Effectiveness of disinfectants in killing Enterobacter sakazakii in suspension, dried on the surface of stainless steel, and in a biofilm

Applied and Environmental Microbiology

Volumn 73, Issue 4, 2007, Pages 1256-1265

  Kim, Hoikyung ^a   Ryu, Jee Hoon ^b   Beuchat, Larry R ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b Korea University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BIOFILMS; CHEMICAL ANALYSIS; DRYING; STAINLESS STEEL; SUSPENSIONS (FLUIDS);

FOOD SERVICE; ORGANIC MATRICES;

DISINFECTANTS;

DISINFECTANT AGENT; STAINLESS STEEL;

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL ACTIVITY; BACTERIUM; BIOFILM; BIOREMEDIATION; CHEMICAL COMPOUND; PLANKTON; STEEL;

ARTICLE; BACTERICIDAL ACTIVITY; BIOFILM; CONTROLLED STUDY; DESICCATION; DISINFECTION; ENTEROBACTER SAKAZAKII; NONHUMAN; SURFACE PROPERTY; SUSPENSION;

BIOFILMS; DESICCATION; DISINFECTANTS; ENTEROBACTER SAKAZAKII; FOOD MICROBIOLOGY; MICROBIAL SENSITIVITY TESTS; STAINLESS STEEL;

ENTEROBACTER SAKAZAKII;

EID: 33847181687     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.01766-06     Document Type: Article

References (55)

1. AOAC International. 2000. Official methods of analysis, 17th ed., method 960.09. AOAC International, Gaithersburg, MD.
2. Bar-Oz, B., A. Preminger, O. Peleg, C. Block, and I. Arad. 2001. Enterobacter sakazakii infection in the newborn. Acta Pediatr. 90:356-358.
3. Berg, J. D., A. Matin, and P. V. Roberts. 1982. Effect of antecedent growth-conditions on sensitivity of Escherichia coli to chlorine dioxide. Appl. Environ. Microbiol. 44:814-818.
4. Beuchat, L. R., B. B. Adler, and M. M. Lang. 2004. Efficacy of chlorine and peroxyacetic acid sanitizer in killing Listeria monocytogenes on iceberg and romaine lettuce using simulated commercial processing conditions. J. Food Prot. 67:1238-1242.
5. Biering, G., S. Karlsson, N. V. C. Clark, K. E. Jonsdottir, P. Ludvigsson, and O. Steingrimsson. 1989. Three cases of neonatal meningitis caused by Enterobacter sakazakii in powdered milk. J. Clin. Microbiol. 27:2054-2056.
6. Block, C., O. Peleg, N. Minster, B. Bar-Oz, A. Simhon, I. Arad, and M. Shapiro. 2002. Cluster of neonatal infections in Jerusalem due to unusual biochemical variant of Enterobacter sakazakii. Eur. J. Clin. Microbiol. Infect. Dis. 21:613-616.
7. Burdette, J. H., and C. Santos. 2000. Enterobacter sakazakii brain abscess in the neonate: the importance of neuroradiologic imaging. Pediatr. Radiol. 30:33-34.
8. Carpentier, B., and O. Cerf. 1993. Biofilms and their consequences, with particular reference to hygiene in the food industry. J. Appl. Bacteriol. 75:499-511.
9. Chen, X., and P. S. Stewart. 1996. Chlorine penetration into artificial biofilm is limited by a reaction-diffusion interaction. Environ. Sci. Technol. 30:2078-2083.
10. Clark, N. C., B. C. Hill, C. M. O'Hara, O. Steingrimsson, and R. C. Cooksey. 1990. Epidemiological typing of Enterobacter sakazakii in two neonatal nosocomial outbreaks. Diagn. Microbiol. Infect. Dis. 13:467-472.
11. Costerton, J. W., Z. Lewandowski, D. E. Caldwell, D. R. Korber, and H. M. Lappin-Scott. 1995. Microbial biofilms. Annu. Rev. Microbiol. 49:711-745.
12. de Beer, D., R. Srinivasan, and P. S. Stewart. 1994. Direct measurement of chlorine penetration into biofilms during disinfection. Appl. Environ. Microbiol. 60:4339-4344.
13. Delissalde, F., and C. F. Amábile-Cuevas. 2004. Comparison of antibiotic susceptibility and plasmid content, between biofilm producing and non-producing clinical isolates of Pseudomonas aeruginosa. Int. J. Antimicrob. Agents 24:405-408.
14. Edelson-Mammel, S. G., and R. L. Buchanan. 2004. Acid resistance of twelve strains of Enterobacter sakazakii, Abstr. P170, p. 107. Program and abstract book, 91st Annu. Mtg. Int. Assn. Food Prot., 8 to 11 August 2004, Phoenix, AZ
15. Exner, M., V. Vacata, B. Hornei, E. Dietlein, and J. Gebel. 2004. Household cleaning and surface disinfection: new insights and strategies. J. Hosp. Infect. 56:S70-S75.
16. Farrell, B. L., A. B. Bonner, and A. C. L. Wong. 1998. Attachment of Escherichia coli O157:H7 in ground beef to meat grinders and survival after sanitation with chlorine and peroxyacetic acid. J. Food Prot. 61:817-822.
17. Folsom, J. P., and J. F. Frank. 2006. Chlorine resistance of Listeria monocytogenes biofilms and relationship to subtype, cell density, and planktonic cell chlorine resistance. J. Food Prot. 69:1292-1296.
18. Frank, J. F., and R. A. Koffi. 1990. Surface-adherent growth of Listeria monocytogenes is associated with increased resistance to surfactant sanitizers and heat. J. Food Prot. 53:550-554.
19. Gallagher, P. G., and W. S. Ball. 1991. Cerebral infarction due to CNS infection with Enterobacter sakazakii. Pediatr. Radiol. 21:135-136.
20. Gurtler, J. B., and L. R. Beuchat. 2005. Performance of media for recovering stressed cells of Enterobacter sakazakii as determined using spiral plating and ecometric techniques. Appl. Environ. Microbiol. 71:7661-7669.
21. Himelright, I., E. Harris, V. Lorch, and M. Anderson. 2002. Enterobacter sakazakii infections associated with the use of powdered infant formula-Tennessee, 2001. JAMA 287:2204-2205.
22. Iversen, C., M. Lane, and S. J. Forsythe. 2004. The growth profile, thermotolerance and biofilm formation of Enterobacter sakazakii grown in infant formula milk. Lett. Appl. Microbiol. 38:378-382.
23. Jones, J. G., and R. W. Pickup. 1989. The effect of organic carbon supply in water on the antibiotic resistance of bacteria. Aqua 33:131-135.
24. Jono, K., T. Takayama, M. Kuno, and E. Higashide. 1986. Effect of alkyl chain length of benzalkonium chloride on the bactericidal activity and binding to organic materials. Chem. Pharm. Bull. (Tokyo) 34:4215-4224.
25. Kennedy, J., J. Bek, and D. Griffin. 2006. Selection and use of disinfectant. Neb-Guide. http:/www.ianrpubs.unl.edu/epublic/pages/publicationD. jsp?publicationId =431.
26. Kim, H., and L. R. Beuchat. 2005. Survival and growth of Enterobacter sakazakii on fresh-cut fruits and vegetables and in unpasteurized juice as affected by storage temperature. J. Food Prot. 68:2541-2552.
27. Kim, H., J.-H. Ryu, and L. R. Beuchat. 2006. Attachment and biofilm formation by Enterobacter sakazakii on stainless steel and enteral feeding tubes. Appl. Environ. Microbiol. 72:5846-5856.
28. Kim, H., J.-H. Ryu, and L. R. Beuchat. 2006. Survival of Enterobacter sakazakii on fresh produce as affected by temperature and effectiveness of sanitizers for its elimination. Int. J. Food Microbiol. 111:134-143.
29. Kitahara, T., N. Koyama, J. Matsuda, Y. Aoyama, Y. Hirakata, S. Kamihira, S. Kohno, M. Nakashima, and H. Sasaki. 2004. Antimicrobial activity of saturated fatty acids and fatty amines against methicillin-resistant Staphylococcus aureus. Biol. Pharm. Bull. 27:1321-1326.
30. Lehner, A., K. Riedel, L. Eberl, P. Breeuwer, B. Diep, and R. Stephan. 2005. Biofilm formation, extracellular polysaccharide production, and cell-to-cell signaling in various Enterobacter sakazakii strains: aspects promoting environmental persistence. J. Food Prot. 68:2287-2294.
31. Lewis, K. 2001. Riddle of biofilm resistance. Antimicrob. Agents Chemother. 45:999-1007.
32. Mah, T. F., and G. A. O'Toole. 2001. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 9:34-39.
33. Marriott, N. G., and R. B. Gravani. 2006. Principles of food sanitation, 5th ed. Springer, New York, NY.
34. Mendonca, A. F., T. L. Amoroso, and S. J. Knabel. 1994. Destruction of gram-negative food-borne pathogens by high pH involves disruption of the cytoplasmic membrane. Appl. Environ. Microbiol. 60:4009-4014.
35. Merianos, J. J. 1991. Quaternary ammonium antimicrobial compounds, p. 225-262. In S. S. Block (ed.), Disinfection, sterilization and preservation, 4th ed. Lea and Febiger, Philadelphia, PA.
36. Mosley, E. B., P. R. Elliker, and H. Hays. 1976. Destruction of food spoilage indicator and pathogenic organisms by various germicides in solution and on a stainless steel surface. J. Milk Food Technol. 39:830-836.
37. Mosteller, T. M., and J. R. Bishop. 1993. Sanitizer efficiency against attached bacteria in milk biofilm. J. Food Prot. 56:34-41.
38. Muytjens, H. L., W. H. Roelofs, and G. H. J. Jasper. 1988. Quality of powdered substitutes for breast milk with regard to members of the family Enterobacteraceae. J. Clin. Microbiol. 26:743-746.
39. Muytjens, H. L., H. C. Zanen, H. J. Sonderkamp, L. A. Kolee, I. K. Wachsmuth, and J. J. Farmer. 1983. Analysis of eight cases of neonatal meningitis and sepsis due to Enterobacter sakazakii. J. Clin. Microbiol. 18:115-120.
40. Noriega, F. R., K. L. Kotloff, M. A. Martin, and R. S. Schwalbe. 1990. Nosocomial bacteremia caused by Enterobacter sakazakii and Leuconostoc mesenteroides resulting from extrinsic contamination of infant formula. Pediatr. Infect. Dis. 9:447-449.
41. Ostrander, W. E., and L. J. Griffith. 1964. Evaluation of disinfectants for hospital housekeeping use. Appl. Microbiol. 12:460-463.
42. Robbins, J. B., C. W. Fisher, A. G. Moltz, and S. E. Martin. 2005. Elimination of Listeria monocytogenes biofilms by ozone, chlorine, and hydrogen peroxide. J. Food Prot. 68:494-498.
43. Ryu, J.-H., and L. R. Beuchat. 2005. Biofilm formation by Escherichia coli O157:H7 on stainless steel: effect of exopolysaccharide and curli production on its resistance to chlorine. Appl. Environ. Microbiol. 71:247-254.
44. Scheepe-Leberkühne, M., and F. Wagner. 1986. Optimization and preliminary characterization of an ecopolysaccharidc synthesized by Enterobacter sakazakii. Biotechnol. Lett. 8:695-700.
45. Sharma, M., and L. R. Beuchat. 2004. Sensitivity of Escherichia coli O157:H7 to commercially available alkaline cleaners and subsequent resistance to heat and sanitizers. Appl. Environ. Microbiol. 70:1795-1803.
46. Shelton, R. S., M. G. Van Campen, C. H. Tilford, H. C. Lang, L. Nisonger, F. J. Bandelin, and H. L. Rubenkoenig. 1946. Quaternary ammonium salts as germicides. I. Non-acylated quarternary ammonium salts derived from aliphatic amines. J. Am. Med. Chem. Soc. 68:753-755.
47. Simmons, B. P., M. S. Gelfand, M. Haas, L. Metts, and J. Ferguson. 1989. Enterobacter sakazakii infections in neonates associated with intrinsic contamination of a powdered infant formula. Infect. Control Hosp. Epidemiol. 10:398-401.
48. Sutton, S. V., D. W. Proud, S. Rachui, and D. K. Brannan. 2002. Validation of microbial recovery from disinfectants. J. Pharm. Sci. Technol. 56:255-266.
49. Taormina, P. J., and L. R. Beuchat. 2002. Survival of Liberia monocytogenes in commercial food-processing equipment cleaning solutions and subsequent sensitivity to sanitizers and heat. J. Appl. Microbiol. 92:71-80.
50. Troller, J. A. 1993. Sanitation in food processing, 2nd ed. Academic Press, San Diego, CA.
51. Van Acker, V., F. de Smet, G. Muyldermans, A. Bougatef, A. Naessens, and S. Lauwers. 2001. Outbreak of necrotizing enterocolitis associated with Enterobacter sakazakii in powdered milk formula. J. Clin. Microbiol. 39:293-297.
52. Vesley, D., and G. S. Michaelsen. 1964. Application of a surface sampling technique to the evaluation of bacteriological effectiveness of certain hospital housekeeping procedures. Health Lab. Sci. 1:107-113.
53. Vijayakumar, C., and C. E. Wolf-Hall. 2002. Minimum bacteriostatic and bactericidal concentrations of household sanitizers for Escherichia coli strains in tryptic soy broth. Food Microbiol. 19:383-388.
54. Walters, M. C., F. Roe, A. Bugnicourt, M. J. Franklin, and P. S. Stewart. 2003. Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob. Agents Chemother. 47:317-323.
55. Xu, X., P. S. Stewart, and X. Chen. 1996. Transport limitation of chlorine disinfection of Pseudomonas aeruginosa entrapped in alginate beads. Biotechnol. Bioeng. 49:93-100.