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Research article

References

  1. Drobniewski FA. 1993. Bacillus cereus and related species. Clin. Microbiol. Rev. 6: 324-338.
    Pubmed PMC CrossRef
  2. Anderson A, Ronner U, Granum PE. 1995. What problems does the food industry have with the spore-forming pathogens Bacillus cereus and Clostridium perfringens? Int. J. Food Microbiol. 28: 145-155.
    CrossRef
  3. Gao YL, Jiang HH. 2005. Optimization of process conditions to inactivate Bacillus subtilis by high hydrostatic pressure and mild heat using response surface methodology. Biochem. Eng. J. 24: 43-48.
    CrossRef
  4. Head DS, Cenkowski S, Holley R, Blank G. 2008. Effects of superheated steam on Geobacillus stearothermophilus spore viability. J. Appl. Microbiol. 104: 1213-1220.
    Pubmed CrossRef
  5. Setlow B, Loshon CA, Genest PC, Cowan AE, Setlow C, Setlow P. 2002. Mechanisms of killing spores of Bacillus subtilis by acid, alkali and ethanol. J. Appl. Microbiol. 92: 362-375.
    Pubmed CrossRef
  6. Elhariry HM. 2011. Attachment strength and biofilm forming ability of Bacillus cereus on green-leafy vegetables:cabbage and lettuce. Food Microbiol. 28: 1266-1274.
    Pubmed CrossRef
  7. Peng JS, Tsai WC, Chou CC. 2002. Inactivation and removal of Bacillus cereus by sanitizer and detergent. Int. J. Food Microbiol. 77: 11-18.
    CrossRef
  8. Flemming HC, Wingender J. 2001. Relevance of microbial extracellular polymeric substance (EPS) – Part I: Structural and ecological aspects. Water Sci. Technol. 43: 1-8.
    Pubmed
  9. Bridier A, Briandet R, Thomas V, Dubois-Brissonnet F. 2011. Resistance of bacterial biofilms to disinfectants: a review. Biofouling 27: 1017-1032.
    Pubmed CrossRef
  10. Kumar CG, Anand SK. 1998. Significance of microbial biofilms in food industry: a review. Int. J. Food Microbiol. 42: 9-27.
    CrossRef
  11. Kreske AC, Ryu JH, Pettigrew CA, Beuchat LR. 2006. 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. J. Food Prot. 69: 2621-2634.
    Pubmed CrossRef
  12. Park HS, Choi HJ, Kim MD, Kim KH. 2013. Addition of ethanol to supercritical carbon dioxide enhances the inactivation of bacterial spores in the biofilm of Bacillus cereus. Int. J. Food Microbiol. 166: 207-212.
    Pubmed CrossRef
  13. Senna PM, Da Silva WJ, Del Bel Cury AA. 2010. Denture disinfection by microwave energy: influence of Candida albicans biofilm. Gerodontology 29: e186-e191.
    Pubmed CrossRef
  14. Gibson H, Taylor JH, Hall KE, Holah JT. 1999. Effectiveness of cleaning techniques used in the food industry in terms of the removal of bacterial biofilms. J. Appl. Microbiol. 87: 41-48.
    Pubmed CrossRef
  15. Woo I, Rhee I, Park H. 2000. Differential damage in bacterial cells by microwave radiation on the basis of cell wall structure. Appl. Environ. Microbiol. 66: 2243-2247.
    Pubmed PMC CrossRef
  16. Celandroni F, Longo I, Tosoratti N, Giannessi F, Ghelardi E, Salvetti S, et al. 2004. Effect of microwave radiation on Bacillus subtilis spores. J. Appl. Microbiol. 97: 1220-1227.
    Pubmed CrossRef
  17. Kim SY, Shin SJ, Song CH, Jo EK, Kim HJ, Park JK. 2009. Destruction of Bacillus licheniformis spores by microwave irradiation. J. Appl. Microbiol. 106: 877-885.
    Pubmed CrossRef
  18. Welt BA, Tong CH, Rossen JL, Lund DB. 1994. Effect of microwave radiation on inactivation of Clostridium sporogenes (PA 3679) spores. Appl. Environ. Microbiol. 60: 482-488.
    Pubmed PMC
  19. Zieli ski M, Ciesielski S, Cydzik-Kwiatkowska A, Turek J, Dębowski M. 2007. Influence of microwave radiation on bacterial community structure in biofilm. Process Biochem. 42: 1250-1253.
  20. Fernández M, Sánchez J. 2002. Nuclease activities and cell death processes associated with the development of surface cultures of Streptomyces antibioticus ETH 7451. Microbiology 148: 405-412.
    Pubmed CrossRef
  21. Myers RH, Montgomery DC. 1995. Response Surface Methodology:Process and Product Optimization Using Designed Experiments. John Wiley & Sons Inc., New York. USA.
  22. Vela GR, Wu JF. 1979. Mechanism of lethal action of 2,450MHz radiation on microorganisms. Appl. Environ. Microbiol. 37: 550-553.
    Pubmed PMC
  23. Jeng DK, Kaczmarek KA, Woodworth AG, Balasky G. 1987. Mechanism of microwave sterilization in the dry state. Appl. Environ. Microbiol. 53: 2133-2137.
    Pubmed PMC
  24. Ponne CT, Bartels PV. 1995. Interaction of electromagnetic energy with biological material - relation to food processing. Radiat. Phys. Chem. 45: 591-607.
    CrossRef
  25. Içier F, Baysal T. 2004. Dielectrical properties of food materials-1: factors affecting and industrial uses. Crit. Rev. Food Sci. Nutr. 44: 465-471.
    Pubmed CrossRef
  26. Hong SM, Park JK, Lee YO. 2004. Mechanisms of microwave irradiation involved in the destruction of fecal coliforms from biosolids. Water Res. 38: 1615-1625.
    Pubmed CrossRef
  27. Dreyfuss MS, Chipley JR. 1980. Comparison of effects of sublethal microwave radiation and conventional heating on the metabolic activity of Staphylococcus aureus. Appl. Environ. Microbiol. 39: 13-16.
    Pubmed PMC
  28. Kim SY, Jo EK, Kim HJ, Bai K, Park JK. 2008. The e ffects of high-power microwaves on the ultrastructure of Bacillus subtilis. Lett. Appl. Microbiol. 47: 35-40.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(7): 1209-1215

Published online July 28, 2017 https://doi.org/10.4014/jmb.1702.02009

Copyright © The Korean Society for Microbiology and Biotechnology.

Effective Thermal Inactivation of the Spores of Bacillus cereus Biofilms Using Microwave

Hyong Seok Park 1, Jungwoo Yang 1, Hee Jung Choi 2 and Kyoung Heon Kim 1*

1Department of Biotechnology, Graduate School, Korea University, Seoul 02841, Republic of Korea, 2Department of Internal Medicine, Division of Infectious Diseases, Ewha Womans University School of Medicine, Seoul 07985, Republic of Korea

Received: February 6, 2017; Accepted: April 10, 2017

Abstract

Microwave sterilization was performed to inactivate the spores of biofilms of Bacillus cereus
involved in foodborne illness. The sterilization conditions, such as the amount of water and
the operating temperature and treatment time, were optimized using statistical analysis based
on 15 runs of experimental results designed by the Box-Behnken method. Statistical analysis
showed that the optimal conditions for the inactivation of B. cereus biofilms were 14 ml of
water, 108°C of temperature, and 15 min of treatment time. Interestingly, response surface
plots showed that the amount of water is the most important factor for microwave sterilization
under the present conditions. Complete inactivation by microwaves was achieved in 5 min,
and the inactivation efficiency by microwave was obviously higher than that by conventional
steam autoclave. Finally, confocal laser scanning microscopy images showed that the principal
effect of microwave treatment was cell membrane disruption. Thus, this study can contribute
to the development of a process to control food-associated pathogens.

Keywords: Bacillus cereus, biofilms, microwave, inactivation, response surface methodology

References

  1. Drobniewski FA. 1993. Bacillus cereus and related species. Clin. Microbiol. Rev. 6: 324-338.
    Pubmed KoreaMed CrossRef
  2. Anderson A, Ronner U, Granum PE. 1995. What problems does the food industry have with the spore-forming pathogens Bacillus cereus and Clostridium perfringens? Int. J. Food Microbiol. 28: 145-155.
    CrossRef
  3. Gao YL, Jiang HH. 2005. Optimization of process conditions to inactivate Bacillus subtilis by high hydrostatic pressure and mild heat using response surface methodology. Biochem. Eng. J. 24: 43-48.
    CrossRef
  4. Head DS, Cenkowski S, Holley R, Blank G. 2008. Effects of superheated steam on Geobacillus stearothermophilus spore viability. J. Appl. Microbiol. 104: 1213-1220.
    Pubmed CrossRef
  5. Setlow B, Loshon CA, Genest PC, Cowan AE, Setlow C, Setlow P. 2002. Mechanisms of killing spores of Bacillus subtilis by acid, alkali and ethanol. J. Appl. Microbiol. 92: 362-375.
    Pubmed CrossRef
  6. Elhariry HM. 2011. Attachment strength and biofilm forming ability of Bacillus cereus on green-leafy vegetables:cabbage and lettuce. Food Microbiol. 28: 1266-1274.
    Pubmed CrossRef
  7. Peng JS, Tsai WC, Chou CC. 2002. Inactivation and removal of Bacillus cereus by sanitizer and detergent. Int. J. Food Microbiol. 77: 11-18.
    CrossRef
  8. Flemming HC, Wingender J. 2001. Relevance of microbial extracellular polymeric substance (EPS) – Part I: Structural and ecological aspects. Water Sci. Technol. 43: 1-8.
    Pubmed
  9. Bridier A, Briandet R, Thomas V, Dubois-Brissonnet F. 2011. Resistance of bacterial biofilms to disinfectants: a review. Biofouling 27: 1017-1032.
    Pubmed CrossRef
  10. Kumar CG, Anand SK. 1998. Significance of microbial biofilms in food industry: a review. Int. J. Food Microbiol. 42: 9-27.
    CrossRef
  11. Kreske AC, Ryu JH, Pettigrew CA, Beuchat LR. 2006. 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. J. Food Prot. 69: 2621-2634.
    Pubmed CrossRef
  12. Park HS, Choi HJ, Kim MD, Kim KH. 2013. Addition of ethanol to supercritical carbon dioxide enhances the inactivation of bacterial spores in the biofilm of Bacillus cereus. Int. J. Food Microbiol. 166: 207-212.
    Pubmed CrossRef
  13. Senna PM, Da Silva WJ, Del Bel Cury AA. 2010. Denture disinfection by microwave energy: influence of Candida albicans biofilm. Gerodontology 29: e186-e191.
    Pubmed CrossRef
  14. Gibson H, Taylor JH, Hall KE, Holah JT. 1999. Effectiveness of cleaning techniques used in the food industry in terms of the removal of bacterial biofilms. J. Appl. Microbiol. 87: 41-48.
    Pubmed CrossRef
  15. Woo I, Rhee I, Park H. 2000. Differential damage in bacterial cells by microwave radiation on the basis of cell wall structure. Appl. Environ. Microbiol. 66: 2243-2247.
    Pubmed KoreaMed CrossRef
  16. Celandroni F, Longo I, Tosoratti N, Giannessi F, Ghelardi E, Salvetti S, et al. 2004. Effect of microwave radiation on Bacillus subtilis spores. J. Appl. Microbiol. 97: 1220-1227.
    Pubmed CrossRef
  17. Kim SY, Shin SJ, Song CH, Jo EK, Kim HJ, Park JK. 2009. Destruction of Bacillus licheniformis spores by microwave irradiation. J. Appl. Microbiol. 106: 877-885.
    Pubmed CrossRef
  18. Welt BA, Tong CH, Rossen JL, Lund DB. 1994. Effect of microwave radiation on inactivation of Clostridium sporogenes (PA 3679) spores. Appl. Environ. Microbiol. 60: 482-488.
    Pubmed KoreaMed
  19. Zieli ski M, Ciesielski S, Cydzik-Kwiatkowska A, Turek J, Dębowski M. 2007. Influence of microwave radiation on bacterial community structure in biofilm. Process Biochem. 42: 1250-1253.
  20. Fernández M, Sánchez J. 2002. Nuclease activities and cell death processes associated with the development of surface cultures of Streptomyces antibioticus ETH 7451. Microbiology 148: 405-412.
    Pubmed CrossRef
  21. Myers RH, Montgomery DC. 1995. Response Surface Methodology:Process and Product Optimization Using Designed Experiments. John Wiley & Sons Inc., New York. USA.
  22. Vela GR, Wu JF. 1979. Mechanism of lethal action of 2,450MHz radiation on microorganisms. Appl. Environ. Microbiol. 37: 550-553.
    Pubmed KoreaMed
  23. Jeng DK, Kaczmarek KA, Woodworth AG, Balasky G. 1987. Mechanism of microwave sterilization in the dry state. Appl. Environ. Microbiol. 53: 2133-2137.
    Pubmed KoreaMed
  24. Ponne CT, Bartels PV. 1995. Interaction of electromagnetic energy with biological material - relation to food processing. Radiat. Phys. Chem. 45: 591-607.
    CrossRef
  25. Içier F, Baysal T. 2004. Dielectrical properties of food materials-1: factors affecting and industrial uses. Crit. Rev. Food Sci. Nutr. 44: 465-471.
    Pubmed CrossRef
  26. Hong SM, Park JK, Lee YO. 2004. Mechanisms of microwave irradiation involved in the destruction of fecal coliforms from biosolids. Water Res. 38: 1615-1625.
    Pubmed CrossRef
  27. Dreyfuss MS, Chipley JR. 1980. Comparison of effects of sublethal microwave radiation and conventional heating on the metabolic activity of Staphylococcus aureus. Appl. Environ. Microbiol. 39: 13-16.
    Pubmed KoreaMed
  28. Kim SY, Jo EK, Kim HJ, Bai K, Park JK. 2008. The e ffects of high-power microwaves on the ultrastructure of Bacillus subtilis. Lett. Appl. Microbiol. 47: 35-40.
    Pubmed CrossRef