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The Recovery and Transfer of Aerosolized Listeria Innocua Calvin The Recovery and Transfer of Aerosolized Listeria innocua Calvin M. Waldron Dissertation submitted to the faculty of the Virginia Polytechnic Institute and State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy In Food Science and Technology Joseph D. Eifert Robert C. Williams Andrew P. Neilson Linsey C. Marr July 26, 2017 Blacksburg, Virginia Keywords: Listeria innocua, bioaerosol chamber, nebulizer, aerosolized, steel, HDPE i The Recovery and Transfer of Aerosolized Listeria innocua Calvin M. Waldron ABSTRACT (academic) Airborne pathogenic bacteria can present a significant public health risk. Pathogenic Listeria monocytogenes can colonize numerous surfaces as well, through direct and indirect cross contamination. The physical environment can also affect the transmission and viability of Listeria (distance from the source, temperature, humidity, air flow). The purpose of this work was to explore the ability of Listeria innocua (a surrogate for L. monocytogenes) to contaminate a surface after it has become aerosolized in a bioaerosol chamber and a walk-in cooler. L. innocua was nebulized into a 154 L biosafety chamber (~5 log CFU in 1 mL) at two relative humidity (RH) levels (83% and 65%). Oxford Listeria agar plates, stainless steel coupons and polyethylene (HDPE) coupons in the chamber were exposed to the aerosolized bacteria for 5, 10, 20 or 40 minutes. Also, at these times, air samples (100 L) were collected on to gelatin filters which were transferred to Oxford agar plates. In the second part of the research, L. innocua was nebulized into an 11 m3 walk-in cooler where RH ranged from ~29-37%. Aerosolized bacteria were collected on to Oxford agar plates for 10 min intervals and with 50 or 100 L air samples. Recovery of L. innocua from steel, plastic and agar was significantly higher at 83% RH (2.7 cells/cm2) compared to 65% RH (0.45 cells/cm2). Mean cell recovery from air samples (gelatin filters) was significantly higher (p<0.05) when collected 5 or 10 minutes after nebulization at 83% humidity (mean 2.2 CFU/L) compared to collection ii after 20 or 40 minutes or compared to all times under 65% humidity (mean 0.4 CFU/L). Recovery from HDPE coupons (1.21 CFU/cm2) was 2.5 X recovery from Oxford agar (0.49 CFU/cm2). In the walk-in cooler, total estimated mean recovery from Oxford media at 10 min after nebulizing was 0.48%, but only 0.04% for samples collected after 60 minutes. The recovery of L. innocua from air samples after 60 min was one-fourth of the number recovered 5 min after nebulizing. No significant difference in recovery was found between plates at different distances (2 – 2.5 m) from the nebulizer in the walk-in cooler. Understanding the survival of aerosolized Listeria and how it can colonize over time on a food contact surface will enhance our efforts to prevent transmission on a small and large scale. The food industry will be able to implement better safety measures to prevent contamination by Listeria species. iii The Recovery and Transfer of Aerosolized Listeria innocua Calvin M. Waldron ABSTRACT (public) Airborne pathogenic bacteria, including Listeria monocytogenes, can present a significant public health risk. Pathogenic bacteria can colonize numerous surfaces as well through direct and indirect cross contamination. The physical environment can also affect the transmission and viability of Listeria (distance from the source, temperature, humidity). The purpose of this work was to explore the ability of Listeria innocua to contaminate a surface after it has become aerosolized in a bioaerosol chamber and a walk-in cooler. Environmental factors of distance from the source, temperature, and relative humidity were explored. L. innocua was nebulized into a 154 L biosafety chamber (~5 log CFU in 1 ml) at two relative humidity (RH) levels (83% and 65%). Oxford Listeria agar plates, stainless steel coupons and polyethylene (HDPE) coupons in the chamber were exposed to the aerosolized bacteria for 5, 10, 20 or 40 minutes. Also, at these times, air samples (100 L) were collected on to gelatin filters which were transferred to Oxford agar plates. In the second part of the research, L. innocua was nebulized into an 11 m3 walk-in cooler where RH ranged from ~29-37%. Aerosolized bacteria were collected with 50 or 100 L air samples. And, Oxford media was placed on the cooler floor in layers (attached to poster boards) at various locations for surface analysis. iv The three surface samples yielded a greater mean recovery of 2.7 cells/cm2 at 83% humidity compared to 0.45 cells/cm2 at 65% humidity. Mean cell recovery from air samples (gelatin filters) was significantly higher (p<0.05) when collected 5 or 10 minutes after nebulization at 83% humidity (mean 2.2 CFU/L) compared to collection after 20 or 40 minutes or compared to all times under 65% humidity (mean 0.4 CFU/L). Recovery from HDPE coupons (1.21 CFU/cm2) was 2.5 X recovery from Oxford agar (0.49 CFU/cm2). In the walk-in cooler, total estimated mean recovery from the Oxford media at 10 min after nebulizing the Listeria innocua was 0.48%, but only 0.04% for samples collected after 60 minutes. The recovery of L. innocua from air samples after 60 min was one-fourth of the number recovered 5 min after nebulizing. Understanding the survival of aerosolized Listeria and how it can colonize over time on a food contact surface will enhance our efforts to prevent transmission on a small and large scale. The food industry will be able to implement better safety measures to prevent contamination by Listeria species. v Acknowledgements I would like to first acknowledge my family and God, for this would not be possible if it wasn’t for them. I would like to thank my parents Calvin V. Waldron and Susan B. Waldron for pushing me and instilling in me great values of hard work and dedication. I hope to become as great of people as you are one day and I love you with all my heart. I would like to thank my sister Susan M. Waldron and my brother Michael K. Waldron for always being there for me and keeping a smile on my face when times became difficult. You both inspire me to challenge myself and strive to hopefully be a good role model for you all. Also, a special thanks to Phillip George, Kristoefer Clegg, Lawrence Stawicki, Brandon Miller, Alicia Beck, Dhaval Kumar, Benjamin Okyere, and all of my friends for their great support. You kept me sane throughout this entire process, whether if it was through words of wisdom and encouragement or through recreational activities and meet-ups just to blow off some steam. I would especially like to thank Dr. Joseph Eifert for being a mentor and committed advisor, for without him none of this project would be possible. He was able to see the potential in this project from the start. I would also like to thank my committee members, Dr. Linsey Marr, Dr. Andrew Neilson, and Dr. Rob Williams, who helped me discover new ways to approach my research as well as giving me their support. To the faculty and staff of the Food Science and Technology Department, thank you for welcoming me into the program and for your continued support. I am truly blessed to have such a great support system, and there are not enough words to express how truly thankful I am. vi Table of Contents Abstract (academic) ......................................................................................................... ii Abstract (public) .............................................................................................................. iv Acknowledgements ......................................................................................................... vi Introduction………………… ............................................................................................ 1 I. Literature Review ......................................................................................................... 6 A. Listeria species………………………………………………………………..…..…6 B. Listeriosis………………………………………………………………………….….7 C. Reducing the Impact of Foodborne Listeriosis…………………………………..11 D. Transmission of Listeria in Food Environments…...…………………….……..19 E. Survival of Airborne and Aerosolized Bacteria………….………………………25 References……………………………………………….…………..………..……….33 II. The Recovery and Transfer of Aerosolized Listeria innocua Within a Bioaerosol Chamber and on Industrial Surfaces….………………………………. 40 1. Introduction………………………………………………………………..….……..42 2. Materials and Methods………………………………………………………….….43 3. Results…………………………………………………………………………….…50 4. Discussion …………………………………………………………………………..52 Acknowledgments.…...………………………………………………………………..57 Figures …………………………………….……………………………………………58 Tables…………………………………………………………………………………...63 References ……………………………………………………………………………..64 vii III. Recovery of Aerosolized Listeria innocua within a Walk-in Refrigeration Unit …..….67 1. Introduction…………………………………………………………………….……69 2. Materials and Methods……………………………………………………………..71 3. Results……………………………………………………………………………….76 4. Discussion…………………………………………………………………………..78 Acknowledgments ……………………………………………………………………..83 Figures ………………………………………………………………………………….84 References ………………………………………………………………….………….89 IV. Conclusion……………………………………………………………………………….... 92 V. Appendices………………………………………………………………………………... 96 Appendix A. Preliminary Research ..................................................................... 96 Appendix B. Images of Bioaerosol Chamber and Refrigeration Unit…………...103 viii Introduction Listeria monocytogenes is one of the world's primary bacterial food safety
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