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Dog-Vector-Parasite Interactions in the Chagas Disease System

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Dog-Vector-Parasite Interactions in the Chagas Disease System DOG-VECTOR-PARASITE INTERACTIONS IN THE CHAGAS DISEASE SYSTEM: CARDIAC CLINIC STATUS OF NATURALLY-INFECTED DOGS ACROSS THE US A Dissertation by ALYSSA CATHERINE MEYERS 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, Sarah A. Hamer Committee Members, Gabriel Hamer Ashley Saunders Kevin Cummings Head of Department, C. Jane Welsh August 2019 Major Subject: Biomedical Sciences Copyright 2019 Alyssa Catherine Meyers ABSTRACT In the southern U.S., triatomine vectors maintain Trypanosoma cruzi- the protozoan parasite that causes Chagas disease in humans and animals- in sylvatic cycles. Infection with T. cruzi may be asymptomatic or lead to heart disease and death. Using dogs as a model host system, our objectives were to improve the ecological and clinical understanding of Chagas disease in the U.S. We collected 461 triatomines from Big Bend National Park from 2015- 2017 and found an overall infection prevalence of 23.1%. Blood meal analysis on 42 triatomines showed DNA evidence of humans, domestic animals, wild birds and mammalian wildlife. In 2015-17, we sampled 1,660 working dogs from 43 states using three independent serology assays to detect a seroprevalence of 7.3% (CI: 6.1-8.6%). To better characterize the cardiac outcomes in T. cruzi infected dogs we applied a 24-hour Holter monitor to 17 T. cruzi-infected, 18 uninfected dogs and 4 dogs with discordant serology results. The presence of ECG abnormalities varied by T. cruzi infection status (p<0.0001) and positive dogs had higher serum concentrations of cardiac troponin I (cTnI), a biomarker for cardiac injury, than both negative dogs (p=0.044) and discordant dogs (p=0.06). Finally, we performed a retrospective study looking at 375 dogs presented to a teaching hospital in Texas. T. cruzi- infected dogs (N=63, 16.8%) were significantly younger than negative dogs (N=312) (mean 5.9 vs. 7.4 yr old respectively; p=0.0069) with no difference in infections by sex or breed. Infected dogs were more likely to have ventricular arrhythmias (28.6%), combinations of ECG abnormalities, and cTnI greater than 0.129 ng/mL (ADVIA assay). Combining ecological and clinical approaches to enhance our understanding of Chagas disease should provide insight for vector control and measures to protect veterinary and public health. ii DEDICATION To my parents for their endless support, encouragement and teaching me to never give up. iii ACKNOWLEDGEMENTS First and foremost, I would like to acknowledge my advisor, Sarah Hamer, for believing in me and accepting me into her lab. I truly appreciate the enthusiasm she approaches each research question with and have valued her unrelenting support over the past four years both in and outside the lab. She has also served as an outstanding role model by successfully balancing both a career in academia and motherhood and supported me while I learn to balance both career and family. It has been an honor to be a part of the Hamer lab and I feel so fortunate to have had Sarah as a mentor. I am grateful for the support and guidance from my committee. I feel fortunate to have had the opportunity to work with and learn from Ashley Saunders. Her mentorship has taught me the importance of balancing epidemiology with clinical medicine to address infectious disease related questions-an understanding I will use throughout my career. She provided a very supportive environment while teaching me the very basics of a cardiology, and I am grateful for the many hours she spent reviewing reports, manuscripts and data with me. I am thankful for Kevin Cummings teaching me an unhealthy appreciation for statistics and for tirelessly answering all of questions. I am very grateful to Gabe Hamer for his insight and constructive feedback on grants and research projects, and his enthusiastic support of networking to assist with my professional development. Special thanks to Lisa Auckland-I couldn’t ask for a better field partner, office mate and friend. I will forever be grateful for her willingness to help with any project and admire her determination to go above and beyond with all tasks asked of her. I would also like to thank both Rachel Curtis-Robles and Carolyn Hodo who were senior graduate students when iv I joined the lab and both served as mentor and friend- providing constructive feedback and showing me the ropes of graduate school and Chagas disease research. I would also like to acknowledge the rest of my lab members (inclusive of the Gabe Hamer lab) for their providing such a positive and supportive environment over the past four years: Italo Zecca, Miranda Bertram, Andrew Golnar, Karen Poh, Estelle Martin, Jillian Wormington, Sujata Balasubramanian, Keswick Killets, Rachel Busselman, Spencer DeBrock, Ed Davila, Valery Roman-Cruz, and Justin Bejcek. I am indebted to a wonderful team of veterinary and undergraduate students who assisted me these past two summers including: Julia Purnell and Megan Ellis, the Andy Castro and Hannah Meyers. They have all have kept a wonderful sense of humor and enthusiasm for our research even during long hours in the field. I would like to thank our collaborators at the Department of Homeland Security. In particular Dr. Marvin Meinders and John Sanders from the Office of Health Affairs, who without their continued enthusiasm for our research and concern for the health and wellbeing of the working dogs, this research would not have been possible. A huge thanks to all of the canine coordinators and supervisors at DHS who have helped me coordinate a country wide sampling of dogs including: Eliut Torres, Richard DeMille, Jose Garcia, Edgar Frausto, Manuel Pagan, Aaron Britton, Dawn Moreno, Dr. Brianne Gustafson, Dr. Megan Keyes, Robyn Sylverson, Martin Valenzuela, Jorge Limon, Devin Luse, Phillip Morgan, Luis Hinojosa, Alejandro Leos, Adam Bauman, Laura Martinez, and Oscar Travino. A special thanks to Alan Mills, Chad Hale, David Morales and Nancy Figueroa who are all coordinating wizards and worked with me these past four years to sample their dogs for v multiple studies-I appreciate their patience and willingness to get ‘just one more dog’ and their sense of humor while we sample at all hours of the day. Thank you to Melissa Berquist, Heather Manley and Chris Scarmardo from Institute for Infectious Animal Disease for their guidance and logistic support on the DHS project. For collaboration on manuscripts published and submitted in this dissertation, I thank my co-authors including Sarah Hamer, Rachel Curtis-Robles, Julia Purnell, Megan Ellis, Lisa Auckland, Marvin Meinders, Ashley Saunders, John Sanders, Italo Zecca, Raymond Skiles, Derrek Matthews and Sonya Gordon. Finally, I would like to thank my family for encouraging my fascination with the natural world and nurturing my determination. I am also grateful to my husband- who has been mentor, colleague and my biggest support on my journey to getting accepted into a Ph.D. program, and in during my time at Texas A&M University. vi CONTRIBUTORS AND FUNDING SOURCES This work was supervised by a dissertation committee consisting of Dr. Sarah Hamer (advisor) of the Veterinary Integrative Biosciences Department, Dr. Ashley Saunders of the Department of Small Animal Clinical Sciences, Dr. Kevin Cummings Department of Population Medicine and Diagnostic Sciences, Cornell University and Dr. Gabriel Hamer of the Department of Entomology. Additional collaborators included Rachel Curtis-Robles, Julia Purnell, Megan Ellis, Lisa Auckland, Dr. Marvin Meinders, John Sanders, Italo Zecca, Raymond Skiles, Derrek Matthews and Sonya Gordon. Stipend funding was provided by the National Science Foundation Graduate Research Fellow Programs (Grant no. 1746932). The students in the Veterinary Medical Summer Research Training Program (J. Purnell, M. Ellis, and A. Castro) were supported by NIH T35 fellowships (5T35OD010991-11). For support of research costs, contributions came from the Department of Homeland Security (HSHQDC-15-J-00217/ HSHQDC-10-A-BOA33, HSHQDC-16-J-00459/HSHQDC-10-A-BOA33 and HSHQDC-17-A-B0005), the Texas A&M AgriLife Research Insect Vector Disease Seed Grant and the Harry L. Willett Foundation. vii NOMENCLATURE AKC American Kennel Club AVB atrioventricular block AV atrioventricular CBP Customs and Border Protection CHF congestive heart failure CT cycle threshold cTnI cardiac troponin I DHS Department of Homeland Security DTU discrete typing unit (strain type) ECG electrocardiogram ELISA enzyme-linked immunosorbent assay IFA indirect fluorescent antibody OR odds ratio SL-IR spliced leader intergenic region TSA Transportation Security Administration TVMDL Texas A&M Veterinary Medical Diagnostic Laboratory VPC ventricular premature contraction VMTH Veterinary Medical Teaching Hospital viii TABLE OF CONTENTS Page ABSTRACT ............................................................................................................................. ii DEDICATION ........................................................................................................................ iii ACKNOWLEDGEMENTS .................................................................................................... iv CONTRIBUTORS AND FUNDING SOURCES ................................................................. vii NOMENCLATURE ............................................................................................................. viii TABLE OF CONTENTS .......................................................................................................
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