Efficacy of chemical sanitizers against Bacillus cereus on food contact surfaces with scratch and biofilm

  • Hyochin Kim
  • Min Ji Moon
  • Choon Young Kim
  • Kyung RyuEmail author


This study was performed to investigate the efficacy of chemical sanitizers (viz., chlorine, chlorine dioxide, alcohol, and quaternary ammonium compound) against Bacillus cereus on five food contact materials under different conditions (smooth vs. scratched and with vs. without biofilms). After incubating materials in B. cereus suspension, cell adhesion on a smooth surface (10 cm2) was in the following ascending order: stainless steel (7.36 ± 0.08 log CFU), glass (7.51 ± 0.26 log CFU), polyethylene (7.66 ± 0.30 log CFU), polypropylene (7.76 ± 0.30 log CFU), and wood (8.02 ± 0.33 log CFU). The efficacy of sanitizers was dramatically reduced in the presence of a biofilm on all materials. Among four different chemical sanitizers, chlorine showed the best bactericidal activity against B. cereus on the surface with scratch and biofilm. Selection of adequate materials, maintenance of a smooth surface, and inhibition of biofilm formation are good practices for food safety.


Bacillus cereus Biofilm Food contact surface Sanitizing efficacy Scratched surface 



The field emission-scanning electron microscopy




The Korea Ministry of Food and Drug Safety






Relative humidity


Stainless steel


Tryptic soy agar


Tryptic soy broth


Quaternary ammonium compound


  1. Adetunji, V.O. and Isola, T.O. 2011. Crystal violet binding assay for assessment of biofilm formation by Listeria monocytogenes and Listeria spp on wood, steel and glass surfaces. Glob. Vet. 6(1): 6–10.Google Scholar
  2. Andersson, A., Granum, P.E. and Rönner, U. 1998. The adhesion of Bacillus cereus spores to epithelial cells might be an additional virulence mechanism. Int. J. Food Microbiol. 39: 93–99.CrossRefGoogle Scholar
  3. Araújo, E.A., Bernardes, P.C., Andrade, N.J., Fernandes, P.E. and Sá, J.P.N. 2009. Gibbs free energy of adhesion of Bacillus cereus isolated from dairy plants on different food processing surfaces evaluated by the hydrophobicity. Int. J. Food Sci. Technol. 44: 2519–2525.CrossRefGoogle Scholar
  4. Bae, Y.-M., Baek, S.-Y. and Lee, S.-Y. 2012. Resistance of pathogenic bacteria on the surface of stainless steel depending on attachment form and efficacy of chemical sanitizers. Int. J. Food Microbiol. 153: 465–473.CrossRefGoogle Scholar
  5. Bae, Y.-M. and Lee, S.-Y. 2012. Inhibitory effects of UV treatment and a combination of UV and dry heat against pathogens on stainless steel and polypropylene surfaces. J. Food Sci. 77(1): M61–M64.CrossRefGoogle Scholar
  6. Bernardes, P.C., Andrade, N.J.D., Ferreira, S.O., Sá, J.P.N.D, Araújo, E.A., Delatorre, D.M.Z. and Luiz, L.M.P. 2010. Assessment of hydrophobicity and roughness of stainless steel adhered by an isolate of Bacillus cereus from a dairy plant. Braz. J. Microbiol. 41: 984–992.Google Scholar
  7. Boulané-Petermann, L. 1996. Processes of bioadhesion on stainless steel surfaces and cleanability: a review with special reference to the food industry. Biofouling 10: 275–300.CrossRefGoogle Scholar
  8. Brooks. J.D. and Flint, S.H. 2008. Biofilms in the food industry: problems and potential solutions. Int. J. Food Sci. Technol. 43: 2163–2176.CrossRefGoogle Scholar
  9. Chaturongkasumrit, Y., Takahashi, H., Keeratipibul, S., Kuda, T. and Kimura, B. 2011. The effect of polyesterurethane belt surface roughness on Listeria monocytogenes biofilm formation and its cleaning efficiency. Food Control 22: 1893–1899.CrossRefGoogle Scholar
  10. Di Ciccio, P., Vergara, A., Festino, A.R., Paludi, D., Zanardi, E., Ghidini, S. and Ianieri, A. 2015. Biofilm formation by Staphylococcus aureus on food contact surfaces: Relationship with temperature and cell surface hydrophobicity. Food Control 50: 930–936.CrossRefGoogle Scholar
  11. Ehling-Schulz, M., Fricker, M. and Scherer, S. 2004. Identification of emetic toxin producing Bacillus cereus strains by a novel molecular assay. FEMS Microbiol. Lett. 232: 189–195.CrossRefGoogle Scholar
  12. Faille, C., Lebret, V., Gavini, F. and Maingonnat, J.-F. 1997. Injury and lethality of heat treatment of Bacillus cereus spores suspended in buffer and in poultry meat. J. Food Prot. 60: 544–547.CrossRefGoogle Scholar
  13. Felske, A. 2004. Ecology of Bacillus species in soil. Bacterial spore formers-probiotics and emerging applications. Horizon. Biosci. Norfolk 35–44.Google Scholar
  14. Fernandes, P.E., Sao Jose, J.F.B., Zerdas, E.R.M.A., Andrade, N.J., Fernandes, C.M. and Silva, L.D. 2014. Influence of the hydrophobicity and surface roughness of mangoes and tomatoes on the adhesion of Salmonella enterica serovar Typhimurium and evaluation of cleaning procedures using surfactin. Food Control 41: 21–26.CrossRefGoogle Scholar
  15. Frank, J.F. 2001. Microbial attachment to food and food contact surfaces. Adv. Food Nutr. Res. 43: 319–370.CrossRefGoogle Scholar
  16. Giaouris, E., Heir, E., Hébraud, M., Chorianopoulos, N., Langsrud, S., Møretrø, T., Habimana, O., Desvaux, M., Renier, S. and Nychas, G.-J. 2014. Attachment and biofilm formation by foodborne bacteria in meat processing environments: causes, implications, role of bacterial interactions and control by alternative novel methods. Meat. Sci. 97: 298–309.CrossRefGoogle Scholar
  17. Granum, P,E. 1994. Bacillus cereus and its toxins. J. Appl. Microbiol. 76. CrossRefGoogle Scholar
  18. Hilbert, L.R., Bagge-Ravn, D.B., Kold, J. and Gram, L. 2003. Influence of surface roughness of stainless steel on microbial adhesion and corrosion resistance. Int. Biodeterior. Biodegrad. 52: 175–185.CrossRefGoogle Scholar
  19. Jahid, I.K. and Ha, S.-D. 2012. A review of microbial biofilms of produce: future challenge to food safety. Food Sci. Biotechnol. 21: 299–316.CrossRefGoogle Scholar
  20. Joseph, B., Otta, S., Karunasagar, I. and Karunasagar, I. 2001. Biofilm formation by Salmonella spp. on food contact surfaces and their sensitivity to sanitizers. Int. J. Food Microbiol. 64: 367–372.CrossRefGoogle Scholar
  21. Jullien, C., Bénézech, T., Carpentier, B., Lebret, V. and Faille, C. 2003. Identification of surface characteristics relevant to the hygienic status of stainless steel for the food industry. J. Food Eng. 56: 77–87.CrossRefGoogle Scholar
  22. Kim, C.Y., Ryu, G.J., Park, H.Y. and Ryu, K. 2017. Resistance of Staphylococcus aureus on food contact surfaces with different surface characteristics to chemical sanitizers. J. Food Safe. Google Scholar
  23. Kim, H., Ryu, J.-H. and Beuchat, L.R. 2007. Effectiveness of disinfectants in killing Enterobacter sakazakii in suspension, dried on the surface of stainless steel, and in a biofilm. Appl. Environ. Microbiol. 73(4): 1256–1265.CrossRefGoogle Scholar
  24. Kim, H.-I., Jeon, D.-H., Yoon, H.-J., Choi, H.-C., Eom, M.-O., Sung, J.-H., Park, N.-Y., Won, S.-A., Kim, N.-Y. and Lee, Y.-J. 2008. Evaluation of the efficacy of sanitizers on food contact surfaces using a surface test method. J. Food Hyg. Safe. 23: 291–296.Google Scholar
  25. Korea Ministry of Food and Drug Safety. 2017. Adapted standard and specifications regarding foods in limited time, Noticifcation No. 2017-36.Google Scholar
  26. Kotiranta, A., Lounatmaa, K. and Haapasalo, M. 2000. Epidemiology and pathogenesis of Bacillus cereus infections. Microbes Infect. 2: 189–198.CrossRefGoogle Scholar
  27. Kramer, J., Gilbert, R. and Doyle, M. 1989. Foodborne bacterial pathogens ( Ed. M.P. Doyle), Marcel Dekker, Inc., New York and Basel. pp 22–70.Google Scholar
  28. Lee, Y.-.D, Yoo, H.-L. and Park, J.-H. 2013. Biocontrol of biofilm-forming Bacillus cereus by using organic acid, ethanol, and sodium chloride. Korean J. Food Sci. Technol. 45: 120–125.CrossRefGoogle Scholar
  29. Lomander, A., Schreuders, P., Russek-Cohen, E and Ali, L. 2004. Evaluation of chlorines’ impact on biofilms on scratched stainless steel surfaces. Bioresour. Technol. 94: 275–283.CrossRefGoogle Scholar
  30. Moltz, A.G. and Martin, S.E. 2005. Formation of biofilms by Listeria monocytogenes under various growth conditions. J. Food Prot. 68: 92–97.CrossRefGoogle Scholar
  31. Monk, I.R., Cook, G.M., Monk, B.C. and Bremer, P.J. 2004. Morphotypic conversion in Listeria monocytogenes biofilm formation: biological significance of rough colony isolates. Appl. Environ. Microbiol. 70: 6686–6694.CrossRefGoogle Scholar
  32. Pan, T.-M., Wang, T.-K., Lee, C.-L., Chien, S.-W. and Horng, C.-B. 1997. Food-borne disease outbreaks due to bacteria in Taiwan, 1986 to 1995. J. Clin. Microbiol. 35: 1260–1262.PubMedPubMedCentralGoogle Scholar
  33. Peng, J.-S., Tsai, W.-C. and Chou, C.-C. 2002. Inactivation and removal of Bacillus cereus by sanitizer and detergent. Int. J Food Microbiol. 77: 11–18.CrossRefGoogle Scholar
  34. Ren, T.-J. and Frank, J.F. 1993. Susceptibility of starved planktonic and biofilm Listeria monocytogenes to quaternary ammonium sanitizer as determined by direct viable and agar plate counts. J. Food Prot. 56: 573–576.CrossRefGoogle Scholar
  35. Ryu, J.-H. and Beuchat, L.R. 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.CrossRefGoogle Scholar
  36. Tauveron, G., Slomianny, C., Henry, C. and Faille, C. 2006. Variability among Bacillus cereus strains in spore surface properties and influence on their ability to contaminate food surface equipment. Int. J. Food. Microbiol. 110: 254–262.CrossRefGoogle Scholar
  37. Van Loosdrecht, M., Lyklema, J., Norde, W., Schraa, G. and Zehnder, A. 1987. The role of bacterial cell wall hydrophobicity in adhesion. Appl. Environ. Microbiol. 53: 1893–1897.PubMedPubMedCentralGoogle Scholar
  38. Zhang, X., Wang, L. and Levänen, E. 2013. Superhydrophobic surfaces for the reduction of bacterial adhesion. RSC Adv. 3: 12003–12020.CrossRefGoogle Scholar

Copyright information

© The Korean Society of Food Science and Technology and Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Hyochin Kim
    • 1
  • Min Ji Moon
    • 2
  • Choon Young Kim
    • 2
  • Kyung Ryu
    • 2
    Email author
  1. 1.Imported Food Analysis DivisionSeoul Regional Office, Ministry of Food and Drug SafetySeoulSouth Korea
  2. 2.Department of Food and NutritionYeungnam UniversityGyeongsanSouth Korea

Personalised recommendations