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THE ECOLOGY of Trypanosoma Cruzi and ITS MAMMALIAN HOSTS in TEXAS

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THE ECOLOGY of Trypanosoma Cruzi and ITS MAMMALIAN HOSTS in TEXAS THE ECOLOGY OF Trypanosoma cruzi AND ITS MAMMALIAN HOSTS IN TEXAS, USA A Dissertation by CAROLYN LOUISE HODO 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 Co-Chair of Committee, C. Jane Welsh Committee Members, Gabriel Hamer Ann B. Kier Head of Department, Ramesh Vemulapalli August 2017 Major Subject: Veterinary Pathobiology Copyright 2017 Carolyn Louise Hodo ABSTRACT Trypanosoma cruzi, agent of Chagas disease, is a zoonotic vector-borne protozoan that infects mammalian hosts throughout the Americas. Spillover from sylvatic cycles occurs when triatomine vectors bridge the parasite from wildlife to humans, dogs, or captive NHPs. Although knowledge of reservoir capacity of diverse wildlife could provide an ecological basis for disease management, most wildlife studies document exposure with little attention to infectiousness to vectors. Additionally, pathology investigations can provide key information on pathogenesis and population impacts. To investigate T. cruzi infection prevalence, strain types, and risk factors in dogs, we collected blood from 611 dogs at shelters across Texas. 18.2% of dogs were seropositive for T. cruzi. Six (1.1%) dogs harbored parasite DNA in their blood, of which 5 were DTU TcI and 1 was TcIV. To determine the trypanosome prevalence in Texas bats, we collected hearts and blood from bats across Texas. Of 593 bats, 1 was positive for T. cruzi (0.17%), 9 for T. dionisii (1.5%), and 5 for Blastocrithidia spp. (0.8%), a group of insect trypanosomes. The T. cruzi-infected bat was carrying TcI. In the T. dionisii-infected bats, we detected three unique variants associated with the three infected bat species. To characterize the T. cruzi reservoir status and associated pathology in coyotes and raccoons in Texas, we collected hearts and/or blood from animals in Central and South Texas. Infection prevalence was greater in raccoons (66.7%) than coyotes (7.5%; Z=-6.8, P<0.0002). Most raccoons with T. cruzi-infected hearts also had positive blood (83%), in contrast to coyotes (17%). Histologic lesions were more severe in coyotes, with 4/6 PCR- ii positive coyotes exhibiting mild to moderate lymphoplasmacytic inflammation and occasional myodegeneration and fibrosis. In contrast, raccoons had only very mild inflammation. At a NHP facility in San Antonio, we tested 145 rats for T. cruzi infection and found no positives. Limited vector surveillance yielded no kissing bugs. At a NHP facility in Bastrop, we tested blood from NHPs, trapped free-ranging wild mammals, and collected kissing bugs. 80% of NHPs were PCR-positive, though parasite concentrations were low and intermittent. Raccoons, opossums, and skunks were highly infected with T. cruzi, while rodents were uninfected. Few kissing bugs were collected, but most were from a building very close to NHP housing. iii ACKNOWLEDGEMENTS I would like to gratefully acknowledge my advisor, Sarah Hamer, for accepting me into her lab and for her unwavering support over these last five years. It has been an honor to be a part of the Hamer lab and I feel that I could not have made a better choice of a mentor. I am also very grateful to the rest of my committee, Gabe Hamer, Jane Welsh, and Ann Kier, for their continued support of my research and professional development. Special thanks to Lisa Auckland, who has been instrumental in helping me learn molecular methods, troubleshooting, and laboratory logistics, and I am very grateful for her constant willingness to help out with anything I asked and for her significant contributions to my many projects. I would also like to acknowledge the rest of my fellow lab members (including those in the G. Hamer lab) for their assistance and support, both material and emotional: Rachel Curtis-Robles, Miranda Bertram, Andrew Golnar, Alyssa Meyers, Italo Zecca, Karen Poh, Matthew Medeiros, and Estelle Martin. I am especially grateful to the fantastic team of vet students I worked with for two different summers: Chloe Goodwin and Nicole Bertolini, then Elise Birkner and Rosa Bañuelos. These young women all had excellent attitudes despite some tough field conditions and PCR challenges, and they all made huge contributions toward my dissertation. I would like to thank the huge collective team of individuals who contributed to both field and laboratory work, including: Lisa Auckland, Jessica Rodriguez, Frida Cano, Alicia Leahy, Trevor Tenney, Zeb Thomas, Faith Weeks, Nicole Bertolini, Jessica Light, Justin Henningsen, Aleyda Galán, Edward Wozniak, John Barnes, Amani Bourji, Elise Birkner, Rosa Bañuelos, Cindy Barron, Kyle Voelker, Don Taylor, Richard Montoya, Chloe iv Goodwin, Valery Roman-Cruz, Martha Hensel, Alyssa Meyers, Italo Zecca, Kim Doll, Beverly Finneburgh, Adam Curtis, and Justin Henefey. For assistance with prior publication of the sections contained in this dissertation, I thank my co-authors Sarah Hamer, Chloe Goodwin, Bonny Mayes, Jacqueline Mariscal, Kenneth Waldrup, Nicole Bertolini, John Bernal, and John VandeBerg. For manuscripts still in preparation, I thank Greg Wilkerson, Stanton Gray, Jessica Rodriguez, Karen Snowden, Kevin Cummings, Edward Wozniak, Rachel Curtis-Robles, Erin Edwards, Elise Birkner, and Rosa Bañuelos. I am very grateful for the funding support of the NIH T32 fellowship (2T32OD011083-06) which made my PhD training possible. The summer vet students (C. Goodwin, N. Bertolini, R. Bañuelos, E. Birkner) were supported by NIH T35 fellowships (2T35OD010991-11). For support of research costs, contributions came from the Bernice Barbour Foundation, the National Center for Veterinary Parasitology, and two TAMU CVM Graduate Studies Student Research Grants. Thanks also go to my friends and colleagues and the Veterinary Pathobiology department faculty and staff for making my time at Texas A&M University a great experience. v 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. Jane Welsh (co-advisor) of the Veterinary Integrative Biosciences Department, Dr. Ann Kier of the Department of Veterinary Pathobiology, and Dr. Gabriel Hamer of the Department of Entomology. Additional collaborators included Greg Wilkerson, Stanton Gray, Edward Wozniak, Karen Snowden, John VandeBerg, John Bernal, Bonny Mayes, Jacqueline Mariscal, Kenneth Waldrup, and Rachel Curtis-Robles. Many individuals assisted in field and laboratory work associated with these projects, including in no particular order: Lisa Auckland, Jessica Rodriguez, Frida Cano, Alicia Leahy, Trevor Tenney, Zeb Thomas, Faith Weeks, Nicole Bertolini, Jessica Light, Justin Henningsen, Aleyda Galán, Edward Wozniak, John Barnes, Amani Bourji, Elise Birkner, Rosa Bañuelos, Cindy Barron, Kyle Voelker, Don Taylor, Richard Montoya, Chloe Goodwin, Valery Roman-Cruz, Martha Hensel, Alyssa Meyers, Italo Zecca, Kim Doll, Beverly Finneburgh, Adam Curtis, and Justin Henefey. All other work for the dissertation was completed independently by the student. Stipend funding was provided by the NIH T32 fellowship (2T32OD011083-06). The summer vet students (C. Goodwin, N. Bertolini, R. Bañuelos, E. Birkner) were supported by NIH T35 fellowships (2T35OD010991-11). For support of research costs, contributions came from the Bernice Barbour Foundation, the National Center for Veterinary Parasitology, and two TAMU CVM Graduate Studies Student Research Grants. vi NOMENCLATURE CF complement fixation DTU discrete typing unit (strain type) ELISA enzyme-linked immunosorbent assay ICT immunochromatographic test IFA indirect fluorescent antibody IHA indirect hemagglutination assay IIF indirect immunofluorescence NHP non-human primate vii TABLE OF CONTENTS Page ABSTRACT ............................................................................................................................. ii ACKNOWLEDGEMENTS .................................................................................................... iv CONTRIBUTORS AND FUNDING SOURCES .................................................................. vi NOMENCLATURE .............................................................................................................. vii TABLE OF CONTENTS ...................................................................................................... viii LIST OF FIGURES ................................................................................................................. x LIST OF TABLES ................................................................................................................. xii 1. INTRODUCTION: TOWARD AN ECOLOGICAL FRAMEWORK FOR ASSESSING RESERVOIRS OF VECTOR-BORNE PATHOGENS: WILDLIFE RESERVOIRS OF Trypanosoma cruzi ACROSS THE SOUTHERN UNITED STATES ............................................................................................................ 1 1.1 Introduction .................................................................................................................... 1 1.2 Ecological Framework for Defining and Characterizing Reservoirs ............................. 3 1.3 Trypanosoma cruzi Background .................................................................................... 9 1.4 Characterizing Reservoirs of T. cruzi in the US .......................................................... 12 1.5 Summary and Conclusion ...........................................................................................
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