Prevalence of bacteria resistant to antibiotics and/or biocides on meat processing plant surfaces throughout meat chain production

International Journal of Food Microbiology

Volumn 161, Issue 2, 2013, Pages 97-106

  Lavilla Lerma, Leyre ^a   Benomar, Nabil ^a   Gálvez, Antonio ^a   Abriouel, Hikmate ^a  

^a UNIVERSITY OF JAÉN   (Spain)

Author keywords

Antibiotic resistance; Biocide resistance; Lactic acid bacteria; Lamb slaughterhouse; Pseudomonas; Psychrotrophs

Indexed keywords

ANTIBIOTIC AGENT; BIOCIDE; CETYLPYRIDINIUM SALT; CIPROFLOXACIN; HEXACHLOROPHENE; QUATERNARY AMMONIUM DERIVATIVE;

ANIMAL EXPERIMENT; ANTIBIOTIC RESISTANCE; ARTICLE; ESCHERICHIA COLI; GOAT; LACTOBACILLUS; LAMB; MEAT INDUSTRY; NONHUMAN; PSEUDOMONAS; SLAUGHTERHOUSE; STAPHYLOCOCCUS;

BACTERIA (MICROORGANISMS); CAPRA HIRCUS; ESCHERICHIA COLI; LACTOBACILLUS SP.; PSEUDOMONAS; PSEUDOMONAS SP.; STAPHYLOCOCCUS SP.;

EID: 84871806427     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2012.11.028     Document Type: Article

References (74)

1. Abriouel H., Lucas R., Ben Omar N., Valdivia E., Maqueda M., Martinez-Cañamero M., Gálvez A. Enterocin AS-48RJ: a variant of enterocin AS-48 chromosomally encoded by Enterococcus faecium RJ16 isolated from food. Systematic and Applied Microbiology 2005, 28:383-397.
2. Ahn Y.T., Lim K.L., Ryu J.C., Kang D.K., Ham J.S., Jang Y.H., Kim H.U. Characterization of Lactobacillus acidophilus isolated from piglets and chicken. Asian- Australasian Journal of Animal Siences 2002, 15:1790-1792.
3. Anthonisen I.-L., Sunde M., Steinum T.M., Sidhu M.S., Sørum H. Organization of the antiseptic resistance gene qacA and Tn552-related b-lactamase genes in multidrug-resistant Staphylococcus haemolyticus strains of animal and human origins. Antimicrobial Agents and Chemotherapy 2002, 46:3606-3612.
4. Atlas R.M., Parks L.C. Handbook of Microbiological Media 1993, CRC Press, Inc., London.
5. Behr H., Reverdy M.E., Mabelat C., Freney J., Fleurette J. Relation entre le niveau des concentrations minimales inhibitrices de cinq antiseptiques et la prèsence du gène qacA. Pathologie et Biologie 1994, 42:438-444.
6. Borck B., Pedersen K. Pulsed-field gel electrophoresis types of Campylobacter spp. in Danish 456 turkeys before and after slaughter. International Journal of Food Microbiology 2005, 101:63-72.
7. Cabo M.L., Herrera J.J., Crespo M.D., Pastoriza L. Comparison among the effectiveness of ozone, nisin and benzalkonium chloride for the elimination of planktonic cells and biofilms of Staphylococcus aureus CECT4459 on polypropylene. Food Control 2009, 20:521-525.
8. Chen Y., Knabel S.J. Multiplex PCR for simultaneous detection of bacteria of the genus Listeria, Listeria monocytogenes, and major serotypes and epidemic clones of L. monocytogenes. Applied and Environmental Microbiology 2007, 73:6299-6304.
9. Chuanchuen R., Beinlich K., Hoang T.T., Becher A., Karkhoff-Schweitzer R.R., Schweizer H.P. Cross-resistance between triclosan and antibiotics in Pseudomonas aeruginosa is mediated by multidrug efflux pumps: exposure of a susceptible mutant strain to triclosan selects for nfxB mutants overexpressing MexCD-OprJ. Antimicrobial Agents and Chemotherapy 2001, 45:428-432.
10. Ciusa M.L., Furi L., Knight D., Decorosi F., Fondi M., Raggi C., Rosado Coelho J., Aragones L., Moce L., Visa P., Freitas A.T., Baldassarri L., Fani R., Viti C., Orefici G., Martinez J.L., Morrissey I., Rinaldo Oggioni M., the BIOHYPO Consortium A novel resistance mechanism to triclosan that suggests horizontal gene transfer and demonstrates a potential selective pressure for reduced biocide susceptibility in clinical strains of Staphylococcus aureus. International Journal of Antimicrobial Agents 2012, 40:210-220.
11. CLSI Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing; Nineteenth Informational Supplement. CLSI Document M100-S19 2009, Clinical and Laboratory Standards Institute, Wayne, Pa.
12. Cosgrove S.E. The relationship between antimicrobial resistance and patient outcomes: mortality, length of hospital stay, and health care costs. Clinical Infectious Diseases 2006, 42:S82e89.
13. Dixon B. Antibiotics as growth promoters: risks and alternatives. ASM News 2000, 66:264-265.
14. Dutka-Malen S., Evers S., Courvalin P. Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant Enterococci by PCR. Journal of Clinical Microbiology 1995, 33:24-27.
15. EFSA Technical guidance prepared by the Panel on Additives and Products or Substances used in Animal Feed (FEEDAP) on the update of the criteria used in the assessment of bacterial resistance to antibiotics of human or veterinary importance. The EFSA Journal 2008, 732:1-15.
16. Ercolini D., Russo F., Nasi A., Ferranti P., Villani F. Mesophilic and psychrotrophic bacteria from meat and their spoilage potential in vitro and in beef. Applied and Environmental Microbiology 2009, 75:1990-2001.
17. Fazlara A., Ekhtelat M. The disinfectant effects of benzalkonium chloride on some important foodborne pathogens. American-Eurasian Journal of Agricultural and Environmental Sciences 2012, 12:23-29.
18. Feinman S.E. Antibiotics in animal feeds-drug resistance revisited. ASM News 1999, 64:24-29.
19. Fraser J.A., Sperber W.H. Rapid detection of Listeria sp. in food and environmental samples by esculin hydrolysis. Journal of Food Protection 1988, 51:762-765.
20. Gilbert P., Allison D.G., McBain A.J. Biofilms in vitro and in vivo: do singular mechanisms imply cross-resistance. Journal of Applied Microbiology 2002, 92:98s-110s.
21. Giolitti C., Cantoni C. A medium for the isolation of staphylococci from foodstuffs. The Journal of Applied Bacteriology 1966, 29:395-398.
22. Guérin-Méchin L., Leveau J.-Y., Dubois-Brissonnet F. Resistance of spheroplasts and whole cells of Pseudomonas aeruginosa to bactericidal activity of various biocides: evidence of the membrane implication. Microbiological Research 2004, 159:51-57.
23. Gutmann L., Williamson R., Moreau N. Cross-resistance to nalidixic acid, trimethoprim, and chloramphenicol associated with alterations in outer membrane proteins of Klebsiella, Enterobacter and Serratia. The Journal of Infectious Diseases 1985, 151:501-507.
24. Heinzel M. Phenomena of biocide resistance in microorganisms. International Biodeterioration and Biodegradation 1998, 41:225-234.
25. Heir E., Sundheim G., Holck A.L. Identification and characterization of quaternary ammonium compound resistant staphylococci from the food industry. International Journal of Food Microbiology 1999, 48:211-219.
26. Hugo W.B. Phenols: a review of their history and development as antimicrobial agents. Microbios 1977, 23:83-85.
27. Hugo W.B. Early studies in the evaluation of disinfectants. The Journal of Antimicrobial Chemotherapy 1978, 4:489-494.
28. Hugo W.B. The mode of action of antiseptics. Handbüch der Antiseptik 1981, 39-77. VEB Verlag Volk und Gesundheit, Berlin. W. Weuffen, A. Kramer, D. Gröschel, G. Berencsi, E. Bulka (Eds.).
29. Hugo W.B. A brief history of heat and chemical preservation and disinfection. The Journal of Applied Bacteriology 1991, 71:9-18.
30. Jensen L.B., Ahrens P., Dons L., Jones R.N., Hammerum A.M., Møller Aarestrup F. Molecular analysis of Tn1546 in Enterococcus faecium isolated from animals and humans. Journal of Clinical Microbiology 1998, 36:437-442.
31. Jeong J.H., Shin K.S., Lee J.W., Park E.J., Son S.Y. Analysis of a novel class 1 integron containing metallo-lactamase gene VIM-2 in Pseudomonas aeruginosa. Journal of Microbiology 2009, 47:753-759.
32. King E.O., Ward M.K., Raney D.E. Media for the demonstration of pyocyanin and fluorescein. The Journal of Laboratory and Clinical Medicine 1954, 44:301-307.
33. K̃ljalg S., Naaber P., Mikelsaar M. Antibiotic resistance as an indicator of bacterial chlorhexidine susceptibility. The Journal of Hospital Infection 2002, 51:106-113.
34. Kraft A.A. Psychrotrophic Bacteria in Foods: Disease and Spoilage 1992, CRC Press, Inc., Boca Raton, Fla.
35. Levy S.B. Antibiotic resistance: an ecological imbalance. Ciba Foundation Symposium 1997, 207:1-9.
36. Levy S.B. The challenge of antibiotic resistance. Scientific American 1998, 278:22-39.
37. Levy S.B. Active efflux, a common mechanism for biocide and antibiotic resistance. Journal of Applied Microbiology 2002, 92:65s-71s.
38. Ma D., Cook D.N., Hearst J.E., Nikaido H. Efflux pumps and drug resistance in gram-negative bacteria. Trends in Microbiology 1994, 2:489-493.
39. Magee J.T., Pritchard E.L., Fitzgerald K.A., Dunstan F.D.J., Howard A.J. Antibiotic prescribing and antibiotic resistance in community practice: retrospective study, 1996-8. British Medical Journal 1999, 319:1239-1240.
40. Marcos J.Y., Soriano A.C., Salazar M.S., Moral C.H., Ramos S.S., Smeltzer M.S., Carrasco G.N. Rapid identification and typing of Staphylococcus aureus by PCR-restriction fragment length polymorphism analysis of the aroA gene. Journal of Clinical Microbiology 1999, 37:570-574.
41. Mayer S., Boos M., Beyer A., Fluit A.C., Schmitz F.-J. Distribution of the antiseptic resistance genes qacA, qacB and qacC in 497 methicillin-resistant European isolates of Staphylococcus aureus. The Journal of Antimicrobial Chemotherapy 2001, 47:896-897.
42. McCallum N., Berger-Bächi B., Senn M.M. Regulation of antibiotic resistance in Staphylococcus aureus. International Journal of Medical Microbiology 2010, 300:118-129.
43. Meyer E., Lunke C., Kist M., Schwab F., Frank U. Antimicrobial resistance in Escherichia coli strains isolated from food, animals and humans in Germany. Infection 2008, 36:59-61.
44. Miles T.D., McLaughlin W., Brown P.D. Antimicrobial resistance of Escherichia coli isolates from broiler chickens and humans. BMC Veterinary Research 2006, 2:7.
45. Morot-Bizot S.C., Talon R., Leroy S. Development of a multiplex PCR for the identification of Staphylococcus genus and four staphylococcal species isolated from food. Journal of Applied Microbiology 2004, 97:1087-1094.
46. Munsch-Alatossava P., Alatossava T. Antibiotic resistance of raw milk associated psychrotrophic bacteria. Microbiological Research 2007, 162:115-123.
47. Padungtod P., Kaneene J.B., Hanson R., Morita Y., Boonmar S. Antimicrobial resistance in Campylobacter isolated from food animals and humans in northern Thailand. FEMS Immunology and Medical Microbiology 2006, 47:217-225.
48. Peyrat M.B., Soumet C., Maris P., Sanders P. Phenotypes and genotypes of campylobacter strains isolated after cleaning and disinfection in poultry slaughterhouses. Veterinary Microbiology 2008, 128:313-326.
49. Reverdy M.E. Les ammonium quaternaires. Antisepsie et Désinfection 1995, 174-198. Editions ESKA, Paris. J. Fleurette, J. Freney, M.E. Reverdy (Eds.).
50. Reynolds J.E.F. Martindale: The Extra Pharmacopoeia. The Royal Pharmaceutical Society of Great Britain, London 1996, 1124-1126. 31th ed.
51. Romanova N.A., Gawande P.V., Brovko L.Y., Griffiths M.W. Rapid methods to assess sanitizing efficacy of benzalkonium chloride to Listeria monocytogenes biofilms. Journal of Microbiological Methods 2007, 71:231-237.
52. Russell A.D. Do biocides select for antibiotic resistant bacteria?. The Journal of Pharmacy and Pharmacology 2000, 52:227-233.
53. Russell A.D. Introduction of biocides into clinical practice and the impact on antibiotic-resistant bacteria. Journal of Applied Microbiology 2002, 92:121s-135s.
54. Russell A.D., Chopra I. Understanding Antibacterial Action and Resistance 1996, 28-206. Ellis Horwood, Hertfordshire. 2nd ed.
55. Russell A.D., McDonnell G. Concentration: a major factor in studying biocidal action. The Journal of Hospital Infection 2000, 44:1-3.
56. Russell A.D., Tattawasart U., Mailard J.-Y., Furr J.R. Possible link between bacterial resistance and use of antibiotics and biocides. Antimicrobial Agents and Chemotherapy 1998, 42:2151.
57. Safdar N., Maki D.G. The commonality of risk factors for nosocomial colonization and infection with antimicrobial-resistant Staphylococcus aureus, Enterococcus, gram-negative bacilli, Clostridium difficile, and Candida. Annals of Internal Medicine 2002, 136:834-844.
58. Sathish S., Swaminathan K. Veterinary anaerobes & diseases molecular characterization of the diversity of Clostridium chauvoei isolates collected from two bovine slaughterhouses: analysis of cross-contamination. Anaerobe 2008, 14:190-199.
59. SCAN Report of the Scientific Committee for Animal Nutrition (SCAN) on the possible risk for humans on the use of avoparcin as feed additive. Opinion expressed 21 May 1996 1996, Office for EC Publications, Luxemburg.
60. SCAN Opinion of the Scientific Committee for Animal Nutrition (SCAN) on the immediate and long-term risk to the value of streptogramins in human medicine posed by the use of virginiamycin as an animal growth promoter 1998, Office for EC Publications, Luxemburg, (10 July 1998).
61. Seidavi A., Mirhosseini Seyed Ziaeddin, Shivazad M., Chamani M., Asghar Sadeghi A., Pourseify R. Detection and investigation of Escherichia coli in contents of duodenum, jejunum, ileum and cecum of broilers at different ages by PCR. Asia-Pacific Journal of Molecular Biology and Biotechnology 2010, 18:321-326.
62. Sidhu M.S., Langsrud S., Holck A. Disinfectant and antibiotic resistance of lactic acid bacteria isolated from the food industry. Microbial Drug Resistance 2001, 7:73-83.
63. Sidhu M.S., Heir E., Leegaard T., Wiger K., Holck A. Frequency of disinfectant resistance genes and genetic linkage with beta-lactamase transposon Tn552 among clinical staphylococci. Antimicrobial Agents and Chemotherapy 2002, 46:2797-2803.
64. Singh A.K., Ramesh A. Succession of dominant and antagonistic lactic acid bacteria in fermented cucumber: insights from a PCR-based approach. Food Microbiology 2008, 25:278-287.
65. Sundheim G., Hagtvedt T., Dainty R. Resistance of meat associated staphylococci to a quarternary ammonium compound. Food Microbiology 1992, 9:161-167.
66. Szita G., Biró G. A new synthetic, selective, liquid medium for determination of coliform bacteria. Acta Veterinaria Hungarica 1986, 34:145-149.
67. Teuber M. Spread of antibiotic resistance with food-borne pathogens. Cellular and Molecular Life Sciences 1999, 56:755-763.
68. Thomas L., Maillard J.-Y., Lambert R.J.W., Russell A.D. Development of resistance to chlorhexidine diacetate in Pseudomonas aeruginosa and the effect of a 'residual' concentration. The Journal of Hospital Infection 2000, 46:297-303.
69. Threlfall E.J., Ward L.R., Frost J.A., Willshaw G.A. The emergence and spread of antibiotic resistance in food-borne bacteria. International Journal of Food Microbiology 2000, 62:1-5.
70. Threlfall E.J., Teale C.J., Davies R.H., Ward L.R., Skinner J.A., Graham A., Cassar C., Speed K. A comparison of antimicrobial susceptibilities in nontyphoidal salmonellas from humans and food animals in England and Wales in 2000. Microbial Drug Resistance 2003, 9:183-189.
71. Van de Weyer A., Devleeschouwer M.J., Dony J. Bactericidal activity of disinfectants on Listeria. The Journal of Applied Bacteriology 1993, 74:480-483.
72. Weisburg W.G., Barns S.M., Pelletier D.A., Lane D.J. 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology 1991, 173:697-703.
73. White D.G., Zhao S., Simjee S., Wagner D.D., McDermott P.F. Antimicrobial resistance of foodborne pathogens. Microbes and Infection 2002, 4:405-412.
74. Yadav J.S., Khan I.U.H., Fakhari F., Soellner M.B. DNA-based methodologies for rapid detection, quantification, and species- or strain-level identification of respiratory pathogens (Mycobacteria and Pseudomonads) in metalworking fluids. Applied Occupational and Environmental Hygiene 2003, 18:966-975.