Evrim Gunes Altuntas, Deniz Kocan, Serap Cosansu, Kamuran Ayhan, Vijay K. Juneja, Luis Materon
Agricultural Research Service, United States Department of Agriculture (USDA), Eastern Regional Research Center, Microbial Food Safety Research Unit, Wyndmoor, USA;.
Biology Department, University of Texas Pan American, Edinburg, USA..
Food Engineering Department, Engineering Faculty, Ankara University, Ankara, Turkey;.
Food Engineering Department, Engineering Faculty, Sakarya University, Sakarya, Turkey;.
Food Technology Department, Guzelyurt Vocational School, Aksaray University, Guzelyurt, Turkey;.
DOI: 10.4236/fns.2012.33052   PDF    HTML     8,377 Downloads   15,424 Views   Citations

Abstract

This study aimed to determine the antibiotic and bacteriocin sensitivity of Listeria monocytogenes strains isolated from animal derived foods. With disc diffusion assay, all fourteen L. monocytogenes strains were suscepti-ble to the antibiotics, including penicillin G, vancomycin, tetracycline, chloramphenicol, rifampicin, erythromycin, gentamicin and trime- thoprim. However, the percentages of fosfomycin and streptomycin resistances were 92.9% and 7.1%, respectively. Multiple resistances were not observed among the tested strains. The results of well diffusion assays showed that all strains were inhibited by the cell-free supernatant of a bacteriocin-producing strain, Pediococcus acidilactici 13, with the inhibition zones ranging from 16.00 to 24.50 mm. These results provide useful information on antibiotic resistance of L. monocytogenes strains isolated from foods, and can potentially be used to develop bacteriocin-based interventions to guard against the hazards associated with L. monocytogenes in ready-to-eat meat and poultry products.

Keywords

Listeria; Antibiotic; Bacteriocin

Share and Cite:

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	M. W. Griffiths, “Listeria: Properties and Occurrence,” In: B. Caballero, L. Trugo and P. M. Finglas, Eds., Encyclopedia of Food Science, Food Technology and Nutrition, 2nd Edition, London Academic Press, London, 2003, pp. 3562-3573. doi:10.1016/B0-12-227055-X/00707-0
[2]	V. K. Juneja, “Predictive Model for the Combined Effect of Temperature, Sodium Lactate and Sodium Diacetate on the Heat Resistance of Listeria monocytogenes in Beef,” Journal of Food Protection, Vol. 66, No. 5, 2003, pp. 804-811.
[3]	S. A. Al-Zeyara, B. Jarvis and B. M. Mackey, “The Inhibitory Effect of Natural Microflora of Food on Growth of Listeria monocytogenes in Enrichment Broths,” International Journal of Food Microbiology, Vol. 145, No. 1, 2011, pp. 98-105. doi:10.1016/j.ijfoodmicro.2010.11.036
[4]	B. Y. Chen, R. Pyla, T. J. Kim, J. L. Silva and Y. S. Jung, “Antibiotic Resistance in Listeria Species Isolated from Catfish Fillets and Processing Environment,” Letters in Applied Microbiology, Vol. 50, No. 6, 2010, pp. 626-632. doi:10.1111/j.1472-765X.2010.02843.x
[5]	U. T. ?ireli and A. Gücüko?lu, “Prevalence and Antibiotic Resistance of Listeria spp. Isolated from Ready-toEat Foods in Ankara,” Turkish Journal of Veterinary and Animal Science, Vol. 32, No. 2, 2008, pp. 131-135.
[6]	L. O’Connor, M. O’Leary, N. Leonard, M. Godinho, C. O’Reilly, L. Coffey, J. Egan and R. O’Mahony, “The Characterization of Listeria spp. Isolated from Food Products and the Food-Processing Environment,” Letters in Applied Microbiology, Vol. 51, No. 5, 2010, pp. 490498. doi:10.1111/j.1472-765X.2010.02928.x
[7]	G. Pesavento, B. Ducci, D. Nieri, N. Comodo and A. Lo Nostro, “Prevalence and Antibiotic Susceptibility of Listeria spp. Isolated from Raw Meat and Retail Foods,” Food Control, Vol. 21, No. 5, 2010, pp. 708-713. doi:10.1016/j.foodcont.2009.10.012
[8]	O. A. Byelashov, H. Daskalov, I. Geornaras, P. A. Kendall, K. E. Belk, J. A. Scanga, G. C. Smith and J. N. Sofos, “Reduction of Listeria monocytogenes on Frankfurters Treated with Lactic Acid Solutions of Various Temperatures,” Food Microbiology, Vol. 27, No. 6, 2010, pp. 783-790. doi:10.1016/j.fm.2010.04.003
[9]	T. M. Osaili, A. R. Alaboudi and E. A. Nesiar, “Prevalence of Listeria spp. and Antibiotic Susceptibility of Listeria monocytogenes Isolated from Raw Chicken and Ready-to-Eat Chicken Products in Jordan,” Food Control, Vol. 22, No. 3-4, 2011, pp. 586-590. doi:10.1016/j.foodcont.2010.10.008
[10]	J. N. Sofos and I. Geornaras, “Overview of Current Meat Hygiene and Safety Risks and Summary of Recent Studies on Biofilms, and Control of Escherichia coli O157:H7 in Nonintact, and Listeria monocytogenes in Ready-to-Eat, Meat Products,” Meat Science, Vol. 86, No. 1, 2010, pp. 2-14. doi:10.1016/j.meatsci.2010.04.015
[11]	A. Sobrino-Lopez and O. Martin-Belloso, “Use of Nisin and Other Bacteriocins for Preservation of Dairy Products,” International Dairy Journal, Vol. 18, No. 4, 2008, pp. 329-343. doi:10.1016/j.idairyj.2007.11.009
[12]	L. H. Deegan, P. D. Cotter, C. Hill and P. Ross, “Bacteriocins: Biological Tools for Bio-Preservation and Shelflife Extension,” International Dairy Journal, Vol. 16, 2006, pp. 1058-1071. doi:10.1016/j.idairyj.2005.10.026
[13]	E. G. Altuntas, S. Cosansu and K. Ayhan, “Some Growth Parameters and Antimicrobial Activity of a Bacteriocin Producing Strain Pediococcus sp 13,” International Journal of Food Microbiology, Vol. 141, No. 1, 2010, pp. 28-31. doi:10.1016/j.ijfoodmicro.2010.04.024
[14]	A. H. ?on, H. Y. G?kalp and M. Kaya, “Antagonistic Effect on Listeria monocytogenes and L. innocua of a Bacteriocin-Like Metabolite Produced by Lactic Acid Bacteria Isolated from Sucuk,” Meat Science, Vol. 59, No. 4, 2001, pp. 437-441. doi:10.1016/S0309-1740(01)00099-7
[15]	S. Cosansu, I. Geornaras, K. Ayhan and J. N. Sofos, “Control of Listeria monocytogenes by a Bacteriocin-Like Metabolite Producing Pediococcus Strain in a Dry Fermented Sausage ‘Sucuk’ and on a Non-Fermented Product ‘Turkey Breast’,” Journal of Food and Nutrition Research, Vol. 49, No. 4, 2010, pp. 206-214.
[16]	M. Zhu, M. Du, J. Cordray and D. U. Ahn, “Control of Listeria monocytogenes Contamination in Ready-to-Eat Meat Products,” Comprehensive Reviews in Food Science and Food Safety, Vol. 4, 2005, pp. 34-42. doi:10.1111/j.1541-4337.2005.tb00071.x
[17]	E. Charpentieer and P. Courvalin, “Antibiotic Resistance in Listeria spp.,” Antimicrobial Agents and Chemotherapy, Vol. 43, No. 9, 1999, pp. 2103-2108.
[18]	S. P. Oliver, S. E. Murinda and B. M. Jayarao, “Impact of Antibiotic Use in Adult Dairy Cows on Antimicrobial Resistance of Veterinary and Human Pathogens: A Comprehensive Review,” Foodborne Pathogens and Disease, Vol. 8, No. 3, 2011, pp. 337-355. doi:10.1089/fpd.2010.0730
[19]	P. Aureli, A. M. Ferini, V. Mannoni, S. Hodzic, C. Wedell-Weergaarda and B. Olivab, “Susceptibility of Listeria monocytogenes Isolated from Food in Italy to Antibiotics,” International Journal of Food Microbiology, Vol. 83, No. 3, 2003, pp. 325-330. doi:10.1016/S0168-1605(02)00381-1
[20]	S. Bertrand, G. Huys, M. Yde, K. D’Haene, F. Trdy, M. Vrints, J. Swings and J. M. Collard, “Detection and Characterization of tet(M) in Tetracycline-Resistant Listeria Strains from Human and Food-Processing Origins in Belgium and France,” Journal of Medical Microbiology, Vol. 54, No. 12, 2005, pp. 1151-1156. doi:10.1099/jmm.0.46142-0
[21]	D. Walsh, G. Duffy, J. J. Sheridan, I. S. Blair and D. A. McDowell, “Antibiotic Resistance among Listeria, including Listeria monocytogenes, in Retail Foods,” Journal of Applied Microbiology, Vol. 90, No. 4, 2001, pp. 517-522. doi:10.1046/j.1365-2672.2001.01273.x
[22]	M. Conter, D. Paludi, V. D’Orio, A. Vergara and A. Ianieri, “Antimicrobial Susceptibility of Listeria monocytogenes Isolated from Food and Food-Processing Environment,” Annali Della Facolta di Medicina Veterina del Studi di Parma, Vol. 27, 2007, pp. 157-164.
[23]	H. Ennaji, M. Timinouni, M. M. Ennaji, M. Hassar and N. Cohen, “Characterization and Antibiotic Susceptibility of Listeria monocytogenes Isolated from Poultry and Red Meat in Morocco,” Journal of Infection and Drug Resistance, Vol. 1, No. 1, 2008, pp. 45-50.
[24]	I. C. Morobe, C. L. Obi, M. A. Nyila, B. A. Gashe and M. I. Matsheka, “Prevalence, Antimicrobial Resistance Profiles of Listeria monocytogenes from Various Foods in Gaborone, Botswana,” African Journal of Biotechnology, Vol. 8, No. 22, 2009, pp. 6383-6387.
[25]	N. Yücel, S. ??tak and M. ?nder, “Prevalence and Antibiotic Resistance of Listeria Species in Meat Products in Ankara, Turkey,” Food Microbiology, Vol. 22, 2005, pp. 241-245. doi:10.1016/j.fm.2004.03.007
[26]	D. Palumbo, M. Iannaccone, A. Porta and R. Capparelli, “Experimental Antibacterial Therapy with Puroindolines, Lactoferrin and Lysozyme in Listeria monocytogenesInfected Mice,” Microbes and Infection, Vol. 12, No. 7, 2010, pp. 538-545. doi:10.1016/j.micinf.2010.03.010
[27]	H. Yan, S. B. Neogi, Z. Mo, W. Guan, Z. Shen, S. Zhang, L. Li, S. Yamasaki, L. Shi and N. Zhong, “Prevalence and Characterization of Antimicrobial Resistance of Foodborne Listeria monocytogenes Isolates in Hebei Province of Northern China, 2005-2007,” International Journal of Food Microbiology, Vol. 144, No. 2, 2010, pp. 310-316. doi:10.1016/j.ijfoodmicro.2010.10.015
[28]	ISO 11290-1, “Microbiology of Food and Animal Feeding Stuffs—Horizontal Method for the Detection and Enumeration of Listeria monocytogenes, Part 1: Detection Method?Amendment 1: Modification of the Isolation Media and the Haemolysis Test, and Inclusion of Precision Data. Brussels: European Committee for Standardization (EN ISO 11290-1:1996?Am1:2004),” 2004.
[29]	D. Ko?an, “Minimum Inhibition Concentration for Determining of Listeria monocytogenes,” PhD Dissertation, Ankara University Graduate School of Natural and Applied Sciences, Ankara, Turkey, 2007.
[30]	S. Cosansu, H. Kuleasan, K. Ayhan and L. Materon, ”Antimicrobial Activity and Protein Profiles of Pediococcus spp. Isolated from Turkish Sucuk,” Journal of Food Processing and Preservation, Vol. 31, No. 2, 2007, pp. 190-200. doi:10.1111/j.1745-4549.2007.00122.x
[31]	M. A. Wikler, “Performance Standards for Antimicrobial Susceptibility Testing, Sixteenth Informational Supplement, M100-S16,” Clinical and Laboratory Standards Institute (CLSI), Vol. 26, No. 3, 2006, Pennsylvania.
[32]	U. Schillinger and F. K. Lücke, “Identification of Lactobacilli from Meat and Meat Products,” Food Microbiology, Vol. 4, No. 3, 1987, pp. 199-208. doi:10.1016/0740-0020(87)90002-5
[33]	H. Hof, “Therapeutic Options,” FEMS Immunology and Medical Microbiology, Vol. 35, No. 3, 2003, pp. 203-205. doi:10.1016/S0928-8244(02)00466-2
[34]	R. Troxler, A. Von Graevenitz, G. Funke, B. Wiedemann and I. Stock, “Natural Antibiotic Susceptibility of Listeria Species: L. grayi, L. innocua, L. ivanovii, L. monocytogenes, L. seeligeri and L. welshimeri Strains,” Clinical Microbiology and Infection, Vol. 6, No. 10, 2000, pp. 525-535. doi:10.1046/j.1469-0691.2000.00168.x
[35]	M. Conter, D. Paludi, E. Zanardi, S. Ghidini, A. Vergara and A. Ianieri, “Characterization of Antimicrobial Resistance of Foodborne Listeria monocytogenes,” International Journal of Food Microbiology, Vol. 128, No. 3, 2009, pp. 497-500. doi:10.1016/j.ijfoodmicro.2008.10.018
[36]	O. R. Rodas-Suárez, J. F. Flores-Pedroche, J. M. Betancourt-Rule, E. I. Qui?ones-Ramírez and C. VázquezSalinas, “Occurrence and Antibiotic Sensitivity of Listeria monocytogenes Strains Isolated from Oysters, Fish, and Estuarine Water,” Applied and Environmental Microbiology, Vol. 72, No. 11, 2006, pp. 7410-7412. doi:10.1128/AEM.00956-06
[37]	A. Galvez, R. L. Lopez and H. Abriouel, “Application of Bacteriocins in the Control of Foodborne Pathogenic and Spoilage Bacteria,” Critical Reviews in Biotechnology, Vol. 28, No. 2, 2008, pp. 125-152. doi:10.1080/07388550802107202
[38]	L. Settani and A. Corsetti, “Application of Bacteriocins in Vegetable Food Biopreservation,” International Journal of Food Microbiology, Vol. 121, No. 2, 2008, pp. 123138. doi:10.1016/j.ijfoodmicro.2007.09.001
[39]	D. Bizani, J. A. C. Morrissy, A. P. M. Dominguez and A. Brandelli, “Inhibition of Listeria monocytogenes in Dairy Products Using the Bacteriocin-Like Peptide Cerein 8A,” International Journal of Food Microbiology, Vol. 121, No. 2, 2008, pp. 229-233. doi:10.1016/j.ijfoodmicro.2007.11.016
[40]	J. W. Nielsen, J. S. Dickson and J. D. Crouse, “Use of a Bacteriocin Produced by Pediococcus acidilactici to Inhibit Listeria monocytogenes Associated with Fresh Meat,” Applied and Environmental Microbiology, Vol. 56, 1990, pp. 2142-2145.
[41]	J. C. Nieto-Lozano, J. I. Reguera-Useros, M. C. PelaezMartinez and A. H. de la Torre, “Effect of a Bacteriocin Produced by Pediococcus acidilactici against Listeria monocytogenes and Clostridium perfringens on Spanish Raw Meat,” Meat Science, Vol. 72, 2006, pp. 57-61. doi:10.1016/j.meatsci.2005.06.004
[42]	V. Vadyvaloo, S. Arous, A. Gravesen, Y. Héchard, R. Chauhan-Haubrock, J. W. Hastings and M. Rautenbach, “Cell-Surface Alterations in Class IIa Bacteriocin-Resistant Listeria monocytogenes Strains,” Microbiology, Vol. 150, No. 9, 2004, pp. 3025-3033. doi:10.1099/mic.0.27059-0
[43]	A. Gravesen, M. Ramnath, K. B. Rechinger, N. Andersen, L. J?nsch, Y. Héchard, J. W. Hastings and S. Kn?chel, “High-Level Resistance to Class IIa Bacteriocins Is Associated with One General Mechanism in Listeria monocytogenes,” Microbiology, Vol. 148, No. 8, 2002, pp. 2361-2369.
[44]	I. M. Barmpalia-Davis, I. Geornaras, P. A. Kendall and J. N. Sofos, “Differences in Survival among 13 Listeria monocytogenes Strains in a Dynamic Model of the Stomach and Small Intestine,” Applied Environmental Microbiology, Vol. 74, No. 17, 2008, pp. 5563-5567. doi:10.1128/AEM.00319-08