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Characteristics of Listeria Monocytogenes Important CHARACTERISTICS OF LISTERIA MONOCYTOGENES IMPORTANT FOR PULSED ELECTRIC FIELD PROCESS OPTIMIZATION DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Beatrice H. Lado, M.S. * * * * * The Ohio State University 2003 Dissertation Committee: Approved by Dr. Ahmed E. Yousef, Adviser Dr. Joshua A. Bomser ____________________________ Dr Polly D. Courtney Adviser Dr Q. Howard Zhang Food Science and Nutrition ABSTRACT Processing-resistant Listeria monocytogenes strains appear sporadically in ready- to-eat food, and constitute a considerable challenge to food processors. Pulsed electric field (PEF) is an alternative to thermal processing and it inactivates pathogens in liquid food. The high-intensity electric pulses kill rapidly microbial contaminants. Since L. monocytogenes is among the most PEF-resistant non-sporing foodborne pathogens, this study focused on identifying characteristics of Listeria that may be useful for PEF process optimization. Resistance to PEF treatment, at 25 kV/cm, varied among L. monocytogenes strains suspended in 0.1% NaCl (pH 7.0) or 50% acid whey (pH 4.2). Listeria monocytogenes OSY-8578 was identified as a potential target strain for process optimization, based on its high PEF-resistance. Resistance to PEF could not be associated with genotypic differences, as determined by pulsed field gel electrophoresis or arbitrarily primed-polymerase chain reaction method. However, the target strain, OSY- 8578, had a unique genotype, which is potentially useful for its identification. Sublethal PEF process (15 kV/cm for 29 ms) did not induce general stress response, a physiological state with over-expression of major molecular chaperones. On the contrary, expression of the chaperones, GroEL, GroES and DnaJ decreased ii within 5 to 20 min after PEF treatment. The decrease in expression was more marked for Scott A (PEF-sensitive) than OSY-8578 (PEF-resistant). Interestingly, the chaperone expression profile, after PEF treatment, paralleled an increased sensitivity of the pathogen to mild heat. This sensitization was not observed when mild heating was applied prior to PEF. Lactobacillus plantarum ATCC 8014, but not L. innocua ATCC 33090, was identified as potential surrogate of the target L. monocytogenes, OSY-8578, when these bacteria were suspended in a neutral simple medium (e.g., 0.1% NaCl solution) and treated at 25 kV/cm for 144 ms. Inactivation of Listeria by PEF was greater in acid or acidified whey (pH 4.2) than in sweet whey (pH 6.8) or in 0.1% NaCl (pH 7.0). In acid or acidified cheese whey, Lb. plantarum was more resistant to PEF than was L. monocytogenes OSY-8578; the former bacterium, therefore, may serve as a surrogate of the latter in such media. iii Dedicated to my parents, Etienne and Michelle Lado, for their unconditional love, support and inspiration iv ACKNOWLEDGMENTS I deeply thank my adviser, Dr. Ahmed E. Yousef, for his excellent guidance and support throughout my graduate studies, for his enthusiasm, and for giving me the wonderful opportunity to develop my creativity in research and my critical thinking. He taught me how to conduct research beyond all my expectations. I thank Dr. Joshua A. Bomser for always being available for suggestions and advices on protein analysis, and for allowing me to conduct part of my experiments in his laboratory. I thank Dr. Polly D. Courtney for her great help and advices in genotyping experiments, and for allowing me to conduct part of my experiments in her laboratory. I thank Dr. Q. Howard Zhang for his invaluable help and advices on pulsed electric field technology. I thank Dr. Chandan K. Sen and his team, at the Davis Heart & Lung Research Institute, for their guidance, support, and for giving me the great opportunity to conduct DNA microarray analysis. I thank Dr. Normand St-Pierre, for his excellent guidance to analyze the data. I am very grateful to Dr. Sudhir Sastry, who made me discover research on alternative processing technologies at the Ohio State University. I thank Charles v Pretzmann, for his valuable technical assistance in conducting arbitrarily primed- polymerase chain reaction experiments. I am grateful to Jenny Diehl and Steve Boomer, who provided the acid whey. I would like to thank the Food Safety group for their enjoyable moments in the laboratory, and more particularly Robert Gilmore, Hussein Mohamed, Luis Rodriguez- Romo, Mustafa Vurma, Dr. Mohamed Khadre, and Dr. Yoon Chung for their great support. My deep appreciation extends to Raymond Diono, Xing-Ya Wang, Carolyn Carlstrom, Oscar Lara, Si-Quan Li, Nurdan Kocaoglu-Vurma, Nidhi Sharma-Trikha, and Ian Lee, for their suggestions, support and friendship. I am grateful to the Center for Advanced Food Processing and Packaging Studies (CAPPS), the US Army Natick Soldier Center, and the Ohio Agricultural Research and Development Center (OARDC) for their generous financial support of my research assistantship and research project. vi VITA December 3, 1975 ………………………... Born, Saint-Etienne, France 1997 ………………………………………. Ingénieur, Institut Supérieur Agricole de Beauvais, France 1997 - 1998 ………..……………………... Microbiologist, Nestlé Research Center, Lausanne, Switzerland 2000 ………………………………………. M.S., University of Wolverhampton, United Kingdom 2000 – present ……………………………. Graduate Research Associate, The Ohio State University PUBLICATIONS Lado, B.H., and Yousef, A.E. 2003. Selection and identification of a Listeria monocytogenes target strain for pulsed electric field process optimization. Appl. Env. Microbiol. 69(4): 2223-2229. vii Lado, B.H., Roy, S., Khanna, S., Sen, C.K. 2002. Vitamin E sensitive genes in the developing rat fetal brain: a high-density oligonucleotides microarray analysis. FEBS Lett. 530(1-3): 17-23. Lado, B.H., and Yousef, A.E. 2002. Alternative food-preservation technologies: efficacy and mechanisms. Microbes Infect. 4(4): 433-440. FIELDS OF STUDY Major Field: Food Science and Nutrition viii TABLE OF CONTENTS Page Abstract ………………………………………………………………………… ii Dedication ……………………………………………………………………… iv Acknowledgments ……………………………………………………………… v Vita ……………………………………………………………………………... vii List of Tables …………………………………………………………………... xi List of Figures ………………………………………………………………….. xiii Chapters: 1. Introduction ………………………………………………………………… 1 2. Characteristics of Listeria monocytogenes important to food processors ….. 5 2.1. Introduction …………………………………….…………………….. 5 2.2. Temperature ………………………………………………………….. 8 2.3. Acidity ………………………………………………………………... 26 2.4. Water activity ………………………………………………………… 32 2.5. Antimicrobial components in food …………………………………... 35 2.6. Biocontrol ……………………………………………………………. 59 2.7. Modified atmosphere ………………………………………………… 63 2.8. Alternative processing technologies …………………………………. 64 2.9. Attachment and biofilm formation ……………….……………..…… 71 2.10. Sanitizers ……………………………………………………………... 75 2.11. Active packaging ……………………………………………………... 83 2.12. Multiple antimicrobial treatments ………………………………..…... 84 2.13. References ……………………………………………………………. 87 ix 3. Selection and identification of a Listeria monocytogenes target strain for pulsed electric field process optimization ………………………………..… 139 Abstract …………………………………………………………………….. 139 Introduction ………………………………………………………………… 140 Materials and methods ……………………………………………………... 143 Results ……………………………………………………………………… 149 Discussion ………………………………………………………………….. 153 References ………………………………………………………………….. 157 4. Pulsed electric field alters molecular chaperone expression and sensitizes Listeria monocytogenes to heat ……………………………………….…… 166 Abstract …………………………………………………………………….. 166 Introduction ………………………………………………………………… 167 Materials and methods ……………………………………………………... 170 Results ……………………………………………………………………… 176 Discussion ………………………………………………………………….. 178 References ………………………………………………………………….. 183 5. Identification of a Listeria monocytogenes surrogate for pulsed electric field process optimization ………………………………………………….. 192 Abstract …………………………………………………………………….. 192 Introduction ………………………………………………………………… 193 Materials and methods ……………………………………………………... 196 Results ……………………………………………………………………… 200 Discussion ………………………………………………………………….. 204 References ………………………………………………………………….. 209 6. Conclusion …………………………………………………………………. 220 Bibliography …………...……………………………………………………….. 223 x LIST OF TABLES Table Page 2.1. Minimum pasteurization processing temperature and time, for dairy products with less than 10% fat, specified in the US Code of Federal Regulations ………………………………... 116 2.2. Organic acids frequently used as food acidifier or antimicrobials ……………………………………………….. 117 2.3. Minimal listeriostatic concentration of lauric, linoleic and linolenic acids in brain heart infusion broth (BHI) incubated at 37°C for 24 h, and effect of these fatty acids on invasion efficiency of Caco-2 cells by L. monocytogenes ……………. 118 2.4. Concentration of compounds from plant oils that inactivated 50% of Listeria monocytogenes population in phosphate- buffered saline and incubated at 37°C for 1 h (BA50%) …….. 119 2.5. Gamma irradiation dose necessary to inactivate 90% of Listeria monocytogenes population (D-value) in food products ………………………………………………..…… 120 2.6. High pressure processing parameters decreasing 4 logs Listeria monocytogenes in food systems ……….……….….. 121 2.7. Pulsed electric field processing parameters decreasing 2 logs Listeria sp. in food systems ……………………………….... 122 2.8. Inactivation of Listeria monocytogenes, in suspension or on food surfaces, exposed to
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