Effects of cinnamaldehyde on the germination and growth of Bacillus cereus spores in ready-to-eat boiled ground beef
Main Article Content
Keywords
Bacillus cereus, boiled ready-to-eat beef, cinnamaldehyde, predictive microbiology
Abstract
The study quantitatively described the effects of cinnamaldehyde on the germination and growth of Bacillus cereus spores in boiled ready-to-eat ground beef. With the combination of the concentrations of cinnamaldehyde 0, 0.1, 0.5, and 1.0% vol/wt at temperatures 12, 20, 28, and 36°C, the Huang model was successfully used as the primary model to predict the lag time (λ) and maximum growth rate (µmax). Thereafter, the cubic polynomial models were used to estimate the values of Ln λ and Ln µmax considering both the storage temperature and cinnamaldehyde concentration. The models were highly accurate, because they produced acceptable root mean squared error (RMSE) values that were close to 0, while the determination (R2), accuracy factor (Af), and bias factor (Bf) values were all close to 1. As indicated by the fitted models, the supplementary of cinnamaldehyde in samples increased the lag time of B. cereus significantly from 17.7 to 75.8 h at 12°C of storage. Increasing the storage temperature from 12 to 36°C led to only 0.80-fold prolongation of lag time from 1.6 to 2.9 h in the sample containing cinnamaldehyde. However, the µmax value declined most obviously at 20°C, while 66% decrease was determined. According to the results, the cinnamaldehyde can be used as a natural antimicrobial agent in boiled ready-to-eat ground beef in staple food industry by inhibiting the germination and growth of B. cereus. The results also provided regressing models that can be used for effectively designing the storage temperature and cinnamaldehyde concentration for a specific requirement.
References
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Doyle, A.A. and Stephens, J.C., 2019. A review of cinnamaldehyde and its derivatives as antibacterial agents. Fitoterapia 139: 104405. 10.1016/j.fitote.2019.104405
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Hou, J., Luo, R., Ni, H., Li, K., Mgomi, F.C., Fan, L. et al., 2021. Antimicrobial potential of kombucha against foodborne pathogens: a review. Quality Assurance and Safety of Crops & Foods 13: 53–61. 10.15586/qas.v13i3.920
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Juneja, V.K., Golden, C.E., Mishra, A., Harrison, M.A., Mohr, T. and Silverman, M., 2019a. Predictive model for growth of Bacillus cereus during cooling of cooked rice. International Journal of Food Microbiology 290: 49–58. 10.1016/j.ijfoodmicro.2018.09.023
Juneja, V.K., Golden, C.E., Mishra, A., Harrison, M.A. and Mohr, T.B., 2019b. Predictive model for growth of Bacillus cereus at temperatures applicable to cooling of cooked pasta. Journal of Food Science 84: 590–598. 10.1111/1750-3841.14448
Juneja, V.K., Mishra, A. and Pradhan, A.K., 2018. Dynamic predictive model for growth of Bacillus cereus from spores in cooked beans. Journal of Food Protection 81: 308–315. 10.4315/0362-028X.JFP-17-391
Kim, J.E., Choi, H.S., Lee, D.U. and Min, S.C., 2017. Effects of processing parameters on the inactivation of Bacillus cereus spores on red pepper (Capsicum annum L.) flakes by microwave-combined cold plasma treatment. International Journal of Food Microbiology 263: 61–66. 10.1016/j.ijfoodmicro.2017.09.014
Kindle, P., Etter, D., Stephan, R. and Johler, S., 2019. Population structure and toxin gene profiles of Bacillus cereus sensu lato isolated from flour products. FEMS Microbiology Letters 366. 10.1093/femsle/fnz240
Kong, L., Yu, S., Yuan, X., Li, C., Yu, P., Wang, J., et al., 2021. An investigation on the occurrence and molecular characterization of Bacillus cereus in meat and meat products in China. Foodborne Pathogens and Disease 18: 306–314. 10.1089/fpd.2020.2885
Le Marc, Y., Baert, L., Buss da Silva, N., Postollec, F., Huchet, V., Baranyi, J. et al., 2021. The effect of pH on the growth rate of Bacillus cereus sensu lato: Quantifying strain variability and modelling the combined effects of temperature and pH. International Journal of Food Microbiology 360: 109420. 10.1016/j.ijfoodmicro.2021.109420
Nyhan, L., Begley, M., Mutel, A., Qu, Y., Johnson, N. and Callanan, M., 2018. Predicting the combinatorial effects of water activity, pH and organic acids on Listeria growth in media and complex food matrices. Food Microbiology 74: 75–85. 10.1016/j.fm.2018.03.002
Omidi-Mirzaei, M., Hojjati, M., Behbahani, B.A. and Noshad, M., 2020. Modeling the growth rate of Listeria innocua influenced by coriander seed essential oil and storage temperature in meat using FTIR. Quality Assurance and Safety of Crops & Foods 12: 1–8. 10.15586/qas.v12iSP1.776
Oscar, T.E., 2005. Validation of lag time and growth rate models for Salmonella Typhimurium: acceptable prediction zone method. Journal of Food Science 70: M129–M137. 10.1111/j.1365-2621.2005.tb07103.x
Park, H.W. and Yoon, W.B., 2019. A quantitative microbiological exposure assessment model for Bacillus cereus in pasteurized rice cakes using computational fluid dynamics and Monte Carlo simulation. Food Research International 125: 108562. 10.1016/j.foodres.2019.108562
Park, K.M., Kim, H.J., Jeong, M. and Koo, M., 2020. Enterotoxin genes, antibiotic susceptibility, and biofilm formation of low-temperature-tolerant Bacillus cereus isolated from green leaf lettuce in the cold chain. Foods 9: 249. 10.3390/foods9030249
Rodrigo, D., Rosell, C.M. and Martinez, A., 2021. Risk of Bacillus cereus in relation to rice and derivatives. Foods 10: 302. 10.3390/foods10020302
Samapundo, S., Heyndrickx, M., Xhaferi, R. and Devlieghere, F., 2011. Incidence, diversity and toxin gene characteristics of Bacillus cereus group strains isolated from food products marketed in Belgium. International Journal of Food Microbiology 150: 34–41. 10.1016/j.ijfoodmicro.2011.07.013
Sun, Q., Li, J., Sun, Y., Chen, Q., Zhang, L. and Le, T., 2020. The antifungal effects of cinnamaldehyde against Aspergillus niger and its application in bread preservation. Food Chemistry 317: 126405. 10.1016/j.foodchem.2020.126405
Suo, B., Li, H., Wang, Y., Li, Z., Pan, Z. and Ai, Z., 2017a. Effects of ZnO nanoparticle-coated packaging film on pork meat quality during cold storage. Journal of the Science of Food and Agriculture 97: 2023–2029. 10.1002/jsfa.8003
Suo, B., Lu, Y.L., Wang, Y.X., Xie, X.H., Xu, C. and Ai, Z.L., 2017b. Thermal inactivation kinetics of Salmonella spp. in ground pork supplemented with cinnamaldehyde. Journal of Food Safety 37: e12322. 10.1111/jfs.12322
Tewari, A., Singh, S.P. and Singh, R., 2015. Incidence and enterotoxigenic profile of Bacillus cereus in meat and meat products of Uttarakhand, India. Journal of Food Science and Technology 52: 1796–1801. 10.1007/s13197-013-1162-0
Valero, M. and Francés, E., 2006. Synergistic bactericidal effect of carvacrol, cinnamaldehyde or thymol and refrigeration to inhibit Bacillus cereus in carrot broth. Food Microbiology 23: 68–73. 10.1016/j.fm.2005.01.016
Valero, M., Leontidis, S., Fernández, P.S., Martı´nez, A. and Salmerón, M.C., 2000. Growth of Bacillus cereus in natural and acidified carrot substrates over the temperature range 5–30°C. Food Microbiology 17: 605–612. 10.1006/fmic.2000.0352
Wang, J., Koseki, S., Chung, M.J. and Oh, D.H., 2017. A novel approach to predict the growth of Staphylococcus aureus on rice cake. Frontiers in Microbiology 8: 1140. 10.3389/fmicb.2017.01140
Wang, Y., Li, X., Lu, Y., Wang, J. and Suo, B., 2020. Synergistic effect of cinnamaldehyde on the thermal inactivation of Listeria monocytogenes in ground pork. Food Science and Technology International 26: 28–37. 10.1177/1082013219867190
Wemmenhove, E., Wells-Bennik, M.H.J. and Zwietering, M.H., 2021. A model to predict the fate of Listeria monocytogenes in different cheese types–A major role for undissociated lactic acid in addition to pH, water activity, and temperature. International Journal of Food Microbiology 357: 109350. 10.1016/j.ijfoodmicro.2021.109350
Ye, K., Wang, H., Zhang, X., Jiang, Y., Xu, X. and Zhou, G., 2013. Development and validation of a molecular predictive model to describe the growth of Listeria monocytogenes in vacuum-packaged chilled pork. Food Control 32: 246–254. 10.1016/j.foodcont.2012.11.017
Zhao, X., Chen, L., Zhao, L., He, Y. and Yang, H.S., 2020. Antimicrobial kinetics of nisin and grape seed extract against inoculated Listeria monocytogenes on cooked shrimps: Survival and residual effects. Food Control 115: 107278. 10.1016/j.foodcont.2020.107278
Ayari, S., Dussault, D., Jerbi, T., Hamdi, M. and Lacroix, M., 2012. Radiosensitization of Bacillus cereus spores in minced meat treated with cinnamaldehyde. Radiation Physics and Chemistry 81: 1173–1176. 10.1016/j.radphyschem.2012.02.022
Baranyi, J., Buss da Silva, N. and Ellouze, M., 2017. Rethinking tertiary models: relationships between growth parameters of Bacillus cereus strains. Frontiers in Microbiology 8: 1890. 10.3389/fmicb.2017.01890
Baranyi, J., Pin, C. and Ross, T., 1999. Validating and comparing predictive models. International Journal of Food Microbiology 48: 159–166. 10.1016/S0168-1605(99)00035-5
Cayemitte, P.E., Gerliani, N., Raymond, P. and Aider, M., 2021. Study of the impacts of electro-activated solutions of calcium lactate, calcium ascorbate and their equimolar mixture combined with moderate heat treatments on the spores of Bacillus cereus ATCC 14579 under model conditions and in fresh salmon. International Journal of Food Microbiology 358: 109285. 10.1016/j.ijfoodmicro.2021.109285
Cetin-Karaca, H. and Morgan, M.C., 2018. Inactivation of Bacillus cereus spores in infant formula by combination of high pressure and trans-cinnamaldehyde. LWT-Food Science and Technology 97: 254–260. 10.1016/j.lwt.2018.07.001
Chitov, T., Dispan, R. and Kasinrerk, W., 2008. Incidence and diarrhegenic potential of Bacillus cereus in pasteurized milk and cereal products in Thailand. Journal of Food Safety 28: 467–481. 10.1111/j.1745-4565.2008.00125.x
de Sarrau, B., Clavel, T., Zwickel, N., Despres, J., Dupont, S., Beney, L., et al., 2013. Unsaturated fatty acids from food and in the growth medium improve growth of Bacillus cereus under cold and anaerobic conditions. Food Microbiology 36: 113–122. 10.1016/j.fm.2013.04.008
Doyle, A.A. and Stephens, J.C., 2019. A review of cinnamaldehyde and its derivatives as antibacterial agents. Fitoterapia 139: 104405. 10.1016/j.fitote.2019.104405
Ellouze, M., Buss Da Silva, N., Rouzeau-Szynalski, K., Coisne, L., Cantergiani, F. and Baranyi, J., 2021. Modeling Bacillus cereus growth and cereulide formation in cereal-, dairy-, meat-, vegetable-based food and culture medium. Frontiers in Microbiology 12. 10.3389/fmicb.2021.639546
Friedman, M., 2017. Chemistry, antimicrobial mechanisms, and antibiotic activities of cinnamaldehyde against pathogenic bacteria in animal feeds and human foods. Journal of Agricultural and Food Chemistry 65: 10406–10423. 10.1021/acs.jafc.7b04344
Guérin, A., Dargaignaratz, C., Broussolle, V., Clavel, T. and Nguyen-the, C., 2016. Combined effect of anaerobiosis, low pH and cold temperatures on the growth capacities of psychrotrophic Bacillus cereus. Food Microbiology 59: 119–123. 10.1016/j.fm.2016.05.015
Hou, J., Luo, R., Ni, H., Li, K., Mgomi, F.C., Fan, L. et al., 2021. Antimicrobial potential of kombucha against foodborne pathogens: a review. Quality Assurance and Safety of Crops & Foods 13: 53–61. 10.15586/qas.v13i3.920
Huang, L., 2008. Growth kinetics of Listeria monocytogenes in broth and beef frankfurters–determination of lag phase duration and exponential growth rate under isothermal conditions. Journal of Food Science 73: E235–E242. 10.1111/j.1750-3841.2008.00785.x
Huang, L., 2013. Optimization of a new mathematical model for bacterial growth. Food Control 32: 283–288. 10.1016/j.foodcont.2012.11.019
Huang, L., 2014. IPMP 2013–a comprehensive data analysis tool for predictive microbiology. International Journal of Food Microbiology 171: 100–107. 10.1016/j.ijfoodmicro.2013.11.019
Hwang, C.-A. and Huang, L., 2019. Growth and survival of Bacillus cereus from spores in cooked rice–One-step dynamic analysis and predictive modeling. Food Control 96: 403–409. 10.1016/j.foodcont.2018.09.036
Jia, Z., Bai, W., Li, X., Fang, T. and Li, C., 2020. Assessing the growth of Listeria monocytogenes in salmon with or without the competition of background microflora–A one-step kinetic analysis. Food Control: 107139. 10.1016/j.foodcont.2020.107139
Juneja, V.K., Golden, C.E., Mishra, A., Harrison, M.A., Mohr, T. and Silverman, M., 2019a. Predictive model for growth of Bacillus cereus during cooling of cooked rice. International Journal of Food Microbiology 290: 49–58. 10.1016/j.ijfoodmicro.2018.09.023
Juneja, V.K., Golden, C.E., Mishra, A., Harrison, M.A. and Mohr, T.B., 2019b. Predictive model for growth of Bacillus cereus at temperatures applicable to cooling of cooked pasta. Journal of Food Science 84: 590–598. 10.1111/1750-3841.14448
Juneja, V.K., Mishra, A. and Pradhan, A.K., 2018. Dynamic predictive model for growth of Bacillus cereus from spores in cooked beans. Journal of Food Protection 81: 308–315. 10.4315/0362-028X.JFP-17-391
Kim, J.E., Choi, H.S., Lee, D.U. and Min, S.C., 2017. Effects of processing parameters on the inactivation of Bacillus cereus spores on red pepper (Capsicum annum L.) flakes by microwave-combined cold plasma treatment. International Journal of Food Microbiology 263: 61–66. 10.1016/j.ijfoodmicro.2017.09.014
Kindle, P., Etter, D., Stephan, R. and Johler, S., 2019. Population structure and toxin gene profiles of Bacillus cereus sensu lato isolated from flour products. FEMS Microbiology Letters 366. 10.1093/femsle/fnz240
Kong, L., Yu, S., Yuan, X., Li, C., Yu, P., Wang, J., et al., 2021. An investigation on the occurrence and molecular characterization of Bacillus cereus in meat and meat products in China. Foodborne Pathogens and Disease 18: 306–314. 10.1089/fpd.2020.2885
Le Marc, Y., Baert, L., Buss da Silva, N., Postollec, F., Huchet, V., Baranyi, J. et al., 2021. The effect of pH on the growth rate of Bacillus cereus sensu lato: Quantifying strain variability and modelling the combined effects of temperature and pH. International Journal of Food Microbiology 360: 109420. 10.1016/j.ijfoodmicro.2021.109420
Nyhan, L., Begley, M., Mutel, A., Qu, Y., Johnson, N. and Callanan, M., 2018. Predicting the combinatorial effects of water activity, pH and organic acids on Listeria growth in media and complex food matrices. Food Microbiology 74: 75–85. 10.1016/j.fm.2018.03.002
Omidi-Mirzaei, M., Hojjati, M., Behbahani, B.A. and Noshad, M., 2020. Modeling the growth rate of Listeria innocua influenced by coriander seed essential oil and storage temperature in meat using FTIR. Quality Assurance and Safety of Crops & Foods 12: 1–8. 10.15586/qas.v12iSP1.776
Oscar, T.E., 2005. Validation of lag time and growth rate models for Salmonella Typhimurium: acceptable prediction zone method. Journal of Food Science 70: M129–M137. 10.1111/j.1365-2621.2005.tb07103.x
Park, H.W. and Yoon, W.B., 2019. A quantitative microbiological exposure assessment model for Bacillus cereus in pasteurized rice cakes using computational fluid dynamics and Monte Carlo simulation. Food Research International 125: 108562. 10.1016/j.foodres.2019.108562
Park, K.M., Kim, H.J., Jeong, M. and Koo, M., 2020. Enterotoxin genes, antibiotic susceptibility, and biofilm formation of low-temperature-tolerant Bacillus cereus isolated from green leaf lettuce in the cold chain. Foods 9: 249. 10.3390/foods9030249
Rodrigo, D., Rosell, C.M. and Martinez, A., 2021. Risk of Bacillus cereus in relation to rice and derivatives. Foods 10: 302. 10.3390/foods10020302
Samapundo, S., Heyndrickx, M., Xhaferi, R. and Devlieghere, F., 2011. Incidence, diversity and toxin gene characteristics of Bacillus cereus group strains isolated from food products marketed in Belgium. International Journal of Food Microbiology 150: 34–41. 10.1016/j.ijfoodmicro.2011.07.013
Sun, Q., Li, J., Sun, Y., Chen, Q., Zhang, L. and Le, T., 2020. The antifungal effects of cinnamaldehyde against Aspergillus niger and its application in bread preservation. Food Chemistry 317: 126405. 10.1016/j.foodchem.2020.126405
Suo, B., Li, H., Wang, Y., Li, Z., Pan, Z. and Ai, Z., 2017a. Effects of ZnO nanoparticle-coated packaging film on pork meat quality during cold storage. Journal of the Science of Food and Agriculture 97: 2023–2029. 10.1002/jsfa.8003
Suo, B., Lu, Y.L., Wang, Y.X., Xie, X.H., Xu, C. and Ai, Z.L., 2017b. Thermal inactivation kinetics of Salmonella spp. in ground pork supplemented with cinnamaldehyde. Journal of Food Safety 37: e12322. 10.1111/jfs.12322
Tewari, A., Singh, S.P. and Singh, R., 2015. Incidence and enterotoxigenic profile of Bacillus cereus in meat and meat products of Uttarakhand, India. Journal of Food Science and Technology 52: 1796–1801. 10.1007/s13197-013-1162-0
Valero, M. and Francés, E., 2006. Synergistic bactericidal effect of carvacrol, cinnamaldehyde or thymol and refrigeration to inhibit Bacillus cereus in carrot broth. Food Microbiology 23: 68–73. 10.1016/j.fm.2005.01.016
Valero, M., Leontidis, S., Fernández, P.S., Martı´nez, A. and Salmerón, M.C., 2000. Growth of Bacillus cereus in natural and acidified carrot substrates over the temperature range 5–30°C. Food Microbiology 17: 605–612. 10.1006/fmic.2000.0352
Wang, J., Koseki, S., Chung, M.J. and Oh, D.H., 2017. A novel approach to predict the growth of Staphylococcus aureus on rice cake. Frontiers in Microbiology 8: 1140. 10.3389/fmicb.2017.01140
Wang, Y., Li, X., Lu, Y., Wang, J. and Suo, B., 2020. Synergistic effect of cinnamaldehyde on the thermal inactivation of Listeria monocytogenes in ground pork. Food Science and Technology International 26: 28–37. 10.1177/1082013219867190
Wemmenhove, E., Wells-Bennik, M.H.J. and Zwietering, M.H., 2021. A model to predict the fate of Listeria monocytogenes in different cheese types–A major role for undissociated lactic acid in addition to pH, water activity, and temperature. International Journal of Food Microbiology 357: 109350. 10.1016/j.ijfoodmicro.2021.109350
Ye, K., Wang, H., Zhang, X., Jiang, Y., Xu, X. and Zhou, G., 2013. Development and validation of a molecular predictive model to describe the growth of Listeria monocytogenes in vacuum-packaged chilled pork. Food Control 32: 246–254. 10.1016/j.foodcont.2012.11.017
Zhao, X., Chen, L., Zhao, L., He, Y. and Yang, H.S., 2020. Antimicrobial kinetics of nisin and grape seed extract against inoculated Listeria monocytogenes on cooked shrimps: Survival and residual effects. Food Control 115: 107278. 10.1016/j.foodcont.2020.107278
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