Benzalkonium chloride and heavy-metal tolerance in Listeria monocytogenes from retail foods

International Journal of Food Microbiology

Volumn 190, Issue , 2014, Pages 24-30

  Xu, Dongyang ^a   Li, Yanli ^a   Shamim Hasan Zahid, M ^b   Yamasaki, Shinji ^a,b   Shi, Lei ^a,b   Li, Jian rong ^c   Yan, He ^a  

^a SOUTH CHINA UNIVERSITY OF TECHNOLOGY   (China)

^b Osaka Prefecture University   (Japan)

^c BOHAI UNIVERSITY   (China)

Author keywords

Benzalkonium chloride; Cadmium; Cadmium resistance determinants; Listeria monocytogenes; QAC resistance determinants; Tolerance

Indexed keywords

BENZALKONIUM CHLORIDE; CADMIUM; RESERPINE; HEAVY METAL; BACTERIAL PROTEIN; BENZALKONIUM;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM ISOLATE; CONTROLLED STUDY; EVOLUTIONARY ADAPTATION; FOOD FREEZING; LISTERIA; LISTERIA MONOCYTOGENES; METAL TOLERANCE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PSEUDOMONAS PUTIDA; RAW MEAT; RICE; STAPHYLOCOCCUS AUREUS; WHEAT; ADAPTATION; FOOD; FOOD INDUSTRY; MULTIDRUG RESISTANCE; SEROTYPE; DRUG EFFECTS; FOOD CONTROL; GENETICS; HUMAN; ISOLATION AND PURIFICATION;

LISTERIA MONOCYTOGENES;

BACTERIAL PROTEINS; BENZALKONIUM COMPOUNDS; DRUG RESISTANCE, BACTERIAL; FOOD MICROBIOLOGY; HUMANS; LISTERIA MONOCYTOGENES; METALS, HEAVY;

EID: 84906730960     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2014.08.017     Document Type: Article

References (47)

1. Aase B., Sundheim G., Langsrud S., Rorvik L.M. Occurrence of and a possible mechanism for resistance to a quaternary ammonium compound in Listeria monocytogenes. Int. J. Food Microbiol. 2000, 62:57-63.
2. Abuzaid A., Hamouda A., Amyes S. Klebsiella pneumoniae susceptibility to biocides and its association with cepA, qacδE and qacE efflux pump genes and antibiotic resistance. J. Hosp. Infect. 2012, 81:87-91.
3. Alonso A., Sanchez P., Martinez J.L. Environmental selection of antibiotic resistance genes. Environ. Microbiol. 2001, 3:1-9.
4. Aminov R.I., Mackie R.I. Evolution and ecology of antibiotic resistance genes. FEMS Microbiol. Lett. 2007, 271:147-161.
5. Baker-Austin C., Wright M.S., Stepanauskas R., McArthur J.V. Co-selection of antibiotic and metal resistance. Trends Microbiol. 2006, 14:176-182.
6. Bjorland J., Steinum T., Sunde M., Waage S., Heir E. Novel plasmid-borne gene qacJ mediates resistance to quaternary ammonium compounds in equine Staphylococcus aureus, Staphylococcus simulans, and Staphylococcus intermedius. Antimicrob. Agents Chemother. 2003, 47:3046-3052.
7. Carpentier B., Cerf O. Review - persistence of Listeria monocytogenes in food industry equipment and premises. Int. J. Food Microbiol. 2011, 145:1-8.
8. Cerf O., Carpentier B., Sanders P. Tests for determining in-use concentrations of antibiotics and disinfectants are based on entirely different concepts: "resistance" has different meanings. Int. J. Food Microbiol. 2010, 136:247-254.
9. Chapman J.S. Disinfectant resistance mechanisms, cross-resistance, and co-resistance. Int. Biodeterior. Biodegrad. 2003, 51:271-276.
10. Conter M., Paludi D., Zanardi E., Ghidini S., Vergara A., Ianieri A. Characterization of antimicrobial resistance of foodborne Listeria monocytogenes. Int. J. Food Microbiol. 2009, 128:497-500.
11. Elhanafi D., Dutta V., Kathariou S. Genetic characterization of plasmid-associated benzalkonium chloride resistance determinants in a Listeria monocytogenes strain from the 1998-1999 outbreak. Appl. Environ. Microbiol. 2010, 76:8231-8238.
12. Frempong-Manso E., Raygada J.L., DeMarco C.E., Seo S.M., Kaatz G.W. Inability of a reserpine-based screen to identify strains overexpressing efflux pump genes in clinical isolates of Staphylococcus aureus. Int. J. Antimicrob. Agents 2009, 33:360-363.
13. Gillings M.R. Biocide use, integrons and novel genetic elements. Microbiol. Aust. 2010, 31:192-194.
14. Gilmour M.W., Graham M., Van Domselaar G., Tyler S., Kent H., Trout-Yakel K.M., Larios O., Allen V., Lee B., Nadon C. High-throughput genome sequencing of two Listeria monocytogenes clinical isolates during a large foodborne outbreak. BMC Genomics 2010, 11:120-135.
15. Glaser P., Frangeul L., Buchrieser C., Rusniok C., Amend A., Baquero F., Berche P., Bloecker H., Brandt P., Chakraborty T. Comparative genomics of Listeria species. Science 2001, 294:849-852.
16. Grinius L., Dreguniene G., Goldberg E.B., Liao C., Projan S.J. A staphylococcal multidrug resistance gene product is a member of a new protein family. Plasmid 1992, 27:119-129.
17. Harvey J., Gilmour A. Characterization of recurrent and sporadic Listeria monocytogenes isolates from raw milk and nondairy foods by pulsed-field gel electrophoresis, monocin typing, plasmid profiling, and cadmium and antibiotic resistance determination. Appl. Environ. Microbiol. 2001, 67:840-847.
18. Hayashi S., Abe M., Kimoto M., Furukawa S., Nakazawa T. The DsbA-DsbB disulfide bond formation system of Burkholderia cepacia is involved in the production of protease and alkaline phosphatase, motility, metal resistance, and multi-drug resistance. Microbiol. Immunol. 2000, 44:41-50.
19. 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.
20. Heir E., Sundheim G., Holck A.L. The Staphylococcus qacH gene product: a new member of the SMR family encoding multidrug resistance. FEMS Microbiol. Lett. 1998, 163:49-56.
21. Heir E., Sundheim G., Holck A.L. The qacG gene on plasmid pST94 confers resistance to quaternary ammonium compounds in staphylococci isolated from the food industry. J. Appl. Microbiol. 1999, 86:378-388.
22. Hof H. An update on the medical management of listeriosis. Expert. Opin. Pharmacother. 2004, 5:1727-1735.
23. Ji X., Shen Q., Liu F., Ma J., Xu G., Wang Y., Wu M. Antibiotic resistance gene abundances associated with antibiotics and heavy metals in animal manures and agricultural soils adjacent to feedlots in Shanghai; China. J. Hazard. Mater. 2012, 235:178-185.
24. Kolpin D.W., Furlong E.T., Meyer M.T., Thurman E.M., Zaugg S.D., Barber L.B., Buxton H.T. Pharmaceuticals, hormones, and other organic wastewater contaminants in US streams, 1999-2000: a national reconnaissance. Environ. Sci. Technol. 2002, 36:1202-1211.
25. Langsrud S., Sidhu M.S., Heir E., Holck A.L. Bacterial disinfectant resistance-a challenge for the food industry. Int. Biodeterior. Biodegrad. 2003, 51:283-290.
26. Lavilla Lerma L., Benomar N., Gálvez A., Abriouel H. Prevalence of bacteria resistant to antibiotics and/or biocides on meat processing plant surfaces throughout meat chain production. Int. J. Food Microbiol. 2013, 161:97-106.
27. Lee S., Rakic-Martinez M., Graves L.M., Ward T.J., Siletzky R.M., Kathariou S. Genetic determinants for cadmium and arsenic resistance among Listeria monocytogenes serotype 4b isolates from sporadic human listeriosis patients. Appl. Environ. Microbiol. 2013, 79:2471-2476.
28. Leelaporn A., Paulsen I.T., Tennent J.M., Littlejohn T.G., Skurray R.A. Multidrug resistance to antiseptics and disinfectants in coagulase-negative staphylococci. J. Med. Microbiol. 1994, 40:214-220.
29. Levy S. Active efflux mechanisms for antimicrobial resistance. Antimicrob. Agents Chemother. 1992, 36:695-703.
30. Margolles A., Mayo B., de Los Reyes-Gavilán C.G. Susceptibility of Listeria monocytogenes and Listeria innocua strains isolated from short-ripened cheeses to some antibiotics and heavy metal salts. Food Microbiol. 2001, 18:67-73.
31. Mereghetti L., Quentin R., Marquet-Van Der Mee N., Audurier A. Low sensitivity of Listeria monocytogenes to quaternary ammonium compounds. Appl. Environ. Microbiol. 2000, 66:5083-5086.
32. Mullapudi S., Siletzky R.M., Kathariou S. Heavy-metal and benzalkonium chloride resistance of Listeria monocytogenes isolates from the environment of turkey-processing plants. Appl. Environ. Microbiol. 2008, 74:1464-1468.
33. Mullapudi S., Siletzky R.M., Kathariou S. Diverse cadmium resistance determinants in Listeria monocytogenes isolates from the turkey processing plant environment. Appl. Environ. Microbiol. 2010, 76:627-630.
34. Noguchi N., Suwa J., Narui K., Sasatsu M., Ito T., Hiramatsu K., Song J.H. Susceptibilities to antiseptic agents and distribution of antiseptic-resistance genes qacA/B and smr of methicillin-resistant Staphylococcus aureus isolated in Asia during 1998 and 1999. J. Med. Microbiol. 2005, 54:557-565.
35. Paulsen I.T., Brown M.H., Littlejohn T.G., Mitchell B.A., Skurray R.A. Multidrug resistance proteins QacA and QacB from Staphylococcus aureus: membrane topology and identification of residues involved in substrate specificity. Proc. Natl. Acad. Sci. 1996, 93:3630-3635.
36. Ploy M., Courvalin P., Lambert T. Characterization of In40 of Enterobacter aerogenes BM2688, a class 1 integron with two new gene cassettes, cmlA2 and qacF. Antimicrob. Agents Chemother. 1998, 42:2557-2563.
37. Ratani S.S., Siletzky R.M., Dutta V., Yildirim S., Osborne J.A., Lin W., Hitchins A.D., Ward T.J., Kathariou S. Heavy metal and disinfectant resistance of Listeria monocytogenes from foods and food processing plants. Appl. Environ. Microbiol. 2012, 78:6938-6945.
38. Romanova N., Favrin S., Griffiths M.W. Sensitivity of Listeria monocytogenes to sanitizers used in the meat processing industry. Appl. Environ. Microbiol. 2002, 68:6405-6409.
39. Romanova N.A., Wolffs P.F., Brovko L.Y., Griffiths M.W. Role of efflux pumps in adaptation and resistance of Listeria monocytogenes to benzalkonium chloride. Appl. Environ. Microbiol. 2006, 72:3498-3503.
40. Sidhu M.S., Heir E., Leegaard T., Wiger K., Holck A. Frequency of disinfectant resistance genes and genetic linkage with β-lactamase transposon Tn552 among clinical staphylococci. Appl. Environ. Microbiol. 2002, 46:2797-2803.
41. Soumet C., Ragimbeau C., Maris P. Screening of benzalkonium chloride resistance in Listeria monocytogenes strains isolated during cold smoked fish production. Lett. Appl. Microbiol. 2005, 41:291-296.
42. Stepanauskas R., Glenn T.C., Jagoe C.H., Tuckfield R.C., Lindell A.H., King C.J., McArthur J.V. Coselection for microbial resistance to metals and antibiotics in freshwater microcosms. Environ. Microbiol. 2006, 8:1510-1514.
43. Summers A.O. Generally overlooked fundamentals of bacterial genetics and ecology. Clin. Infect. Dis. 2002, 34:S85-S92.
44. Swaminathan B., Gerner-Smidt P. The epidemiology of human listeriosis. Microbes Infect. 2007, 9:1236-1243.
45. Yan H., Neogi S.B., Mo Z., Guan W., Shen Z., Zhang S., Li L., Yamasaki S., Shi L., Zhong N. Prevalence and characterization of antimicrobial resistance of foodborne Listeria monocytogenes isolates in Hebei province of Northern China, 2005-2007. Int. J. Food Microbiol. 2010, 144:310-316.
46. Yucel N., Citak S., Onder M. Prevalence and antibiotic resistance of Listeria species in meat products in Ankara. Turkey. Food Microbiol. 2005, 22:241-245.
47. Zhou Y.Q., Lu K.L. Genes resistant to disinfectant-sulfanilamide, class 1 integrase and aminoglycoside-modifying enzyme in Acinetobacter baumannii. Chin. J. Nosoconmiol. 2005, 15:728-731. (in Chinese with English abstract).