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Characterizing the Fecal Shedding of Swine Infected with Japanese Encephalitis Virus

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Characterizing the Fecal Shedding of Swine Infected with Japanese Encephalitis Virus Characterizing the fecal shedding of swine infected with Japanese encephalitis virus by Konner Cool B.S., Kansas State University, 2017 A REPORT submitted in partial fulfillment of the requirements for the degree MASTER OF SCIENCE Department of Diagnostic Medicine/Pathobiology College of Veterinary Medicine KANSAS STATE UNIVERSITY Manhattan, Kansas 2020 Approved by: Major Professor Dr. Dana Vanlandingham Copyright © Konner Cool 2020. Abstract Japanese encephalitis virus (JEV) is an enveloped, single-stranded, positive sense Flavivirus with five circulating genotypes (GI to GV). JEV has a well described enzootic cycle in endemic regions between swine and avian populations as amplification hosts and Culex species mosquitoes which act as the primary vector. Humans are incidental hosts with no known contributions to sustaining transmission cycles in nature. Vector-free routes of JEV transmission have been described through oronasal shedding of viruses among infected swine. The aim of this study was to characterize the fecal shedding of JEV from intradermally challenged swine. The objective of the study was to advance our understanding of how JEV transmission can be maintained in the absence of arthropod vectors. Our hypothesis is that JEV RNA will be detected in fecal swabs and resemble the shedding profile observed in swine oral fluids, peaking between days three and five. In this study fecal swabs were collected throughout a 28-day JEV challenge experiment in swine and samples were analyzed using reverse transcriptase-quantitative polymerase chain reaction (RT-qPCR). Quantification of viral loads in fecal shedding will provide a more complete understanding of the potential host-host transmission in susceptible swine populations. Our results show that fecal shedding of JEV appears to mimic that of oral shedding, with peak viral loads detected around day five post-infection. The detection of JEV viral genomes in fecal specimens indicate a potential for fecal shedding to contribute to transmission of JEV in the absence of vectors. These findings are significant in developing control strategies to mitigate the agricultural and public health threats created by JEV in endemic regions. Table of Contents List of Figures ................................................................................................................................ vi Acknowledgements ....................................................................................................................... vii Chapter 1 - An Overview of Japanese Encephalitis Virus .............................................................. 1 Introduction ................................................................................................................................. 1 History ........................................................................................................................................ 2 Ecology ....................................................................................................................................... 3 Epidemiology of Japanese Encephalitis Virus ............................................................................ 5 Geographic Distribution of Japanese Encephalitis Virus ....................................................... 5 Incidence ................................................................................................................................. 6 Human and Animal Diseases Caused by Japanese Encephalitis Virus .................................. 7 Control .................................................................................................................................... 9 Transmission ............................................................................................................................. 10 Host-Pathogen Interactions ....................................................................................................... 12 Vector – Pathogen Interaction............................................................................................... 13 Vertebrate Host – Pathogen Interaction ................................................................................ 15 Vector-Free Transmission ......................................................................................................... 16 Molecular Biology of Japanese encephalitis virus ................................................................... 18 Diagnosis and molecular detection of Japanese encephalitis virus .......................................... 24 Chapter 2 - Materials and Methods ............................................................................................... 27 Introduction ............................................................................................................................... 27 Cell lines ................................................................................................................................... 27 Virus .......................................................................................................................................... 28 Determination of Infectious Titers ............................................................................................ 28 Animals ..................................................................................................................................... 29 Sample Collection ..................................................................................................................... 29 Extraction of RNA .................................................................................................................... 30 RT-qPCR .................................................................................................................................. 31 Chapter 3 - Profile of Fecal Shedding Throughout JEV Infection in Domestic Pigs ................... 34 Introduction ............................................................................................................................... 34 iv Results ....................................................................................................................................... 35 Kinetic Profile of Intradermally Challenged Domestic Pigs ................................................ 35 Conclusion ................................................................................................................................ 39 Chapter 4 - Conclusion and Future Directions ............................................................................. 40 References ..................................................................................................................................... 43 v List of Figures Figure 1.1. Enzootic transmission cycle of JEV is supported by competent mosquito vectors (Culex species), swine amplification hosts, ardeid avian species reservoir hosts. Humans are considered incidental, dead-end hosts. Dotted lines represent hypothesized (fecal-oral) and experimentally demonstrated (oronasal) transmission events that occur between swine and are not known to occur in nature. .......................................................................................... 12 Figure 2.1. JEV genome with structural (C, prM, E) and non-structural (NS1, NS2, NS3, NS4, NS5) genes and associated nucleotide positions. The targeted nucleotide positions at 10224 – 10286 for the primer and probe are highlighted in red. Modified from Lyons 2018......... 32 8 Figure 2.2. Standard curve generated from JE-91 stock of 8.95 x 10 TCID50/mL. Y= - 2 1.422ln(x)+37.838, R =0.9979, LOD at Cq value of 34 = 14.865 g.e.q. to TCID50/mL. ..... 33 Figure 3.1. Average of daily RT-qPCR results from fecal swabs collected on days 0-7 dpi. from 7 3-week-old white-line crossbred pigs ID inoculated with 10 TCID50 JE-91. b-e) Daily profile of individual pigs with detectable viral RNA. Values below the threshold cutoff Cq value of 34 (red line) are not pictured. .................................................................................. 37 Figure 3.2. Box-and-whisker plot representing the mean (X), median, range, and interquartile 7 range through 7 days of fecal shedding in domestic pigs inoculated ID with JEV 10 TCID50 JE-91. Values below the threshold cutoff Cq value of 34 are not pictured. ......................... 38 vi Acknowledgements I would like to extend my gratitude to the following: Dr. Dana Vanlandingham for acquisition of funding and MS program mentorship and to my committee members, Dr. Stephen Higgs and Dr. Yan-Jang (Scott) Huang for their expertise and guidance throughout this program. Dr. So Lee Park and team for the study design and fecal sample collection. Dr. Yan-Jang (Scott) Huang and Ms. Amy Lyons for the preliminary work on primer selection and technical training on extraction methods and RT-qPCR. This project is the result of funding provided by the USDA ARS Agreement No. 58-5430- 4-021, Biology of Mosquito Vectors of Arbovirus Transmission Associated with Emerging Disease Threats of Livestock, the State of Kansas National Bio and Agro-Defense Facility Transition Fund. Preliminary work supporting the development and validation of RT-qPCR assays that aided in the successful completion of this project was also supported by the Swine Health Information Center project 16–258, with additional funding provided by the United States Department of Homeland Security Science and Technology Directorate's Homeland Security Advanced Research Projects Agency
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