Inhibition of Salmonella enterica Cells in Deli-Type Salad by Enterocin AS-48 in Combination with Other Antimicrobials

  1. Cobo Molinos, Antonio
  2. Lucas López, Rosario
  3. Abriouel, Hikmate
  4. Ben Omar, Nabil
  5. Valdivia, Eva
  6. Gálvez, Antonio
Revista:
Probiotics and Antimicrobial Proteins

ISSN: 1867-1306 1867-1314

Año de publicación: 2009

Volumen: 1

Número: 1

Páginas: 85-90

Tipo: Artículo

DOI: 10.1007/S12602-009-9005-Z GOOGLE SCHOLAR lock_openAcceso abierto editor

Otras publicaciones en: Probiotics and Antimicrobial Proteins

Resumen

The cyclic antibacterial peptide enterocin AS-48 acted synergistically with p-hydroxybenzoic acid methyl ester (PHBME) and with 2-nitropropanol against Salmonella enterica serovar Enteritidis CECT 4300 in Russian salad. In challenge tests on a cocktail of Salmonella strains (S. enterica ssp. enterica serotype Typhi CECT 409, S. enterica ssp. enterica serovar Choleraesuis CECT 915, S. enterica ssp. enterica serovar Enteritidis CECT 4300, S. enterica ssp. arizonae serovar Arizonae CECT 4395, and S. enterica ssp. salamae CECT 4000) in salad at 10°C, the combinations of PHBME and AS-48 (80 μg/g) or 2-nitropropanol and AS-48 (40 μg/g) reduced the concentrations of viable Salmonella from 4.27 to 4.75 log CFU/g down to the limit of detection for 7 days. Salmonella populations did not increase in control samples (without any antimicrobials or in the presence of AS-48 alone) probably due to the low pH of this type of salad and low temperature of incubation, but retained over 85% viability after 1 week. This work opens new possibilities to expand the spectrum of inhibition of enterocin AS-48 against Salmonella enterica.

Referencias bibliográficas

  • Abriouel H, Valdivia E, Gálvez A, Maqueda M (1998) Response of Salmonella choleraesuis LT2 spheroplasts and permeabilized cells to the bacteriocin AS-48. Appl Environ Microbiol 64:4623–4626
  • Abriouel H, Valdivia E, Martínez-Bueno M, Maqueda M, Gálvez A (2003) A simple method for semi-preparative-scale production and recovery of enterocin AS-48 derived from Enterococcus faecalis subsp. liquefaciens A-48-32. J Microbiol Methods 55:599–605
  • Ananou S, Gálvez A, Martínez-Bueno M, Maqueda M, Valdivia E (2005) Synergistic effect of enterocin AS-48 in combination with outer membrane permeabilizing treatments against Escherichia coli O157:H7. J Appl Microbiol 99:1364–1372
  • Anderson RC, Callaway TR, Van Kessel JS, Jung YS, Edrington TS, Nisbet DJ (2003) Effect of select nitro compounds on ruminal fermentation; an initial look at their potential to reduce economic and environmental costs associated with ruminal methanogenesis. Bioresour Technol 90:59–63
  • Brandl MT (2006) Fitness of human enteric pathogens on plants and implications for food safety. Annu Rev Phytopathol 44:367–392
  • Centers for Disease Control and Prevention (CDC) (2006) Surveillance for foodborne-disease outbreaks—United States, 1998–2002. Morb Mortal Weekly Rep 55(SS10):1–34
  • Centers for Disease Control and Prevention (CDC) (2007) Multistate outbreaks of Salmonella infections associated with raw tomatoes eaten in restaurants—United States, 2005–2006. Morbid Mortal Weekly Rep 56:909–911
  • Cleveland J, Montville TJ, Nes IF, Chikindas ML (2001) Bacteriocins: safe, natural antimicrobials for food preservation. Int J Food Microbiol 71:1–20
  • Cobo Molinos A, Abriouel H, Ben Omar N, Valdivia E, Lucas R, Maqueda M et al (2005) Effect of immersion solutions containing enterocin AS-48 on Listeria monocytogenes in vegetable foods. Appl Environ Microbiol 71:7781–7787
  • Devlieghere F, Vermeiren L, Debevere J (2004) New preservation technologies: possibilities and limitations. Int Dairy J 14:273–285
  • Eucast definitive document E.Def 1.2 (2000) Terminology relating to methods for the determination of susceptibility of bacteria to antimicrobial agents. European Committee for Antimicrobial Susceptibility Testing (EUCAST) of the European Society of Clinical Microbiology and Infectious Diseases (ESCMID). Clin Microbiol Infect Dis 6:503–508
  • Gálvez A, Abriouel H, Lucas López R, Ben Omar N (2007) Bacteriocin-based strategies for food biopreservation. Int J Food Microbiol 120:51–70
  • Grande MJ, Lucas R, Abriouel H, Valdivia E, Ben Omar N, Maqueda M et al (2006) Inhibition of toxicogenic Bacillus cereus in rice-based foods by enterocin AS-48. Int J Food Microbiol 106:185–194
  • Grande MJ, Lucas R, Abriouel H, Valdivia E, Ben Omar N, Maqueda M et al (2007) Treatment of vegetable sauces with enterocin AS-48 alone or in combination with phenolic compounds to inhibit proliferation of Staphylococcus aureus. J Food Prot 70:405–411
  • Grande MJ, Abriouel H, Lucas R, Valdivia E, Ben Omar N, Martínez-Cañamero M et al (2007) Efficacy of enterocin AS-48 against bacilli in ready-to-eat vegetable soups and purees. J Food Prot 70:2339–2345
  • Heaton JC, Jones K (2008) Microbial contamination of fruit and vegetables and the behaviour of enteropathogens in the phyllosphere: a review. J Appl Microbiol 104:613–626
  • Jay JM, Loessner MJ, Golden AA (2005) Modern food microbiology, 7th edn. Aspen Publishers Inc., Gaithersburg
  • Jiménez MS, Velarte R, Castillo JR (2007) Direct determination of phenolic compounds and phospholipids in virgin olive oil by micellar liquid chromatography. Food Chem 100:8–14
  • Jung YS, Anderson RC, Edrington TS, Genovese KJ, Byrd JA, Callaway TR et al (2004) Experimental use of 2-nitropropanol for reduction of Salmonella typhimurium in the ceca of broiler chicks. J Food Prot 67:1945–1947
  • Jung YS, Anderson RC, Callaway TR, Edrington TS, Genovese KJ, Harvey RB et al (2004) Inhibitory activity of 2-nitropropanol against select food-borne pathogens in vitro. Lett Appl Microbiol 39:471–476
  • Lucas R, Grande MJ, Abriouel H, Maqueda M, Ben Omar N, Valdivia E et al (2006) Application of the broad-spectrum bacteriocin enterocin AS-48 to inhibit Bacillus coagulans in low-pH canned fruit and vegetable foods. Food Chem Toxicol 44:1774–1781
  • Majak W, Clark LJ (1980) Metabolism of aliphatic nitrocompounds in bovine rumen fluid. Can J Animal Sci 60:319–325
  • Maqueda M, Gálvez A, Martínez Bueno M, Sánchez-Barrena MJ, González C, Albert A et al (2004) Peptide AS-48: prototype of a new class of cyclic bacteriocins. Curr Protein Pept Sci 5:399–416
  • Martinez-Bueno M, Galvez A, Valdivia E, Maqueda M (1990) A transferable plasmid associated with AS-48 production in Enterococcus faecalis. J Bacteriol 172:2817–2818
  • Mokhtari A, Moore CM, Yang H, Jaykus LA, Morales R, Cates SC et al (2006) Consumer-phase Salmonella enterica serovar Enteritidis risk assessment for egg-containing food products. Risk Anal 26:753–768
  • Muñoz A, Maqueda M, Gálvez A, Martínez-Bueno M, Rodriguez A, Valdivia E (2004) Biocontrol of psychrotrophic enterotoxigenic Bacillus cereus in a non fat hard type cheese by an enterococcal strain-producing enterocin AS-48. J Food Prot 67:1517–1521
  • Muñoz A, Ananou S, Gálvez A, Martínez-Bueno M, Rodríguez A, Maqueda M et al (2007) Inhibition of Staphylococcus aureus in dairy products by enterocin AS-48 produced in situ and ex situ: bactericidal synergism through heat and AS-48. Int Dairy J 17:760–769
  • Pakalniskiene J, Falkenhorst G, Lisby M, Madsen SB, Olsen KE, Nielsen EM et al (2008) A foodborne outbreak of enterotoxigenic E. coli and Salmonella Anatum infection after a high-school dinner in Denmark, November 2006. Epidemiol Infect 6:1–6
  • Smittle RB (2000) Microbiological safety of mayonnaise, salad dressings, and sauces produced in the United States: a review. J Food Prot 63:1144–1153
  • Unicomb L, Bird P, Dalton C (2003) Outbreak of Salmonella Potsdam associated with salad dressing at a restaurant. Commun Dis Intell 27:508–512