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Eco-Epidemiological Implications of the Diversity of Triatominae (Hemiptera

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Eco-Epidemiological Implications of the Diversity of Triatominae (Hemiptera Eco-epidemiological Implications of the Diversity of Triatominae (Hemiptera: Reduviidae) in Ecuador: what do we know and what do we need to do? A dissertation presented to the faculty of the College of Arts and Sciences of Ohio University In partial fulfillment of the requirements for the degree Doctor of Philosophy Anita G. Villacís Salazar May 2020 © 2020 Anita G. Villacís. All Rights Reserved. This dissertation titled 2 Eco-epidemiological Implications of the Diversity of Triatominae (Hemiptera: Reduviidae) in Ecuador: what do we know and what do we need to do? by ANITA G. VILLACÍS has been approved for the Department of Biological Sciences and the College of Arts and Sciences by Mario J. Grijalva Professor of Biomedical Sciences Florenz Plassmann Dean, College of Arts and Sciences 3 Abstract VILLACIS SALAZAR ANITA GABRIELA, Ph.D., May 2020, Biological Sciences Eco-epidemiological Implications of the Diversity of Triatominae (Hemiptera: Reduviidae) In Ecuador: what do we know and what do we need to do? Director of Dissertation: Mario J. Grijalva Chagas disease affects Latin-American countries and Ecuador is not the exception. The kissing bugs, Triatominae are vectors of Trypanosoma cruzi the causative agent of this disease. At least 151 triatomine species have been recognized as potential vectors worldwide. Sixteen species of Triatominae have been reported in Ecuador, distributed in twenty of the twenty-four provinces. Over the last 10 years, our group from the Center for Research Health in Latin America (CISeAL) at the Pontificia Universidad Católica del Ecuador, and the Infectious and Tropical Disease Institute at Ohio University carried out intensive research in two very different provinces, Manabí (central coastal region) and Loja (southern Andean region), which they reported as having the highest level of triatomine infestations within the country. These two regions differ from each other specifically in their: 1) bioclimatic conditions, 2) material of the house construction (domicile), 3) peridomicile structures and 4) sylvatic environments. In order to improve the knowledge of the transmission cycles of CD, we need to first comprehend the distribution of the different species of triatominae in both regions. Then, I investigated the presence of sylvatic populations of Triatomines in the palms and nests surrounding human dwellings in approximately 70 communities in the Ecuadorian central coastal region, to understand the dynamics of sylvatic cycle of Chagas disease. 4 After that, I explored the genetic variability, spatial structuring, and demographic history of the main vector of CD in Ecuador, R. ecuadoriensis, collected in this central coast region. Finally, I evaluated the effectiveness of the manual search method for detecting the presence of the triatomines in the DUs (Domiciliary Units) through repeated sampling in six rural communities in southern Andean region of Ecuador. With this work, I 1) understood the patterns of sylvatic sites infestation all over the central coast region of Ecuador. 2) Showed that the absence of spatial genetic structure could be due to climatic conditions and to passive transportation of palms tree materials (leaves and fruits) where R. ecuadoriensis are living. 3) Suggested that several infested microhabitats (domestic and peridomestic) might be undetected during a single examination, especially when vector density is low. A wrong evaluation of DUs infestation misconstrue transmission risk assessment and mislead program managers’ decisions. Therefore, recommendations to improve triatomine control-surveillance systems in the both regions were proposed and discussed in each chapter. Key words: Chagas disease, central coastal region, southern Andean region, habitats, Triatomines Ecuador 5 Dedication To God for giving me health and life. To my parents for their example. To my brothers for their love and support. To my husband for his unconditional love and patience. 6 Acknowledgments I am very grateful to a number of people who helped me during the dissertation process. Without them, I could not have completed this project. First, I would like to acknowledge to my advisor, Dr. Mario J. Grijalva, a wonderful mentor who introduced me to the world of Chagas disease and Triatomines. I am grateful for him showing me the importance and true meaning of research, seeking as a fundamental goal to help and be concerned about the welfare of others, especially the people exposed to this neglected and silent disease. Second, to the members of my dissertation committee: Dr. Sarah Wyatt, Dr. Calvin James and Dr. Benjamin Bates, for their invaluable help, advice, and constructive criticism during this process. Third, to Dr. Simone Frédérique Brenière, for her guidance, support, patience and friendship. Thank you, for encouraging me during the last 5 years. Fourth, to Dr. Dawn Bikowski, Lara Wallace and Edna Lima for their valuable advice and patience during their classes. Fifth, to Dr. Stéphanie Depickère and Christian Barnabé from the Institut de recherche pour le développement (IRD-France), for their technical support. To my technicians and students (Marco Orozco, Katherine Mosquera, Dino Sánchez, Anabel Padilla, Juan José Bustillos, María Soledad Santillán, Frances Castillo, Álvaro Lara, Daphne Armas), at the Center for Research on Health in Latin America (CISeAL), for their help during the period time as a professor. 7 To Dra. Sofía Ocaña and Ana Lucía Moncayo, for their friendship and technical advice. Thank you, for encouraging and strengthening me throughout this process. I would like to than to Lori Lammert, María José Carrasco, Angela Méndez, Andrea Padilla, Patricia Mora and all the staff from the Infectious and Tropical Disease Institute (ITDI) of Ohio University. Special thanks to the personnel of the National Service for Malaria Eradication (SNEM) of the Ecuadorian Ministry of Health for their help in field studies. Finally, I would like to share my fraternal and immense gratitude to the people of the rural communities, for their hospitality. Thank you for open doors and hearts. Financial support was received from IRD (UMR-INTERTRYP, CIRAD, University of Montpellier), the Pontifical Catholic University of Ecuador (C13025 [Grijalva], E13027 [Grijalva], G13042 [Baus], G13026 [Grijalva], H13174 [Grijalva], I13048 [Grijalva], J13067 [Yumiseva], J13039 [Grijalva], K13063 [Villacís], L13255 [Yumiseva], L13254 [Villacís] and M13480 [Villacís], European Union PF7. ChagasEpiNet (project 223034) [Grijalva], National Institutes of Health (www.nih.gov), grant number: R15 AI105749-01A1 [Grijalva], FOGARTI. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. Funding agencies did not play any role in the design of the study or in the data analyses and drafting of this dissertation. 8 Table of Contents Page Abstract ...............................................................................................................................3 Dedication ...........................................................................................................................5 Acknowledgements .............................................................................................................6 Chapter 1: Introduction ......................................................................................................15 1.1. References .............................................................................................................22 Chapter 2: Filling the knowledge gap of sylvatic Triatomines in the central coastal region of Ecuador ..........................................................................................................................24 2.1. Abstract ..................................................................................................................24 2.2. Introduction ............................................................................................................25 2.3. Methods ..................................................................................................................29 2.3.1. Study area .........................................................................................................29 2.3.2. Capture site registration and triatomine collection ..........................................30 2.3.2.1. Triatomine collection in mammal in bird nests in trees ............................30 2.3.2.1. Triatomine collection in palm trees, Phytelephas aequatorialis ..............30 2.3.2.1. Triatomine collection for evaluation of baited vs. manual collection ......31 2.3.3. Registration ....................................................................................................31 2.3.4. Collection and transport of triatomines ...........................................................32 2.3.5. Processing of the triatomine species in the laboratory ....................................32 2.3.6. Data analysis ...................................................................................................33 2.4. Results ....................................................................................................................34 2.4.1. Entomological indexes in mammal and bird nests in trees .............................34 2.4.2. Entomological indices in Phytelephas aequatorialis palm trees from north to south of Manabí province in sylvatic environment .......................................................36 2.4.3. Triatomine
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