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Vector-Borne Diseases Transmission in Ecuador: Implication of Vertebrate Hosts As Vector-Borne Diseases Transmission in Ecuador: Implication of Vertebrate Hosts as Food Source of Triatomines in Chagas Disease, and the Diversity of Anopheles Mosquites in Malaria 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 Sofia B. Ocana-Mayorga May 2020 © 2020 Sofia B. Ocana-Mayorga. All Rights Reserved. 2 This dissertation titled Vector-Borne Diseases Transmission in Ecuador: Implications of Vertebrate Hosts as Food Source of Triatomines in Chagas Disease and the Diversity of Anopheles Mosquitoes in Malaria by SOFIA B. OCANA-MAYORGA 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 OCANA-MAYORGA, SOFIA B., Ph.D., May 2020, Biological Sciences Vector-Borne Diseases Transmission in Ecuador: Implications of Vertebrate Hosts as Food Source of Triatomines in Chagas Disease and the Diversity of Anopheles Mosquitoes in Malaria Director of Dissertation: Mario J. Grijalva Malaria and Chagas disease are two of the most important vector-borne parasitic infections in Ecuador. A better understanding on the transmission scenarios is needed to propose effective strategies for disease control. In Chagas disease, human-vector dynamics is not well understood; however, the presence of active transmission in endemic areas has been demonstrated. The pattern of blood meals of insects that are vector of diseases is fundamental to unveil transmission dynamics. In this study DNA from intestinal contents of triatomines were used to amplify fragments of cytb mitochondrial genes. The results showed that humans are a main source of food for triatomines, indicating that the vector-human contact is more frequent than previously thought. Although other groups of mammals such as rodents are also an available source of blood, birds (particularly chickens) might have a predominant role in the maintenance of triatomines in these areas. The presence of human blood meal in 42% of the samples, even in peridomiciliar and sylvatic environments, together with high infection rates with Trypanosoma cruzi (the causal agent of Chagas disease) indicate that humans are not accidental host, but an important source of blood for triatomines in all environments, and with high risk of T. cruzi transmission. Consequently, domestic-centered strategies might 4 not prevent vectorial transmission and data of Chagas disease cases might be underestimated. Strategies for Chagas disease control in Ecuador require to evaluate capacity dispersal of triatomines and outdoor activities as risk factors for parasite transmission in Ecuador. In the case of malaria, the lack of a complete inventory of vector species is a barrier for an understanding of malaria transmission. Even more, implication on transmission of reported species is still poorly understood. Identification of species is mainly carried out by morphological characteristics; however, it fails in discriminating species closely related. Molecular tools are a good alternative to discriminate species. In this study, the internal transcribed spacer 2 (ITS2) and the cytochrome oxidase I (COI), were used for species identification. The Restriction Fragment Length Polymorphism (RFLP) of the ITS2 is a technique that allows the analysis of a great amount of samples and it is cheaper than sequencing. However, variability within species and populations needs to be further known. The results demonstrated the great complexity of taxonomic identification of species, particularly of individuals from species complex, such as the case of the Oswaldoi group which species are sympathric in the Amazon region. In Ecuador, particularly, in the Amazon region we recommend the sequence of COI for anopheline identification until a better knowledge of the diversity is obtained. This study confirmed Ny. albimanus as the most abundant species in the Pacific coast and it also extends the geographic distribution of An. calderoni. In the Amazon region, Ny. benarrochi B is reported for first time in the Ecuadorian Amazon. A comprehensive survey of Anopheles and Nyssorhynchus species in Ecuador is required to facilitate and targeted malaria control strategies in Ecuador. 5 DEDICATION To my parents, to Romina and Martin, and to my brothers and sisters of blood and by choice. 6 ACKNOWLEDGMENTS My gratitude to Dr. Mario J. Grijalva who has been my mentor and inspiration to pursue a carreer in infectious disease. Thank you for teaching me why we do what we do. To Dr. Simone Frédérique Brèniere for being an incredible support during this journey and for being my female role model in science. I also want to thank my colleagues, without them I could not have achieve it: Anita Villacis, César Yumiseva, Ana Lucía Moncayo, Fabían Sáenz, Juan José Bustillos, Giovan Gómez for sharing your knowledge and time during the field research, collection and analysis of the data. A sincere gratitude to the community members of Loja, Manabi and El Oro provinces, for their selfless support. An special acknowledgment to the institutions that funded this study: Pontifica Universidad Católica del Ecuador (N234369, I13054, J13034, K13069) UNICEF/UNDP/World Bank/WHO Special Programme for Reseach and Training in Tropical Diseases (TDR) (A20785), Pan American Health Organization (A60655), the European Commission Framework Programme 7 Project (ChagasEpiNet-contract No. 223034), Fogarty International Center (TW008261). 7 TABLE OF CONTENTS Page Abstract ............................................................................................................................... 3 Dedication ........................................................................................................................... 5 Acknowledgments............................................................................................................... 6 List of Tables .................................................................................................................... 10 List of Figures ................................................................................................................... 11 Chapter 1: Introduction ..................................................................................................... 12 1.1. Vector-borne Transmission of Chagas Disease and Malaria in Ecuador ....... 12 Chapter 2: Triatomine Feeding Profiles, Trypanosoma cruzi Infection and transmission Implications in Domestic and Sylvatic Habitats ............................................................... 15 2.1. Abstract ........................................................................................................... 15 2.2. Background ..................................................................................................... 17 2.3. Methodology ................................................................................................... 20 2.3.1. Triatomine Selection ............................................................................... 20 2.3.2. DNA Extraction and Natural Infection with Trypanosomes ................... 21 2.3.3. Comparison of Primer Sets for Detection of Blood Meals ..................... 22 2.3.4. Amplification and Identification of the Sources of Blood Meals ........... 22 2.4. Results ............................................................................................................. 24 2.4.1. Sensitivity of the Different Primer Sets .................................................. 24 2.4.2. Vertebrate Blood Meal Source Diversity ................................................ 24 2.4.3. Blood Meal Diversity and Trypanosoma cruzi Infection in the Different Environments ........................................................................................................ 25 2.4.4. Vertebrate Blood Meal Source per Triatomine Species, Stages and Collection Environment ........................................................................................ 28 2.5. Discussion ....................................................................................................... 32 2.5.1. Diversity of Mammal Hosts and its Implication in Trypanosoma cruzi Transmission ......................................................................................................... 33 2.5.2. Birds and its Role in Triatomine Population Maintenance ..................... 36 2.5.3. Triatomine Species and Blood Meal Preference ..................................... 37 2.5.4. Triatomine Dispersal and Access to Vertebrate Hosts ............................ 38 2.6. Conclusions ..................................................................................................... 40 2.7. References ....................................................................................................... 41 8 Chapter 3: Human Blood Meals in Sylvatic Triatomines Challenges Domestic-Centered Strategies for Prevention of Trypanosoma cruzi Transmission in Ecuador ..................... 47 3.1. Abstract ........................................................................................................... 47 3.2. Background ..................................................................................................... 49 3.3. Methodology ................................................................................................... 52 3.3.1. Study Area
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