Impact of Chlorine, Temperature and Freezing Shock on the Survival Behavior of Escherichia coli O157:H7 on Ready-to-Eat Meats

Shiowshuh Sheen, Cheng-An Hwang, Vijay K. Juneja

Food Safety and Intervention Technologies Research Unit, USDA, Agricultural Research Service, Research Facility, Eastern Regional Research Center, Wyndmoor, USA.
Residue Chemistry and Predictive Microbiology Research Unit, USDA, Agricultural Research Service, Research Facility, Eastern Regional Research Center, Wyndmoor, USA..

DOI: 10.4236/fns.2012.34075                

Abstract

Foodborne pathogens continue to pose a potential food safety hazard in ready-to-eat (RTE) meat. Chlorine is commonly used to sanitize processing equipment where Escherichia coli O157:H7 (Ec) may survive and contaminate food products. The objective of this study was to characterize the survival behavior of Ec with different stresses on RTE meats. A multi-strain cocktail of Ec was pre-treated with freezing shock for 15 - 20 h and/or chlorine (0, 25, and 50 ppm) for one hour, and then inoculated onto RTE meat surfaces to obtain about 3.0 log CFU/g. Samples were stored at three abuse temperatures (12℃, 18℃, and 24℃) and Ec was enumerated during the storage. The freezing shock impact was studied using the Ec cocktail stored in a freezer overnight followed by chlorine exposure for one hour. The lag phase and growth rate of Ec were estimated using DMFit (Combase, Baranyi’s model). Results indicated that Ec growth was suppressed by chlorine treatment. Freezing shock was found to have little impact in terms of lag time and growth rate. The lag phase of Ec after exposure to 0 ppm of chlorine (50.3 h) was shorter than that of Ec treated with 25 ppm (54.6 h) and 50 ppm (164.1 h) at 12℃. However, the lag phase decreased with an increase in temperature, e.g. at 25 ppm, lag times were 54.6, 51.1 and 48.9 h for 12℃, 18℃ and 24℃, respectively. Lag times increased with an increase in chlorine concentration. At 24℃, lag times were 15.8, 48.9, and 52.4 h for 0, 25, and 50 ppm, respectively. The growth rate increased with an increase in temperature for 0 and 25 ppm chlorine levels, but decreased at 50 ppm level. Growth rate and lag phase as a function of temperature and chlorine concentration can be described by polynomial models and modified Ratkowsky-type and Zwietering-type models. Results of this study will contribute to risk assessment of RTE meats.

Keywords

Chlorine; Lag Time; Growth Rate; E. coli O157:H7; Modeling

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	J. Tilden Jr., W. Young, A. M. McNamara, C. Custer, B. Boesel, M. A. Lambert-Fair, J. Majkowski, D. Vugia, S. B. Werner, J. Hollingsworth and J. G. J. Morris, “A New Route of Transmission for Escherichia coli: Infection from Dry Fermented Salami,” American Journal Public Health, Vol. 86, 1996, pp. 1142-1145. doi:10.2105/AJPH.86.8_Pt_1.1142
[2]	E. coli Blog, “Surveillance & Analysis on E. coli News and Outbreaks,” 2011. http://www.ecoliblog.com/
[3]	Centers for Disease Control and Prevention (CDC), “CDC Report 1 in 6 Get Sick from Foodborne Illnesses Each Year, New Estimates More Precise,” 2010. http://www.cdc.gov/media/pressrel/2010/r101215.html
[4]	Foodborne Diseases Active Surveillance Network (FoodNet), “FoodNet Annual Report,” 2007. http://www.cdc.gov/foodnet/annual/2007/2007_annual_report_508.pdf
[5]	P. D. Frenzen, A. Drake and F. J. Angulo, “Emerging Infections Program FoodNet Working Group: Economic Cost of Illness due to Escherichia coli O157 Infections in the United States,” Journal of Food Protection, Vol. 68, No. 12, 2005, pp. 2623-2630.
[6]	E. W. Rice, R. M. Clark and C. H. Johnson, “Chlorine Inactivation of Escherichia coli O157:H7,” Emerging Infectious Diseases, Vol. 5, No.3, 1999, pp. 461-463. doi:10.3201/eid0503.990322
[7]	M. Sharma, G. M. Richards and L. R. Beuchat, “Escherichia coli O157:H7,” Center for Food Safety, University of Georgia, Griffin, 2004. http://www.ugacfs.org/research/pdfs/escherichiacoli1572004.pdf
[8]	R. Virto, P. Maňas, I. álvarez, S. Condon and J. Raso, “Membrane Damage and Microbial Inactivation by Chlorine in the Absence and Presence of a Chlorine-Demanding Substrate,” Applied Environmental Microbiology, Vol. 71, No. 9, 2005, pp. 5022-5028. doi:10.1128/AEM.71.9.5022-5028.2005
[9]	P. J. Taormina and L. R. Beuchat, “Survival and Heat Resistance of Listeria monocytogenes after Exposure to Alkali and Chlorine,” Applied Environmental Microbiology, Vol. 67, No. 6, 2001, pp. 2555-2563. doi:10.1128/AEM.67.6.2555-2563.2001
[10]	J. Samelis, J. N. Sofos, P. A. Kendall and G. C. Smith, “Survival or Growth of Escherichia coli O157:H7 in a Model System of Fresh Meat Decontamination Runoff Waste Fluid and Its Resistance to Subsequent Lactic Acid Stress,” Applied Environmental Microbiology, Vol. 71, No. 10, 2005, pp. 6228-6234. doi:10.1128/AEM.71.10.6228-6234.2005
[11]	M. N. Wan Norhana, S. E. Poole, H. C. Deeth and G. A. Dykes, “The Effects of Temperature, Chlorine and Acids on the Survival of Listeria and Salmonella Strains Associated with Uncooked Shrimp Carapace and Cooked Shrimp Flesh,” Food Microbiology, Vol. 27, No. 2, 2010, pp. 250-256. doi:10.1016/j.fm.2009.10.008
[12]	A. Rajkovic, N. Smigic, M. Uyttendaele, H. Medic, L. de Zutter and F. Devlieghere, “Resistance of Listeria monocytogenes, Escherichia coli O157:H7 and Campylobacter jejuni after Exposure to Repetitive Cycles of Mild Bactericidal Treatments,” Food Microbiology, Vol. 26, No. 8, 2009, pp. 889-895. doi:10.1016/j.fm.2009.06.006
[13]	K. Aarnisalo, J. Lunden, H. Korkeala and G. Wirtanen, “Susceptibility of Listeria monocytogenes Strains to Disinfectants and Chlorinated Alkaline Cleaners at Cold Temperatures,” LWT—Food Science and Technology, Vol. 40, No. 6, 2007, pp. 1041-1048. doi:10.1016/j.lwt.2006.07.009
[14]	Food Safety and Inspection Service (FSIS), “Fact Sheets: Meat Preparation—Ground Beef and Food Safety,” 2011. http://www.fsis.usda.gov/factsheets/fround_beef_and_food_safety/index.asp
[15]	J. Bollman, A. Ismond and G. Blank, “Survival of Escherichia coli O157:H7 in Frozen Foods: Impact of the Cold Shock Response,” International Journal of Food Microbiology, Vol. 64, No. 1-2, 2001, pp. 127-138. doi:10.1016/S0168-1605(00)00463-3
[16]	D. Grzadkowska and M. W. Griffiths, “Cryotolerance of Escherichia coli O157:H7 in Laboratory Media and Food,” Journal of Food Science, Vol. 66, No. 8, 2001, pp. 1169-1173. doi:10.1111/j.1365-2621.2001.tb16100.x
[17]	T. Tasara and R. Stephan, “Cold Stress Tolerance of Listeria monocytogenes: A Review of Molecular Adaptive Mechanism and Food Safety Implications,” Journal of Food Protection, Vol. 69, No. 6, 2006, pp. 1473 1484.
[18]	J. Baranyi and T. A. Roberts, “A Dynamic Approach to Predicting Bacterial Growth in Food,” International Journal of Food Microbiology, Vol. 23, No. 3-4, 1994, pp. 277-294. doi:10.1016/0168-1605(94)90157-0
[19]	S. Sheen, C. A. Hwang and V. K. Juneja, “Modeling the Impact of Chlorine on The Behavior of Listeria monocytogenes on Ready-to-Eat Meats,” Food Microbiology, Vol. 28, No. 5, 2011, pp. 1095-1100. doi:10.1016/j.fm.2011.01.001
[20]	M. Cheroutre-Vialette and A. Lebert, “Growth of Listeria monocytogenes as a Function of Dynamic Environment at 10 C and Accuracy of Growth Predictions with Available Models,” Food Microbiology, Vol. 17, No. 1, 2000, pp. 83-92. doi:10.1006/fmic.1999.0290
[21]	H. E. Uljas, D. W. Schaffner, S. Duffy, L. Zhao and T. C. Ingham, “Modeling of Combined Processing Steps for Reducing Escherichia coli O157:H7 Populations in Apple Cider,” Applied Environmental Microbiology, Vol. 67, No. 1, 2001, pp. 133-141. doi:10.1128/AEM.67.1.133-141.2001
[22]	A. K. Pradhan, R. Ivanek, Y. T. Gr?hn, I. Geornaras, J. N. Sofos and M. Wiedmann, “Quantitative Risk Assessment for Listeria monocytogenes in Selected Categories of Deli Meats: Impact of Lactate and Diacetate on Listeriosis Cases and Deaths,” Journal of Food Protection, Vol. 72, No. 5, 2009, pp. 978-989.
[23]	K. Koutsoumanis and A. S. Angelidis, “Probabilistic Modeling Approach for Evaluating the Compliance of Ready-to-Eat Foods with New European Union Safety Criteria for Listeria monocytogenes,” Applied Environmental Microbiology, Vol. 73, No. 15, 2007, pp. 49965004. doi:10.1128/AEM.00245-07
[24]	D. A. Ratkowsky, R. K. Lowry, T. A. McMeekin, A. N. Stokes and R. E. Chandler, “Model for Bacterial Culture Growth Rate Throughout the Entire Biokinetic Temperature Range,” Journal Bacteriology, Vol. 154, No. 3, 1983, pp. 1222-1226.
[25]	M. H. Zwietering, H. G. A. M. Cuppers, J. C. De Wit and K. van’t Riet, “Evaluation of Data Transformations and Validation of Models for the Effect of Temperature on Bacterial Growth,” Applied Environmental Microbiology, Vol. 60, No. 1, 1994, pp. 195-203.
[26]	T. P. Oscar, “Development and Validation of a Tertiary Simulation Model for Predicting the Potential Growth of Salmonella typhimurium on Cooked Chicken,” International Journal of Food Microbiology, Vol. 76, No. 3, 2002, pp. 177-190. doi:10.1016/S0168-1605(02)00025-9
[27]	W. A. Rutala, E. C. Cole, C. A. Thomann and D. J. Weber, “Stability and Bactericidal Activity of Chlorine Solution,” Infection Control Hospital Epidemiology, Vol. 19, No. 5, 1998, pp. 323-327. doi:10.1086/647822
[28]	T. Wijtzes, F. M. Rombouts, M. L. Kant-Muermans, K. van’t Riet and M. Zwietering, “Development and Validation of a Combined Temperature, Water Activity, pH Model for Bacterial Growth Rate of Lactobacillus curvatus,” International Journal of Food Microbiology, Vol. 63, No. 1-2, 2001, pp. 57-64. doi:10.1016/S0168-1605(00)00401-3
[29]	T. Ross and P. Dalgaard, “Secondary Models,” In: R. C. McKellar and X. Lu, Eds., Modeling Microbial Responses in Food, CRC Press, New York, 2004.
[30]	T. A. McMeekin, R. E. Chandler, P. E. Doc, C. D. Garland, J. Olley, S. Putro and D. A. Ratkowsky, “Model for the Combined Effect of Temperature and Salt Concentration/Water Activity on Growth Rate of Staphylococcus xylosus,” Journal of Applied Bacteriology, Vol. 62, No. 6, 1987, pp. 543-550. doi:10.1111/j.1365-2672.1987.tb02687.x
[31]	M. R. Adams, C. L. Little and M. C. Easter, “Modelling the Effect of pH, Acidulant and Temperature on Growth of Yersinia enterocolitica,” Journal of Applied Bacteriology, Vol. 71, No. 1, 1991, pp. 65-71.
[32]	T. Ross, D. A. Ratkowsky, L. A. Mellefont and T. A. McMeekin, “Modelling the Effects of Temperature, Water Activity, pH and Lactic Acid Concentration on the Growth Rate of Escherichia coli,” International Journal of Food Microbiology, Vol. 82, No. 1, 2003, pp. 33-43. doi:10.1016/S0168-1605(02)00252-0
[33]	L. Huang, “Growth Kinetics of Escherichia coli O157:H7 in Mechanically-Tenderized Beef,” International Journal of Food Microbiology, Vol. 140, No. 1, 2010, pp. 40-48. doi:10.1016/j.ijfoodmicro.2010.02.013
[34]	T. A. McMeekin, J. N. Olley, T. Ross and D. A. Ratkowsky, “Predictive Microbiology: Theory and Application,” Research Studies Press Ltd., Taunton, 1993.