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Inhibition of Bacterial Foodborne Pathogens on The INHIBITION OF BACTERIAL FOODBORNE PATHOGENS ON THE SURFACES OF FRESH PRODUCE USING PLANT-DERIVED ANTIMICROBIAL ESSENTIAL OILS IN SURFACTANT MICELLES A Dissertation by SONGSIRIN RUENGVISESH Submitted to the Office of Graduate and Professional Studies of Texas A&M University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Chair of Committee, T. Matthew Taylor Committee Members, Alejandro Castillo Rhonda Miller Luis Cisneros-Zevallos Head of Department, Boon Chew May 2016 Major Subject: Food Science and Technology Copyright 2016 Songsirin Ruengvisesh ABSTRACT This research was undertaken to: i) quantify numbers of native microbiota on leafy greens, jalapeno peppers, tomatoes, and cantaloupes; ii) study internalization in fresh produce with and without aid of temperature and pressure differential; iii) formulate essential oil component (EOC)-containing nano-micelles and analyze rheological and loading characteristics of particles; iv) identify the minimum inhibitory concentrations (MIC) and minimum bactericidal concentrations (MBC) of antimicrobial essential oil-containing micelles against Escherichia coli O157:H7 and Salmonella enterica serotype Saintpaul; and v) determine inactivation efficacy of EOC-containing micelles and other antimicrobial agents against E. coli O157:H7, S. Saintpaul, and epiphytic microbiota on surfaces of fresh produce. Numbers of native microbiota on leafy greens obtained from South Texas in spring harvest seasons ranged from 0.7±0.0 to 6.2±0.1 log10 CFU/g. Higher counts of certain microbial groupings were observed with leafy green samples collected at higher ambient temperature. Native microbiota on surfaces of jalapeno pepper, tomato, and cantaloupe obtained from spring and fall harvest seasons were in the range of 0.2±0.0 to 2 2 3.9±0.7 log10 CFU/cm , 0.2±0.0 to 3.8±0.9 log10 CFU/cm , and 1.1±1.3 to 6.0±0.8 log10 CFU/cm2, respectively. In general, stem scars of tomato and cantaloupe bore greater counts of native microbiota versus skins/rinds. Dye penetration in intact and non-intact tomatoes with aid of temperature and pressure differential was 1.71±1.36 cm and 0.10±0.06 cm, respectively. The study of microbial internalization without aid of temperature and pressure differential showed ii that internalization of E. coli K12 occurred through stem scar channels; however, E. coli K12 was unable to travel deeply in the stem. The study of maximum additive concentration (MAC) of EOCs in surfactant micelles showed that sodium dodecyl sulfate (SDS) possessed the highest encapsulation efficiency among all tested surfactants. Carvacrol and eugenol encapsulated in SDS and CytoGuard LA20 (CG) micelles were most effective for pathogen inhibition in microbroth assay. In produce commodities, overall, encapsulated eugenol, free eugenol, chlorine, and empty micelles were similarly effective in reducing pathogens and native microbiota on tomato surfaces at 5 °C during 10 days of storage. At 15 °C, empty micelles were less effective than other antimicrobial treatments in reducing pathogens on tomato surfaces. Compared to encapsulated eugenol, free eugenol and empty micelles, decreased antifungal effect of chlorine was also observed at 15 °C in tomatoes. For spinach, encapsulated eugenol, free eugenol, and chlorine seemed to be similarly effective in reducing pathogen levels and were more effective than empty micelles and water at 5 and 15 °C. Overall, encapsulated eugenol and free eugenol were more effective than other treatments in reducing levels of aerobic bacteria and Enterobacteriaceae during storage at 5 and 15 °C. Excepting water, antifungal effects of all treatments did not differ during the entire storage period. The study suggests EOC- loaded micelles could be used as an alternative to conventional intervention methods for decontamination of fresh produce as well as increasing shelf life of fresh produce. iii ACKNOWLEDGEMENTS I would like to express my sincerest and deepest gratitude to my PhD advisor, Dr. Matthew Taylor, for his unwavering support, guidance and encouragement throughout my research. I would like to thank my committee members, Dr. Castillo, Dr. Miller, and Dr. Cisneros for their guidance and their support. I would also like to thank my lab-mates and student workers for their help and support throughout my research project. Finally, I would like to thank my family and Thai friends for their love and encouragement throughout my PhD studies. iv TABLE OF CONTENTS Page ABSTRACT .......................................................................................................................ii ACKNOWLEDGEMENTS .............................................................................................. iv TABLE OF CONTENTS ................................................................................................... v LIST OF FIGURES ........................................................................................................... ix LIST OF TABLES ...........................................................................................................xii CHAPTER I INTRODUCTION ........................................................................................ 1 CHAPTER II NATIVE MICROBIOTA OF FRESH PRODUCE ..................................... 3 CHAPTER III PRODUCE CONTAMINATION .............................................................. 8 3.1 Foodborne Illnesses Associated with Fresh Produce ............................................... 8 3.2 Potential Routes of Pathogen Contamination in Fresh Produce ............................ 11 3.2.1 Pre-harvest Sources of Pathogen Contamination ............................................ 12 3.2.2 Harvest and Post-harvest Sources of Pathogen Contamination ...................... 15 3.3 Preventive Measures for Controlling Hazards in Produce ..................................... 17 3.3.1 Good Agricultural Practices (GAPs) ............................................................... 17 3.3.2 Current Good Manufacturing Practices (cGMPs) ........................................... 19 3.3.3 Hazard Analysis and Critical Control Points (HACCP) ................................. 19 CHAPTER IV PATHOGEN INTERVENTIONS FOR PRODUCE DECONTAMINATION AND SANITIZATION ............................................................ 21 4.1 Chlorine .................................................................................................................. 21 4.2 Chlorine Dioxide .................................................................................................... 23 4.3 Acidified Sodium Chlorite ..................................................................................... 24 4.4 Peroxyacetic Acid .................................................................................................. 25 CHAPTER V ESCHERICHIA COLI O157:H7 AND SALMONELLA ENTERICA........27 v 5.1 Escherichia coli ...................................................................................................... 27 5.1.1 Introduction ..................................................................................................... 27 5.1.2 Escherichia coli O157:H7 ............................................................................... 27 5.2 Salmonella enterica ................................................................................................ 34 CHAPTER VI ESSENTIAL OIL COMPONENTS ........................................................ 38 6.1 Introduction ............................................................................................................ 38 6.2 Mechanisms of Action of Essential Oil Components ............................................ 39 CHAPTER VII SURFACTANTS AND MICELLES ..................................................... 43 7.1 Surfactants .............................................................................................................. 43 7.2 Micelles .................................................................................................................. 43 7.3 Surfactant-based Antimicrobial Encapsulated-Nanoparticles for Inhibition of Foodborne Pathogens ................................................................................................... 45 CHAPTER VIII ENUMERATION OF NATIVE MICROBIOTA ON FRESH PRODUCE ....................................................................................................................... 48 8.1 Materials and Methods ........................................................................................... 48 8.1.1 Preliminary Study for Tomato Sampling Procedures ..................................... 48 8.1.2 Enumeration of Native Microbiota on Fresh Produce Commodities .............. 49 8.1.3 Statistical Analyses ......................................................................................... 50 8.2 Results and Discussion ........................................................................................... 51 8.2.1 Preliminary Study on Tomato Sampling Procedures ...................................... 51 8.2.2 Native Microbiota on Leafy Greens ................................................................ 53 8.2.2.1 Native Microbiota on Lettuce .................................................................. 53 8.2.2.2 Native Microbiota on Spinach .................................................................. 55 8.2.2.3 Native Microbiota on Parsley ................................................................... 57 8.2.2.4 Native Microbiota on Jalapeño
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