Antimicrobial activity of lactic acid bacteria in dairy products and gut: Effect on pathogens

BioMed Research International

Volumn 2015, Issue , 2015, Pages

  Arqués, Juan L ^a   Rodríguez, Eva ^a   Langa, Susana ^a   Landete, José María ^a   Medina, Margarita ^a  

^a INIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AS 48; BACTERIOCIN; NISIN; PEDIOCIN; PROBIOTIC AGENT; ANTIINFECTIVE AGENT; LACTIC ACID;

ANTIMICROBIAL ACTIVITY; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIUM CONTAMINATION; BACTERIUM CULTURE; DAIRY PRODUCT; HIGH THROUGHPUT SEQUENCING; HUMAN; INFECTION PREVENTION; INTESTINE FLORA; LACTIC ACID BACTERIUM; NONHUMAN; REVIEW; ANIMAL; FOOD CONTROL; GASTROINTESTINAL TRACT; LACTOBACILLUS; METABOLISM; MICROBIOLOGY;

ANIMALS; ANTI-INFECTIVE AGENTS; DAIRY PRODUCTS; FOOD MICROBIOLOGY; GASTROINTESTINAL TRACT; HUMANS; LACTIC ACID; LACTOBACILLUS; PROBIOTICS;

EID: 84926443393     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2015/584183     Document Type: Review

References (77)

1. C. Farrokh, K. Jordan, F. Auvray et al., "Review of Shiga-toxin-producing Escherichia coli (STEC) and their significance in dairy production," International Journal of Food Microbiology, Vol. 162, no. 2, pp. 190-212, 2013.
2. E. J. Cartwright, K. A. Jackson, S. D. Johnson, L. M. Graves, B. J. Silk, and B. E. Mahon, "Listeriosis outbreaks and associated food vehicles, United States, 1998-2008," Emerging Infectious Diseases, Vol. 19, no. 1, pp. 1-9, 2013.
3. F. Allerberger and M. Wagner, "Listeriosis: a resurgent food-borne infection," Clinical Microbiology and Infection, Vol. 16, no. 1, pp. 16-23, 2010.
4. R. Bennett, "Staphylococcus aureus," in Bad Bug Book. Food-borne Pathogenic Microorganisms and Natural Toxins, K. A. Lampel, S. Al-Khaldi, and S. M. Cahill, Eds., pp. 87-92, US Food and Drug Administration (FDA), Silver Spring, Md, USA, 2nd edition, 2012.
5. E. E. Jackson, E. S. Erten, N. Maddi et al., "Detection and enumeration of four foodborne pathogens in raw commingled silo milk in the United States," Journal of Food Protection, Vol. 75, no. 8, pp. 1382-1393, 2012.
6. M. Cretenet, S. Even, and Y. Le Loir, "Unveiling Staphylococcus aureus enterotoxin production in dairy products: a review of recent advances to face new challenges," Dairy Science & Technology, Vol. 91, no. 2, pp. 127-150, 2011.
7. EFSA, "The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2010," The EFSA Journal, Vol. 10, p. 2597, 2012.
8. D. Gilliss, A. Cronquist, M. Cartter et al., "Vital signs: incidence and trends of infection with pathogens transmitted commonly through food - foodborne diseases active surveillance network, 10 U.S. sites, 1996-2010," Morbidity and Mortality Weekly Report, Vol. 60, no. 22, pp. 749-755, 2011.
9. B. M. Lund and S. J. O'Brien, "The occurrence and prevention of foodborne disease in vulnerable people," Foodborne Pathogens and Disease, Vol. 8, no. 9, pp. 961-973, 2011.
10. S. M. Morgan, M. Galvin, R. P. Ross, and C. Hill, "Evaluation of a spray-dried lacticin 3147 powder for the control of Listeria monocytogenes and Bacillus cereus in a range of food systems," Letters in Applied Microbiology, Vol. 33, no. 5, pp. 387-391, 2001.
11. M. J. Pucci, E. R. Vedamuthu, B. S. Kunka, and P. A. Vandenbergh, "Inhibition of Listeria monocytogenes by using bacteriocin PA-1 produced by Pediococcus acidilactici PAC 1.0," Applied and Environmental Microbiology, Vol. 54, no. 10, pp. 2349-2353, 1988.
12. K. Wan, J. Harmark, B. E. Davidson et al., "Inhibition of Listeria monocytogenes by piscicolin 126 in milk and Camembert cheese manufactured with a thermophilic starter," Journal of Applied Microbiology, Vol. 82, no. 3, pp. 273-280, 1997.
13. M. E. Farías, M. Nuñez De Kairuz, F. Sesma, J. Palacios, A. P. de Ruiz Holgado, and G. Oliver, "Inhibition of Listeria monocytogenes by the bacteriocin enterocin CRL35 during goat cheese making," Milchwissenschaft, Vol. 54, no. 1, pp. 30-32, 1999.
14. S. Maisnier-Patin, S. N. Deschamps, S. R. Tatini, and J. Richard, "Inhibition of Listeria monocytogenes in Cammembert cheese made with a nisin-producing starter," Lait, Vol. 72, pp. 249-263, 1992.
15. E. Rodríguez, J. L. Arqués, P. Gaya, M. Nuñez, and M. Medina, "Control of Listeria monocytogenes by bacteriocins and monitoring of bacteriocin-producing lactic acid bacteria by colony hybridization in semi-hard raw milk cheese," Journal of Dairy Research, Vol. 68, no. 1, pp. 131-137, 2001.
16. O. McAuliffe, C. Hill, and R. P. Ross, "Inhibition of Listeria monocytogenes in cottage cheese manufactured with a lacticin 3147-producing starter culture," Journal of Applied Microbiology, Vol. 86, no. 2, pp. 251-256, 1999.
17. M. Nuñez, J. L. Rodríguez, E. García, P. Gaya, and M. Medina, "Inhibition of Listeria monocytogenes by enterocin 4 during the manufacture and ripening of Manchego cheese," Journal of Applied Microbiology, Vol. 83, no. 6, pp. 671-677, 1997.
18. N. Buyong, J. Kok, and J. B. Luchansky, "Use of a genetically enhanced, pediocin-producing starter culture, Lactococcus lactis subsp. lactis MM217, to control Listeria monocytogenes in Cheddar cheese," Applied and Environmental Microbiology, Vol. 64, no. 12, pp. 4842-4845, 1998.
19. S. Ennahar, O. Assobhei, and C. Hasselmann, "Inhibition of Listeria monocytogenes in a smear-surface soft cheese by Lactobacillus plantarum WHE 92, a pediocin AcH producer," Journal of Food Protection, Vol. 61, no. 2, pp. 186-191, 1998.
20. E. Rodríguez, J. Calzada, J. L. Arqués, J. M. Rodríguez, M. Nuñez, and M. Medina, "Antimicrobial activity of pediocin-producing Lactococcus lactis on Listeria monocytogenes, Staphylococcus aureus and Escherichia coli O157:H7 in cheese," International Dairy Journal, Vol. 15, no. 1, pp. 51-57, 2005.
21. P. D. Cotter, C. Hill, and R. P. Ross, "Bacteriocins: developing innate immunity for food," Nature Reviews Microbiology, Vol. 3, no. 10, pp. 777-788, 2005.
22. E. F. O'Shea, P. D. Cotter, C. Stanton, R. P. Ross, and C. Hill, "Production of bioactive substances by intestinal bacteria as a basis for explaining probiotic mechanisms: bacteriocins and conjugated linoleic acid," International Journal of Food Microbiology, Vol. 152, no. 3, pp. 189-205, 2012.
23. J. Nissen-Meyer, P. Rogne, C. Oppergård, H. S. Haugen, and P. E. Kristiansen, "Structure-function relationships of the non-lanthionine-containing peptide (class II) bacteriocins produced by gram-positive bacteria," Current Pharmaceutical Biotechnology, Vol. 10, no. 1, pp. 19-37, 2009.
24. K. A. Stevens, B. W. Sheldon, N. A. Klapes, and T. R. Klaenhammer, "Nisin treatment for inactivation of Salmonella species and other gram-negative bacteria," Applied and Environmental Microbiology, Vol. 57, no. 12, pp. 3613-3615, 1991.
25. L. H. Deegan, P. D. Cotter, C. Hill, and P. Ross, "Bacteriocins: biological tools for bio-preservation and shelf-life extension," International Dairy Journal, Vol. 16, no. 9, pp. 1058-1071, 2006.
26. A. Sobrino-López and O. Martín-Belloso, "Use of nisin and other bacteriocins for preservation of dairy products," International Dairy Journal, Vol. 18, no. 4, pp. 329-343, 2008.
27. S. Mills, C. Stanton, C. Hill, and R. P. Ross, "New developments and applications of bacteriocins and peptides in foods," Annual Review of Food Science and Technology, Vol. 2, pp. 299-329, 2011.
28. J. Delves-Broughton, P. Blackburn, R. J. Evans, and J. Hugenholtz, "Applications of the bacteriocin, nisin," Antonie van Leeuwenhoek, Vol. 69, no. 2, pp. 193-202, 1996.
29. L. J. Harris, H. P. Flemming, and T. R. Klaenhammer, "Sensitivity and resistance of Listeria monocytogenes ATCC 19115, Scott A and UAL 500 to nisin," Journal of Food Protection, Vol. 54, pp. 836-840, 2001.
30. R.-O. Benech, E. E. Kheadr, R. Laridi, C. Lacroix, and I. Fliss, "Inhibition of Listeria innocua in cheddar cheese by addition of nisin Z in liposomes or by in situ production in mixed culture," Applied and Environmental Microbiology, Vol. 68, no. 8, pp. 3683-3690, 2002.
31. P. D. S. Malheiros, D. J. Daroit, N. P. da Silveira, and A. Brandelli, "Effect of nanovesicle-encapsulated nisin on growth of Listeria monocytogenes in milk," Food Microbiology, Vol. 27, no. 1, pp. 175-178, 2010.
32. A. G. M. Scannell, C. Hill, R. P. Ross, S. Marx, W. Hartmeier, and E. K. Arendt, "Development of bioactive food packaging materials using immobilised bacteriocins lacticin 3147 and nisaplin," International Journal of Food Microbiology, Vol. 60, no. 2-3, pp. 241-249, 2000.
33. L. Cao-Hoang, A. Chaine, L. Grégoire, and Y. Waché, "Potential of nisin-incorporated sodium caseinate films to control Listeria in artificially contaminated cheese," Food Microbiology, Vol. 27, no. 7, pp. 940-944, 2010.
34. M. Bouksaim, C. Lacroix, P. Audet, and R. E. Simard, "Effects of mixed starter composition on nisin Z production by Lactococcus lactis subsp. lactis biovar. diacetylactis UL 719 during production and ripening of Gouda cheese," International Journal of Food Microbiology, Vol. 59, no. 3, pp. 141-156, 2000.
35. B. Martinez, J. E. Suárez, and A. Rodriguez, "Antimicrobials produced by wild lactococcal strains isolated from homemade cheeses," Journal of Food Protection, Vol. 58, no. 10, pp. 1118-1123, 1995.
36. E. Rodríguez, B. González, P. Gaya, M. Nuñez, and M. Medina, "Diversity of bacteriocins produced by lactic acid bacteria isolated from raw milk," International Dairy Journal, Vol. 10, no. 1-2, pp. 7-15, 2000.
37. M. P. Ryan, M. C. Rea, C. Hill, and R. P. Ross, "An application in Cheddar cheese manufacture for a strain of Lactococcus lactis producing a novel broad-spectrum bacteriocin, lacticin 3147," Applied and Environmental Microbiology, Vol. 62, no. 2, pp. 612-619, 1996.
38. B. Dal Bello, L. Cocolin, G. Zeppa, D. Field, P. D. Cotter, and C. Hill, "Technological characterization of bacteriocin producing Lactococcus lactis strains employed to control Listeria monocytogenes in Cottage cheese," International Journal of Food Microbiology, Vol. 153, no. 1-2, pp. 58-65, 2012.
39. C. Reviriego, A. Fernández, N. Horn et al., "Production of pediocin PA-1, and coproduction of nisin a and pediocin PA-1, by wild Lactococcus lactis strains of dairy origin," International Dairy Journal, Vol. 15, no. 1, pp. 45-49, 2005.
40. C. Reviriego, L. Fernández, and J. M. Rodríguez, "A food-grade system for production of pediocin PA-1 in nisin-producing and non-nisin-producing Lactococcus lactis strains: application to inhibit Listeria growth in a cheese model system," Journal of Food Protection, Vol. 70, no. 11, pp. 2512-2517, 2007.
41. S. Mills, L. M. Serrano, C. Griffin et al., "Inhibitory activity of Lactobacillus plantarum LMG P-26358 against Listeria innocua when used as an adjunct starter in the manufacture of cheese," Microbial Cell Factories, Vol. 10, supplement 1, article S7, 2011.
42. J.-C. Ogier and P. Serror, "Safety assessment of dairy microorganisms: the Enterococcus genus," International Journal of Food Microbiology, Vol. 126, no. 3, pp. 291-301, 2008.
43. A. Gálvez, R. Lucas López, H. Abriouel, E. Valdivia, and N. B. Omar, "Application of bacteriocins in the control of food-borne pathogenic and spoilage bacteria," Critical Reviews in Biotechnology, Vol. 28, no. 2, pp. 125-152, 2008.
44. S. M. Morgan, R. P. Ross, T. Beresford, and C. Hill, "Combination of hydrostatic pressure and lacticin 3147 causes increased killing of Staphylococcus and Listeria," Journal of Applied Microbiology, Vol. 88, no. 3, pp. 414-420, 2000.
45. J. L. Arqués, E. Rodríguez, P. Gaya, M. Medina, B. Guamis, and M. Nuñez, "Inactivation of Staphylococcus aureus in raw milk cheese by combinations of high-pressure treatments and bacteriocin-producing lactic acid bacteria," Journal of Applied Microbiology, Vol. 98, no. 2, pp. 254-260, 2005.
46. J. L. Arqués, E. Rodríguez, P. Gaya, M. Medina, and M. Nuñez, "Effect of combinations of high-pressure treatment and bacteriocin-producing lactic acid bacteria on the survival of Listeria monocytogenes in raw milk cheese," International Dairy Journal, Vol. 15, no. 6-9, pp. 893-900, 2005.
47. E. Rodriguez, J. L. Arques, M. Nuñez, P. Gaya, and M. Medina, "Combined effect of high-pressure treatments and bacteriocin-producing lactic acid bacteria on inactivation of Escherichia coli O157:H7 in raw-milk cheese," Applied and Environmental Microbiology, Vol. 71, no. 7, pp. 3399-3404, 2005.
48. J. L. Arqués, J. Fernández, P. Gaya, M. Nuñez, E. Rodríguez, and M. Medina, "Antimicrobial activity of reuterin in combination with nisin against food-borne pathogens," International Journal of Food Microbiology, Vol. 95, no. 2, pp. 225-229, 2004.
49. J. L. Arqués, M. Nuñez, M. Medina, and E. Rodríguez, "Synergistic effect of reuterin in combination with nisin on Staphylococcus aureus in milk," Milchwissenschaft, Vol. 59, no. 7-8, pp. 373-375, 2004.
50. J. L. Arqués, E. Rodríguez, M. Nuñez, and M. Medina, "Inactivation of Gram-negative pathogens in refrigerated milk by reuterin in combination with nisin or the lactoperoxidase system," European Food Research and Technology, Vol. 227, no. 1, pp. 77-82, 2008.
51. FAO/WHO, "Evaluation of health and nutritional properties of powder milk with live lactic acid bacteria," FAO/WHO Expert Consultation, FAO/WHO, Cordoba, Argentina, 2001.
52. A. Dobson, P. D. Cotter, R. P. Ross, and C. Hill, "Bacteriocin production: a probiotic trait?" Applied and Environmental Microbiology, Vol. 78, no. 1, pp. 1-6, 2012.
53. M. C. Rea, D. Alemayehu, R. Paul Ross, and C. Hill, "Gut solutions to a gut problem: bacteriocins, probiotics and bacteriophage for control of Clostridium difficile infection," Journal of Medical Microbiology, Vol. 62, pp. 1369-1378, 2013.
54. R. Hammami, B. Fernandez, C. Lacroix, and I. Fliss, "Anti-infective properties of bacteriocins: an update," Cellular and Molecular Life Sciences, Vol. 70, no. 16, pp. 2947-2967, 2013.
55. P. D. Cotter, R. P. Ross, and C. Hill, "Bacteriocins - a viable alternative to antibiotics?" Nature Reviews Microbiology, Vol. 11, no. 2, pp. 95-105, 2013.
56. C. Piper, P. G. Casey, C. Hill, P. D. Cotter, and R. P. Ross, "The lantibiotic lacticin 3147 prevents systemic spread of Staphylococ-cus aureus in a murine infection model," International Journal of Microbiology, Vol. 2012, Article ID 806230, 6 pages, 2012.
57. A. Campion, P. G. Casey, D. Field, P. D. Cotter, C. Hill, and R. P. Ross, "In vivo activity of nisin A and nisin V against Listeria monocytogenes in mice," BMC Microbiology, Vol. 13, no. 1, article 23, 2013.
58. D. Field, L. Quigley, P. M. O'Connor et al., "Studies with bioengineered nisin peptides highlight the broad-spectrum potency of nisin V," Microbial Biotechnology, Vol. 3, no. 4, pp. 473-486, 2010.
59. M. C. Rea, E. Clayton, P. M. O'Connor et al., "Antimicrobial activity of lacticin 3147 against clinical Clostridium difficile strains," Journal of Medical Microbiology, Vol. 56, no. 7, pp. 940-946, 2007.
60. M. C. Rea, A. Dobson, O. O'Sullivan et al., "Effect of broad- and narrow-spectrum antimicrobials on Clostridium difficile and microbial diversity in a model of the distal colon," Proceedings of the National Academy of Sciences of the United States of America, Vol. 108, supplement 1, pp. 4639-4644, 2011.
61. N. Bernbom, T. R. Licht, C.-H. Brogren et al., "Effects of Lactococcus lactis on composition of intestinal microbiota: role of nisin," Applied and Environmental Microbiology, Vol. 72, no. 1, pp. 239-244, 2006.
62. N. Dabour, A. Zihler, E. Kheadr, C. Lacroix, and I. Fliss, "In vivo on the effectiveness of pediocin PA-1 and Pediococcus acidilactici UL5 at inhibiting Listeria monocytogenes," International Journal of Food Microbiology, Vol. 133, no. 3, pp. 225-233, 2009.
63. N. J. Stern, B. V. Eruslanov, V. D. Pokhilenko et al., "Bacteriocins reduce Campylobacter jejuni colonization while bacteria producing bacteriocins are ineffective," Microbial Ecology in Health and Disease, Vol. 20, no. 2, pp. 74-79, 2008.
64. A. Dobson, F. Crispie, M. C. Rea et al., "Fate and efficacy of lacticin 3147-producing Lactococcus lactis in the mammalian gastrointestinal tract," FEMS Microbiology Ecology, Vol. 76, no. 3, pp. 602-614, 2011.
65. G. E. Gardiner, M. C. Rea, B. O'Riordan et al., "Fate of the two-component lantibiotic lacticin 3147 in the gastrointestinal tract," Applied and Environmental Microbiology, Vol. 73, no. 21, pp. 7103-7109, 2007.
66. M. Millette, G. Cornut, C. Dupont, F. Shareck, D. Archambault, and M. Lacroix, "Capacity of human nisin- and pediocin-producing lactic acid bacteria to reduce intestinal colonization by vancomycin-resistant enterococci," Applied and Environmental Microbiology, Vol. 74, no. 7, pp. 1997-2003, 2008.
67. N. Bernbom, T. R. Licht, P. Saadbye, F. K. Vogensen, and B. Nørrung, "Lactobacillus plantarum inhibits growth of Listeria monocytogenes in an in vitro continuous flow gut model, but promotes invasion of L. monocytogenes in the gut of gnotobiotic rats," International Journal of Food Microbiology, Vol. 108, no. 1, pp. 10-14, 2006.
68. S. C. Corr, Y. Li, C. U. Riedel, P. W. O'Toole, C. Hill, and C. G. M. Gahan, "Bacteriocin production as a mechanism for the anti-infective activity of Lactobacillus salivarius UCC118," Proceedings of the National Academy of Sciences of the United States of America, Vol. 104, no. 18, pp. 7617-7621, 2007.
69. E. Riboulet-Bisson, M. H. J. Sturme, I. B. Jeffery et al., "Effect of Lactobacillus salivarius bacteriocin ABP118 on the mouse and pig intestinal microbiota," PLoS ONE, Vol. 7, no. 2, Article ID e31113, 2012.
70. P. G. Casey, G. E. Gardiner, G. Casey et al., "A five-strain probiotic combination reduces pathogen shedding and alleviates disease signs in pigs challenged with Salmonella enterica serovar Typhimurium," Applied and Environmental Microbiology, Vol. 73, no. 6, pp. 1858-1863, 2007.
71. M. C. Walsh, G. E. Gardiner, O. M. Hart et al., "Predominance of a bacteriocin-producing Lactobacillus salivarius component of a five-strain probiotic in the porcine ileum and effects on host immune phenotype," FEMS Microbiology Ecology, Vol. 64, no. 2, pp. 317-327, 2008.
72. H. M. Timmerman, C. J. M. Koning, L. Mulder, F. M. Rombouts, and A. C. Beynen, "Monostrain, multistrain and multispecies probiotics - a comparison of functionality and efficacy," International Journal of Food Microbiology, Vol. 96, no. 3, pp. 219-233, 2004.
73. C. M. C. Chapman, G. R. Gibson, and I. Rowland, "Health benefits of probiotics: are mixtures more effective than single strains?" European Journal of Nutrition, Vol. 50, no. 1, pp. 1-17, 2011.
74. M. Kleerebezem, L. E. N. Quadri, O. P. Kuipers, and W. M. De Vos, "Quorum sensing by peptide pheromones and two-component signal-transduction systems in Gram-positive bacteria," Molecular Microbiology, Vol. 24, no. 5, pp. 895-904, 1997.
75. R. di Cagno, M. de Angelis, M. Calasso et al., "Quorum sensing in sourdough Lactobacillus plantarum DC400: induction of plantaricin a (PlnA) under co-cultivation with other lactic acid bacteria and effect of PlnA on bacterial and Caco-2 cells," Proteomics, Vol. 10, no. 11, pp. 2175-2190, 2010.
76. M. Calasso, R. D. Cagno, M. D. Angelis, D. Campanella, F. Minervini, and M. Gobbetti, "Effects of the peptide pheromone plantaricin a and cocultivation with Lactobacillus sanfranciscensis DPPMA174 on the exoproteome and the adhesion capacity of Lactobacillus plantarum DC400," Applied and Environmental Microbiology, Vol. 79, no. 8, pp. 2657-2669, 2013.
77. S. van Hemert, M. Meijerink, D. Molenaar et al., "Identification of Lactobacillus plantarum genes modulating the cytokine response of human peripheral blood mononuclear cells," BMC Microbiology, Vol. 10, article 293, 2010.