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I CHARACTERIZATION of ORTHOREOVIRUSES ISOLATED from AMERICAN CROW (CORVUS BRACHYRHYNCHOS) WINTER MORTALITY EVENTS in EASTERN CA

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I CHARACTERIZATION of ORTHOREOVIRUSES ISOLATED from AMERICAN CROW (CORVUS BRACHYRHYNCHOS) WINTER MORTALITY EVENTS in EASTERN CA CHARACTERIZATION OF ORTHOREOVIRUSES ISOLATED FROM AMERICAN CROW (CORVUS BRACHYRHYNCHOS) WINTER MORTALITY EVENTS IN EASTERN CANADA A Thesis Submitted to the Graduate Faculty in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY In the Department of Pathology and Microbiology Faculty of Veterinary Medicine University of Prince Edward Island Anil Wasantha Kalupahana Charlottetown, P.E.I. July 12, 2017 ©2017, A.W. Kalupahana i THESIS/DISSERTATION NON-EXCLUSIVE LICENSE Family Name: Kalupahana Given Name, Middle Name (if applicable): Anil Wasantha Full Name of University: Atlantic Veterinary Collage at the University of Prince Edward Island Faculty, Department, School: Department of Pathology and Microbiology Degree for which thesis/dissertation was Date Degree Awarded: July 12, 2017 presented: PhD DOCTORThesis/dissertation OF PHILOSOPHY Title: Characterization of orthoreoviruses isolated from American crow (Corvus brachyrhynchos) winter mortality events in eastern Canada Date of Birth. December 25, 1966 In consideration of my University making my thesis/dissertation available to interested persons, I, Anil Wasantha Kalupahana, hereby grant a non-exclusive, for the full term of copyright protection, license to my University, the Atlantic Veterinary Collage at the University of Prince Edward Island: (a) to archive, preserve, produce, reproduce, publish, communicate, convert into any format, and to make available in print or online by telecommunication to the public for non-commercial purposes; (b) to sub-license to Library and Archives Canada any of the acts mentioned in paragraph (a). I undertake to submit my thesis/dissertation, through my University, to Library and Archives Canada. Any abstract submitted with the thesis/dissertation will be considered to form part of the thesis/dissertation. I represent that my thesis/dissertation is my original work, does not infringe any rights of others, including privacy rights, and that I have the right to make the grant conferred by this non- exclusive license. If third party copyrighted material was included in my thesis/dissertation for which, under the terms of the Copyright Act, written permission from the copyright owners is required I have obtained such permission from the copyright owners to do the acts mentioned in paragraph (a) above for the full term of copyright protection I retain copyright ownership and moral rights in my thesis/dissertation, and may deal with the copyright in my thesis/dissertation, in any way consistent with rights granted by me to my University in this non-exclusive license. I further promise to inform any person to whom I may hereafter assign or license my copyright in my thesis/dissertation of the rights granted by me to my University in this non-exclusive license. Signature Date ii University of Prince Edward Island Faculty of Veterinary Medicine Charlottetown CERTIFICATION OF THESIS WORK We, the undersigned, certify that Anil Wasantha Kalupahana B.V.Sc., M.Sc., candidate for the degree of Doctor of Philosophy has presented his thesis with the following title: ‘characterization of orthoreoviruses isolated from American crow (Corvus brachyrhynchos) winter mortality events in eastern Canada’ that the thesis is acceptable in form and content, and that a satisfactory knowledge of the field covered by the thesis was demonstrated by the candidate through an oral examination held on July 12, 2017. Examiners ____________________________________ Dr. ___________________________________ Dr. ___________________________________ Dr. ___________________________________ Dr. ___________________________________ Dr. iii ABSTRACT A putative reovirus has been isolated from mortality events in American crows, of eastern Canada. The purpose of this research is to establish biological characteristics of this American crow reovirus, its genetic relatedness to other reoviruses and to determine its pathogenic significance for commercial poultry. The growth properties of the isolates were assessed in VERO and QM 5 cell lines, the partial S2 and S4 genome segments were sequenced and phylogenetic analysis were performed and a pathogenicity trial in SPF chickens was done. Twenty-six suspect orthoreoviruses (2 from PEI and 24 from Ontario) were isolated from winter mortality events affecting American crow in eastern Canada. Fourteen isolates exhibiting CPE were analyzed (2 from PEI and 12 from Ontario) using avian orthoreovirus genome segment-specific primers for segments S2 and S4, in a conventional one-step RT-PCR assay. Results confirmed that 14 of the 26 viruses were from the family Reoviridae, 100 % of the PEI isolates (2/2) and 91.67% of the Ontario isolates (11/12) were avian orthoreoviruses; and 1/24 (4.2%) of the Ontario isolates was a rotavirus. This is the first report of isolation and accurate identification of avian orthoreoviruses from American crow mortality events supporting the etiological role of American crow orthoreoviruses in the winter crow mortality syndrome. Analysis of the S2 sequences discovered that the PEI and Ontario isolates had sequence similarity to avian orthoreovirus isolates of commercial poultry. Analysis of the S4 sequences revealed that both isolates had the highest sequence similarity with Tvärminne avian virus (TVAV). S2 and S4 genome segments of the two isolates had 99.8% and 95.2% sequence similarity respectively with each other. iv Phylogenetic analysis of S2 sequences placed these viruses in the same cluster with avian orthoreoviruses of commercial poultry. However, the S4 phylogenetics established that American crow orthoreovirus isolates have a closer relationship to the TVAV. These American crow isolates are genetically distinct from most other avian- origin orthoreoviruses and have a reassorted S4 segment which has been acquired from the TVAV. In the experimental infection of SPF chickens, American crow orthoreovirus isolates crossed the species barrier resulted in clinical disease with high morbidity and low mortality producing enteric lesions in the lower gastrointestinal tract from ventriculus to jejunum. The sensitivity and specificity of S4 genome segment specific conventional one- step RT-PCR assay for American crow orthoreovirus was assessed. The assay had a 100% analytical specificity, however virus isolation in VERO cells had higher detection limit than the RT-PCR. Application of this assay for the detection of American crow orthoreovirus in intestinal tissue confirmed 9 positives out of 44 samples tested. In addition to the 9 RT-PCR positives, another 5 samples of the 44 produced characteristic CPE in VERO cells. Infected first passage VERO cell lysate of these 5 samples yielded orthoreovirus S4 segment specific PCR band confirming the CPE observed in VERO cells was due to American crow orthoreovirus. This RT-PCR assay is useful as an ancillary diagnostic tool for routine detection of avian orthoreoviruses. v ACKNOWLEDGEMENTS First and foremost I’d like to gratefully acknowledge the excellent supervision and contribution of my co-supervisors Drs. Fred Kibenge and Scott McBurney. It was a privilege to work with these two gentlemen who guided me the way to be an independent scientist. I wish to express my gratitude to my supervisory committee members Drs. Barb Horney, Paul Hanna, Jonathan Spears and Davor Ojkic for their best intellectual inputs, invaluable support, direction and constructive advice. I would like to acknowledge the research support provided by Aquatic Virology Collaborating Centre and financial support by the Graduate Student Scholarship awarded by the Department of Pathology and Microbiology. I am sincerely thankful to Drs. Ted Leighton and Oswin Perera for providing travel expenses. My special appreciation goes to Dr Molly Kibenge for her encouragement, kind counsel and wise advice in hard times. My acknowledgement extend to Toki, Darlene, and Fiep for their kind assistance. My thanks are due to the staff of AVC North Barn experimental animal facility, post mortem lab and the histology lab who assisted me on various points. I’d like to thank my family especially Ruwani for her love and support and my two daughters Amanda and Janudi for their patience and understanding. My gratefulness is for my friends Drs. Sarath Chandrasekere, Swarna Chandrasekere, Sarath Ekanayaka, and Muditha Balasuriya for their encouragement and excellent support to pursue the goal of this doctorate. Last but not least I extend my appreciation to the PEI Sri Lankan community for the fun and caring we shared. vi I wish to dedicate this thesis to my parents, wife and daughters. I profoundly thank them for their support, encouragement and understanding. vii TABLE OF CONTENTS TITLE PAGE i THESIS/DISSERTATION NON-EXCLUSIVE LICENCE ii CERTIFICATION OF THESIS WORK iii ABSTRACT iv ACKNOWLEDGEMENT vi DEDICATION vii TABLE OF CONTENTS viii LIST OF TABLES xiv LIST OF FIGURES xvi ABBREVIATIONS xviii 1. GENERAL INTRODUCTION 1 1.1. The family Reoviridae 1 1.1.1. Virus classification and taxonomy 1 1.1.2. The genus Orthoreovirus 2 1.2. Avian orthoreovirus – virion properties and replication 4 1.2.1. Molecular structure 4 1.2.1.1. Electron microscopy (virus morphology) 4 1.2.1.2. Genome 5 1.2.1.3. Viral proteins 6 1.2.1.4. Physicochemical properties 12 1.2.2. Propagation of avian orthoreoviruses 14 1.2.2.1. Embryonated eggs 14 1.2.2.2. Primary cell cultures 15 1.2.2.3. Continuous cell lines 17 1.2.3. Antigenic characteristics of avian orthoreoviruses 20 1.2.3.1. Common precipitin antigen 21 1.2.3.2. Neutralizing antigen 21 1.3. Pathogenesis of avian orthoreovirus infection in chickens 23 1.3.1. General pathogenesis 23 1.3.1.1. The effects of age at infection on avian orthoreovirus disease 26 1.3.1.2. The effects of virus strain, dose and the route of infection on avian orthoreovirus pathogenicity 28 1.3.1.3. The effect of breed on avian orthoreovirus pathogenesis 28 1.3.1.4. The effect of co-infections on the ability of avian orthoreovirus to cause disease 29 1.3.1.5. The effect of dietary factors on avian orthoreovirus disease 30 1.3.2. Pathogenic avian orthoreovirus isolates 30 1.3.3. Tenosynovitis/viral arthritis 33 1.3.4.
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