Acta Vet. Brno 2026, 95: 85-98

https://doi.org/10.2754/avb202695010085

Factors influencing the risk of Clostridium perfringens germination and growth in hot ready-to-eat meals during courier delivery

Tomáš Komprda1, Alena Zouharová2, Marta Dušková2, Josef Kameník2, Gabriela Franke1, Michaela Čutová2, Petr Kouřil1, Vojtěch Kumbár3, Veronika Švehlová1, Milena Matejovičová1, Olga Cwiková1, Blanka Macharáčková2, Michaela Králová2, Miroslav Jůzl1

1Mendel University in Brno, Faculty of AgriSciences, Department of Food Technology, Brno, Czech Republic
2University of Veterinary Sciences Brno, Faculty of Veterinary Hygiene and Ecology, Department of Animal Origin Food and Gastronomic Sciences, Brno, Czech Republic
3Mendel University in Brno, Faculty of AgriSciences, Department of Technology and Automobile Transport, Brno, Czech Republic

Received December 17, 2025
Accepted March 2, 2026

References

1. Aditya DS, Mahadevarprasat KN, Santhosh KN, Hemavahti AB, Halakarni M, Yoon H, Nataraj SK 2024: Sustainable and eco-friendly membranes from sugarcane bagasse: An upcycling approach for wastewater treatment and energy storage. Chem Eng J 488: 150910 <https://doi.org/10.1016/j.cej.2024.150910>
2. Andersen KG, Hansen TB, Knøchel S 2004: Growth of heat-treated enterotoxin-positive Clostridium perfringens and the implications for safe cooling rates. J Food Prot 67: 83-89 <https://doi.org/10.4315/0362-028X-67.1.83>
3. Andler R, Tiso T, Blank L, Andreeßen C, Zampolli J, D’Afonseca V, Guajardo C, Díaz-Barrera A 2022: Current progress on the biodegradation of synthetic plastics: From fundamentals to biotechnological applications. Rev Environ Sci Biotechnol 2: 829-850 <https://doi.org/10.1007/s11157-022-09631-2>
4. Athira G, Bahurudeen A, Appari S 2021: Thermochemical conversion of sugarcane bagasse: composition, reaction kinetics, and characterisation of by-products. Sugar Tech 23: 433-452 <https://doi.org/10.1007/s12355-020-00865-4>
5. Bendary MM, Abd El-Hamid MI, El-Tarabili RM, Hefny AA, Algendy RM, Elzohairy NA, Ghoneim MM, Al-Sanea MM, Nahari MH, Moustafa WH 2022: Clostridium perfringens associated with foodborne infections of animal origins: Insights into prevalence, antimicrobial resistance, toxin genes profiles, and toxinotypes. Biology 11: 551 <https://doi.org/10.3390/biology11040551>
6. Brynestad S, Granum PE 2002: Clostridium perfringens and foodborne infections. Int J Food Microbiol 74: 195-202 <https://doi.org/10.1016/S0168-1605(01)00680-8>
7. Coşkun CK, Yeşilçubuk NŞ, Özyurt AM 2021: Effect of cooling rate on Clostridium perfringens survival trends in selected home-made cooked, reheated, and recooled meals with different consumer scenarios. J Food Process Preserv 45: e15906 <https://doi.org/10.1111/jfpp.15906>
8. Decree No. 121/2023 Coll. 2023: On Requirements for Food; Collection of Laws; Ministry of Agriculture of the Czech Republic: Prague, Czech Republic, 63: 1763–1768. Retrieved from https://www.zakonyprolidi.cz/cs/2023-121. Accessed January 1, 2024
9. EFSA 2024: The European Union one health 2023 zoonoses report. EFSA J 22: e9106
10. García S, Heredia N 2011: Clostridium perfringens: a dynamic foodborne pathogen. Food Bioprocess Technol 4: 624-630 <https://doi.org/10.1007/s11947-009-0182-2>
11. Ghaderi M, Mousavi M, Yousefi H, Labbafi M 2014: All-cellulose nanocomposite film made from bagasse cellulose nanofibers for food packaging application. Carbohydr Polym 104: 59-65 <https://doi.org/10.1016/j.carbpol.2014.01.013>
12. Gkogka E, Reij MW, Gorris LGM, Zwietering MH 2020: Risk assessment of Clostridium perfringens in Cornish pasties in the UK. Food Control 108: 106822 <https://doi.org/10.1016/j.foodcont.2019.106822>
13. Glass KA, Austin CB, Bohn MA, Golden MC, Schill KM, Ricke SC, Shrestha S 2024: Inhibition of Clostridium perfringens and Bacillus cereus by dry vinegar and cultured sugar vinegar during extended cooling of uncured beef and poultry products. J Food Prot 87: 100317 <https://doi.org/10.1016/j.jfp.2024.100317>
14. Gohari IM, Navarro MA, Li J, Shrestha A, Uzal F, McClane BA 2021: Pathogenicity and virulence of Clostridium perfringens. Virulence 12: 723-753 <https://doi.org/10.1080/21505594.2021.1886777>
15. Huang L, Li C 2020: Growth of Clostridium perfringens in cooked chicken during cooling: One-step dynamic inverse analysis, sensitivity analysis, and Markov Chain Monte Carlo simulation. Food Microbiol 85: 103285 <https://doi.org/10.1016/j.fm.2019.103285>
16. ISO 15213-2 2023: Microbiology of the food chain — Horizontal method for the detection and enumeration of Clostridium spp. Part 2: Enumeration of Clostridium perfringens by colony-count technique, Geneva, Switzerland, 44 p.
17. Jaloustre S, Guillier L, Poumeyrol G, Morelli E, Delignette-Muller ML 2013: Efficiency of a reheating step to inactivate Clostridium perfringens vegetative cells: How to measure it? Food Control 29: 422-428 <https://doi.org/10.1016/j.foodcont.2012.07.003>
18. Jing X, Li Y, Zhu J, Chang L, Maganti S, Naik N, Bin Xu B, Murugadoss V, Huang M, Guo Z 2022: Improving thermal conductivity of polyethylene/polypropylene by styrene-ethylene-propylene-styrene wrapping hexagonal boron nitride at the phase interface. Adv Compos Hybrid Mater 5: 1090-1099 <https://doi.org/10.1007/s42114-022-00438-x>
19. Juneja VK, Marks H, Thippareddi HH 2010: Predictive model for growth of Clostridium perfringens during cooling of cooked ground pork. Innov Food Sci Emerg Technol 11: 146-154 <https://doi.org/10.1016/j.ifset.2009.10.010>
20. Juneja VK, Marmer BS, Miller AJ 1994: Growth and sporulation potential of Clostridium perfringens in aerobic and vacuum-packaged cooked beef. J Food Prot 57: 393-398 <https://doi.org/10.4315/0362-028X-57.5.393>
21. Kalinowski RM, Tompkin RB, Bodnaruk PW, Pruett Jr WP 2003: Impact of cooking, cooling, and subsequent refrigeration on the growth or survival of Clostridium perfringens in cooked meat and poultry products. J Food Prot 66: 1227-1232 <https://doi.org/10.4315/0362-028X-66.7.1227>
22. Kameník J, Dušková M, Zouharová A, Čutová M, Dorotíková K, Králová M, Macharáčková B, Hulánková R 2025: The germination and growth of two strains of Bacillus cereus in selected hot dishes after cooking. Foods 14: 194 <https://doi.org/10.3390/foods14020194>
23. Kim SH, Chung BD 2024: Integrated food delivery problem considering both single-order and multiple order deliveries. Comput Ind Eng 196: 110458 <https://doi.org/10.1016/j.cie.2024.110458>
24. Komprda T, Rozíková V, Zamazalová N, Škultéty O, Vícenová M, Trčková M, Faldyna M 2017: Effect of dietary fish oil on fatty acid deposition and expression of cholesterol homeostasis controlling genes in the liver and plasma lipid profile: Comparison of two animal models. J Anim Physiol Anim Nutr 101: 1093-1102 <https://doi.org/10.1111/jpn.12581>
25. Komprda T, Jůzl M, Matejovičová M, Piechowiczová M, Popelková V, Vymazalová P, Nedomová Š, Levá L 2021: Fatty acid composition, oxidative stability, and sensory evaluation of the sausages produced from the meat of pigs fed a diet enriched with 8% of fish oil. J Food Sci 86: 2312-2326 <https://doi.org/10.1111/1750-3841.15749>
26. Komprda T, Cwiková O, Kumbár V, Franke G, Kouřil P, Patloka O, Kameník J, Dušková M, Zouharová A 2025: Key factors influencing Bacillus cereus contamination in hot ready-to-eat meal delivery. Foods 14: 2605 <https://doi.org/10.3390/foods14152605>
27. Li J, Paredes-Sabja D, Sarker MR, McClane BA 2016: Clostridium perfringens sporulation and sporulation-associated toxin production. Microbiol Spectr 4: TBS-0022-2015 <https://doi.org/10.1128/microbiolspec.TBS-0022-2015>
28. Li M, Huang L, Zhu Y, Wei Q 2019: Growth of Clostridium perfringens in roasted chicken and braised beef during cooling – One-step dynamic analysis and modeling. Food Control 106: 106739 <https://doi.org/10.1016/j.foodcont.2019.106739>
29. Loh YR, Sujan D, Rahman ME, Das CA 2013: Sugarcane bagasse—The future composite material: A literature review. Resour Conserv Recycl 75: 14-22 <https://doi.org/10.1016/j.resconrec.2013.03.002>
30. Mahapatra AK, Ekefre DE, Pattaniak NK, Jena U, Williams AL, Latimore M 2017: Thermal properties of sweet sorghum bagasse as a function of moisture content. Agric Eng Int: CIGR J 19: 108-113
31. Mahmud MA, Anannya FR 2021: Sugarcane bagasse—A source of cellulosic fiber for diverse applications. Heliyon 7: e07771 <https://doi.org/10.1016/j.heliyon.2021.e07771>
32. Márquez-González M, Cabrera-Díaz E, Hardin MD, Harris KB, Lucia LM, Castillo A 2012: Survival and germination of Clostridium perfringens spores during heating and cooling of ground pork. J Food Prot 75: 682-689 <https://doi.org/10.4315/0362-028X.JFP-11-409>
33. Meldrum RJ, Mannion PT, Garside J 2009: Microbiological quality of ready-to-eat food served in schools in Wales, United Kingdom. J Food Prot 72: 197-201 <https://doi.org/10.4315/0362-028X-72.1.197>
34. Ohnishi T, Watanabe M, Yodotani Y, Nishizato E, Araki S, Sasaki S, Hara-Kudo Y, Kojima Y, Misawa N, Okabe N 2025: Contamination of Japanese retail foods with enterotoxigenic Clostridium perfringens spores. J Food Prot 88: 100429 <https://doi.org/10.1016/j.jfp.2024.100429>
35. Packer S, Day J, Hardman P, Cameron J, Kennedy M, Turner J, Willis J, Amar C, Nozad B, Gobin M 2020: A cohort study investigating a point source outbreak of Clostridium perfringens associated with consumption of roasted meat and gravy at a buffet on Mothering Sunday 2018, South West, England. Food Control 112: 107097 <https://doi.org/10.1016/j.foodcont.2020.107097>
36. Paiva R, Veroneze IB, Wrona M, Nerín C, Cruz SA 2022: The role of residual contaminants and recycling steps on rheological properties of recycled polypropylene. J Polym Environ 3: 494-503 <https://doi.org/10.1007/s10924-021-02214-2>
37. Poumeyrol G, Morelli E, Rosset P, Noel V 2014: Probabilistic evaluation of Clostridium perfringens potential growth in order to validate a cooling process of cooked dishes in catering. Food Control 35: 293-299 <https://doi.org/10.1016/j.foodcont.2013.07.008>
38. Rantuch P 2022: The thermal degradation of polymer materials. In Rantuch P (Ed): Ignition of Polymers. Springer International Publishing, pp 1-43
39. Regulation (EU) No 1169/2011 2011: Regulation (EU) No 1169/2011 of the European Parliament and of the Council of 25 October 2011 on the provision of food information to consumers, amending Regulations (EC) No 1924/2006 and (EC) No 1925/2006 of the European Parliament and of the Council, and repealing Commission Directive 87/250/EEC, Council Directive 90/496/EEC, Commission Directive 1999/10/EC, Directive 2000/13/EC of the European Parliament and of the Council, Commission Directives 2002/67/EC and 2008/5/EC and Commission Regulation (EC) No 608/2004. Official Journal of the European Union, L 304, 18. Retrieved from https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:02011R1169-20250401&qid=1765283952548. Accessed April 1, 2025
40. Saha NC, Ghosh AK, Garg M, Sadhu SD 2022: Food Packaging: Materials,Techniques and Environmental Issues. 1st edn, Springer Nature
41. Savard L, Moundanga S, Guyot S, Mtimet N, Firmesse O, Dupont S, Beney L 2026: Persistence of vegetative and sporulated forms of Clostridium perfringens exposed to air at different relative humidities. Food Microbiol 135: 104968 <https://doi.org/10.1016/j.fm.2025.104968>
42. Singh P, Singh P, Singh J 2021: Sugarcane bagasse: A potential and economical source for raising sugarcane nursery in sub-tropical India. Sugar Tech 23: 1211-1217 <https://doi.org/10.1007/s12355-021-01028-9>
43. Smith S, Juneja V, Schaffner DW 2004: Influence of several methodological factors on the growth of Clostridium perfringens in cooling rate challenge studies. J Food Prot 67: 1128-1132 <https://doi.org/10.4315/0362-028X-67.6.1128>
44. Sumner J, Ross T, Jenson I, Pointon A 2005: A risk microbiological profile of the Australian red meat industry: Risk ratings of hazard–product pairings. Int J Food Microbiol 105: 221-232 <https://doi.org/10.1016/j.ijfoodmicro.2005.03.016>
45. Teggar M, Atia A, Rocha TTM, Laouer A 2025: Long and short-term storage of food and agriculture products: Prospects of latent heat thermal energy storage. Therm Sci Eng Prog 59: 103324 <https://doi.org/10.1016/j.tsep.2025.103324>
46. Tessi MA, Aringoli EE, Pirovani ME, Vincenzini AZ, Sabbag NG, Costa SC, García CC, Zannier MS, Silva ER, Moguilevsky MA 2002: Microbiological quality and safety of ready-to-eat cooked foods from a centralized school kitchen in Argentina. J Food Prot 65: 636-642 <https://doi.org/10.4315/0362-028X-65.4.636>
47. Tran C, Poezevara T, Maladen V, Guillier L, Mtimet N, Malayrat C, Coadou T, Jambou L, Rouxel S, Le Bouquin S, Huneau-Salaün A, Thomas R, Lopez-Rizo C, Le Roux A, Houry B, Bičche-Terrier C, Ledormand P, Feurer C, Le Maréchal C, Firmesse O, Firmesse O 2026: Isolation rate, genetic diversity, and toxinotyping of Clostridium perfringens isolated from French cattle, pig or poultry slaughterhouses. Food Microbiol 133: 104898 <https://doi.org/10.1016/j.fm.2025.104898>
48. Tun A, Baranov IV 2019: Review of the specific heat of food models. J Int Acad Refrig 3: 82-86 <https://doi.org/10.17586/1606-4313-2019-18-3-82-86>
49. Wang W, Mai X, Wang D, Zheng Y, Liu F, Sun Z 2023: Mathematical modeling of temperature and natural antimicrobial effects on germination and outgrowth of Clostridium perfringens in chilled chicken. LWT Food Sci Technol 177: 114555 <https://doi.org/10.1016/j.lwt.2023.114555>
50. Yin H, Liu C, Wang B, Li Y, Hu X, Yin J, Liu J, Zhao G, Yang J 2024: Comparison of thermal conductivities of polypropylene fibers and fibrils. Heat Mass Transf 60: 677-684 <https://doi.org/10.1007/s00231-024-03463-2>
51. Zemanová J 2020: Obsah toxických látok v obalových materiáloch a ich možná migrácia do potravín (in Slovak, The content of toxic substances in packaging materials and their possible migration into food). SciCell Mag 3: 1-2. Retrieved from https://www.scicell.org/2020/08/05/obsah-toxickych-latok-v-obalovych-materialoch-a-ich-mozna-migracia-do-potravin/. Accessed August 5, 2020
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