Skip to main content
Log in

Modeling of Listeria innocua, Escherichia coli, and Salmonella Enteritidis inactivation in milk treated by gamma irradiation

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

Abstract

Measuring microbial inactivation in food is useful for food technology as it allows for predicting the growth or death of microorganisms. This study aimed to investigate the effect of gamma irradiation on the lethality of microorganisms inoculated in milk, estimate the mathematical model of inactivation of each microorganism, and evaluate kinetic indices to determine the efficient dose in the treatment of milk. Raw milk samples were inoculated with cultures of Salmonella enterica subsp. enterica serovar Enteritidis (ATCC 13076), Escherichia coli (ATCC 8739), and Listeria innocua (ATCC 3309), irradiated at doses of 0, 0.5, 1, 1.5, 2, 2.5, and 3 kGy. The fitting of the models to the microbial inactivation data was performed using the GinaFIT software. The results demonstrated a significant effect of irradiation doses on the population of microorganisms, with the application of a dose of 3 kGy, a reduction of approximately 6 logarithmic cycles is observed for L. innocua and 5 for S. Enteritidis and E. coli. The model with the best fit was different for each microorganism studied: for L. innocua, the model was log-linear + shoulder; for S. Enteritidis and E. coli, the model that showed the best fit was the biphasic. The studied model fitted well (R2 ≥ 0.9; R2 adj. ≥ 0.9 and smallest RMSE values) for the inactivation kinetics. The lethality of the treatment, considering a reduction in the 4D value, was achieved with the predicted dose of doses of ±2.22, ±2.10, and ±1.77 kGy, for L. innocua, S. Enteritidis, and E. coli, respectively.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Code Availability

Not applicable.

References

  1. Menezes MFC, Simeoni CP, Etchepare MA, Katira Huerta K, Bortoluzzi DP, Menezes CR (2014) Microbiota e conservação do leite. Rev do Cent de Ciências Nat e Ex 18:76–89. https://doi.org/10.5902/2236117013033

    Article  Google Scholar 

  2. Leite JR, Torrano ADM, Gelli DS (2000) Qualidade microbiológica do leite tipo C pasteurizado, comercializado em João Pessoa, Paraíba. Rev Hig Alim 74:45–49

    Google Scholar 

  3. Timm CD, Dias C, Gonzalez HL, Oliveira DS, Büchle J, Alexis MA, Coelho FJO, Porto C (2003) Avaliação da qualidade microbiológica do leite pasteurizado integral, produzido em micro-usinas da região sul do Rio Grande do Sul. Revista Higiene Alimentar 17:100–104

    Google Scholar 

  4. CODEX ALIMENTARIUS COMISSION. Definition of “Pasteurization” - Section 2.9 of the Recommended International Code of Hygienic Practice for Dried Milk. chrome-extension://efaidnbmnnnibpcajpcglclefindmkaj/https://www.fao.org/fao-who-codexalimentarius/sh-proxy/de/?lnk=1&url=https%253A%252F%252Fworkspace.fao.org%252Fsites%252Fcodex%252FMeetings%252FCX-712-23%252Fal89_13e.pdf. Accessed 20 Dec 2021

  5. Smith JS, Pillai S (2004) Irradiation and food safety. Food Technol Mag 58:45–55. https://www.ift.org/newsandpublications/foodtechnologymagazine/issues/2004/november/features/irradiation-and-food-safety. Accessed 10 Dec 2021

  6. Satin M (2002) Use of irradiation for microbial decontamination of meat: Situation and perspectives. Meat Sci 62:277–283. https://doi.org/10.1016/S0309-1740(02)00129-8

    Article  PubMed  Google Scholar 

  7. Mcmeekin T, Olley J, Ross T, Ratkowsky D (1993) Predictive microbiology: theory and application. Research Studies Press Ltd, Taunton, UK, pp 11–84

    Google Scholar 

  8. Dannenhauer CE (2010) Desenvolvimento de um aplicativo computacional para microbiologia preditiva. Universidade Federal de Santa Catarina, Dissertação

    Google Scholar 

  9. Coll Cárdenas F, Giannuzzi L, Noia MA, Zaritzky N (2001) El modelado matemático: Una herramienta útil para la industria alimenticia. Facultad de Ciencias Veterinarias. https://www.semanticscholar.org/paper/Elmodeladomatem%C3%A1tico%3Aunaherramienta%C3%BAtilparaC%C3%A1rdenasGiannuzzi/479553dc9d9a2abe4233c617c6cbb1824b0b33ea. Accessed 2 Dec 2021

  10. Alves CCDC (2010) Comportamento da Escherichia coli em queijo Minas Frescal elaborado com utilização de Lactobacillus acidophilus e de acidificação direta. Dissertação, Universidade Federal Fluminense, Niterói. https://higieneveterinaria.uff.br/wp-content/uploads/sites/270/2020/08/Clara_Calil.pdf. Accessed 2 Dec 2021

  11. Torquato FPL (2007) Sensibilidade de Escherichia coli, Salmonella typhimurium, Staphylococcus aureus e Pseudomonas aeruginosa à desinfecção com luz natural e artificial: avaliação da capacidade de reativação bacteriana. Universidade Federal de Campina Grande, Dissertação

    Google Scholar 

  12. Geeraerd AH, Valdramidis VP, Van Impe JF (2005) GInaFIT, a freeware tool to assess non-log-linear microbial survivor curves. Int J of Food Microbiol 102:95–105. https://doi.org/10.1016/j.ijfoodmicro.2004.11.038

    Article  CAS  Google Scholar 

  13. Souza PM (2012) Study of short-wave ultraviolet treatments (UV-C) as a non-thermal preservation process for liquid egg products. Doctoral Thesis, Instituto de Agroquímica y Tecnología de Alimentos, Valencia

    Google Scholar 

  14. Mcclure PJ, Blackburn C, Cole W et al (1994) Modelling the growth, survival and death of microorganisms in foods: the UK Food MicroModel Approach. Int J of Food Microbiol 23:265–275. https://doi.org/10.1016/0168-1605(94)90156-2

    Article  CAS  Google Scholar 

  15. Ross T (1996) Indices for performance evaluation of predictive models in food microbiology. J of Appl Bacteriol 81:501–508. https://doi.org/10.1111/j.1365-2672.1996.tb03539.x

    Article  CAS  Google Scholar 

  16. Possas A, Valero A, García-Gimeno RM, Pérez-Rodríguez F, Souza PM (2018) Influence of temperature on the inactivation kinetics of Salmonella Enteritidis by the application of UV-C technology in soymilk. Food Control 94:132–139. https://doi.org/10.1016/j.foodcont.2018.06.033

    Article  CAS  Google Scholar 

  17. Silva ACO (2008) Efeito da radiação gama sobre lipídios, microbiota contaminante e validade comercial do leite cru integral refrigerado e sobre características sensoriais do leite pasteurizado integral refrigerado. Universidade Federal Fluminense, Tese

    Google Scholar 

  18. Silva ACO, Oliveira ATO, Jesus EFOJ, Cortez MAS, Alves CCC, Monteiro MLG, Junior CAC (2015) Effect of gamma irradiation on the bacteriological and sensory analysis of raw whole milk under refrigeration. J of Food Process and Preserv 39:2404–2411. https://doi.org/10.1111/jfpp.12490

    Article  CAS  Google Scholar 

  19. Silva VAM, Rivas PM, Zanela MB et al (2010) Avaliação da qualidade físico-química e microbiológica do leite cru, do leite pasteurizado tipo A e de pontos de contaminação de uma Granja Leiteira no RS. Acta Scientiae Veterinariae 1:51–57

    Google Scholar 

  20. Neves MW, Carbonera N, Espírito Santo MLP (2012) Avaliação da qualidade do leite e seu processamento na produção de leite em pó associado a Análise de Perigos e Pontos Críticos de Controle. Rev Inst Adolfo Lutz 71(2):266–273

    Google Scholar 

  21. Souza PM (2007) Estudo comparativo da pasteurização de leite pelo método convencional e por microondas. Universidade Estadual de Campinas, Dissertação

    Google Scholar 

  22. Fellows PJ (2006) Tecnologia do processamento de alimentos: princípios e prática. Artmed, Porto Alegre

    Google Scholar 

  23. Franco BDGM, Landgraf M (1999) Microbiologia dos alimentos. Atheneu, São Paulo

    Google Scholar 

  24. Muller DC (2018) Avaliação das condições higiênico-sanitárias e multiplicação de Escherichia coli, Staphylococcus aureus e Bacillus cereus em sushis preparados em Porto Alegre. Trabalho de Conclusão de Curso, Universidade Federal do Rio Grande do Sul

    Google Scholar 

  25. Albert I, Mafart P (2005) A modified Weibull model for bacterial inactivation. Int J of Food Microbiol 100:197–211. https://doi.org/10.1016/j.ijfoodmicro.2004.10.016

    Article  CAS  Google Scholar 

  26. Inguglia ES, Tiwari BK, Kerry JP, Burgess CM (2018) Effects of high intensity ultrasound on the inactivation profiles of Escherichia coli K12 and Listeria innocua with salt and salt replacers. Ultrasonics Sonochem 48:492–498. https://doi.org/10.1016/j.ultsonch.2018.05.007

    Article  CAS  Google Scholar 

  27. Jantzen MM (2006) Listeria monocytogenes: detecção de células injuriadas por altas pressões e efeito de pré-enriquecimentos na PCR em tempo real. Universidade de Pelotas, Tese

    Google Scholar 

  28. Van der Waal Z (2017) GInaFiT—a user guide. Newcastle University

    Google Scholar 

  29. Sastry SK, Datta AK, Worobo RW (2000) Ultraviolet light. J Food Sci Suppl 65:90–92. https://doi.org/10.1111/j.1750-3841.2000.tb00623.x

    Article  Google Scholar 

  30. Preetha P, Varadharaju N, Kennedy J, Malathi D (2017) Modelling for the survival of Escherichia coli in tender coconut (Cocos nucifera l.) water by non-thermal pulsed light treatment. Madras Agricult J 104:10.29321/MAJ.04.000431

    Google Scholar 

  31. Mustapha AT, Zhou C, Amanor-Atiemoh R, Owusu-Fordjour M, Wahia H, Fakayode OA, Ma H (2020) Kinetic modeling of inactivation of natural microbiota and Escherichia coli on cherry tomato treated with fixed multi-frequency sonication. Ultrasonics Sonochem 64:105035. https://doi.org/10.1016/j.ultsonch.2020.105035

    Article  CAS  Google Scholar 

  32. Rodríguez-Chueca J, Ormad MP, Mosteo R, Ovelleiro JL (2015) Kinetic modeling of Escherichia coli and Enterococcus sp. inactivation in wastewater treatment by photo-Fenton and H2O2/UV–vis processes. Chem Eng Sci 138:730–740. https://doi.org/10.1016/j.ces.2015.08.051

    Article  CAS  Google Scholar 

  33. Corradini MG, Normand MD, Peleg M (2007) Modeling non-isothermal heat inactivation of microorganisms having biphasic isothermal survival curves. Int J Food Microbiol 116(3):391–399. https://doi.org/10.1016/j.ijfoodmicro.2007.02.004

    Article  CAS  PubMed  Google Scholar 

  34. Chun H, Kim J, Chung K, Won M, Song KB (2009) Inactivation kinetics of Listeria monocytogenes, Salmonella enterica serovar Typhimurium, and Campylobacter jejuni in ready-to-eat sliced ham using UV-C irradiation. Meat Sci 83(4):599–603. https://doi.org/10.1016/j.meatsci.2009.07.007

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank UFVJM and CDTN for their support in conducting the experiments, the Coordination for the Improvement of Higher Education Personnel (CAPES) for resources provided to the Graduate Program in Food Science and Technology, and the Foundation for Research Support of the State of Minas Gerais (FAPEMIG) for the scholarship granted to graduate students.

Funding

This work was supported by the Foundation for Research Support of the State of Minas Gerais (FAPEMIG) (13100).

Author information

Authors and Affiliations

Authors

Contributions

Fabiana Regina Lima: conceptualization; methodology; formal analysis; data curation; investigation; resources; writing—original draft.

Paulo de Souza Costa Sobrinho: resources; methodology; writing—review and editing.

Larissa de Oliveira Ferreira Rocha: resources; writing—review and editing.

Poliana Mendes de Souza: conceptualization; methodology; resources; writing—review and editing; supervision; project administration.

Corresponding author

Correspondence to Fabiana Regina Lima.

Ethics declarations

Ethics approval

Not applicable

Consent to participate

Not applicable

Consent for publication

Not applicable

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

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

Responsible Editor: Luis Augusto Nero

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lima, F.R., de Souza Costa Sobrinho, P., de Oliveira Ferreira Rocha, L. et al. Modeling of Listeria innocua, Escherichia coli, and Salmonella Enteritidis inactivation in milk treated by gamma irradiation. Braz J Microbiol 54, 1047–1054 (2023). https://doi.org/10.1007/s42770-023-00931-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-023-00931-5

Keywords

Navigation