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Ellison Dissertationfinal .Pdf Physiological Correlates of Bat Rabies Pathogenesis and Epizootiology by James Alec Ellison, Jr. A dissertation submitted to the Graduate Faculty of Auburn University in partial fulfillment of the requirements for the Degree of Doctor of Philosophy Auburn, Alabama August 2, 2014 Keywords: bats; lyssavirus; rabies virus pathogenesis; thermography; surveillance; emerging infectious diseases Copyright 2014 by James Alec Ellison, Jr. Approved by Mary T. Mendonça, Chair, Professor, & Graduate Program Officer of Biological Sciences Charles E. Rupprecht, Professor of Public Health and Epidemiology Haruka Wada, Assistant Professor of Biological Sciences James Wright, Professor of Pathobiology Abstract Rabies virus (RABV) is one model pathogen to consider for studying the dynamics of emerging infectious diseases under both laboratory and field conditions. The evolutionary history of RABV is characterized by regularly documented spillover infections and a series of notable host shifts. RABV is not a single, genetically homogeneous and unvarying virus, but a virus that has undergone genetic changes in adapting to local hosts and local habitats, such that each variant occupies a unique ecologic niche. The opportunity for re-emergence of rabies in mesocarnivores and the likelihood of sustained transmission of RABV in different species is influenced in part by host and variant-specific factors. Understanding pathogen maintenance and transmission within the natural reservoir may facilitate early detection strategies and targeted interventions prior to human spillover. As such, the general focus of this dissertation is to integrate a contemporary molecular, comparative, and ecological approach to complement our existing knowledge on bat rabies epizootiology and pathogenesis. The multidisciplinary approach of Chapter 2 consists of examining the physiologic response and phylogenetic relationships among bat RABV variants circulating the United States, including those implicated in recent and historical spillover infections in humans and mesocarnivores. To gain insight into viral pathogenesis and identify clinical features among individuals associated with experimental RABV infection, I along with the help of many collaborators evaluated the use of infrared thermography to detect thermographic changes associated with experimental RABV infection in captive big brown bats. These data suggest that infrared thermography has utility for ii discriminating rabid bats in natural field settings. In addition, focusing upon RABV circulating in the United States between 2008 - 2013 confirmed spillover events of bat RABV among carnivores and identified cross-species transmission events caused by four lineages of RABV associated with insectivorous bats. Rabies in bats is considered enzootic throughout the New World, but few comparative data are available for most countries in the region. The remedy for this lack of knowledge, Chapter 3 extends information on the geographic distribution of RABV circulation among bats to assess the broader public and veterinary health risks associated with bats in Guatemala. The detection of RABV neutralizing antibodies demonstrated viral circulation among multiple bat species in Guatemala. These data indicate that the proportion of seropositive bats varies significantly across trophic guilds, suggestive of complex intraspecific compartmentalization of RABV perpetuation. Chapter 4 seeks to address potential host shifts by examining differences in susceptibility, pathogenesis, and neurovirulence of major US RABV variants associated with bats and carnivores. The results of this study determined that the incubation period is influenced significantly by variant. These data also support the concept that spillover infections of biologically relevant North American RABV can be transient or dead ends, but dependent upon the isolate, dose, and route, could result in a sustained transmission when epizootiological conditions are ideal. Taken together, this dissertation suggests that the balance between pathogenesis and epizootiology is unique to the RABV variant and particular host. iii Table of Contents Abstract ......................................................................................................................................... ii List of Tables ............................................................................................................................... vi List of Figures ............................................................................................................................. vii List of Abbreviations ................................................................................................................... ix Chapter 1 ..................................................................................................................................... 1 References ...................................................................................................................... 13 Chapter 2 ................................................................................................................................... 19 Introduction .................................................................................................................... 20 Materials and Methods .................................................................................................. 23 Results ............................................................................................................................ 26 Discussion ..................................................................................................................... 29 References ...................................................................................................................... 42 Chapter 3 ................................................................................................................................... 44 Introduction .................................................................................................................... 48 Materials and Methods .................................................................................................. 51 Results ............................................................................................................................ 56 Discussion ..................................................................................................................... 59 Acknowledgements ........................................................................................................ 63 References ...................................................................................................................... 64 Chapter 4 ................................................................................................................................... 80 iv Introduction .................................................................................................................... 81 Materials and Methods .................................................................................................. 84 Results ............................................................................................................................ 89 Discussion ..................................................................................................................... 91 Acknowledgements ........................................................................................................ 94 References .................................................................................................................... 102 Chapter 5 ................................................................................................................................. 106 References .................................................................................................................... 116 v List of Tables Chapter 2 Table 1 Facial temperature of individual bats before inoculation of rabies virus and at time of euthanasia along with observed clinical signs ........................................................................... 33 Table 2 RABV specimens referred in this study ........................................................................ 35 Table 3 Glycoprotein primers used in this study ........................................................................ 37 Chapter 3 Table 1 Bats collected for rabies testing from nineteen field sites in Guatemala, 2009-2012 ... 67 Table 2 Bat sera tested for rabies virus neutralizing antibodies (positive/tested) from ten collection sites in Guatemala ...................................................................................................... 68 Table 3 Antigenic patterns of bat rabies viruses from Guatemala .............................................. 69 Table 4 Cell culture isolation attempts, and primary/ hemi-nested (nRT-PCR) from rabid bat specimens collected in Guatemala. ............................................................................................. 70 Table S List of nucleoprotein sequences included in the data set from Central and South American vampire bat RABV. .................................................................................................... 76 Chapter 4 Table 1 Survival following experimental RABV infection in red foxes by variant .................. 96 Table 2 RABV isolated from SMSGs by mouse inoculation test and pairwise comparison of nucleotide and amino-acid sequence identities of
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