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ABSTRACT Title: ECOLOGY AND MOLECULAR EPIDEMIOLOGY OF AVIAN AND SWINE INFLUENZA A VIRUSES IN GUATEMALA Ana Silvia Gonzalez Reiche, Ph.D., 2015 Directed By: Professor Dr. Daniel R. Perez, Department of Veterinary Medicine The greatest diversity of Influenza A viruses (IAV) is found in waterfowl species from numerous geographic locations. In addition, multiple IAV are, and continue to be, perpetuated in swine populations around the globe. Due to the zoonotic potential of IAV, and to respond more effectively to potential agricultural and public health threats, there is a need to increase surveillance in avian and swine hosts in understudied geographical regions. In Latin America, avian influenza surveillance has been scarce, localized only to places where outbreaks in poultry have occurred. Similarly, active swine influenza surveillance was implemented only after the emergence of the 2009 pandemic strain (pH1N1). The main objective of the project presented here was to investigate the circulation of IAV in wild birds and pigs in Guatemala. Over 2200 birds were sampled during six consecutive migration seasons from 2007 to 2013 in different locations. Virus prevalence detected by rRT-PCR in positive species ranged from 5.2% to 38%. Preliminary data indicates temporal variation of IAV prevalence in migratory waterfowl. Eighty-three viruses were recovered with 22 different subtype combinations. Through phylogenetic inferences and the analysis of virus genotypes and gene constellations of 60 fully sequenced genomes, we provide a detailed description of the genetic structure of avian IAV circulating in Guatemala. Our results suggest that the virus diversity in this location is sourced from multiple migration flyways from North America. Overlap of these flyways, in a natural geographical bottleneck such as the Neotropics, may contribute to the patterns of extensive genetic reassortment observed at a continental scale. In addition, the results from two nationwide multistage random surveys in pigs demonstrated circulation of swine influenza in commercial and peridomestic herds in Guatemala. Herd prevalence of IAV was 36.3% in 2010 and 34.6% in 2011. Viruses of the H1N1 and H3N2 subtypes and antibodies against viruses of distinct genetic lineages of these subtypes were detected. Our results indicate that human-animal contact likely plays a role in the IAV epidemiology in local swine populations. The findings from this research constitute the most abundant data on the ecology and epidemiology of animal influenza currently available for Central America. ECOLOGY AND MOLECULAR EPIDEMIOLOGY OF AVIAN AND SWINE INFLUENZA A VIRUSES IN GUATEMALA by Ana Silvia Gonzalez Reiche Dissertation submitted to the Faculty of the Graduate School of the University of Maryland, College Park, in partial fulfillment of the requirements for the degree of Doctor of Philosophy 2015 Advisory Committee: Professor Daniel R. Perez, Chair Professor Jeffrey DeStefano Associate Professor Najib El-Sayed Assistant Professor George Belov Dr. John Patton © Copyright by Ana Silvia Gonzalez Reiche 2015 Dedication To my grandmothers, Berta y Magdalena, for setting the example and show me to not limit my self, and encourage self-cultivation as part of pursuing freedom and happiness. ii Acknowledgements I would like to extent sincere thanks to my advisor, Dr. Daniel Perez, for giving me the opportunity to pursue a scientific career, and for believing in me to develop my work. For his advice and encouragement throughout the completion of my program. His mentoring and guidance beyond academics would be part of the many life lessons learned during my time in the lab. I would also like to thank all members of my dissertation committee Dr. George Belov, Dr. Najib El-Sayed, Dr. John Patton and Prof. Jeffrey DeStefano, for their time and valuable recommendations for improving this work and helping me to obtain my degree. I would like to thank Dr. Maria E. Morales-Betoulle, her mentoring during the time we worked together gave me the confidence to pursue higher education abroad. To Celia Cordón-Rosales, for trusting me the responsibility to undertake this project, her working ethics has set an example for my professional career. I would like to acknowledge the contribution of many friends and colleges from Universidad del Valle de Guatemala; Maria Luisa Müller, Ana Lucía Ramírez, Silvia Sosa, Maria Renee López, Carmen Lucia Contreras, Danilo Alvarez, who are all wonderful persons and scientist. The completion of this research would have been impossible without their work. I thank equally Dr. David Orellana and staff members of the Ministerio de Agricultura, Ganadería y Alimentación for their help obtaining the samples for the swine study. I would also like to thank Dr. Xhaoping Zhu, for his guidance during my coursework and graduate studies at the University of Maryland. To members of the Perez lab, past and present, Gloria Ramirez-Nieto, Matthew Angel, Troy Sutton, Courtney iii Finch, Adebimpe Obadam, Kemin Xu, Danielle Hickman, Hongjun Chen, Brian Kimble, Lindomar Pena, Jefferson Santos, Diego Lopez, Ashok Chockalingam, Yibin Cai, Erin Sorrell, Hongxia Shao and Jianqiang Ye. All the moments spent in the lab (including the coffee breaks) contributed not only to cultivate invaluable friendships, but also to my academic and professional growth. To Johanna Lavigne, for her constant support and unconditional friendship. To all faculty and staff from the Department of Veterinary Medicine; a special thanks to Andrea Ferrero-Perez and Judy Knight for their help way beyond assisting with the shipment of samples, and travels between Maryland and Guatemala related to this research. To Cheryl Nichols from the University of Maryland’s EEIGS program for English editing of chapters 1, 4, 5 and 6. To my friends in Maryland, Maíra, Juliet, Iraní and Viví, for the fun and all the moments spend together that helped to keep me sane. To Alvaro and Marcia Molina- Cruz, Sophia and Fernando for becoming my family during the time being away from home. A very special thanks to João for his constant encouragement, love and support. Without your company it would have been much harder to achieve my goal. Your constant questioning and constructive input during many thoughtful discussions helped me to improve my work; may that continue for years to come. Finally to my family, my father Luis, mother Liliana, and siblings Luisa and Luis Pedro, there are no words to describe how grateful I am to you. You showed me, each on you own way, to not set boundaries to my aspirations. I thank you from the bottom of my heart for all the sacrifices and help to make reality this dream. Thank you for being a constant source of happiness and motivation throughout my life. iv Table of Contents Dedication .......................................................................................................................... ii Acknowledgements .......................................................................................................... iii Table of Contents .............................................................................................................. v List of Figures .................................................................................................................. vii List of tables...................................................................................................................... xi List of abbreviations ...................................................................................................... xiv Chapter 1. Introduction ........................................................................................................ 1 1.1. Literature Review: Influenza A virus ................................................................... 1 1.1.1. Classification.................................................................................................. 1 1.1.2. Virus structure ................................................................................................ 2 1.1.3. Genome structure ........................................................................................... 2 1.1.4. Viral proteins ................................................................................................. 3 1.1.5. Replication cycle ............................................................................................ 7 1.1.6. Evolution of Influenza A Virus.................................................................... 10 1.1.7. Influenza A viruses in animal hosts ............................................................. 14 1.1.8. Influenza A viruses in wild birds ................................................................. 15 1.1.9. Influenza A viruses in pigs .......................................................................... 20 1.2. Rationale for this work........................................................................................ 27 1.3. Research objectives ............................................................................................. 29 Chapter 2. Influenza A Viruses from Wild Birds in Guatemala Belong to the North American Lineage ............................................................................................ 31 2.1. Abstract ............................................................................................................... 31 2.2. Introduction ......................................................................................................... 32 2.3. Materials
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