Lethality of chlorine, chlorine dioxide, and a commercial produce sanitizer to Bacillus cereus and Pseudomonas in a liquid detergent, on stainless steel, and in biofilm

Journal of Food Protection

Volumn 69, Issue 11, 2006, Pages 2621-2634

  Kreske, Audrey C ^a   Ryu, Jee Hoon ^a,b   Pettigrew, Charles A ^c   Beuchat, Larry R ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b Korea University   (South Korea)

^c PROCTER AND GAMBLE COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLUS CEREUS; BACTERIA (MICROORGANISMS); EQUUS CABALLUS; PSEUDOMONAS;

EID: 33751206882     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X-69.11.2621     Document Type: Article

References (44)

1. Anderson, K. 1962. The contamination of hexachlorophene soap with Pseudomonas pyocyanea. Med. J. Aust. 2:463.
2. Babic, I., S. Roy, A. E. Watada, and W. P. Wergin. 1996. Changes in microbial populations on fresh cut spinach. Int. J. Food Microbiol. 31:107-119.
3. Beuchat, L. R. 1998. Surface decontamination of fruits and vegetables eaten raw: a review. WHO/FSF/FOS/98.2. Food Safety Unit, World Health Organization, Geneva.
4. Beuchat, L. R. 2000. Use of sanitizers in raw fruit and vegetable processing, chap. 4, p. 63-78. In S. M. Alzamora, M. S. Tapia, and A. Lopez-Malo (ed.), Minimally processed fruits and vegetables: fundamental aspects and applications. Aspen Publications, Gaithersburg, Md.
5. Beuchat, L. R., C. A. Pettigrew, M. E. Tremblay, B. J. Roselle, and A. J. Scouten. 2004. Lethality of chlorine, chlorine dioxide, and a commercial fruit and vegetable sanitizer to vegetative cells and spores of Bacillus cereus and spores of Bacillus thuringiensis. J. Food Prot. 67:1702-1708.
6. Cords, B. R., S. L. Burnett, J. Hilgren, M. Finley, and J. Magnuson. 2005. Sanitizers: halogens, surface-active agents, and peroxides, p. 507-572. In P. M. Davidson, J. N. Sofos, and A. L. Branen (ed.), Antimicrobials in food, 3rd ed. Taylor and Francis, Boca Raton, Fla.
7. Denton, M., and K. G. Kerr. 1998. Microbiological and clinical aspects of infection associated with Stenotrophomonas maltophilia. Clin. Microbiol. Rev. 11:57-80.
8. Deza, M. A., M. Araujo, and M. J. Garrido. 2005. Inactivation of Escherichia coli, Listeria monocytogenes, Pseudomonas aeruginosa and Staphylococcus aureus on stainless steel and glass surfaces by neutral electrolysed water. Lett. Appl. Microbiol. 40:341-346.
9. Dotsi, B., Z. Guzel-Seydim, and A. K. Greene. 2005. Effectiveness of ozone, heat, and chlorine for destroying common food spoilage bacteria in synthetic media and biofilms. Int. J. Dairy Technol. 58: 19-24.
10. Dychdala, G. R. 2001. Chlorine and chlorine compounds, p. 135-158. In S. S. Block (ed.), Disinfection, sterilization and preservation, 5th ed. Lippincott Williams and Wilkins, Philadelphia.
11. Engelhart, S., L. Krizel, A. Glasmacher, E. Fischnaller, G. Marklein, and M. Exner. 2002. Pseudomonas aeruginosa outbreak in a haematology-oncology unit associated with contaminated surface cleaning equipment. J. Hosp. Infect. 52:93-98.
12. Foegeding, P. M., V. Hemstapat, and F. G. Giesbracht. 1986. Chlorine dioxide inactivation of Bacillus and Clostridium spores. J. Food Sci. 51:197-201.
13. Granum, P. E., and T. Lung. 1997. Bacillus cereus and its food poisoning toxins. FEMS Microbiol. Lett. 157:223-228.
14. Granum, P. E., and J. Magnussen. 1987. The effect of pH on hypochlorite as disinfectant. Int. J. Food Microbiol. 4:183-186
15. Green, S. K., M. N. Schroth, J. J. Cho, S. D. Kominos, and V. B. Vitanza-Jack. 1974. Agricultural plants and soil as a reservoir for Pseudomonas aeruginosa. Appl. Microbiol. 28:987-991.
16. Hamilton-Miller, J. M. T, and S. Shah. 2001. Identity and antibiotic susceptibility of enterobacterial flora of salad vegetables. Int. J. Antimicrob. Agents 18:81-83.
17. Hamon, M. A., and B. A. Lazazzera. 2001. The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Mol. Microbiol. 42:1199-1209.
18. Harmon, S. M., D. A. Kautter, and H. M. Solomon. 1987. Bacillus cereus contamination of seeds and vegetable sprouts grown in a home sprouting kit. J. Food Prot. 50:62-65.
19. Huffman, P N., J. E. Death, and D. Coates. 1981. The stability of sodium hypochlorite solutions, p. 77-83. In C. H. Collins, M. C. Allwood, S. F. Bloomfield, and A. Fox (ed.), Disinfectants: their use and evaluation of effectiveness. Academic Press, New York.
20. Jay, J. M. 2000. Food poisoning caused by gram-positive bacteria, p. 461-484. In Modern food microbiology, 6th ed. Aspen Publications, Gaithersburg, Md.
21. Josephson, K. L., J. R. Rubino, and I. L. Pepper. 1997. Characterization and quantification of bacterial pathogens and indicator organisms in household kitchens with and without the use of a disinfector cleaner. J. Appl. Microbiol. 83:737-750.
22. Kominos, S. D., C. E. Copeland, B. Grosiak, and B. Postic. 1972. Introduction of Pseudomonas aeruginosa into a hospital via vegetables. Appl. Microbiol. 24:567-570.
23. Kreske, A. C., J.-H. Ryu, and L. R. Beuchat. 2006. Evaluation of chlorine, chlorine dioxide, and a peroxyacetic acid-based sanitizer for effectiveness in killing Bacillus cereus and Bacillus thuringiensis spores in suspension, on stainless steel, and on apples. J. Food Prot. 69:1892-1903.
24. Lindsay, D., V. S. Brözel, J. F. Mostert, and A. von Holy. 2002. Differential efficacy of chlorine dioxide against single species and binary biofilms of a dairy-associated Bacillus cereus and a Pseudomonas fluorescens isolate. J. Appl. Microbiol. 92:352-361.
25. Lindsay, D., V. S. Brözel, and A. von Holy. 2005. Spore formation in Bacillus subtilis biofilms. J. Food Prot. 68:860-865.
26. Lindsay, D., V. S. Brözel, and A. von Holy. 2006. Biofilm-spore response in Bacillus cereus and Bacillus subtilis during nutrient limitation. J. Food Prot. 69:1168-1172.
27. Lindsay, D., and A. von Holy. 1998. Nutrient limitation affects growth and attachment of two food spoilage bacteria, Bacillus subtilis and Pseudomonas fluorescens S. Afr. J. Sci. 94:393-396.
28. Lindsay, D., and A. von Holy. 1999. Different responses of planktonic and attached Bacillus subtilis and Pseudomonas fluorescens to sanitizer treatment. J. Food Prot. 62:368-379.
29. Marriott, N. G. 1999. Sanitizers, p. 138-157. In Principles of food sanitation, 4th ed. Aspen Publications, Gaithersburg, Md.
30. Mercer, W. A., and I. I. Somers. 1957. Chlorine in food plant sanitation. Adv. Food Res. 7:129-160.
31. Oosthuizen, M. C., B. Steyn, J. Theron, P. Cosette, D. Lindsay, A. von Holy, and V. S. Brözel. 2002. Proteomic analysis reveals differential protein expression by Bacillus cereus during biofilm formation. Appl. Environ. Microbiol. 68:2770-2780.
32. Padaga, M., G. M. Heard, J. E. Paton, and G. H. Fleet. 2000. Microbial species associated with different sections of broccoli harvested from three regions in Australia. Int. J. Food Microbiol. 60: 15-24.
33. Parkar, S. G., S. H. Flint, J. S. Palmer, and J. D. Brooks. 2001. Factors influencing attachment of thermophilic bacilli to stainless steel. J. Appl. Microbiol. 90:901-908.
34. Peng, J.-S., W.-C. Tsai, and C.-C. Chou. 2001. Surface characteristics of Bacillus cereus and its adhesion to stainless steel. Int. J. Food Microbiol. 65:105-111.
35. Pitten, F.-A., B. Panzig, G. Schroder, K. Tietzer, and A. Kramer. 2001. Transmission of a multiresistant Pseudomonas aeroginosa strain in a German university hospital. J. Hosp. Infect. 47:125-130.
36. Qureshi, A., L. Mooney, M. Demon, and K. G. Kerr. 2005. Stenotrophomonas maltophilia in salad. Emerg. Infect. Dis. 11:1157-1158.
37. Ringen, L. M., and C. H. Drake. 1952. A study of the incidence of Pseudomonas aeruginosa from various natural sources. J. Bacteriol. 64:841-845.
38. Roselle, B., G. Huntington, M. Tremblay, C. Pettigrew, and F. Barnabas. 25 November 2004. U.S. patent application US2004/0231977 A1. Compositions, devices, and methods for stabilizing and increasing the efficacy of halogen dioxide. Procter & Gamble Co., Cincinnati, Ohio.
39. Rossoni, E. M. M., and C. C. Gaylarde. 2000. Comparison of sodium hypochlorite and peracetic acid as sanitizing agents for stainless steel food processing surfaces using epifluorescence microscopy. Int. J. Food Microbiol. 61:81-85.
40. Ryu, J.-H., and L. R. Beuchat. 2005. Biofilm formation and sporulation by Bacillus cereus on a stainless steel surface, and subsequent resistance of vegetative cells and spores to chlorine, chlorine dioxide, and a peroxyacetic acid-based sanitizer. J. Food Prot. 68:2614-2622.
41. Soriano, J. M., H. Rico, J. C. Molto, and J. Manes. 2000. Assessment of the microbiological quality and wash treatments of lettuce served in university restaurants. Int. J. Food Microbiol. 58:123-128.
42. Taylor, J. H., S. J. Rogers, and J. T. Holah. 1999. A comparison of the bactericidal efficacy of 18 disinfectants used in the food industry against Escherichia coll O157:H7 and Pseudomonas aeruginosa at 10 and 20°C. J. Appl. Microbiol 87:718-725.
43. Valero, M., L. A. Hernandez-Herrero, P. S. Fernandez, and M. C. Salmeron. 2002. Characterization of Bacillus cereus isolates from fresh vegetables and refrigerated minimally processed foods by biochemical and physiological tests. Food Microbiol. 19:491-499.
44. Young, S. B., and P. Setlow. 2003. Mechanisms of killing of Bacillus subtilis spores by hypochlorite and chlorine dioxide. J. Appl Microbiol. 95:54-67.