Biocide and antibiotic susceptibility of Salmonella isolates obtained before and after cleaning at six Danish pig slaughterhouses

International Journal of Food Microbiology

Volumn 181, Issue , 2014, Pages 53-59

  Gantzhorn, Mette Rørbæk ^a   Pedersen, Karl ^b   Olsen, John Elmerdahl ^a   Thomsen, Line Elnif ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

Antibiotic; Biocide; Prevalence; Resistance; Salmonella; Slaughterhouse

Indexed keywords

AMIKACIN; ANTIBIOTIC AGENT; AZTREONAM; BIOCIDE; CEFEPIME; CEFOTAXIME; CEFTAZIDIME; CIPROFLOXACIN; COLISTIN; COTRIMOXAZOLE; DISINFECTANT AGENT; DORIPENEM; DOXYCYCLINE; ERTAPENEM; GENTAMICIN; IMIPENEM; LEVOFLOXACIN; MEROPENEM; MINOCYCLINE; PIPERACILLIN PLUS TAZOBACTAM; POLYMYXIN B; TIGECYCLINE; TIMENTIN; TOBRAMYCIN; TRICLOSAN;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIUM ISOLATE; CLEANING; DENMARK; DISINFECTION; FOOD INDUSTRY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PORK; PREVALENCE; SALMONELLA; SEROTYPING; SLAUGHTERHOUSE;

ANTIBIOTIC; BIOCIDE; PREVALENCE; RESISTANCE; SALMONELLA; SLAUGHTERHOUSE;

ABATTOIRS; ANTI-BACTERIAL AGENTS; DENMARK; DISINFECTANTS; DISINFECTION; DRUG RESISTANCE; ENVIRONMENTAL MICROBIOLOGY; GENES, BACTERIAL; MICROBIAL SENSITIVITY TESTS; SALMONELLA; SEROTYPING;

EID: 84899914097     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2014.04.021     Document Type: Article

References (41)

1. Aarestrup F.M., Hasman H. Susceptibility of different bacterial species isolated from food animals to copper sulphate, zinc chloride and antimicrobial substances used for disinfection. Vet. Microbiol. 2004, 100:83-89.
2. Aarestrup F.M., Knöchel S., Hasman H. Antimicrobial susceptibility of Listeria monocytogenes from food products. Foodborne Pathog. Dis. 2007, 4:216-221.
3. Alonso-Hernando A., Capita R., Prieto M., Alonso-Calleja C. Comparison of antibiotic resistance patterns in Listeria monocytogenes and Salmonella enterica strains pre-exposed and exposed to poultry decontaminants. Food Control 2009, 20:1108-1111.
4. Anonymous Annual Report on Zoonoses in Denmark 2011 2012, National Food Institute, Technical University of Denmark, Søborg, Denmark.
5. Anonymous Nøgletal - Danish Crown (Retrieved 2013-09-18, 2013, from). http://www.danishcrown.dk/Om-os/Noegletal.aspx.
6. Arguello H., Álvarez-Ordoñez A., Carvajal A., Rubio P., Prieto M. Role of slaughtering in Salmonella spreading and control in pork production. J. Food Prot. 2013, 76:899-911.
7. Arguello H., Sorensen G., Carvajal A., Baggesen D.L., Rubio P., Pedersen K. Prevalence, serotypes and resistance patterns of Salmonella in Danish pig production. Res. Vet. Sci. 2013, 95:334-342.
8. Bailey A.M., Constantinidou C., Ivens A., Garvey M.I., Webber M.A., Coldham N., Hobman J.L., Wain J., Woodward M.J., Piddock L.J.V. Exposure of Escherichia coli and Salmonella enterica serovar Typhimurium to triclosan induces a species-specific response, including drug detoxification. J. Antimicrob. Chemother. 2009, 64:973-985.
9. Bates D., Maechler M., Bolker B., Walker S. lme4: Linear Mixed-Effects Models using Eigen and S4 1.0-4 Ed 2013.
10. Beier R.C., Anderson P.N., Hume M.E., Poole T.L., Duke S.E., Crippen T.L., Sheffield C.L., Caldwell D.J., Byrd J.A., Anderson R.C., Nisbet D.J. Characterization of Salmonella enterica isolates from turkeys in commercial processing plants for resistance to antibiotics, disinfectants, and a growth promoter. Foodborne Pathog. Dis. 2011, 8:593-600.
11. Birošová L., Mikulášová M. Development of triclosan and antibiotic resistance in Salmonella enterica serovar Typhimurium. J. Med. Microbiol. 2009, 58:436-441.
12. Botteldoorn N., Heyndrickx M., Rijpens N., Grijspeerdt K., Herman L. Salmonella on pig carcasses: positive pigs and cross contamination in the slaughterhouse. J. Appl. Microbiol. 2003, 95:891-903.
13. Braoudaki M., Hilton A.C. Adaptive resistance to biocides in Salmonella enterica and Escherichia coli O157 and cross-resistance to antimicrobial agents. J. Clin. Microbiol. 2004, 42:73-78.
14. Christensen E.G., Gram L., Kastbjerg V.G. Sublethal triclosan exposure decreases susceptibility to gentamicin and other aminoglycosides in Listeria monocytogenes. Antimicrob. Agents Chemother. 2011, 55:4064-4071.
15. Chuanchuen R., Pathanasophon P., Khemtong S., Wannaprasat W., Padungtod P. Susceptibilities to antimicrobials and disinfectants in Salmonella isolates obtained from poultry and swine in Thailand. J. Vet. Sci. 2008, 70:595-601.
16. Condell O., Iversen C., Cooney S., Power K.A., Walsh C., Burgess C., Fanning S. Efficacy of biocides used in the modern food industry to control Salmonella enterica, and links between biocide tolerance and resistance to clinically relevant antimicrobial compounds. Appl. Environ. Microbiol. 2012, 78:3087-3097.
17. Copitch J.L., Whitehead R.N., Webber M.A. Prevalence of decreased susceptibility to triclosan in Salmonella enterica isolates from animals and humans and association with multiple drug resistance. Int. J. Antimicrob. Agents 2010, 36:247-251.
18. Cottell A., Denyer S.P., Hanlon G.W., Ochs D., Maillard J.-Y. Triclosan-tolerant bacteria: changes in susceptibility to antibiotics. J. Hosp. Infect. 2009, 72:71-76.
19. De Zutter L., De Smedt J.M., Abrams R., Beckers H., Catteau M., de Borchgrave J., Debevere J., Hoekstra J., Jonkers F., Lenges J., Notermans S., van Damme L., Vandermeersch R., Verbraeken R., Waes G. Collaborative study on the use of motility enrichment on modified semisolid Rappaport-Vassiliadis medium for the detection of Salmonella from foods. Int. J. Food Microbiol. 1991, 13:11-20.
20. Development Core Team R. R: A Language and Environment for Statistical Computing, Version 2.14.0 Ed 2011, R Foundation for Statistical Computing, Vienna, Austria.
21. E.F.S.A. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2011. EFSA J. 2013, 11:3129.
22. Grimont P.A.D., Weill F.-X. Antigenic Formulae of the Salmonella Serovars 2007, Institut Pasteur, Paris. 9th ed.
23. Hegstad K., Langsrud S., Lunestad B.T., Scheie A.A., Sunde M., Yazdankhah S.P. Does the wide use of quaternary ammonium compounds enhance the selection and spread of antimicrobial resistance and thus threaten our health?. Microb. Drug Resist. 2010, 16:91-104.
24. Hothorn T., Bretz F., Westfall P. Simultaneous inference in general parametric models. Biom. J. 2008, 50:346-363.
25. Karatzas K.A.G., Webber M.A., Jorgensen F., Woodward M.J., Piddock L.J.V., Humphrey T.J. Prolonged treatment of Salmonella enterica serovar Typhimurium with commercial disinfectants selects for multiple antibiotic resistance, increased efflux and reduced invasiveness. J. Antimicrob. Chemother. 2007, 60:947-955.
26. Marouani-Gadri N., Firmesse O., Chassaing D., Sandris-Nielsen D., Arneborg N., Carpentier B. Potential of Escherichia coli O157:H7 to persist and form viable but non-culturable cells on a food-contact surface subjected to cycles of soiling and chemical treatment. Int. J. Food Microbiol. 2010, 144:96-103.
27. McDowell S.W.J., Porter R., Madden R., Cooper B., Neill S.D. Salmonella in slaughter pigs in Northern Ireland: prevalence and use of statistical modelling to investigate sample and abattoir effects. Int. J. Food Microbiol. 2007, 118:116-125.
28. Midelet G., Kobilinsky A., Carpentier B. Construction and analysis of fractional multifactorial designs to study attachment strength and transfer of Listeria monocytogenes from pure or mixed biofilms after contact with a solid model food. Appl. Environ. Microbiol. 2006, 72:2313-2321.
29. Olsen J.E., Brown D.J., Madsen M., Bisgaard M. Cross-contamination with Salmonella on a broiler slaughterhouse line demonstrated by use of epidemiological markers. J. Appl. Microbiol. 2003, 94:826-835.
30. Ortega Morente E., Fernández-Fuentes M.A., Grande Burgos M.J., Abriouel H., Pérez Pulido R., Gálvez A. Biocide tolerance in bacteria. Int. J. Food Microbiol. 2013, 162:13-25.
31. Randall L.P., Cooles S.W., Piddock L.J.V., Woodward M.J. Effect of triclosan or a phenolic farm disinfectant on the selection of antibiotic-resistant Salmonella enterica. J. Antimicrob. Chemother. 2004, 54:621-627.
32. Randall L.P., Cooles S.W., Coldham N.G., Penuela E.G., Mott A.C., Woodward M.J., Piddock L.J.V., Webber M.A. Commonly used farm disinfectants can select for mutant Salmonella enterica serovar Typhimurium with decreased susceptibility to biocides and antibiotics without compromising virulence. J. Antimicrob. Chemother. 2007, 60:1273-1280.
33. Rasmussen L.H., Kjeldgaard J., Christensen J.P., Ingmer H. Multilocus sequence typing and biocide tolerance of Arcobacter butzleri from Danish broiler carcasses. BMC Res. Notes 2013, 6:322.
34. Rasschaert G., Houf K., De Zutter L. Impact of the slaughter line contamination on the presence of Salmonella on broiler carcasses. J. Appl. Microbiol. 2007, 103:333-341.
35. Ribot E.M., Fair M.A., Gautom R., Cameron D.N., Hunter S.B., Swaminathan B., Barrett T.J. Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. Foodborne Pathog. Dis. 2006, 3:59-67.
36. Sidhu M.S., Sørum H., Holck A. Resistance to quaternary ammonium compounds in food-related bacteria. Microb. Drug Resist. 2002, 8:393-399.
37. Small A., James C., James S., Davies R., Liebana E., Howell M., Hutchison M., Buncic S. Presence of Salmonella in the red meat abattoir lairage after routine cleansing and disinfection and on carcasses. J. Food Prot. 2006, 69:2342-2351.
38. van Hoek A.H.A.M., de Jonge R., van Overbeek W.M., Bouw E., Pielaat A., Smid J.H., Malorny B., Junker E., Lofstrom C., Pedersen K., Aarts H.J.M., Heres L. A quantitative approach towards a better understanding of the dynamics of Salmonella spp. in a pork slaughter-line. Int. J. Food Microbiol. 2012, 153:45-52.
39. Wallis T.S., Paulin S.M., Plested J.S., Watson P.R., Jones P.W. The Salmonella dublin virulence plasmid mediates systemic but not enteric phases of salmonellosis in cattle. Infect. Immun. 1995, 63:2755-2761.
40. Warnes G.R., Bolker B., Bonebakker L., Gentleman R., Liaw W.H.A., Lumley T., Maechler M., Magnusson A., Moeller S., Schwartz M., Venables B. gplots: Various R Programming Tools for Plotting Data, 2.11.3 Ed 2013.
41. Whitehead R.N., Overton T.W., Kemp C.L., Webber M.A. Exposure of Salmonella enterica serovar Typhimurium to high level biocide challenge can select multidrug resistant mutants in a single step. PLoS ONE 2011, 6:e22833.