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.
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
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
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
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
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
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
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
Mcmeekin T, Olley J, Ross T, Ratkowsky D (1993) Predictive microbiology: theory and application. Research Studies Press Ltd, Taunton, UK, pp 11–84
Dannenhauer CE (2010) Desenvolvimento de um aplicativo computacional para microbiologia preditiva. Universidade Federal de Santa Catarina, Dissertação
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
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
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
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
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
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
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
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
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
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
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
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
Souza PM (2007) Estudo comparativo da pasteurização de leite pelo método convencional e por microondas. Universidade Estadual de Campinas, Dissertação
Fellows PJ (2006) Tecnologia do processamento de alimentos: princípios e prática. Artmed, Porto Alegre
Franco BDGM, Landgraf M (1999) Microbiologia dos alimentos. Atheneu, São Paulo
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
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
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
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
Van der Waal Z (2017) GInaFiT—a user guide. Newcastle University
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
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
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
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
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
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
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
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
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.
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42770-023-00931-5