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Ecology and Epidemiology of Antimicrobial Resistance in Urban

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Ecology and Epidemiology of Antimicrobial Resistance in Urban ECOLOGY AND EPIDEMIOLOGY OF ANTIMICROBIAL RESISTANCE IN URBAN AND PERI-URBAN MESOCARNIVORES A DISSERTATION SUBMITTED TO THE FACULTY OF THE UNIVERSITY OF MINNESOTA BY KATHERINE E. L. WORSLEY-TONKS IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHYLOSOPHY MEGGAN E. CRAFT (ADVISOR) TIMOTHY J. JOHNSON (CO-ADVISOR) DECEMBER 2020 © Katherine Worsley-Tonks, 2020 Acknowledgements My time at the University of Minnesota has been filled with energy, opportunities, development, and joy. This is because I have been surrounded by brilliant and stimulating mentors, colleagues, and friends. I do not think I could have asked for a better experience. I have been challenged and supported at the same time, which sets up a perfect training environment, and I am extremely grateful for that. I first would like to express my deepest gratitude to my main advisor Meggan Craft. Meggan, thank you for taking me on as a student, keeping me motivated throughout my PhD, and reminding me to always aim high. You have taught me how to be an effective, steady, and rigorous scientist. You have set-up so many opportunities for me, including taking part in other research projects, putting me in touch with your collaborators, and pushing me to really make the most of my PhD by going to conferences, workshops, and even doing an internship at EcoHealth Alliance. I am extremely grateful for everything that you have done for me, and I feel very fortunate to have been your student. I would also like to extend my deepest appreciation to my co-advisor, Tim Johnson, for welcoming me into his research group once I had decided to work on antimicrobial resistance for my PhD. Tim, I could not have done this PhD without your guidance. Thank you so much for walking me through the world of antimicrobial resistance, for redirecting me when needed, and for giving me the opportunity to learn from you and your research group. Thank you so much to James Forester, Jeff Bender, and Dominic Travis for serving on my committee, for their rigorous feedback, and for challenging me throughout my PhD. James, thank you for challenging my methods and for helping troubleshoot approaches, i especially towards the end of my PhD. Thank you, Jeff, for helping me develop my research project and for reminding me to stay motivated and press on. I am especially grateful for your guidance on how to make my research more applied and for helping me identify additional funding when needed. Dom, I cannot thank you enough for helping me break-down my broad research ideas and making them into concrete objectives. I felt lucky to have had a cubicle next to your office because it meant that I could seek your guidance more easily, possibly more often than you had time for. Thank you for always dropping what you were doing to provide guidance. Our conversations about my PhD work, ecosystem health, and my next career step were invaluable. Thank you so much for letting me take up so much of your time. While not on my committee, I must also give a big thanks to Randy Singer as he has greatly contributed to my training throughout my PhD. Randy, I have learnt so much about the epidemiology of antimicrobial resistance from working with you, and I can’t thank you enough for that. I am so grateful that you helped train me during the second half of my PhD. Elizabeth Miller was also critical for my training. Liz, thank you for trouble-shooting methods with me, for letting me ask you hundreds of questions, and for being a great mentor more generally. I am indebted to Stan Gehrt, who allowed me to conduct this research as part of his long- term urban mesocarnivore project in Chicago. Thank you, Stan, for being such an amazing mentor and for giving me so much of your time and scientific insight. Your passion for carnivore ecology and conservation is infectious, and your success at developing and maintaining a research project for 25+ years has inspired me to strive for something similar in the future. Chris Anchor was also an important mentor for me in ii Chicago. Thank you, Chris, for letting me use your laboratory and for letting me pick your brain on some of my research ideas. I continue to marvel at how much knowledge you have on the history of Chicago both in terms of landscape and wildlife management, and I am so grateful that you shared some of that knowledge with me. Thank you to Shane McKenzie for helping me take my research ideas and implement them in the field. Shane is the reason why we were able to collect so much data on raccoons, coyotes, and opossums. Thank you, Shane, for training me on how to do urban mesocarnivore field work and for being so patient with me despite the numerous hiccups along the way. I am beyond grateful to have had the opportunity to interact with the late Donna Alexander, the primary funder of Stan Gehrt’s research. Donna set-up multiple opportunities for me in Chicago. Her devotion to her work and to what she believed in was truly inspiring. I am so sad that she is not able to see the final product of this work but hope that it would have met her standards. There are several students and research assistants who have played a huge part in this project and/or in my training that I cannot thank enough. These include members of the Craft lab, including Nick Fountain-Jones, Luis Escobar, Lauren White, Marie Gilbertson, Janine Mistrick, and Matt Michalska-Smith. Nick and Luis were especially important in my training. I have learnt so much from working with them and I am very grateful that they so willingly taught me countless skills. The help and feedback I got from the Johnson and Singer labs was also invaluable, and I especially am thankful to Bonnie Weber and Alison Millis for their help with processing the samples in the lab. Thank you also to members of the Gehrt lab for helping with the field work, especially on days iii where we captured 30+ raccoons. Andy Burmesch, Yasmine Hentati, Lauren Ross, and Steven Winter were especially important to this achievement. I also would like to thank my colleagues and faculty at the University of Minnesota for their feedback on my work and for teaching me how to be a dedicated scientist. A large part of my training and scientific thinking come from conversations I have had with Tiffany Wolf, Kim VanderWaal, and Julio Alvarez. Thank you also to the members of the Wildlife Epidemiology Journal Club and Ecosystem Health group for their feedback at different stages of my PhD. Thank you also to the College of Veterinary Medicine more broadly, for funding most of my work. Finally, and possibly most importantly, I am eternally grateful for the support and encouragement from my family and friends. Thank you to my parents, Pam and Mal, for being the first to encourage me to do this PhD despite probably preferring that I stay closer to home. Thank you for coaching me throughout my PhD, for believing in me, and for reminding me to fight for what I believe in, to stay strong during challenging times, and to have a healthy work-life balance. Thank you to my brothers, David, Andrew, and Richard, for instilling in me an interest in nature as a child, and thank you especially to Richard for inspiring me to pursue a PhD. Thank you to my friends at Minnesota, particularly Irene Bueno, Jessica Deere, Kaushi Kanankege, Amy Kinsley, Cata Picasso, Kim VanderWaal, Liz Miller, Shiv Hayer, George Omondi, Nick Fountain-Jones, Luis Escobar, for making my time in Minnesota so enjoyable. I will never forget the happy hours, barbecues, hikes, etc. we have had together. Thank you to Claire Aupetit, Floriane Giraud, Camille Gomez, Suzie Kenny, Camilla Ryan, Sara Heisel, Erin Abernethy, and Cecilia Sanchez for all the Skype chats that kept me upbeat and sane over the years. iv Lastly, thank you to Abdel Lachgar for appearing in my life during the second half of my PhD. Thank you so much for your love, support, and friendship. v Abstract Use of antibiotics in human and animal medicine has led to the emergence of many forms of antimicrobial resistant bacteria (ARB). As well as undermining the successful treatment of bacterial infections, intensive use has led to the dissemination of ARB in the community and the environment. While extensive progress has been made in understanding the spread and fate of ARB in the community, the environment has had far less attention. Yet, detection of clinically relevant ARB and associated antimicrobial resistance genes (ARG) in water and soil indicates that the environment could act as an additional exposure pathway for people and domestic animals. ARB have also been isolated from wildlife present in these contaminated environments. Because of this, wildlife are considered to be good candidates for understanding environmental antimicrobial resistance (AMR). While ARB and ARG have been detected in numerous wildlife species across the globe, several questions remain unanswered regarding exposure pathways and what the consequences might be for human and domestic animal health. The goal of this thesis was to assess the contribution of several anthropogenic sources in shaping the AMR profile of wildlife. To do this, we investigated the ecology of AMR in an urban-suburban context, specifically in the city of Chicago. The wildlife species of focus was the raccoon (Procyon lotor) and the ARB were clinically relevant extended- spectrum cephalosporin resistant (ESC-R) Escherichia coli.
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