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VIRULENCE and PATHOGENESIS of NEWCASTLE DISEASE VIRUS ISOLATES for DOMESTIC CHICKENS by GLAUCIA DENISE KOMMERS (Under the Direct

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VIRULENCE and PATHOGENESIS of NEWCASTLE DISEASE VIRUS ISOLATES for DOMESTIC CHICKENS by GLAUCIA DENISE KOMMERS (Under the Direct VIRULENCE AND PATHOGENESIS OF NEWCASTLE DISEASE VIRUS ISOLATES FOR DOMESTIC CHICKENS by GLAUCIA DENISE KOMMERS (Under the Direction of Corrie C. Brown and Daniel J. King) ABSTRACT Newcastle disease virus (NDV) isolates vary greatly in virulence and pathogenicity depending on several factors including the host species and the infecting virus strain. This research was performed in order to investigate the effect of serial passages of several NDV isolates in domestic chickens. Six isolates were recovered from pigeons and six isolates had heterogeneous origin (recovered from chickens, wild, and exotic birds). A monoclonal antibody (MAb) panel revealed that four of the pigeon-origin isolates were the variant pigeon paramyxovirus-1 (PPMV-1) and two of them were avian paramyxovirus-1 (APMV-1) isolates. Pathotyping tests performed before and after passage in chickens demonstrated increased virulence of the passaged PPMV-1 isolates and high virulence of the original isolates of APMV-1. However, the PPMV-1 were still of moderate virulence for chickens after passages. The fusion protein cleavage site amino acid sequence of all six pigeon-origin (PPMV-1 and APMV-1) isolates was typical of virulent NDVs. Although the results of the pathotyping tests indicated a virulence increase of all passaged PPMV-1 isolates, clinical disease was limited to depression and nervous signs in some of the chickens inoculated intraconjunctivally. However, severe lesions were observed mostly affecting the heart and brain after intraconjunctival inoculation with passaged PPMV-1 isolates. Pigeons must be considered seriously as a potential source of NDV infection and disease for commercial poultry flocks. All six heterogeneous-origin isolates were characterized by reactivity to MAbs as members of the APMV-1 serotype. Three isolates showed low virulence for chickens before and after passage and had the F protein cleavage site typical of low virulence viruses. The other three heterogeneous-origin isolates were classified by the pathotyping tests and sequence analysis of the F protein cleavage site as moderate to highly virulent for chickens. An isolate recovered from an exotic dove had marked virulence increase after passage. The exact mechanism for the virulence increase observed with this isolate remains undefined. A pathogenesis study with the chicken-passaged isolates revealed that two of them were highly virulent for chickens, with marked tropism for lymphoid tissues. The results reported here demonstrate the high risk for domestic chickens represented by some NDV- infected non-poultry species. INDEX WORDS: Apoptosis, Avian paramyxovirus-1, Avian virology, Chickens, Immunohistochemistry, In situ hybridization, Newcastle disease, Nucleotide sequence analysis, Pathogenesis, Pigeon paramyxovirus-1, Veterinary Pathology VIRULENCE AND PATHOGENESIS OF NEWCASTLE DISEASE VIRUS ISOLATES FOR DOMESTIC CHICKENS by GLAUCIA DENISE KOMMERS Médico Veterinário, Universidade Federal de Santa Maria, Brazil, 1987 M.S., Universidade Federal de Santa Maria, Brazil, 1993 A Dissertation Submitted to the Graduate Faculty of The University of Georgia in Partial Fulfillment of the Requirement for the Degree DOCTOR OF PHILOSOPHY ATHENS, GEORGIA 2002 © 2002 Glaucia Denise Kommers All Rights Reserved. VIRULENCE AND PATHOGENESIS OF NEWCASTLE DISEASE VIRUS ISOLATES FOR DOMESTIC CHICKENS by GLAUCIA DENISE KOMMERS Approved: Major Professors: Corrie C. Brown Daniel J. King Committee: K. Paige Carmichael Barry Harmon Bruce Seal Pedro Villegas Electronic Version Approved: Gordhan L. Patel Dean of the Graduate School The University of Georgia May 2002 iv DEDICATION I dedicate this work to my family. Your every day prayers and your love made me stronger than I thought I could ever be. Muito obrigado!!!!! v ACKNOWLEDGMENTS First of all, I would like to thank God for his care, for his love, and for his answers to all my prayers over the last four years. I would like to thank my major professors, Drs. Corrie Brown and Jack King, for their expert guidance and patience with me and with this work. Both of them went far beyond their call of duty as major professors, giving me their friendship and care. I would like to thank all my committee members, Drs. Paige Carmichael, Barry Harmon, Bruce Seal, and Pedro Villegas for their expert input and for all the time spent reviewing this work. I would like to thank all the faculty of the Department of Pathology for their teaching, patience, time, and for making me want to be an excellent pathologist as all of them are. I would like to thank all graduate students who shared sometime with me during this journey. My special thanks goes to my first three officemates, Drs. Anapatricia García, Lucia García-Camacho, and Suzana Tkalcic, and to my last three officemates, Drs. Yong-Baek Kim, Laura Perkins, and Nobuko Wakamatsu. Without their friendship I probably would not have done the work I came here to do. I would like to thank all the staff members of the Department of Pathology. My special thanks goes to Amanda Crawford, “my guardian angel”, who always stood by me as a friend and cared for me as a member of her wonderful family. I would also like to thank Erica Behling-Kelly, Joyce Bennett, Phillip Curry, Melissa Scott, and Dr. James Stanton for their excellent technical assistance and patience in the laboratory. vi I would like to thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; Brasília, DF - Brazil), for supporting me with a scholarship. I wish to thank the U.S. Poultry and Egg Association and USDA-ARS-CRIS for their support. I also wish to thank Dr. David Swayne for allowing me to do a major part of my work in the Southeast Poultry Research Laboratory (SEPRL - USDA). I would like to thank all faculty of the Department of Pathology at the Universidade Federal of Santa Maria (UFSM; Santa Maria – RS, Brazil). My special thanks goes to Dr. Claudio Barros for all his efforts in helping me to be accepted as an UGA PhD student. My special thanks also goes to all my friends who were giving me their support, sharing with me their experiences, and making me look forward to achieving my goals along the last four years. This is a very long list represented here by the ones I have met in the USA: Maria Rosa Ferreira, Eleonora and Marcos Machado, Monica and Carlos Costa, Eugenia and Cármelo de Los Santos, and Carolina Realini. vii TABLE OF CONTENTS Page ACKNOWLEDGMENTS................................................................................................... v CHAPTER 1 INTRODUCTION............................................................................................. 1 2 LITERATURE REVIEW.................................................................................. 5 3 VIRULENCE OF PIGEON-ORIGIN NEWCASTLE DISEASE VIRUS ISOLATES FOR DOMESTIC CHICKENS................................................... 52 4 PATHOGENESIS OF SIX PIGEON-ORIGIN ISOLATES OF NEWCASTLE DISEASE VIRUS FOR DOMESTIC CHICKENS............... 92 5 VIRULENCE OF SIX HETEROGENEOUS-ORIGIN NEWCASTLE DISEASE VIRUS ISOLATES BEFORE AND AFTER SEQUENTIAL PASSAGES IN DOMESTIC CHICKENS ................................................... 124 6 PATHOGENESIS OF CHICKEN-PASSAGED NEWCASTLE DISEASE VIRUSES ISOLATED FROM CHICKENS, WILD, AND EXOTIC BIRDS ............................................................................................ 167 7 CONCLUSIONS............................................................................................ 201 CHAPTER 1 INTRODUCTION Newcastle disease (ND) is one of the most important avian diseases because of its potential economic impact on the poultry industry. Virulent ND is a reportable disease in most countries of the world and is reportable as a List A disease for member countries of the Office International des Epizooties (OIE).8 List A diseases are those that are highly transmissible and their occurrence is of major importance for the international trade of animals and animal products. 8 Newcastle disease is caused by an avian paramyxovirus serotype 1 (APMV-1), synonymous with Newcastle disease virus (NDV).1, 2 NDV has been classified according to five pathotypes that relate to the disease signs produced in infected chickens: a) asymptomatic enteric NDV (avirulent viruses); b) lentogenic NDV (low virulence viruses); c) mesogenic NDV (moderately virulent viruses); d) neurotropic velogenic NDV (NVNDV; highly virulent neurotropic viruses); and e) viscerotropic velogenic NDV (VVNDV; highly virulent viscerotropic viruses).1, 2, 6 There is an international trend that started in 1992 with the ND definition in the European Union (EU) Council Directive 92/66/EEC,4 valid for countries belonging to the EU, to separate NDV isolates into two virulence groups: the low virulence viruses (asymptomatic enteric and lentogens) and the virulent viruses (mesogens and velogens), based on the intracerebral pathogenicity index (ICPI) as a differential test.5 Following this international trend, the OIE established new standards during 1999 with a major change in the official definition of ND.7 ND is now defined as an infection 2 of birds caused by a virulent virus of the APMV-1 serotype. An isolate will be classified as virulent for chickens if it has an ICPI of 0.7 or greater or if it has multiple basic amino acids at the fusion (F) protein cleavage site.7 Currently, the United States Code of Federal Regulations (US-CFR) refers to the presence of “exotic Newcastle disease” (END) as any velogenic ND. END is defined as “an acute, rapidly spreading,
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