Giardia and Giardiasis Biology, Pathogenesis, and Epidemiology

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1 Giardia and Giardiasis Biology, Pathogenesis, and Epidemiology

2 Giardia and Giardiasis Biology, Pathogenesis, and Epidemiology Edited by Stanley L. Erlandsen University of Minnesota Minneapolis, Minnesota and Ernest A. Meyer Oregon Health Sciences University Portland, Oregon Springer Science+Business Media, LLC

3 Library of Congress Cataloging in Publication Data Main entry under title: Giardia and giardiasis. Includes bibliographies and index. 1. Giardia. 2. Giardiasis Transmission. 3. Epidemiology. I. Erlandsen, Stanley L. II. Meyer, Ernest A. (Ernest Alan) [DNLM: 1. Giardia. 2. Giardiasis. WC 700 G435] QR201.G45G ' ISBN ISBN DOI / ISBN (ebook) Springer Science+Business Media New York 1984 Originally published by Plenum Press, New York in 1984 Softcover reprint of the hardcover 1st edition 1984 All rights reserved No part of this book may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher

4 Contributors R. F. Anders Laboratory of Immunoparasitology and Clinical Research Unit The Walter and Eliza Hall Institutf' of Medical Research and Royal Melbourne Hospital Victoria 3050, Australia Robert J. Barnard Division of Microbiology Food and Drug Administration Washington, D.C William J. Bemrick Department of Pathobiology College of Veterinary Medicine University of Minnesota St. Paul, Minnesota Miriam A. Bertram Clinical Microbiology Laboratory UCLA Hospital and Clinics Los Angeles, California David G. Chase Cell Biology Laboratory Veterans Administration Hospital Sepulveda, California v

5 VI CONTRIB UTORS Gunther F. Craun United States Environmental Protection Agency Cincinnati, Ohio Foppe B. DeWalle Department of Environmental Health University of Washington Seattle, Washington Stanley L. Erlandsen Department of Anatomy School of Medicine University of Minnesota Minneapolis, Minnesota Dennis E. Feely Department of Oral Biology College of Dentistry University of Nebraska Medical Center Lincoln, Nebraska Anne Ferguson Castro-Intestinal Unit University of Edinburgh and Western General Hospital Edinburgh EH4 2XU, Scotland, United Kingdom Frances D. Gillin Laboratory of Parasitic Diseases National Institute of Allergy and Infectious Diseases National Institutes of Health Bethesda, Maryland Present address: Department of Pathology, H 811-F University of California at San Diego Medical Center San Diego, California J. Gillon Castro-Intestinal Unit University of Edinburgh and Western Ceneral Hospital Edinburgh EH4 2XU, Scotland, United Kingdom

6 CONTRIBUTORS VII George R. Healy Centers for Disease Control Public Health Service United States Department of Health and Human Services Atlanta, Georgia David W. Hendricks Department of Civil Engineering Colorado State University Fort Collins, Colorado John C. Hoff Drinking Water Research Division United States Environmental Protection Agency Cincinnati, Ohio George J. Jackson Division of Microbiology Food and Drug Administration Washington, D.C Walter Jakubowski Health Effects Research Laboratory United States Environmental Protection Agency Cincinnati, Ohio Edward L. J arroll Department of Preventive Medicine New York State College of Veterinary Medicine Cornell University Ithaca, New York Donald G. Lindmark Department of Preventive Medicine New York State College of Veterinary Medicine Cornell University Ithaca, New York Gary S. Logsdon Drinking Water Research Division United States Environmental Protection Agency Cincinnati, Ohio 45268

7 viii CONTRIBUTORS Ernest A. Meyer Department of Microbiology and 1/11/111/1/(//11,1;.")' Oregon Health Sciences University Portland, Oregon Patrick Muller Department of Microbiology and Immunology Oregon Health Sciences University Portland, Oregon Robert L. Owen Department of Medicine University of California, San Francisco, California and Cell Biology Section Veterans Administration Medical Center San Francisco, California Simona Radulescu Cantacuzino Institute Bucharest, Romania I. C. Roberts-Thomson Laboratory of Immunoparasitology and Clinical Research Unit The Walter and Eliza Hall Institute of Medical Research and Royal Melbourne Hospital Victoria 3050, Australia Frank W. Schaefer, III Microbiology Branch Toxicology and Microbiology Division Health Effects Research Laboratory United States Environmental Protection Agency Cincinnati, Ohio Phillip D. Smith Laboratory of Microbial Immunity National Institute of Allergy and Infectious Diseases National Institutes of Health Bethesda, Maryland 20205

8 CONTRIBUTORS ix Govinda S. Visvesvara Centers for Disease Control Public Health Service United States Department of Health and Human Services Atlanta, Georgia Martin S. Wolfe Department of Medicine George Washington Medical School and Georgetown Medical School Washington, D.C. and Office of Medical Services Department of State Washington, D.C Patrick K. Woo Department of Zoology College of Biological Science University of Guelph Guelph, Ontario NIG 2WI, Canada

9 Preface The intestinal protozoan Giardia was first described over 300 years ago in 1681 by Leeuwenhoek, from his own stools. In his description of Giardia, he noted the size, movement, and morphology of the organism, and associated its presence with the diarrheic nature of his stools and his dietary habits. This truly remarkable account contains the first description of Giardia in morphologic, pathogenic, and epidemiologic terms. Our knowledge of the organisms in the genus Giardia has advanced tremendously in the past two decades. With the advent of new technologies, including techniques in electron microscopy, biochemistry, immunochemistry, tissue culture, and physiology, a tidal wave of information has appeared on the organization and function of this parasitic protozoan and its interaction with its host. The purpose of this book is to celebrate the tricentennial discovery of Giardia by Leeuwenhoek by presenting the above-mentioned advances in our knowledge of Giardia and giardiasis. In the first section of this book, the dominant theme is the biology of the organism and the correlation of structure-function relationships. How does the trophozoite attach to surfaces? What are the similarities and differences between members of this genus? What is known about its metabolism and requirements for growth and attachment? Are there morphological or biochemical parameters that may help to facilitate speciation? What factors are involved in excystation? The second section of this volume deals with the diagnosis and treatment of giardiasis and the immunological reactions that occur within the host. What are the best treatments for giardiasis? Does the xi

10 XII PREFACE immune system play a role in regulating the growth and attachment of Giardia in the small intestine? Can cellular or humoral immune responses be used to assist diagnosis of giardiasis? What animal models exist for the study of giardiasis? The third section contains recent studies related to the epidemiology of giardiasis. How important is drinking water as a source of giardiasis? What is the status of techniques for detecting, removing, and disinfecting Giardia cysts in drinking water? What types of factors are involved in the spread of giardiasis? Are there distinct species of Giardia and can certain animals serve as potential reservoirs for Giardia spp. that infect man? These questions and more are addressed by the authors of this volume. It is hoped that the variety of information from these multidisciplinary sources will give the reader a greater understanding of Giardia as an individual cell, the interaction of this parasite with the small intestinal mucosa of its host to produce the disease giardiasis, and the factors involved in the epidemiology of the disease. S. L. Erlandsen E. A. Meyer

11 Contents I. STRUCTURE AND PHYSIOLOGY CHAPTER 1 Structure of the Trophozoite and Cyst DENNIS E. FEELY, STANLEY L. ERLANDSEN, and DAVID G. CHASE 1. Introduction Morphology of the Trophozoite General Morphology The Ventral Disc Flagella and Flagella-Associated Structures The Median Body Other Organelles Bacterial and Viral Symbionts Morphology of the Cyst General Description Excystation References Xlll

12 XIV CONTENTS CHAPTER 2 Trophozoite Motility and the Mechanism of Attachment STANLEY L. ERLANDSEN and DENNIS E. FEELY 1. Description of Motility Discovery of Trophozoite Motility and Organelles of Locomotion Motility of Giardia Trophozoites Types of Motile Systems in Giardia Attachment of Giardia Trophozoites to Substratum Early Descriptions of Giardia Attachment Mechanism for Attachment of Giardia Trophozoites to Substratum Detachment of Trophozoites from Substratum Relationship of Trophozoites Attachment to Giardiasis References CHAPTER 3 Metabolism of Trophozoites DONALD G. LINDMARK and EDWARD L. JARROLL 1. Introduction Carbohydrate and Energy Metabolism Respiration... ' End Products of Metabolism Enzymes Lipid Metabolism Cellular Lipids Uptake of Lipids and Lipid Precursors Nucleic Acid Metabolism Purines Pyrimidines' Hydrolases Summary References

13 CONTENTS xv CHAPTER 4 Giardia Isozymes MIRIAM A. BERTRAM, PATRICK MULLER, and ERNEST A. MEYER 1. Introduction Materials and Methods Results Discussion References CHAPTER 5 Methods of Isolating Trophozoites and Cysts DENNIS E. FEELY 1. Introduction Methods for Isolation of Trophozoites Isolation and Purification by Nylon Fiber Columns Isolation by Vibration and Sedimentation Isolation by Attachment of Trophozoites Methods for Isolation of Cysts Method of Rendtorff Sucrose Density Gradient Centrifugation References CHAPTER 6 In Vitro Cultivation of Giardia Trophozoites ERNEST A. MEYER and SIMONA RADULESCU 1. Introduction Trophozoites of the C. duodenalis Type Trophozoites of the C. muris Type Trophozoites of the C. agilis Type Future Prospects References

14 XVI CONTENTS CHAPTER 7 The Role of Reducing Agents and the Physiology of Trophozoite Attachment FRANCES D. GILLIN 1. Introduction... III 2. Trophozoite Attachment during Axenic Growth The Role of Reducing Agents in the Biology of G. LambLia Reducing Agents in the Growth of G. LambLia The Role of Cysteine and Ascorbic Acid in Protecting G. LambLia Trophozoites from Oxygen Cysteine Is Required for Attachment in Complex Growth Medium The Role of Reducing Agents in Trophozoite Attachment in Maintenance Media in the Absence of Growth The Role of Serum Factors in Trophozoite Attachment Stimulation of Trophozoite Attachment and Survival by Serum Activity of Various Serum Fractions Effect of Serum Cohn Fraction III on the Kinetics of Attachment and Survival Physiological Factors in Attachment Effect of ph Effect of Ionic Composition Effect of Temperature Summary References CHAPTERS Models for Excystation ERNEST A. MEYER and FRANK W. SCHAEFER, III 1. Introduction The Studies of Bingham and Meyer The Studies of Rice and Schaefer Summary References

15 CONTENTS XVII II. GIARDIASIS CHAPTER 9 Symptomatology, Diagnosis, and Treatment MARTIN S. WOLFE 1. Clinical Features Incubation and Prepatent Periods.: Acute Stage Subacute and Chronic Stage Asymptomatic Cyst-Passing Stage Post-Giardia Lactose Intolerance Diagnosis Stool Examinations Examination of Intestinal Fluid Small Bowel Biopsy Serologic Tests Gastrointestinal Radiology Empiric Treatment Treatment Quinacrine (Atabrine) Metronidazole (Flagyl) Furazolidone (Furoxone) Paromomycin (Humatin) Drugs Unavailable in the United States Pregnancy Asymptomatic Cyst Passers Posttreatment Considerations References CHAPTER 10 Changes in the Small Intestinal Mucosa in Giardiasis J. GILLON and ANNE FERGUSON 1. General Considerations Distribution of Parasites in the Intestine Attachment of Trophozoites to the Mucosa and Penetration of the Epithelium

16 xviii CONTENTS 2. Pathological Changes in the Mucosa of the Small Intestine in Human Giardiasis Histological Changes in Patients without Immunodeficiency Intraepithelial Lymphocyte Counts in Patients with Giardiasis Changes in Lamina Propria Plasma Cells and Secretory Antibodies in Patients with Giardiasis Histological Changes in Hypogammaglobulinemic Patients with Giardiasis Ultrastructural Abnormalities of Mucosal Morphology 2.6. Abnormalities of Jejunal Disaccharidases in Giardiasis Patients Small Intestinal Abnormalities in Experimental Murine Giardiasis General Aspects Small Intestinal Mucosa in Primary Giardia Infection in Mice Effects of Chronic G. muris Infection on the Intestinal Mucosa Conclusions References CHAPTER 11 Cellular and Humoral Immunity in Giardiasis I. C. ROBERTS THOMSON and R. F. ANDERS 1. Introduction Immunologic Mechanisms Giardia Antigens G. Lamblia G. muris Immunoglobulin Levels Human Studies Experimental Studies Anti-Giardia Antibodies G. Lamblia G. muris

17 CONTENTS XIX 6. Cell-Mediated Immunity Human Studies Experimental Studies Passive Transfer of Immunity Stimulation of Immunity Nonlymphoid Effector Cells l. Mast Cells Macrophages Eosinophils Conclusion References CHAPTER 12 Human Immune Responses to Giardia lamblia PHILLIP D. SMITH l. Introduction G. Lamblia Strain Humoral Response Cell-Mediated Response l. Lymphocyte Proliferation Spontaneous Cell-Mediated Cytotoxicity Antibody-Dependent Cellular Cytotoxicity (ADCC) Conclusions References CHAPTER 13 Antigenicity of Giardia lamblia and the Current Status of Serologic Diagnosis of Giardiasis GOVINDA S. VISVESV ARA and GEORGE R. HEALY 1. Introduction Immunologic Response in Giardiasis Current Status of Serologic Tests l. Indirect Immunofluorescence (IIF) Test Immunodiffusion (ID) Test Enzyme-Linked Immunosorbent Assay (ELISA)

18 xx CONTENTS 3.4. Counterimmunoelectrophoresis (CIE) Test Role of Antibody in Protection Antigenic Makeup of C. lamblia References CHAPTER 14 Animal Models for Giardiasis ERNEST A. MEYER, STANLEY L. ERLANDSEN, and SIMONA RADULESCU l. Introduction Animal Models Employing C. muris-type Organisms in Mice Animal Models Employing C. duodenalis-type Organisms Summary References CHAPTER 15 III. EPIDEMIOLOGY Waterborne Outbreaks of Giardiasis: Current Status GUNTHER F. CRAUN l. Waterborne Giardiasis in Travelers Endemic Waterborne Giardiasis Outbreaks of Waterborne Giardiasis in the United States, Water Supply Considerations References CHAPTER 16 Detection of Giardia Cysts in Drinking Water: State of the Art WALTER JAKUBOWSKI l. Introduction Estimated Levels of Cysts in Sewage and Water

19 CONTENTS XXI 3. Detection Methods Membrane Filter Methods Particulate Filter Methods Microporous Depth Filters Primary Concentration versus Processing Multilaboratory Evaluation of Giardia-Seeded Water Samples Background Protocol Results and Discussion Recommendations of a Giardia Methods Workshop Background Issues and Recommendations Reference Method Discussion State of the Art References CHAPTER 17 Filtration as a Barrier to Passage of Cysts in Drinking Water GARY S. LOGSDON, FOPPE B. DEWALLE, and DAVID W. HENDRICKS 1. Introduction Experimental Methods Microspheres Giardia Cysts Raw Water Sources Pilot Filter Facilities Results DE Filtration Results Granular Media Filtration Results Slow Sand Filtration Results Discussion DE Filtration Granular Media Filtration Slow Sand Filtration Summary and Conclusions DE Granular Media Filtration

20 XXII CONTENTS 5.3. Slow Sand Filtration Multiple Barrier Concept References CHAPTER 18 Resistance of Cysts to Disinfection Agents EDWARD L. JARROLL, JOHN C. HOFF, and ERNEST A. MEYER 1. Early Concept Determination of Cyst Viability by Vital Stain Exclusion Disinfection Experiments Modern Concept Determination of Cyst Viability Disinfection Experiments References CHAPTER 19 Direct Fecal-Oral Transmission of Giardiasis ROBERT L. OWEN 1. Parasite Factors in Direct Transmission Host Factors in Direct Transmission Institutional Transmission by Infants and the Retarded Venereal Transmission Pets as a Possible Focus of Direct Transmission References CHAPTER 20 Evidence for Animal Reservoirs and Transmission of Giardia Infection between Animal Species PATRICK K. WOO 1. Introduction Toward Species Definition in Giardia

21 XXllI 3. Review of Host Specificity of Giardia Giardia in Humans Giardia in Nonprimates Discussions on the Cross-Transmission Studies Characterization of Giardia spp Host Specificity Morphological Morphometrical Biochemical Immunological Conclusion References CHAPTER 21 Giardia lamblia: The Transfer of Human Infections by Foods ROBERT J. BARNARD and GEORGE J. JACKSON 1. Historical Aspects and Transmission of Related Protozoa through Foods Methods for Detecting Giardia Cysts in Foods Formalin-Ether Sedimentation Sucrose Gradient Discontinuous Density Sucrose Gradient Sedimentation/Zinc Sulfate Flotation Outbreaks of Foodborne Giardiasis Current and Future Status of Foodborne Giardiasis References CHAPTER 22 Some Perspectives on the Transmission of Giardiasis WILLIAM J. BEMRICK 1. Introduction Animal Feeding Experiments Chemical Tagging Methods Immunological Methods for Detecting Giardia Populations

22 XXIV CONTENTS 5. Other Methods with Potential for Specifically Identifying Giardia Populations Waterborne Transmission of Human Giardiasis and the Role of the Beaver Waterborne Transmission in General The Beaver Transmission by Contaminated Food... : Sexual Transmission Final Analysis of Present Data References Index