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Heterobilharzia Americana in Dogs: Characterizing Clinical View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Texas A&M Repository HETEROBILHARZIA AMERICANA IN DOGS: CHARACTERIZING CLINICAL INFECTION, EVALUATING DIAGNOSTIC TEST PERFORMANCE, AND EXPLORING NOVEL METHODS OF DIAGNOSIS A Dissertation by JESSICA YVONNE RODRIGUEZ Submitted to the Office of Graduate and Professional Studies of Texas A&M University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Chair of Committee, Karen Snowden Committee Members, Christine Budke Charles Criscione Barbara Lewis Head of Department, Ramesh Vemulapalli August 2017 Major Subject: Veterinary Pathobiology Copyright 2017 Jessica Yvonne Rodriguez ABSTRACT Heterobilharzia americana is a waterborne trematode parasite (Family: Schistosomatidae) of dogs. More complete information regarding clinical, geographic, and diagnostic aspects of this parasite is needed to aid in more effective awareness and diagnosis. A total of 238 cases diagnosed through the Texas A&M Veterinary Medical Diagnostic Laboratory, Texas A&M Veterinary Medical Teaching Hospital, Texas A&M Diagnostic Parasitology Service, and Texas A&M Gastrointestinal Laboratory were reviewed. Cases were distributed primarily in the eastern region of Texas. Clinical signs were diarrhea (67%), weight loss (38%), anorexia/hyporexia (27%), vomiting (22%), hematochezia (20%), lethargy (17%), and polyuria/polydipsia (6%). H. americana was attributed to death in 20 of 39 necropsy cases. Trematode eggs were identified histologically in the small intestine (84%), liver (84%), large intestine (39%), pancreas (35%), lung (9%), lymph node (8%), and spleen (4%). A total of 69 dogs were enrolled in a diagnostic methods comparison study. Relative test sensitivities were 50% (29.1-70.9) for fecal saline sedimentation, 58.3% (36.6-77.9) for PCR of fresh feces, and 95.8% (78.9-99.9) for PCR of fecal sediment. PCR of fresh feces was no more sensitive than fecal saline sedimentation. Circulating anodic antigen was detected in the serum of 8 dogs using the Schistosoma mansoni point-of-care assay (POC- CAA). Circulating cathodic antigen was detected in urine of 7 dogs using the POC-CCA test. Next generation sequencing technology and the Galaxy-based RepeatExplorer computation pipeline were used to discover highly repetitive DNA sequences in the H. ii americana genome. A novel probe-based real-time PCR diagnostic assay targeting these highly repetitive sequences was developed. No DNA amplification was detected when testing DNA of common parasites indicating that the assay is highly specific. The real-time assay detected 9 samples as positive that were negative by conventional PCR targeting a segment of the 18S ribosomal DNA. Increased awareness of H. americana by veterinarians is crucial for a timely diagnosis. Promising methods to increase test sensitivity include sample concentration before DNA extraction, and using highly repetitive DNA targets in a real-time PCR assay. Circulating antigens were detected in some dogs; however, more sensitive test modalities should be developed in order to make circulating antigens accurate diagnostic targets. iii CONTRIBUTORS AND FUNDING SOURCES Committee This work was supervised by a dissertation committee consisting of Dr. Karen Snowden (advisor) and Dr. Barbara Lewis of the Department of Veterinary Pathobiology (VTPB), Dr. Christine Budke of the Department of Veterinary Integrative Biosciences (VIBS), and Dr. Charles Criscione of the Department of Biology (BIOL). Student/collaborator contributions PI, Karen Snowden, oversaw project design and provided critical review of the scientific manuscript writing of the student. Chapter 1 The literature review was performed independently by the student. Chapter 2 Dr. Barbara Lewis facilitated case record collection from the Texas A&M Veterinary Medical Diagnostic Laboratory. Drs. Jörg Steiner and Jan Suchodolski provided GI Laboratory case records. Dr. Tom Craig provided Texas A&M diagnostic parasitology laboratory case records. The student compiled and analyzed the records independently. Chapter 3 Dr. Govert van Dam provided point-of-care diagnostic assays and assisted in trouble shooting results. Statistics were performed by the student, with input from Dr. Christine Budke. Kathleen Logan and Beverly Finneburgh provided technical support for fecal DNA extraction and PCR and sequencing. The student performed the majority of the laboratory work independently. iv Chapter 4 The student performed the bioinformatics and PCR design and optimization with guidance and support from Dr. Steven Williams (Department of Biological Sciences, Smith College, Northampton, MA) and Nils Pilotte, MS (Molecular and Cellular Biology Program, University of Massachusetts Amherst, Amherst, MA) at Smith College. Dr. William’s lab also provided human parasite DNA for specificity analysis of the PCR. Dr. Charles Criscione facilitated obtaining Trichobilharzia sp. DNA through Dr. Sara Brant (Division of parasites, University of New Mexico, Albuquerque, NM). Real-time PCR thermocycler use was provided by the Molecular Genomics Shared Workspace of the Texas A&M Institute for Genome Sciences and Society. The student performed all real-time PCR tests independently. Funding sources Graduate study was supported by the Texas A&M University Graduate Diversity Fellowship and by Merial and the National Center of Veterinary Parasitology (NCVP). Research was supported by two NCVP grants (2013 & 2015), a Burroughs-Wellcome Fund Collaborative Research Travel Award (2015), and the Texas A&M CORE Facilities Grant (2016). v TABLE OF CONTENTS Page ABSTRACT .............................................................................................................................. ii CONTRIBUTORS AND FUNDING SOURCES ................................................................... iv TABLE OF CONTENTS ......................................................................................................... vi LIST OF FIGURES ............................................................................................................... viii LIST OF TABLES ................................................................................................................... ix CHAPTER I INTRODUCTION AND LITERATURE REVIEW .......................................... 1 Family: Schistosomatidae ..................................................................................................... 1 Life cycle ............................................................................................................................ 11 Pathogenesis ........................................................................................................................ 12 Intestinal schistosomiasis ................................................................................................ 13 Hepatic schistosomiasis .................................................................................................. 14 Schistosomiasis in other organs/aberrant locations ........................................................ 16 Secondary pathological lesions ....................................................................................... 17 Cercarial dermatitis ......................................................................................................... 18 Clinical pathology ........................................................................................................... 18 Clinical signs ................................................................................................................... 21 Diagnostics .......................................................................................................................... 22 Parasitological ................................................................................................................. 22 Immunodiagnostics ......................................................................................................... 27 Molecular ........................................................................................................................ 36 Surgical ........................................................................................................................... 39 Imaging ........................................................................................................................... 39 Treatment ............................................................................................................................ 40 Dissertation aims ................................................................................................................. 41 CHAPTER II DISTRIBUTION AND CHARACTERIZATION OF HETEROBILHARZIA AMERICANA IN DOGS IN TEXAS .................................................. 43 Introduction ......................................................................................................................... 43 Materials and methods ........................................................................................................ 44 Results ................................................................................................................................. 46 Discussion ........................................................................................................................... 54 vi CHAPTER III DETECTING CIRCULATING CATHODIC AND ANODIC ANTIGENS IN DOGS NATURALLY INFECTED WITH HETEROBILHARZIA AMERICANA: A COMPARATIVE DIAGNOSTIC METHODS
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