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Association of Wolbachia with Heartworm Disease in Cats and Dogs

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Association of Wolbachia with Heartworm Disease in Cats and Dogs ASSOCIATION OF WOLBACHIA WITH HEARTWORM DISEASE IN CATS AND DOGS By PATRICIA ANN DINGMAN A THESIS PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE UNIVERSITY OF FLORIDA 2009 1 © 2009 Patricia Ann Dingman 2 To my cats, Sara and CC and my dog, Ellington Foxworthy 3 ACKNOWLEDGMENTS I thank Nicholas Ronnquist for being patient and understanding. I thank my mentor and inspiration, Dr. Julie Levy. She has given me so many opportunities to succeed and has greatly contributed to my personal and professional growth. I would like to thank Dr. Calvin Johnson, Dr. Ellis Greiner, and Dr. Charles Courtney for their patience and support. 4 TABLE OF CONTENTS page ACKNOWLEDGMENTS ...............................................................................................................4 LIST OF TABLES...........................................................................................................................7 LIST OF FIGURES .........................................................................................................................8 ABSTRACT ....................................................................................................................................9 CHAPTER 1 DIROFILARIA IMMITIS ........................................................................................................11 Identification...........................................................................................................................11 Life Cycle/Pathogenesis .........................................................................................................11 Epidemiology..........................................................................................................................13 Heartworm Disease.................................................................................................................13 Heartworm-Associated Lung Pathology.................................................................................14 Diagnosis of Heartworm Infection .........................................................................................15 Heartworm Treatment.............................................................................................................15 2 WOLBACHIA..........................................................................................................................17 Biology ...................................................................................................................................17 Endosymbiotic Relationship with D. immitis .........................................................................17 3 EXPERIMENTAL DESIGN..................................................................................................20 Materials and Methods ...........................................................................................................20 Animals............................................................................................................................20 Sample Collection ...........................................................................................................21 Serology...........................................................................................................................21 Parasitology .....................................................................................................................22 Pulmonary Histologic Morphometry...............................................................................22 Wolbachia DNA Detection..............................................................................................23 Wolbachia Immunohistochemistry..................................................................................24 Statistical Analyses..........................................................................................................24 4 RESULTS...............................................................................................................................32 Statistical Analyses.................................................................................................................32 Serology...........................................................................................................................32 Parasitology .....................................................................................................................32 Detection of Wolbachia...................................................................................................33 Pulmonary Histologic Morphometry...............................................................................33 5 5 DISCUSSION.........................................................................................................................44 6 CONCLUSIONS ....................................................................................................................46 LIST OF REFERENCES...............................................................................................................47 BIOGRAPHICAL SKETCH .........................................................................................................51 6 LIST OF TABLES Table page 3-1 Pulmonary arteriolar lesion scoring system.......................................................................25 3-2 Bronchiolar lesion scoring system.....................................................................................26 3-3 Pulmonary interstitial and alveolar smooth muscle scoring system. .................................27 4-2 The prevalence of Ancylostoma spp. and ascarids in cats and dogs with pulmonary lesions ..............................................................................................................36 4-3 Frequency of pulmonary lesions in cats and dogs with and without Wolbachia...............37 7 LIST OF FIGURES Figure page 3-1 Representative feline pulmonary tissues demonstrating lesion scores in arterioles.............................................................................................................................28 3-2 Representative feline pulmonary tissues demonstrating lesion scores in bronchioles.........................................................................................................................29 3-3 Representative feline pulmonary tissues demonstrating lesion scores in alveolar smooth muscle......................................................................................................30 3-4 Representative feline pulmonary tissues demonstrating lesion scores in interstitium .........................................................................................................................31 4-1 Feline D. immitis antibody titer versus Wolbachia surface protein (WSP) antibody titer in all cats......................................................................................................38 4-2 Canine D. immitis antibody titer versus Wolbachia surface protein (WSP) antibody titer in all dogs ....................................................................................................39 4-3 Severity of pulmonary lesions in cats with or without detectable Wolbachia DNA and/or Wolbachia surface protein in lung tissues.....................................................40 4-4 Severity of pulmonary lesions in dogs with or without detectable Wolbachia DNA and/or Wolbachia surface protein in lung tissues.....................................................41 4-5 Severity of pulmonary lesions in cats with or without detectable circulating Wolbachia surface protein antibodies (WSP Ab) ..............................................................42 4-6 Severity of pulmonary lesions in dogs with or without detectable circulating Wolbachia surface protein antibodies (WSP Ab) ..............................................................43 8 Abstract of Thesis Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Master of Science ASSOCIATION OF WOLBACHIA WITH HEARTWORM DISEASE IN CATS AND DOGS By Patricia Ann Dingman May 2009 Chair: Julie Levy Major: Veterinary Medical Sciences Although the presence of adult Dirofilaria immitis in the pulmonary arteries and its associated arteritis and thromboembolic disease can explain some of the manifestations of canine and feline heartworm disease, the cause of other findings remains unclear. For example, cats with D. immitis antibodies but lacking adult parasites in the pulmonary arteries frequent develop histological lesions of Heartworm-Associated Respiratory Disease. All D. immitis parasites harbor Wolbachia and D. immitis-infected animals can have circulating Wolbachia antibodies and pro-inflammatory Wolbachia antigens deposited in tissues. Little is known about the role Wolbachia plays in the pulmonary pathology of animals naturally infected with D. immitis. The purpose of this study was to determine the contribution of Wolbachia to the pathogenesis of natural heartworm disease in cats and dogs. We hypothesized that animals having sufficient Wolbachia burden to be detected in pulmonary tissue by immunohistochemistry and/or by PCR would have more severe pulmonary disease than those with bacteria below the limits of detection. We further hypothesized that animals that were immunoreactive to pro- inflammatory WSP would have more severe pulmonary lesions than those
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