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Role of Oxidative Stress on the Temporal Development Of ROLE OF OXIDATIVE STRESS ON THE TEMPORAL DEVELOPMENT OF MORBIDITY AND MORTALITY FOLLOWING SULFUR MUSTARD INHALATION by CAMERON SHEA MCELROY B.S., University of Toledo, OH, 2008 M.S., University of Toledo, OH, 2010 A thesis submitted to the Faculty of the Graduate School of the University of Colorado in partial fulfillment of the requirements for the degree of Doctor of Philosophy Toxicology Program 2016 ii This thesis for the Doctor of Philosophy degree by Cameron Shea McElroy has been approved for the Toxicology Program by Dennis Petersen, Chair Brian J. Day, Advisor Manisha Patel Carl White Hong-Wei Chu Date: 5/20/2016 iii McElroy, Cameron Shea (Ph.D Toxicology) Role of Oxidative Stress on the Temporal Development of Morbidity and Mortality Following Sulfur Mustard Inhalation Thesis directed by Professor Brian J. Day ABSTRACT Sulfur mustard (bis 2-chloroethyl ethyl sulfide, SM) is a powerful bi-functional vesicating chemical warfare agent. SM tissue injury is partially mediated by the overproduction of reactive oxygen species resulting in oxidative stress. It was hypothesized that mitigating the oxidative stress component of SM induced injury would alleviate the toxic effects of SM inhalation. To test this hypothesis, adult Sprague-Dawley rats were intubated and exposed to a lethal dose of SM (1.4mg/kg). Suppression of oxidative stress was achieved through repeated dosing of the catalytic antioxidant AEOL 10150. Rats were randomized and treated with either sterile PBS or AEOL 10150 beginning 1-hour post SM exposure. Non-invasive animal monitoring was employed to evaluate clinical status, oxygen saturations and heart rates in live animals following exposures. Rats were euthanized at multiple times between 6-48 hours post exposure to monitor biochemical and histological development of SM induced injury. Catalytic antioxidant treatment was able to improve survival after SM inhalation in a dose-dependent manner, up to 52% over SM PBS at 48H post-exposure. At euthanasia, pulse oximetry revealed antioxidant mediated improvements in oxygen saturations by 10% and heart rates by 22%. Subjective evaluations of respiratory quality and activity was quantified and these clinical scores were improved by 57% after SM exposure in the catalytic antioxidant treatment group. Markers of oxidative stress, inflammatory cytokines, and pulmonary fibrosis were found to be significantly elevated in iv the lung 24 hours after exposure to SM, and reduced by antioxidant treatment. Tissue analysis showed the formation of occlusive airway cast was detectable in airways as early as 6 hours after SM inhalation, and continued to expand 24 hours after exposure. Catalytic antioxidant therapy was able to decrease airway cast formation in a dose and time dependent manner resulting in a 69% improvement in cast reduction at 48 hours post SM exposure. Persistent leukopenia was also noted between 6-48 hours which was improved with antioxidant administration. Additionally, it was found that the protective effect on survival exerted by antioxidant treatments was sustained out to 72 hours following treatment cessation at 48 hours post exposure. These findings indicate that catalytic antioxidants may be useful medical countermeasures against inhaled SM exposure. v ACKNOWLEDGEMENTS First I would like to thank my mentor, Dr. Brian Day for his unwavering support and guidance throughout this project. His great advice, patience, encouragement, and commitment to quality research have helped me realize the kind of scientist I want to be. I would also like to thank my committee members Dr. Carl White, Dr. Hong Wei Chu, Dr. Dennis Petersen, and Dr. Manisha Patel for their valuable recommendations for keeping this project moving forward. I would like to thank the members of the Day lab, whose wonderful personalities made all the long hours at the bench bearable. Thank you to past Day lab members including Remy Kachadourian, Neal Gould, and Joshua Chandler who were always willing to share protocols and lend a helping hand on experiments. Thank you to Jie Huang who trained me on DNA extraction techniques and helped me to run several samples. Special thanks also to Elysia Min who trained me on HPLC and GC/MS methods, traveled to Maryland numerous times to provide much needed support in conducting large animal experiments, and was always a source of lively conversation. I would to again like to thank Dr. White for generously allowing me to use equipment in his lab which was instrumental in this research, as well as the technical support from his lab members. Among the White lab members who helped me the most were Tara Hendry- Hofer, Rhonda Garlick, Joan Loader, and Jackie Rioux who took the time to teach me animal handling, dosing, and necropsy procedures in addition to providing support for several of the experiments presented here. I would like to thank Dr. Livia Veress for her role in developing many of the techniques which were used to perform this research, including optimization of airway cast scoring, clinical scoring, and pulse oximetry systems. Dr. Veress also vi participated in early experiments involving AEOL 10150 which helped to make this research possible. I would also like to thank Russell Smith for training me on the cast scoring techniques. Thank you to the Army Medical Research Institute for Chemical Defense team including Dana Anderson, Wesley Holmes, and Danielle Paradiso. Each of the ICD members lost many hours of sleep while working incredibly long shifts with me to cover the round-the-clock dosing required for these studies. My thanks go out to my friends and family members who provided moral support of the years and never lost faith that I would eventually graduate and get a real job. I would especially like to thank my parents who always encouraged me stick with it when things looked bleak. Finally, and most importantly, I would like to thank my wonderful wife Pallavi Bhuyan McElroy. She has endured the best and worst times of graduate school with me, and was a constant reminder of a future worth the hard work. I would never have made it here without you. vii TABLE OF CONTENTS CHAPTER I. INTRODUCTION ............................................................................................................. 1 Brief History of Sulfur Mustard as a Chemical Warfare Agent ........................................ 1 Clinical Pathology of Sulfur Mustard Exposures and Suggested Therapies ..................... 4 Molecular Mechanisms of Toxicity, Disposition, and Exposure Models of Sulfur Mustard .............................................................................................................................. 8 Oxidative Stress in Chemical Warfare Agent Exposures ................................................ 15 Catalytic Antioxidants / AEOL 10150 ............................................................................ 18 Summary .......................................................................................................................... 23 II. DOSE-DEPENDENT EFFECTS OF ANTIOXIDANT TREATMENTS ON …...MORBIDITY AND MORTALITY AFTER SULFUR MUSTARD INHALATION .... 24 Abstract ............................................................................................................................ 24 Introduction ...................................................................................................................... 25 Methods ........................................................................................................................... 29 Results.............................................................................................................................. 32 Discussion ........................................................................................................................ 42 III. EVALUATION OF OXIDATIVE STRESS AND INFLAMMATION MARKERS IN …...AN ACUTE MODEL OF SM INHALATION ............................................................... 47 Abstract ............................................................................................................................ 47 Introduction ...................................................................................................................... 48 Methods ........................................................................................................................... 51 Results.............................................................................................................................. 59 Discussion ........................................................................................................................ 72 viii IV. TEMPORAL EFFECTS OF OXIDATIVE STRESS SUPPRESSION ON AIRWAY …...CAST FORMATION, HEMATOLOGY, AND EXTENDED SURVIVAL …...FOLLOWING SM INHALATION ................................................................................. 82 Abstract ............................................................................................................................ 82 Introduction ...................................................................................................................... 83 Methods ........................................................................................................................... 85 Results.............................................................................................................................. 90 Discussion .......................................................................................................................
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