, Jalonen L, He F, Hiramatsu M, Salminen S. Adhesion and competitive inhibition and displacement of human enteropathogens by selected lactobacilli. Food Research International 2006; 39 (4): 467-71.
Galdeano CM, Perdigon G. The probiotic bacterium Lactobacillus casei induces activation of the gut mucosal immune system through innate immunity. Clin Vaccine Immunol. 2006; 13 (2): 219-26.
Ortiz, Z. ¿Qué son las revisiones sistemáticas? [Internet]. Disponible en: htpp://www.epidemiologia.anm.edu.ar. Consultado Octubre de 2013.
Manterola C. Revisión sistemática de la literatura síntesis de la evidencia. Rev méd Clín Condes. 2009; 20 (6): 897-903.
Letelier M, Manriquez J, Rada G. Revisiones sistemáticas y metaanálisis: ¿son la mejor evidencia? Rev Med Chile 2005; 133 (2): 246-9.
Marín F, Meca J, López J. El metaanálisis en el ámbito de las Ciencias de la Salud una metodología imprescindible para la eficiente acumulación del conocimiento. Fisioterapia 2009; 31 (3): 107-14.
Arqués JL, Rodríguez E, Nuñez M, Medina M. Combined effect of reuterin and lactic acid bacteria bacteriocins on the inactivation of food-borne pathogens in milk. Food Control. 2011; 22 (3-4): 457-61.
Chang JY, Chang HC. Improvements in the Quality and Shelf Life of Kimchi by Fermentation with the Induced Bacteriocin-Producing Strain, Leuconostoc citreum GJ7 as a Starter. J Food Sci. 2010; 75 (2): M103-M10.
Cobo Molinos A, Abriouel H, Ben Omar N, López RL, Gálvez A. Microbial diversity changes in soybean sprouts treated with enterocin AS-48. Food Microbiol. 2009; 26 (8): 922-6.
Molinos A, Abriouel H, Ben Omar N, Martinez-Canamero M, Gálvez A. A quantitative real-time PCR Assay for quantification of viable listeria monocytogenes cells after bacteriocin injury in food-first insights. Curr Microbiol. 2010; 61 (6): 515-9.
Dal Bello B, Cocolin L, Zeppa G, Field D, Cotter PD, Hill C. Technological characterization of bacteriocin producing Lactococcus lactis strains employed to control Listeria monocytogenes in cottage cheese. Int J Food Microbiol. 2012; 153 (1-2): 58-65.
Dimitrieva-Moats GY, Ünlü G. Development of Freeze-Dried Bacteriocin-Containing Preparations from Lactic Acid Bacteria to Inhibit Listeria monocytogenes and Staphylococcus aureus. Probiotics and Antimicro Prot. 2012; 4 (1): 27-38.
Dortu C, Huch M, Holzapfel WH, Franz CMAP, Thonart P. Anti-listerial activity of bacteriocin-producing Lactobacillus curvatus CWBI-B28 and Lactobacillus sakei CWBI-B1365 on raw beef and poultry meat. Lett Appl Microbiol. 2008; 47 (6): 581-6.
Hartmann HA, Wilke T, Erdmann R. Efficacy of bacteriocin-containing cell-free culture supernatants from lactic acid bacteria to control Listeria monocytogenes in food. In J Food Microbiol. 2011; 146 (2): 192-9.
Jofré A, Aymerich T, Garriga M. Improvement of the food safety of low acid fermented sausages by enterocins A and B and high pressure. Food Control. 2009; 20 (2): 179-84.
Kouakou P, Ghalfi H, Destain J, Dubois-Dauphin R, Evrard P, Thonart P. Effects of curing sodium nitrite additive and natural meat fat on growth control of Listeria monocytogenes by the bacteriocinproducing Lactobacillus curvatus strain CWBI-B28. Food Microbiol. 2009; 26 (6): 623-8.
Liu L, O’Conner P, Cotter PD, Hill C, Ross RP. Controlling Listeria monocytogenes in Cottage cheese through heterologous production of enterocin a by Lactococcus lactis. J Appl Microbiol. 2008; 104 (4): 1059-66.
Malheiros PdS, Sant’Anna V, Barbosa MdS, Brandelli A, Franco BD. Effect of liposome-encapsulated nisin and bacteriocin-like substance P34 on Listeria monocytogenes growth in Minas frescal cheese. Int J Food Microbiol. 2012; 156 (3): 272-7.
Ragazzo-Sánchez JA, Sánchez-Prado L, Gutiérrez-Martínez P, Luna-Solano G, Gomez-Gil B, CalderonSantoyo M. Inhibition of Salmonella spp. isolated from mango using bacteriocin-like produced by lactobacilli. Inhibición de Salmonella spp aislada de mango usando sustancias tipo bacteriocinas producidas por lactobacilos. CyTA Journal of Food. 2009; 7 (3): 181-7.
Sarika AR, Lipton AP, Aishwarya MS, Dhivya RS. Isolation of a bacteriocin-producing lactococcus lactis and application of its bacteriocin to manage spoilage bacteria in high-value marine fish under different storage temperatures. Appl Biochem Biotechnol. 2012; 167 (5): 1280-9.
Settanni L, Franciosi E, Cavazza A, Cocconcelli PS, Poznanski E. Extension of Tosèla cheese shelf-life using non-starter lactic acid bacteria. Food Microbiol. 2011; 28 (5): 883-90.
Siboukeur A, Siboukeur O. Effect of cameline nisin isolated from Lactococcus lactis sub sp. lactis on Staphylococcus aureus sp. Emirates J Food and Agriculture. 2013; 25 (5): 398-402.
Singh AK, Ramesh A. Succession of dominant and antagonistic lactic acid bacteria in fermented cucumber: Insights from a PCR-based approach. Food Microbiol. 2008; 25 (2): 278-87.
Tahiri I, Desbiens M, Kheadr E, Lacroix C, Fliss I. Comparison of different application strategies of divergicin M35 for inactivation of Listeria monocytogenes in cold-smoked wild salmon. Food Microbiol. 2009; 26 (8): 783-93.
Trias R, Badosa E, Montesinos E, Bañeras L. Bioprotective Leuconostoc strains against Listeria monocytogenes in fresh fruits and vegetables. International Journal of Food Microbiol. 2008; 127 (1-2): 91-8.
Trmčić A, Obermajer T, Majhenič AC, Rogelj I, Matijašić BB. In-situ inhibition of Staphylococcus aureus by lactic acid bacteria consortia from two traditional Slovenian raw milk cheeses. Mljekarstvo 2010; 60 (3): 183-90.
Udhayashree N, Senbagam D, Senthilkumar B, Nithya K, Gurusamy R. Production of bacteriocin and their application in food products. Asian Pacific J Tropical Biomedicine 2012; 2 (1 Supp.): S406-S10.
Vera Pingitore E, Todorov SD, Sesma F, Franco BD. Application of bacteriocinogenic Enterococcus mundtii CRL35 and Enterococcus faecium ST88Ch in the control of Listeria monocytogenes in fresh Minas cheese. Food Microbiol. 2012; 32 (1): 38-47.
Viedma PM, Abriouel H, Omar NB, López RL, Gálvez A. Antistaphylococcal effect of enterocin AS-48 in bakery ingredients of vegetable origin, alone and in combination with selected antimicrobials. J Food Sci. 2009; 74 (7): M384-M9.
Food and Agricultural Organization of the United Nations (FAO), World Health Organization (WHO). Guidelines for the evaluation of probiotics in food. FAo and WHO. [Internet]. Disponible en: ftp://ftp.fao.org/es/esn/food/wgreport2.pdf. Consultado Octubre de 2013.
Lin CM, Zhang L, Doyle MP, Swaminathan B. Comparison of media and sampling locations for isolation of Listeria monocytogenes in queso fresco cheese. J Food Prot. 2006; 69 (9): 2151-6.
Pinto AL, Fernandes M, Pinto C, Albano H, Castilho F, Teixeira P. et al. Characterization of anti-Listeria bacteriocins isolated from shellfish: Potential antimicrobials to control non-fermented seafood. Int J Food Microbiol. 2009; 129 (1): 50-8.
Cho GS, Hanak A, Huch M, Holzapfel WH, Franz C. Investigation into the Potential of Bacteriocinogenic Lactobacillus plantarum BFE 5092 for Biopreservation of Raw Turkey Meat. Probiotics and Antimicro Prot. 2010; 2 (4): 241-9.
Uribe C, Suárez M. Salmonelosis no tifoidea y su transmisión a través de alimentos de origen aviar. Colombia Médica 2006; 37 (2): 151-8.
Méndez I, Badillo C, Ortiz P, Faccini A. Caracterización microbiológica de Salmonella en alimentos de venta callejera en un sector universitario de Bogotá, Colombia. Julio a octubre de 2010. Médicas UIS 2011; 26 (1): 25-32.
Santos J, Gaviria A. Decreto 539 de 2014. Por el cual se expide el reglamento técnico sobre los requisitos sanitarios que deben cumplir los importadores y exportadores de alimentos para el consumo humano, materias primas e insumos para alimentos destinados al consumo humano y se establece el procedimiento para habilitar fábricas de alimentos ubicadas en el exterior. Bogotá D. C.: República de Colombia - Gobierno Nacional; 2014.
Urrego M, Cadavid L. Efecto sobre la calidad microbiológica, sensorial y reológica, de la aplicación de tres diferentes niveles de ácido láctico en un corte de carne de res (Huevo de Solomo). Medellín: Universidad Nacional de Colombia; 2005.
Klaenhammer T, Barranqou R, Buck BL, Azcarate M, Altermann E. Genomic features of lactic acid bacteria efecting bioprocessing and health. FEMS Microbioly Rev. 2005; 29 (3): 393-409.
Vásquez S, Suárez H, Montoya O. Crude bacteriocin extract effect on the microbiological and sensorial characteristics of solomo redondo (Longissimus dorsi) vacuum-packaging. Efecto del extracto crudo de bacteriocinas sobre las características microbiológicas y sensoriales de solomo redondo (Longissimus dorsi) empacado al vacío. Vitae. 2009; 16 (2): 191-200.
Abrams D, Barbosa J, Albano H, Silva J, Gibbs PA, Teixeira P. Characterization of bacPPK34 a bacteriocin produced by Pediococcus pentosaceus strain K34 isolated from “Alheira”. Food Control. 2011; 22 (6): 940-6.
Concha-Meyer A, Schöbitz R, Brito C, Fuentes R. Lactic acid bacteria in an alginate film inhibit Listeria monocytogenes growth on smoked salmon. Food Control. 2011; 22 (3-4): 485-9.
Vásquez S, Suarez H, Zapata S. Utilización de sustancias antimicrobianas producidas por Bacterias ácido Lácticas en la conservación de la carne. Rev Chil Nutr. 2009; 36 (1): 64-71.
Suarez H, De Francisco A, Beira L. Influencia de bacteriocinas producicas por Lactobacillus plantarum LPBM10 sobre la vida útil de filetes del híbrido de cachama Piaractus brachypomus x Colossoma macropomum empacado al vacio. Vitae 2008; 15 (1): 32-40.
Gueimonde M, Jalonen L, He F, Hiramatsu M, Salminen S. Adhesion and competitive inhibition and displacement of human enteropathogens by selected lactobacilli. Food Research International 2006; 39 (4): 467-71.
Galdeano CM, Perdigon G. The probiotic bacterium Lactobacillus casei induces activation of the gut mucosal immune system through innate immunity. Clin Vaccine Immunol. 2006; 13 (2): 219-26.
Ortiz, Z. ¿Qué son las revisiones sistemáticas? [Internet]. Disponible en: htpp://www.epidemiologia.anm.edu.ar. Consultado Octubre de 2013.
Manterola C. Revisión sistemática de la literatura síntesis de la evidencia. Rev méd Clín Condes. 2009; 20 (6): 897-903.
Letelier M, Manriquez J, Rada G. Revisiones sistemáticas y metaanálisis: ¿son la mejor evidencia? Rev Med Chile 2005; 133 (2): 246-9.
Marín F, Meca J, López J. El metaanálisis en el ámbito de las Ciencias de la Salud una metodología imprescindible para la eficiente acumulación del conocimiento. Fisioterapia 2009; 31 (3): 107-14.
Arqués JL, Rodríguez E, Nuñez M, Medina M. Combined effect of reuterin and lactic acid bacteria bacteriocins on the inactivation of food-borne pathogens in milk. Food Control. 2011; 22 (3-4): 457-61.
Chang JY, Chang HC. Improvements in the Quality and Shelf Life of Kimchi by Fermentation with the Induced Bacteriocin-Producing Strain, Leuconostoc citreum GJ7 as a Starter. J Food Sci. 2010; 75 (2): M103-M10.
Cobo Molinos A, Abriouel H, Ben Omar N, López RL, Gálvez A. Microbial diversity changes in soybean sprouts treated with enterocin AS-48. Food Microbiol. 2009; 26 (8): 922-6.
Molinos A, Abriouel H, Ben Omar N, Martinez-Canamero M, Gálvez A. A quantitative real-time PCR Assay for quantification of viable listeria monocytogenes cells after bacteriocin injury in food-first insights. Curr Microbiol. 2010; 61 (6): 515-9.
Dal Bello B, Cocolin L, Zeppa G, Field D, Cotter PD, Hill C. Technological characterization of bacteriocin producing Lactococcus lactis strains employed to control Listeria monocytogenes in cottage cheese. Int J Food Microbiol. 2012; 153 (1-2): 58-65.
Dimitrieva-Moats GY, Ünlü G. Development of Freeze-Dried Bacteriocin-Containing Preparations from Lactic Acid Bacteria to Inhibit Listeria monocytogenes and Staphylococcus aureus. Probiotics and Antimicro Prot. 2012; 4 (1): 27-38.
Dortu C, Huch M, Holzapfel WH, Franz CMAP, Thonart P. Anti-listerial activity of bacteriocin-producing Lactobacillus curvatus CWBI-B28 and Lactobacillus sakei CWBI-B1365 on raw beef and poultry meat. Lett Appl Microbiol. 2008; 47 (6): 581-6.
Hartmann HA, Wilke T, Erdmann R. Efficacy of bacteriocin-containing cell-free culture supernatants from lactic acid bacteria to control Listeria monocytogenes in food. In J Food Microbiol. 2011; 146 (2): 192-9.
Jofré A, Aymerich T, Garriga M. Improvement of the food safety of low acid fermented sausages by enterocins A and B and high pressure. Food Control. 2009; 20 (2): 179-84.
Kouakou P, Ghalfi H, Destain J, Dubois-Dauphin R, Evrard P, Thonart P. Effects of curing sodium nitrite additive and natural meat fat on growth control of Listeria monocytogenes by the bacteriocinproducing Lactobacillus curvatus strain CWBI-B28. Food Microbiol. 2009; 26 (6): 623-8.
Liu L, O’Conner P, Cotter PD, Hill C, Ross RP. Controlling Listeria monocytogenes in Cottage cheese through heterologous production of enterocin a by Lactococcus lactis. J Appl Microbiol. 2008; 104 (4): 1059-66.
Malheiros PdS, Sant’Anna V, Barbosa MdS, Brandelli A, Franco BD. Effect of liposome-encapsulated nisin and bacteriocin-like substance P34 on Listeria monocytogenes growth in Minas frescal cheese. Int J Food Microbiol. 2012; 156 (3): 272-7.
Ragazzo-Sánchez JA, Sánchez-Prado L, Gutiérrez-Martínez P, Luna-Solano G, Gomez-Gil B, CalderonSantoyo M. Inhibition of Salmonella spp. isolated from mango using bacteriocin-like produced by lactobacilli. Inhibición de Salmonella spp aislada de mango usando sustancias tipo bacteriocinas producidas por lactobacilos. CyTA Journal of Food. 2009; 7 (3): 181-7.
Sarika AR, Lipton AP, Aishwarya MS, Dhivya RS. Isolation of a bacteriocin-producing lactococcus lactis and application of its bacteriocin to manage spoilage bacteria in high-value marine fish under different storage temperatures. Appl Biochem Biotechnol. 2012; 167 (5): 1280-9.
Settanni L, Franciosi E, Cavazza A, Cocconcelli PS, Poznanski E. Extension of Tosèla cheese shelf-life using non-starter lactic acid bacteria. Food Microbiol. 2011; 28 (5): 883-90.
Siboukeur A, Siboukeur O. Effect of cameline nisin isolated from Lactococcus lactis sub sp. lactis on Staphylococcus aureus sp. Emirates J Food and Agriculture. 2013; 25 (5): 398-402.
Singh AK, Ramesh A. Succession of dominant and antagonistic lactic acid bacteria in fermented cucumber: Insights from a PCR-based approach. Food Microbiol. 2008; 25 (2): 278-87.
Tahiri I, Desbiens M, Kheadr E, Lacroix C, Fliss I. Comparison of different application strategies of divergicin M35 for inactivation of Listeria monocytogenes in cold-smoked wild salmon. Food Microbiol. 2009; 26 (8): 783-93.
Trias R, Badosa E, Montesinos E, Bañeras L. Bioprotective Leuconostoc strains against Listeria monocytogenes in fresh fruits and vegetables. International Journal of Food Microbiol. 2008; 127 (1-2): 91-8.
Trmčić A, Obermajer T, Majhenič AC, Rogelj I, Matijašić BB. In-situ inhibition of Staphylococcus aureus by lactic acid bacteria consortia from two traditional Slovenian raw milk cheeses. Mljekarstvo 2010; 60 (3): 183-90.
Udhayashree N, Senbagam D, Senthilkumar B, Nithya K, Gurusamy R. Production of bacteriocin and their application in food products. Asian Pacific J Tropical Biomedicine 2012; 2 (1 Supp.): S406-S10.
Vera Pingitore E, Todorov SD, Sesma F, Franco BD. Application of bacteriocinogenic Enterococcus mundtii CRL35 and Enterococcus faecium ST88Ch in the control of Listeria monocytogenes in fresh Minas cheese. Food Microbiol. 2012; 32 (1): 38-47.
Viedma PM, Abriouel H, Omar NB, López RL, Gálvez A. Antistaphylococcal effect of enterocin AS-48 in bakery ingredients of vegetable origin, alone and in combination with selected antimicrobials. J Food Sci. 2009; 74 (7): M384-M9.
Food and Agricultural Organization of the United Nations (FAO), World Health Organization (WHO). Guidelines for the evaluation of probiotics in food. FAo and WHO. [Internet]. Disponible en: ftp://ftp.fao.org/es/esn/food/wgreport2.pdf. Consultado Octubre de 2013.
Lin CM, Zhang L, Doyle MP, Swaminathan B. Comparison of media and sampling locations for isolation of Listeria monocytogenes in queso fresco cheese. J Food Prot. 2006; 69 (9): 2151-6.
Pinto AL, Fernandes M, Pinto C, Albano H, Castilho F, Teixeira P. et al. Characterization of anti-Listeria bacteriocins isolated from shellfish: Potential antimicrobials to control non-fermented seafood. Int J Food Microbiol. 2009; 129 (1): 50-8.
Cho GS, Hanak A, Huch M, Holzapfel WH, Franz C. Investigation into the Potential of Bacteriocinogenic Lactobacillus plantarum BFE 5092 for Biopreservation of Raw Turkey Meat. Probiotics and Antimicro Prot. 2010; 2 (4): 241-9.
Uribe C, Suárez M. Salmonelosis no tifoidea y su transmisión a través de alimentos de origen aviar. Colombia Médica 2006; 37 (2): 151-8.
Méndez I, Badillo C, Ortiz P, Faccini A. Caracterización microbiológica de Salmonella en alimentos de venta callejera en un sector universitario de Bogotá, Colombia. Julio a octubre de 2010. Médicas UIS 2011; 26 (1): 25-32.
Santos J, Gaviria A. Decreto 539 de 2014. Por el cual se expide el reglamento técnico sobre los requisitos sanitarios que deben cumplir los importadores y exportadores de alimentos para el consumo humano, materias primas e insumos para alimentos destinados al consumo humano y se establece el procedimiento para habilitar fábricas de alimentos ubicadas en el exterior. Bogotá D. C.: República de Colombia - Gobierno Nacional; 2014.
Urrego M, Cadavid L. Efecto sobre la calidad microbiológica, sensorial y reológica, de la aplicación de tres diferentes niveles de ácido láctico en un corte de carne de res (Huevo de Solomo). Medellín: Universidad Nacional de Colombia; 2005.
Klaenhammer T, Barranqou R, Buck BL, Azcarate M, Altermann E. Genomic features of lactic acid bacteria efecting bioprocessing and health. FEMS Microbioly Rev. 2005; 29 (3): 393-409.
Vásquez S, Suárez H, Montoya O. Crude bacteriocin extract effect on the microbiological and sensorial characteristics of solomo redondo (Longissimus dorsi) vacuum-packaging. Efecto del extracto crudo de bacteriocinas sobre las características microbiológicas y sensoriales de solomo redondo (Longissimus dorsi) empacado al vacío. Vitae. 2009; 16 (2): 191-200.
Abrams D, Barbosa J, Albano H, Silva J, Gibbs PA, Teixeira P. Characterization of bacPPK34 a bacteriocin produced by Pediococcus pentosaceus strain K34 isolated from “Alheira”. Food Control. 2011; 22 (6): 940-6.
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