Skip to main content
SpringerLink
Log in

Inactivation of Escherichia coli O157:H7 by ozone in different substrates

  • Food Microbiology - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Ozone has a broad antimicrobial spectrum and each microorganism species has inherent sensitivity to the gas. The objective of this study was to evaluate the effect of ozone gas on Escherichia coli O157:H7 inoculated on an organic substrate, and the efficacy of ozonated water in controlling the pathogen. For the first experiment, E. coli O157:H7 (ATCC® 43890™) was inoculated in milk with different compositions and in water, which was ozonated at concentrations of 35 and 45 mg L−1 for 0, 5, 15, and 25 min. In the second experiment, water was ozonated at 45 mg L−1 for 15 min. E. coli O157:H7 was exposed for 5 min to the ozonated water immediately after ozonation, and after storage for 0.5, 1.0, 1.5, 3.0, and 24 h at 8 °C. The results showed that the composition of the organic substrate interfered with the action of ozone on E. coli O157:H7. In lactose-free homogenized skim milk, reductions of 1.5 log cycles were obtained for ozonation periods of 25 min at the concentrations tested. Ozonated water was effective in inactivating of E. coli O157:H7 in all treatments. The efficiency of ozone on E. coli O157:H7 is influenced by the composition of the organic substrates, reinforcing the need for adequate removal of organic matter before sanitization. Furthermore, refrigerated ozonated water stored for up to 24 h is effective in the control of E. coli O157:H7.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Franco BD, Landgraf M (2008) Microbiologia dos alimentos, 2nd edn. Atheneu, São Paulo

    Google Scholar 

  2. Davidson PM, Branen AL (2005) Food antimicrobials – an introduction. In: Davidson PM, Sofos JN, Branen AL (eds) Antimicrobials in food. CRC Press, Boca Raton, pp 1–10

    Chapter  Google Scholar 

  3. Campos LC, Trabulsi LR (2002) Escherichia. In: Trabulsi LR, Alterthum F, Gompertz OF, Candeias JAN (eds) Microbiologia. Atheneu, São Paulo, pp 215–228

    Google Scholar 

  4. Chernaki-Leffer AM, Biesdorf SM, Almeida LM, Leffer EV, Vigne F (2002) Isolamento de enterobactérias em Alphitobius diaperinus e na cama de aviários no oeste do estado do Paraná, Brasil. Rev Bras Cienc Avic 4:243–247

    Article  Google Scholar 

  5. Blanco M, Blanco JE, Mora A, Rey J, Alonso JM, Hermoso M, Hermoso J, Alonso MP, Dahbi G, Gonzalez EA, Bernardez MI, Blanco J (2003) Serotypes, virulence genes, and intimin types of Shiga toxin (verotoxin)-producing Escherichia coli isolates from healthy sheep in Spain. J Clin Microbiol 41:1351–1356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Pianciola L, Chinen I, Mazzeo M, Miliwebsky E, González G, Muller C (2014) Genotypic characterization of Escherichia coli O157:H7 strains that cause diarrhea and hemolytic uremic syndrome in Neuquén, Argentina. J Med Microbiol 304:499–504

    Article  CAS  Google Scholar 

  7. CDC – Centers for Disease Control and Prevention (2014) Multistate outbreak of Shiga toxin-producing Escherichia coli O157:H7 infections linked to ground beef (final update). http://www.cdc.gov/ecoli/2014/O157H7-05-14/index.html/. Accessed 20 Dec 2015

  8. Lund BM, O'Brien SJ (2009) Microbiological safety of food in hospitals and other healthcare settings. J Hosp Infect 73:109–120

    Article  PubMed  Google Scholar 

  9. Feng P, Weagant SD, Jinneman K (2011) BAM: diarrheagenic Escherichia coli. http://www.fda.gov/Food/FoodScienceResearch/LaboratoryMethods/ucm070080.htm/. Accessed 10 Nov 2015

  10. Liu Y, Gill A, McMullen L, Ganzle MG (2015) Variation in heat and pressure resistance of verotoxigenic and nontoxigenic Escherichia coli. J Food Prot 78:111–120

    Article  CAS  PubMed  Google Scholar 

  11. Nascimento MS, Silva N, Catanozi MP, Silva KC (2003) Effects of different disinfection treatments on the natural microbiota of lettuce. J Food Prot 66:1697–1700

    Article  CAS  PubMed  Google Scholar 

  12. Chen Y, Wang H, Xu Y, Wu J, Xiao G (2013) Effect of treatment with dimethyl dicarbonate on microorganisms and quality of chinese cabbage. Postharvest Biol Technol 76:139–144

    Article  CAS  Google Scholar 

  13. Selma MV, Ibaneza AM, Allende A, Cantwella M, Suslow T (2008) Effect of gaseous ozone and hot water on microbial and sensory quality of cantaloupe and potential transference of Escherichia coli O157:H7 during cutting. Food Microbiol 25:162–168

    Article  CAS  PubMed  Google Scholar 

  14. Shen C, Luo Y, Nan X et al (2012) Enhanced inactivation of Salmonella and Pseudomonas biofilms on stainless steel by use of t-128, a fresh-produce washing aid, in chlorinated wash solutions. Appl Environ Microbiol 78:6789–6798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Alvaro JE, Moreno S, Dianez F, Santos M, Carrasco G, Urrestarazu M (2009) Effects of peracetic acid disinfectant on the postharvest of some fresh vegetables. J Food Eng 95:11–15

    Article  CAS  Google Scholar 

  16. Rahman SM, Jin YG, Oh DH (2011) Combination treatment of alkaline electrolyzed water and citric acid with mild heat to ensure microbial safety, shelf-life and sensory quality of shredded carrots. Food Microbiol 28:484–491

    Article  CAS  PubMed  Google Scholar 

  17. Cavalcante DA, Leite Júnior BR, Tribst AA, Cristianini M (2014) Inativação de Escherichia coli O157:H7 e Bacillus subtilis por água ozonizada. B Cent Pesqui Proc 32:105–112

    Google Scholar 

  18. Cavalcante DA, Leite Júnior BR, Tribst AA, Cristianini M (2015) Vida de prateleira de alface americana tratada com água ozonizada. Cienc Rural 45:2089–2096

    Article  Google Scholar 

  19. FDA - Food and Drug Administration (2001) Secondary direct food additives permitted in food for human consumption. https://www.gpo.gov/fdsys/pkg/FR-2001-06-26/html/01-15963.htm/. Accessed 20 June 2018

  20. Guzel-Seydim Z, Greene AK, Seydim AC (2004) Use of ozone in the food industry. Food Sci Technol 37:453–460

    CAS  Google Scholar 

  21. Cullen PJ, Tiwari BK, O'Donnell CP, Muthukumarappan K (2009) Modelling approaches to ozone processing of liquid foods. Trends Food Sci Technol 20:125–136

    Article  CAS  Google Scholar 

  22. Kim J, Yousef AE, Dave S (1999) Application of ozone for enhancing the microbiological safety and quality of foods: a review. J Food Prot 62:1071–1087

    Article  CAS  PubMed  Google Scholar 

  23. Clescerl LS, Greenberg AE, Eaton AD (1999) Standard methods for the examination of water and wastewater, 20th edn. American Water Works Association, Denver

    Google Scholar 

  24. Couto EP, Alencar ER, Gonçalves VSP, Santos AJ, Ribeiro JL, Ferreira M (2016) Effect of ozonation on the Staphylococcus aureus innoculated in milk. Semina Cienc Agrar 37:1911–1918

    Article  Google Scholar 

  25. Khadre M, Yousef AE, Kim J (2001) Microbiological aspects of ozone applications in food: a review. J Food Sci 66:1242–1252

    Article  CAS  Google Scholar 

  26. Alwi NA, Ali A (2014) Reduction of Escherichia coli O157, Listeria monocytogenes and Salmonella enterica sv. Typhimurium populations on fresh-cut bell pepper using gaseous ozone. Food Control 46:304–311

    Article  Google Scholar 

  27. Sung HJ, Song WJ, Kim KP, Ryu S, Kang DH (2014) Combination effect of ozone and heat treatments for the inactivation of Escherichia coli O157:H7, Salmonella typhimurium, and Listeria monocytogenes in apple juice. J Food Microbiol 171:147–153

    Article  CAS  Google Scholar 

  28. Sanchez BA, Alencar ER, Pineli LL, Ferreira WF, Roberto MA (2016) Tracing interactions among column height, exposure time and gas concentration to dimension peanut antifungal ozonation. Food Sci Technol 65:668–675

    CAS  Google Scholar 

  29. Manousaridis G, Nerantzaki A, Paleologos EK, Tsiotsias A, Savvaidis IN, Kontominas MG (2005) Effect of ozone on microbial, chemical and sensory attributes of shucked mussels. Food Microbiol 22:1–9

    Article  CAS  Google Scholar 

  30. Restaino L, Frampton E, Hemphill J, Palnikar P (1995) Efficacy of ozonated water against various food-related microorganisms. Appl Environ Microbiol 61:3471–3475

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Güzel-Seydim Z, Bever PI, Greene AK (2004) Efficacy of ozone to reduce bacterial populations in the presence of food components. Food Microbiol 21:475–479

    Article  CAS  Google Scholar 

  32. Choi MR, Liu Q, Lee SY, Jin JH, Ryu S, Kang DH (2012) Inactivation of Escherichia coli O157:H7, Salmonella typhimurium and Listeria monocytogenes in apple juice with gaseous ozone. Food Microbiol 32:191–195

    Article  CAS  PubMed  Google Scholar 

  33. Beltrán FJ (2005) Ozone reaction kinetics for water and wastewater systems, 1st edn. CRC Press, Boca Raton

    Google Scholar 

  34. Berton A, Rouvellac S, Robert B, Rousseau F, Lopez C, Cremon I (2012) Effect of the size and interface composition of milk fat globules on their in vitro digestion by the human pancreatic lipase: native versus homogenized milk fat globules. Food Hydrocoll 29:123–134

    Article  CAS  Google Scholar 

  35. Graves E, Beaulieu A, Drackley J (2007) Factors affecting the concentration of sphingomyelin in bovine milk. J Dairy Sci 90:706–715

    Article  CAS  PubMed  Google Scholar 

  36. Mari M, Bertolini P, Pratella G (2003) Non-conventional methods for the control of post-harvest pear diseases. J Appl Microbiol 94:761–766

    Article  CAS  PubMed  Google Scholar 

  37. Beltrán D, Selma MV, Alicia M, Gil MI (2005) Ozonated water extends the shelf life of fresh-cut lettuce. J Agric Food Chem 53:5654–5663

    Article  CAS  PubMed  Google Scholar 

  38. Inatsu Y, Kitagawa T, Nakamura N, Kawasaki S (2013) Effectiveness of stable ozone microbubble containing water on reducing bacteria load on selected leafy vegetables. Acta Hortic (989):161–166

  39. Tachikawa M, Yamanaka K, Nakamuro K (2009) Studies on the disinfection and removal of biofilms by ozone water using an artificial microbial biofilm system. Ozone Sci Eng 31:3–9

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. College of Agronomy and Veterinary, University of Brasilia, Brasilia, DF, CEP: 70910-900, Brazil

    Stefania Marcia de Oliveira Souza, Ernandes Rodrigues de Alencar, Jaqueline Lamounier Ribeiro & Marcia de Aguiar Ferreira

Authors
  1. Stefania Marcia de Oliveira Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ernandes Rodrigues de Alencar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jaqueline Lamounier Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marcia de Aguiar Ferreira
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ernandes Rodrigues de Alencar.

Ethics declarations

Conflicts of interest

The authors declare that they have no conflicts of interest.

Additional information

Responsible Editor: Luis Augusto Nero

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Oliveira Souza, S.M., de Alencar, E.R., Ribeiro, J.L. et al. Inactivation of Escherichia coli O157:H7 by ozone in different substrates. Braz J Microbiol 50, 247–253 (2019). https://doi.org/10.1007/s42770-018-0025-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-018-0025-2

Keywords

Search

Navigation