journal article·2025-05-30Open access

Inactivation Kinetics of Listeria monocytogenes Applying Mild Temperatures and Fractionated Mexican Oregano Essential Oil (Poliomintha longiflora Gray) in a Modified Simulated Meat Medium

Mariana Pimentel-González, Arícia Possas, Antonio Valero, Eduardo Sánchez-García, José Rodríguez-Rodríguez, Sandra Castillo

Applied Sciences· Volume 15· Issue 11

Abstract

Meat products are highly susceptible to contamination with Listeria monocytogenes, a foodborne pathogen associated with high mortality. To mitigate this risk, this study explored the use of Poliomintha longiflora oregano essential oil, both in its pure (PEO) and fractionated (FIV, fraction IV obtained at 140 °C) forms, as part of a hurdle technology combining natural antimicrobials with mild thermal treatments. In vitro thermal inactivation experiments were conducted at 52, 54, 57.5, and 63 °C using a simulated meat medium. The FIV group, characterized by 60.23% carvacrol and 21.17% thymol, exhibited significantly enhanced bactericidal activity, achieving up to 5.5 log-reductions in L. monocytogenes at 57.5 °C within 3 min, compared to <2 log-reductions for the control group. Inactivation kinetics were well described by the Weibull–Mafart model. The δ-values, defined as the time required to achieve a 1-log reduction in bacterial population, were consistently lower for FIV compared to the control across all tested temperatures (e.g., δ52°C = 0.64 min vs. 8.47 min for control). The estimated z-values, which represent the temperature increase required to achieve a tenfold change in δ-value, were 5.75 °C (control), 5.20 °C (PEO), and 5.00 °C (FIV), suggesting a consistent thermal sensitivity but enhanced inactivation efficacy with the essential oils. These findings suggest that fractionated oregano essential oil is a promising hurdle to shorten thermal treatments in meat products, thereby lowering L. monocytogenes contamination risk while preserving product quality.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Essential Oils and Antimicrobial Activity · Listeria monocytogenes in Food Safety · Microbial Inactivation Methods

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Facultad de Ciencias Biológicas, Universidad Autónoma de Nuevo León, Avenida Universidad s/n, Ciudad Universitaria, San Nicolás de los Garza 66455, Nuevo León, Mexico

Department of Food Science and Technology, UIC Zoonosis y Enfermedades Emergentes (ENZOEM), CeiA3, Universidad de Córdoba, Campus Rabanales, 14014 Córdoba, Spain

Tecnológico de Monterrey, Escuela de Ingeniería y Ciencias, Av. Eugenio Garza Sada 2501 Sur, Monterrey 64849, Nuevo León, Mexico

Funding

Consejo Nacional de Humanidades, Ciencias y Tecnologías (CONAHCYT) · Secretaría de Ciencia, Humanidades, Tecnología e Innovación (SECIHTI)

References (83)

Show source-provided references
1. Food and Drug Administration (2025, April 16). Hazard Analysis and Risk-Based Preventive Controls for Human Food: Draft Guidance for Industry, Available online: https://www.regulations.gov/document/FDA-2016-D-2343-0092.
2. Food and Drug Administration (2022). Bad Bug Book-Foodborne Pathogenic Microorganisms and Natural Toxins-Second Edition 2 Bad Bug Book Handbook of Foodborne Pathogenic Microorganisms and Natural Toxins, Food and Drug Administration.
3. Ricci, A., Allende, A., Bolton, D., Chemaly, M., Davies, R., Fernández Escámez, P.S., Girones, R., Herman, L., Koutsoumanis, K., and Nørrung, B. (2018). Listeria monocytogenes contamination of ready-to-eat foods and the risk for human health in the EU. EFSA J., 16.10.2903/j.efsa.2018.5134 ↗
4. Koutsoumanis, K., Allende, A., Bolton, D., Bover-Cid, S., Chemaly, M., De Cesare, A., Herman, L., Hilbert, F., Lindqvist, R., and Nauta, M. (2024). Persistence of microbiological hazards in food and feed production and processing environments. EFSA J., 22.10.2903/j.efsa.2024.8521 ↗
5. CDC (2025, March 09). Listeria Outbreak Linked to Leafy Greens—February, Available online: https://www.cdc.gov/listeria/outbreaks/monocytogenes-02-23/index.html.
6. CDC (2025, March 09). Listeria Outbreak Linked to Ice Cream—August, Available online: https://www.cdc.gov/listeria/outbreaks/ice-cream-08-23/index.html.
7. CDC (2025, March 09). Listeria Outbreak Linked to Queso Fresco and Cotija Cheese—February, Available online: https://www.cdc.gov/listeria/outbreaks/cheese-02-24/index.html.
8. CDC (2025, March 09). Listeria Outbreak Linked to Ready-To-Eat Meat and Poultry Products, Available online: https://www.cdc.gov/listeria/outbreaks/meat-and-poultry-products-11-24/index.html.
9. CDC (2025, March 09). More Illnesses and Deaths in Listeria Outbreak Linked to Deli Meats Is Reminder to Avoid Recalled Products, Available online: https://www.cdc.gov/media/releases/2024/s0828-listeria-outbreak-deli-meats.html.
10. CDC (2025, March 09). Outbreak Investigation of Listeria monocytogenes: Frozen Supplemental Shakes (February 2025), Available online: https://www.fda.gov/food/outbreaks-foodborne-illness/outbreak-investigation-listeria-monocytogenes-frozen-supplemental-shakes-february-2025.
11. Guel-García, P., De León, F.J.G., Aguilera-Arreola, G., Mandujano, A., Mireles-Martínez, M., Oliva-Hernández, A., Cruz-Hernández, M.A., Vasquez-Villanueva, J., Rivera, G., and Bocanegra-García, V. (2024). Prevalence and Antimicrobial Resistance of Listeria monocytogenes in Different Raw Food from Reynosa, Tamaulipas, Mexico. Foods, 13.10.3390/foods13111656 ↗
12. Matle, I., Mbatha, K.R., and Madoroba, E. (2020). A review of Listeria monocytogenes from meat and meat products: Epidemiology, virulence factors, antimicrobial resistance, and diagnosis. Onderstepoort J. Veter-Res., 87.10.4102/ojvr.v87i1.1869 ↗
13. Mahgoub, S.A., El-Mekkawy, R.M., El-Hack, M.E.A., El-Ghareeb, W.R., Suliman, G.M., Alowaimer, A.N., and Swelum, A.A. (2019). Inactivation of Listeria monocytogenes in ready-to-eat smoked turkey meat by combination with packaging atmosphere, oregano essential oil and cold temperature. AMB Express, 9.10.1186/s13568-019-0775-8 ↗
14. Effects of pH, sodium chloride, and temperature on the growth of Listeria monocytogenes biofilms10.1556/066.2023.00017 ↗
15. Comprehensive metagenomic analysis of stress-resistant and -sensitive Listeria monocytogenes10.1007/s00253-023-12693-z ↗
16. Persistent and non-persistent strains of Listeria monocytogenes: A focus on growth kinetics under different temperature, salt, and pH conditions and their sensitivity to sanitizers10.1016/j.fm.2016.02.005 ↗
17. Modeling the effects of the preculture temperature on the lag phase of Listeria monocytogenes at 25 °C10.4315/0362-028X.JFP-19-117 ↗
18. Wei, J., Ismael, M., Huang, M., Han, T., and Zhong, Q. (2025, March 22). The Bactericidal Effects of Combined Sterilization Methods on Listeria monocytogenes and the Application in Prepared Salads. Available online: https://ssrn.com/abstract=5102418.10.2139/ssrn.5102418 ↗
19. Antilisterial effects of antibacterial formulations containing essential oils, nisin, nitrite and organic acid salts in a sausage model10.1007/s13197-016-2232-x ↗
20. Organic acids as antimicrobials to control Salmonella in meat and poultry products10.1016/j.foodres.2011.04.043 ↗
21. Puvača, N., Milenković, J., Coghill, T.G., Bursić, V., Petrović, A., Tanasković, S., Pelić, M., Pelić, D.L., and Miljković, T. (2021). Antimicrobial activity of selected essential oils against selected pathogenic bacteria: In vitro study. Antibiotics, 10.10.3390/antibiotics10050546 ↗
22. de Souza Pedrosa, G.T., Pimentel, T.C., Gavahian, M., de Medeiros, L.L., Pagán, R., and Magnani, M. (2021). The combined effect of essential oils and emerging technologies on food safety and quality. LWT, 147.10.1016/j.lwt.2021.111593 ↗
23. Vidaković Knežević, S., Knežević, S., Vranešević, J., Kravić, S., Lakićević, B., Kocić-Tanackov, S., and Karabasil, N. (2023). Effects of Selected Essential Oils on Listeria monocytogenes in Biofilms and in a Model Food System. Foods, 12.10.3390/foods12101930 ↗
24. Tejada-Muñoz, S., Cortez, D., Rascón, J., Chavez, S.G., Caetano, A.C., Díaz-Manchay, R.J., Sandoval-Bances, J., Huyhua-Gutierrez, S., Gonzales, L., and Chenet, S.M. (2024). Antimicrobial Activity of Origanum vulgare Essential Oil against Staphylococcus aureus and Escherichia coli. Pharmaceuticals, 17.10.3390/ph17111430 ↗
25. Pinto, L., Cervellieri, S., Netti, T., Lippolis, V., and Baruzzi, F. (2024). Antibacterial Activity of Oregano (Origanum vulgare L.) Essential Oil Vapors against Microbial Contaminants of Food-Contact Surfaces. Antibiotics, 13.10.3390/antibiotics13040371 ↗
26. Maggio, F., Rossi, C., Chaves-López, C., Valbonetti, L., Desideri, G., Paparella, A., and Serio, A. (2022). A single exposure to a sublethal concentration of Origanum vulgare essential oil initiates response against food stressors and restoration of antibiotic susceptibility in Listeria monocytogenes. Food Control, 132.10.1016/j.foodcont.2021.108562 ↗
27. Physical, Chemical and Sensory Changes in Meat and Meat Products Induced by the Addition of Essential Oils: A Concise Review
28. Ortega, A.R., Guinoiseau, E., Poli, J.-P., Quilichini, Y., Serra, D.d.R., Novelles, M.d.C.T., Castaño, I.E., Pérez, O.P., Berti, L., and Lorenzi, V. (2023). The Primary Mode of Action of Lippia graveolens Essential Oil on Salmonella enterica subsp. Enterica Serovar Typhimurium. Microorganisms, 11.10.3390/microorganisms11122943 ↗
29. Chemical Composition and Antimicrobial Activity of Oregano (Lippia palmeri S. Wats) Essential Oil
30. Zapién-Chavarría, K.A., Plascencia-Terrazas, A., Venegas-Ortega, M.G., Varillas-Torres, M., Rivera-Chavira, B.E., Adame-Gallegos, J.R., González-Rangel, M.O., and Nevárez-Moorillón, G.V. (2019). Susceptibility of multidrug-resistant and biofilm-forming uropathogens to Mexican oregano essential oil. Antibiotics, 8.10.3390/antibiotics8040186 ↗
31. Levario-Gómez, A., Ávila-Sosa, R., Gutiérrez-Méndez, N., López-Malo, A., and Nevárez-Moorillón, G.V. (2020). Modeling the Combined Effect of pH, Protein Content, and Mexican Oregano Essential Oil Against Food Spoilage Molds. Front. Sustain. Food Syst., 4.10.3389/fsufs.2020.00034 ↗
32. Mora-Zúñiga, A.E., Treviño-Garza, M.Z., Guerra, C.A.A., Rodríguez, S.A.G., Castillo, S., Martínez-Rojas, E., Rodríguez-Rodríguez, J., and Báez-González, J.G. (2022). Comparison of Chemical Composition, Physicochemical Parameters, and Antioxidant and Antibacterial Activity of the Essential Oil of Cultivated and Wild Mexican Oregano Poliomintha longiflora Gray. Plants, 11.10.3390/plants11141785 ↗
33. García, E.S., Torres-Alvarez, C., Sosa, E.G.M., Pimentel-González, M., Treviño, L.V., Guerra, C.A.A., Castillo, S., and Rodríguez, J.R. (2024). Essential Oil of Fractionated Oregano as Motility Inhibitor of Bacteria Associated with Urinary Tract Infections. Antibiotics, 13.10.3390/antibiotics13070665 ↗
34. Rostro-Alanis, M.d.J., Báez-González, J., Torres-Alvarez, C., Parra-Saldívar, R., Rodriguez-Rodriguez, J., and Castillo, S. (2019). Chemical composition and biological activities of oregano essential oil and its fractions obtained by vacuum distillation. Molecules, 24.10.3390/molecules24101904 ↗
35. Cabrera-Díaz, E., Martínez-Chávez, L., Gutiérrez-González, P., Pérez-Montaño, J.A., Rodríguez-García, M.O., and Martínez-Gonzáles, N.E. (2022). Effect of storage temperature and time on the behavior of Salmonella, Listeria monocytogenes, and background microbiota on whole fresh avocados (Persea americana var Hass). Int. J. Food Microbiol., 369.10.1016/j.ijfoodmicro.2022.109614 ↗
36. Márquez-González, M., Osorio, L.F., Velásquez-Moreno, C.G., and García-Lira, A.G. (2022). Thermal Inactivation of Salmonella enterica and Listeria monocytogenes in Quesillo Manufactured from Raw Milk. Int. J. Food Sci., 2022.10.1155/2022/2507867 ↗
37. Detection of Listeria monocytogenes, Salmonella and Yersinia enterocolitica in beef at points of sale in Mexico
38. High-pressure processing in inactivation of Salmonella spp. in food products10.1016/j.tifs.2020.11.025 ↗
39. Soni, A., Bremer, P., and Brightwell, G. (2022). A Comprehensive Review of Variability in the Thermal Resistance (D-Values) of Food-Borne Pathogens—A Challenge for Thermal Validation Trials. Foods, 11.10.3390/foods11244117 ↗
40. Stavropoulou, E., and Bezirtzoglou, E. (2019). Predictive modeling of microbial behavior in food. Foods, 8.10.3390/foods8120654 ↗
41. Harter, R.W. (2013). Application of Predictive Models in Quantitative Risk Assessment and Risk Management. Predictive Microbiology in Foods, Springer.
42. Application of predictive models to assess the influence of thyme essential oil on Salmonella enteritidis behaviour during shelf life of ready-to-eat turkey products10.1016/j.ijfoodmicro.2016.08.003 ↗
43. Dogruyol, H., Mol, S., and Cosansu, S. (2020). Increased thermal sensitivity of Listeria monocytogenes in sous-vide salmon by oregano essential oil and citric acid. Food Microbiol., 90.10.1016/j.fm.2020.103496 ↗
44. Fernández-Martínez, N.F., Ruiz-Montero, R., Briones, E., Baños, E., Rodríguez-Alarcón, L.G.S.M., Chaves, J.A., Abad, R., Varela, C., on behalf of the LISMOAN team, and Lorusso, N. (2022). Listeriosis outbreak caused by contaminated stuffed pork, Andalusia, Spain, July to October 2019. Eurosurveillance, 27.10.2807/1560-7917.ES.2022.27.43.2200279 ↗
45. Lazou, T.P., and Chaintoutis, S.C. (2023). Comparison of disk diffusion and broth microdilution methods for antimicrobial susceptibility testing of Campylobacter isolates of meat origin. J. Microbiol. Methods, 204.10.1016/j.mimet.2022.106649 ↗
46. Effects of sub-lethal concentrations of thyme and oregano essential oils, carvacrol, thymol, citral and trans-2-hexenal on membrane fatty acid composition and volatile molecule profile of Listeria monocytogenes, Escherichia coli and Salmonella enteritidis10.1016/j.foodchem.2015.02.136 ↗
47. Thermal inactivation of foodborne pathogens and the USDA pathogen modeling program10.1007/s10973-011-1453-5 ↗
48. Sigmoidal thermal inactivation kinetics of Listeria innocua in broth: Influence of strain and growth phase10.1016/j.foodcont.2009.03.007 ↗
49. Mathematical approach for the Listeria monocytogenes inactivation during high hydrostatic pressure processing of a simulated meat medium10.1016/j.ifset.2018.03.012 ↗
50. Pérez-Rodríguez, F., Valero, A., and Bolivar, A. (2025). Development and Validation of Microbial Inactivation Models Using Bioinactivation4. Basic Protocols in Predictive Microbiology Softwares. Methods and Protocols in Food Science, Humana.10.1007/978-1-0716-4112-5 ↗
51. Garre, A., González-Tejedor, G.A., Aznar, A., Fernández, P.S., and Egea, J.A. (2019). Mathematical modelling of the stress resistance induced in Listeria monocytogenes during dynamic, mild heat treatments. Food Microbiol., 84.10.1016/j.fm.2019.06.002 ↗
52. A modified Weibull model for bacterial inactivation10.1016/j.ijfoodmicro.2004.10.016 ↗
53. The Logarithmic Nature of Thermal Death Time Curves10.1093/infdis/29.5.528 ↗
54. Huertas, J.-P., Ros-Chumillas, M., Garre, A., Fernández, P.S., Aznar, A., Iguaz, A., Esnoz, A., and Palop, A. (2021). Impact of Heating Rates on Alicyclobacillus acidoterrestris Heat Resistance under Non-Isothermal Treatments and Use of Mathematical Modelling to Optimize Orange Juice Processing. Foods, 10.10.3390/foods10071496 ↗
55. The Weibull Model for Microbial Inactivation10.1007/s12393-021-09291-y ↗
56. Effect of grapefruit seed extract on thermal inactivation of Listeria monocytogenes during sous-vide processing of two marinated Mexican meat entrées10.4315/0362-028X.JFP-15-352 ↗
57. Effect of sous-vide processing of fish on the virulence and antibiotic resistance of Listeria monocytogenes10.1016/j.nfs.2023.05.003 ↗
58. Salazar, J.K., Fay, M.L., Fleischman, G., Khouja, B.A., Stewart, D.S., and Ingram, D.T. (2024). Inactivation kinetics of Listeria monocytogenes and Salmonella enterica on specialty mushroom garnishes based on ramen soup broth temperature. Front. Microbiol., 15.10.3389/fmicb.2024.1485398 ↗
59. Kutner, M.H., Nachtsheim, C., Neter, J., and Li, W. (2005). Applied Linear Statistical Models, McGraw-Hill Irwin. [5th ed.].
60. A primer on model selection using the Akaike Information Criterion
61. Tarlak, F. (2023). The Use of Predictive Microbiology for the Prediction of the Shelf Life of Food Products. Foods, 12.10.3390/foods12244461 ↗
62. Pouillot, R., Kiermeier, A., Guillier, L., Cadavez, V., and Sanaa, M. (2024). Updated Parameters for Listeria monocytogenes Dose–Response Model Considering Pathogen Virulence and Age and Sex of Consumer. Foods, 13.10.3390/foods13050751 ↗
63. Milkievicz, T., Badia, V., Souza, V.B., Longhi, D.A., Galvão, A.C., and Robazza, W.d.S. (2020). Development of a general model to describe Salmonella spp. growth in chicken meat subjected to different temperature profiles. Food Control, 112.10.1016/j.foodcont.2020.107151 ↗
64. Dudek-Wicher, R., Paleczny, J., Kowalska-Krochmal, B., Szymczyk-Ziółkowska, P., Pachura, N., Szumny, A., and Brożyna, M. (2021). Activity of liquid and volatile fractions of essential oils against biofilm formed by selected reference strains on polystyrene and hydroxyapatite surfaces. Pathogens, 10.10.3390/pathogens10050515 ↗
65. Guo, P., Li, Z., Cai, T., Guo, D., Yang, B., Zhang, C., Shan, Z., Wang, X., Peng, X., and Liu, G. (2024). Inhibitory effect and mechanism of oregano essential oil on Listeria monocytogenes cells, toxins and biofilms. Microb. Pathog., 194.10.1016/j.micpath.2024.106801 ↗
66. Evaluation of the Antibacterial Activity of Essential Oils Against E. coli Isolated From Rabbits10.36103/ijas.v53i4.1592 ↗
67. Essential oils: Their antibacterial properties and potential applications in foods—A review10.1016/j.ijfoodmicro.2004.03.022 ↗
68. Fang, T., Wu, Y., Xie, Y., Sun, L., Qin, X., Liu, Y., Li, H., Dong, Q., and Wang, X. (2021). Inactivation and Subsequent Growth Kinetics of Listeria monocytogenes After Various Mild Bactericidal Treatments. Front. Microbiol., 12.10.3389/fmicb.2021.646735 ↗
69. Modelling of Listeria monocytogenes Scott A after a mild heat treatment in the presence of thymol and carvacrol: Effects on culturability and viability10.1016/j.jfoodeng.2018.07.014 ↗
70. Pasteurizing Cold Smoked Salmon (Oncorhynchus nerka): Thermal Inactivation Kinetics of Listeria monocytogenes and Listeria innocua10.1080/10498850.2013.808303 ↗
71. Effect of temperature and salt on thermal inactivation of Listeria monocytogenes in salmon roe10.1016/j.foodcont.2016.08.027 ↗
72. Moura-Alves, M., Gouveia, A.R., de Almeida, J.M.M., Monteiro-Silva, F., Silva, J.A., and Saraiva, C. (2020). Behavior of Listeria monocytogenes in beef Sous vide cooking with Salvia officinalis L. essential oil, during storage at different temperatures. LWT, 132.10.1016/j.lwt.2020.109896 ↗
73. Synergistic effect of cinnamaldehyde on the thermal inactivation of Listeria monocytogenes in ground pork10.1177/1082013219867190 ↗
74. Effects of carvacrol, (E)-2-hexenal, and citral on the thermal death kinetics of Listeria monocytogenes10.4315/0362-028X.JFP-11-064 ↗
75. Guevara, L., Antolinos, V., Palop, A., and Periago, P.M. (2015). Impact of Moderate Heat, Carvacrol, and Thymol Treatments on the Viability, Injury, and Stress Response of Listeria monocytogenes. BioMed Res. Int., 2015.10.1155/2015/548930 ↗
76. Characterization of Mexican coriander (Eryngium foetidum) essential oil and its inactivation of Listeria monocytogenes in vitro and during mild thermal pasteurization of pineapple juice10.4315/0362-028X.JFP-13-323 ↗
77. Modeling the effects of temperature, sodium chloride, and green tea and their interactions on the thermal inactivation of Listeria monocytogenes in Turkey10.4315/0362-028X.JFP-14-124 ↗
78. Butler, F., Hunt, K., Redmond, G., Donofrio, F., Barron, U.G., Fernandes, S., Cadavez, V., Iannetti, L., Centorotola, G., and Pomilio, F. (2023). Application of novel predictive microbiology techniques to shelf-life studies on Listeria monocytogenes in ready-to-eat foods (ListeriaPredict). EFSA Support. Publ., 20.10.2903/sp.efsa.2023.EN-8418 ↗
79. Environmental Protection Agency (EPA) (2025, April 05). Thymol; Exemption from the Requirement of a Tolerance. Federal Register 2022, 87. May 2025, Available online: https://www.govinfo.gov/content/pkg/FR-2022-09-07/pdf/2022-19294.pdf.
80. When nanoemulsified, d-limonene reduces Listeria monocytogenes heat resistance about one hundred times10.1016/j.foodcont.2015.07.020 ↗
81. Oficial Journal of the European Union (2025, April 05). Commision Implementing Regulation (EU) 2024/1989. 2024. May 2025. Available online: http://data.europa.eu/eli/reg/2003/1831/oj.
82. Jackson-Davis, A., White, S., Kassama, L.S., Coleman, S., Shaw, A., Mendonca, A., Cooper, B., Thomas-Popo, E., Gordon, K., and London, L. (2023). A Review of Regulatory Standards and Advances in Essential Oils as Antimicrobials in Foods. J. Food Prot., 86.10.1016/j.jfp.2022.100025 ↗
83. Contreras-Soto, M., Medrano-Félix, J., Ibarra-Rodríguez, J., Martínez-Urtaza, J., Chaidez, Q., and Castro-del Campo, N. (2019). The last 50 years of Salmonella in Mexico: Sources of isolation and factors that influence its prevalence and diversity. Bio Cienc., 6.