MECHANISMS IN THE PATHOGENESIS OF ENTERIC DISEASES

ADVANCES IN EXPERIMENTAL MEDICINE AND BIOLOGY

Editorial Board:

NATHAN BACK, State University of New York at Buffalo

!RUN R. COHEN, The Weizmann Institute of Science

DAVID KRITCHEVSKY, Wistar Institute

ABEL LAJTHA, N. S. Kline Institute for Psychiatric Research

RODOLFO PAOLETTI, University of Milan

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MECHANISMS IN THE PATHOGENESIS OF ENTERIC DISEASES

Edited by

Prem S. Paul Iowa State University Ames, Iowa

David H. Francis South Dakota State University Brookings, South Dakota

and

David A. Benfield South Dakota State University Brookings, South Dakota

SPRINGER SCIENCE+BUSINESS MEDIA, LLC

Llbrary of Congress Cataloglng-ln-Publlcatlon Data

Mechan1s•s in the pathogenesis of enteric d1seases 1 edited by Preo S. Paul, David H. Francis, and David A. Benfield.

p. c•. -- <Advances 1n experioental oedicine and biology ; v. 412)

"Proceed1ngs of the First International Rushoore Conference on Mechanisos in the Pathogenesis of Enteric Dlseases. held Septeober 28-30. 1995, In Rapid City, South Dakota"--T.p. verso.

Includes bibliographical references and index. ISBN 978-1-4899-1830-7 ISBN 978-1-4899-1828-4 (eBook)

DOI 10.1007/978-1-4899-1828-4 1. Infect1on--Pathogenes1s--Congresses. 2. Cooounicable diseases-

-Pathogenes1s--Congresses. I. Paul. Preo S. II. Francis, David H. III. Benf1eld, David A. IV. International Rushoore Conference on Mechan1sms 1n the Pathogenesis of Enteric Diseases 11st 1995 Rap 1 d C 1 t y. S. D. l V. Ser ies.

[DNLM· 1. Gastrointestinal Diseases--physlopathology--congresses. 2. Gastro1ntestinal Diseases--etiology--congresses. Wl AD559 v.412 1997 1 WI 140 M486 1997] RB153.M43 1997 616.3'307--dc21 DNLM/DLC for Library of Congress 97-5561

CIP

Proceedings of the First International Rushmore Conference on Mechanisms in the Pathogenesis of Enteric Diseases, held September 28-30, 1995, in Rapid City, South Dakota

ISBN 978-1-4899-1830-7

© 1997 Springer Science+Business Media New York Originally published by Plenum Press, New York in 1997 Softcover reprint of the hardcover 1 st edition 1997

http:/ /www. plenum.com

10987654321

Ali rights reserved

No part ofthis 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

PREFACE

This book, Mechanisms in the Pathogenesis of Enteric Diseases, is the outcome of the First International Rushmore Conference on Mechanisms in the Pathogenesis of En­teric Diseases, held in September 1995 at Rapid City, South Dakota. The meeting was or­ganized by members of the North-Central Regional Research Committee "NC-62," a United States Department of Agriculture-sponsored consortium of swine enteric disease researchers from land-grant institutions. This conference was conceived as a forum for an interdisciplinary discussion of mechanisms of infectious diseases. It was intended that such a discussion would stimulate cross-fostering of ideas and nurture synergistic collabo­rations among scientists working on enteric diseases of humans and animals_. In atten­dance, there were more than 140 participants from the United States and 12 foreign countries representing all of the world's continents. Participants brought expertise from many disciplines in both human and veterinary medicine. Multiple perspectives and an in­formal atmosphere provided an environment for lively and thought-provoking discussions. Conference topics included Pathobiology of Gastroenteric Diseases, Mechanisms of Iden­tity and Interaction between Host and Pathogen, Effector Mechanisms in the Pathogenesis of Enteric Diseases, Regulation of Pathogenic Activity in Enteric Diseases, and Novel Ap­proaches to Prevention and Therapy of Enteric Diseases.

Ten internationally renowned scientists gave keynote presentations in addition to 30 oral presentations and 39 poster presentations. The keynote speakers were Drs. Harley Moon, USDA Plum Island Animal Disease Center, Greenport, New York, USA, presently at Iowa State University; Robert Argenzio, College of Veterinary Medicine, North Caro­lina State University, Raleigh, North Carolina, USA; Kathryn Holmes, University of Colo­rado Health Sciences Center, Denver, Colorado, USA; Michele Mouricout, Faculty of the Sciences, University of Limoges, Limoges, France; Harry Greenberg, Stanford University School of Medicine, Stanford, California, USA; Kirsten Sandvig, Institute for Cancer Re­search, The Norwegian Radium Hospital, Oslo, Norway; James Kaper, University of Maryland School of Medicine, Baltimore, Maryland, USA; Brett Finlay, University of British Columbia, Vancouver, Canada (Dr. Finlay's speech was given by Murry Stein of his laboratory); Dr. Charles Elson, Department of Medicine, University of Alabama at Birmingham, Birmingham, Alabama, USA; and Dr. Mary Estes, Division of Molecular Virology, Department of Medicine, Baylor College of Medicine, Houston, Texas, USA. The reviews prepared by the keynote speakers provided latest information on the mecha­nisms of pathogenesis of enteric diseases and will serve as authoritative references for re­searchers working on enteric diseases.

Members of the conference organizing committee were Drs. David Francis and David Benfield, South Dakota State University; Lynn Joens, University of Arizona, Rod-

v

vi Preface

ney Moxley, University of Nebraska; Mike Murtaugh, University of Minnesota; Prem Paul and Mike Wannemuehler, Iowa State University; and Linda Saif, Ohio State Univer­sity. Drs. Francis and Benfield were the conference hosts.

The results of a survey of conference participants indicated a high degree of satis­faction with the meeting. Participants expressed enthusiastic support for a second meeting on the same subject. Hence, the organizing committee is pleased to announce the Second International Rushmore Conference on Mechanisms in the Pathogenesis of Enteric Dis­eases to be held in Rapid City, South Dakota, USA, September 30 through October 3, 1998. All enteric disease researchers and interested persons are invited to attend the con­ference. The conference organizing committee expresses sincere thanks to all who gave presentations at the First International Rushmore Conference, those who joined in discus­sions, and participants who provided an enthusiastic environment. The organizing com­mittee expresses special gratitude to organizations whose financial support made the conference possible.

Financial contributions were from the following sources: USDA NRICGP (confer­ence support grant); NSF EPSCoR of South Dakota, USA; Sayer-Agriculture Division, Shawnee Mission, Kansas, USA; Pfizer-Central Research Division, Lincoln, Nebraska, USA; Solvay Animal Health, Mendota Heights, Minnesota, USA; Boehringer Ingelheim Animal Health, Saint Joseph, Missouri, USA; Grand Laboratories, Inc., Freeman, South Dakota, USA; Ambico, Inc., Dallas Center, Iowa, USA; Eli Lilly and Company Founda­tion, Indianapolis, Indiana, USA; NOBL Laboratories, Inc., Sioux Center, Iowa, USA; Oxford Veterinary Labs, Inc., Worthington, Minnesota; Rural Technologies, Inc., Brook­ings, South Dakota, USA; and the College of Agriculture and Biological Sciences, the Ag­ricultural Experiment Station, and the Department of Veterinary Science, South Dakota State University, USA.

Prem S. Paul David Francis David A. Benfield

CONTENTS

I. Comparative Histopathology of Intestinal Infections Harley W. Moon

2. Neuro-Immune Pathobiology of Infectious Enteric Disease Robert A. Argenzio

3. Application oflntestinal Xenografts to the Study of Enteropathogenic Infectious

21

Disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31 Howard B. Gelberg, Joseph D. Thulin, and Mark S. Kuhlenschmidt

4. An Overview of Immunological and Genetic Methods for Detecting Swine Coronaviruses, Transmissible Gastroenteritis Virus, and Porcine Respiratory Coronavirus in Tissues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37

Theerapol Sirinarumitr, Prem S. Paul, Patrick G. Halbur, and John P. Kluge

5. Pathogenesis of0157:H7 Escherichia coli Infection in Neonatal Calves 47 Evelyn A. Dean-Nystrom, BradT. Bosworth, and Harley W. Moon

6. Variation in Virulence in the Gnotobiotic Pig Model of0157:H7 Escherichia coli Strains of Bovine and Human Origin . . . . . . . . . . . . . . . . . . . . . . . . . . 53

Diane R. Baker, Rodney A. Moxley, and David H. Francis

7. Attaching and Effacing E. coli: Microscopic and Ultrastructural Observations of Intestinal Infections in Pigs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59

R. J. Higgins, G. R. Pearson, and C. Wray

8. Dynamics of Clostridium dif.ficile Infection: Control Using Diet Peter B. Ward and Graeme P. Young

9. Detection and Differentiation of 3 K88 Serogroups Using Polymerase Chain

63

Reaction Techniques: K88 Serogroup Detection and Differentiation 77 M.A. Franklin and A. G. Mathew

10. Specific Identification of Escherichia coli 0157: H7 Using a Multiplex PCR Assay . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81

Y. P. 1. Gannon, S. D'Souza, T. Graham, and R. K. King

vii

viii Contents

II. Variation in Manifestation of E. coli H7 Antigen . . . . . . . . . . . . . . . . . . . . . . . . . . 83 C. W. Bailey and C. A. Carson

12. Verotoxigenic Escherichia coli in Slaughter Cattle and Ground Beef in South Dakota . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 87

Christine J. Reitsma, David R. Henning, Christopher Chase, and David J. Hurley

13. Immunoglobulin Response to Salmonella enteritidis Outer Membrane Proteins: Use for Evaluating Infectious Status . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89

Carol W. Maddox, Suzanne E. Baker, Patricia A. Dunn, and Anthony E. Castro

14. Sequence Analysis ofVP7 Gene of a Bovine Rotavirus with G6 Subtype 93 Srinivas Mummidi, Prem Paul, and Robert Holland

15. Detection of the Fimbria! Gene F18 (F107) from Swine Enteritis Escherichia coli . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 95

Linda Schultz, William Fales, Carol Maddox, and James Turk

16. A Chick Model for the Study of" Attaching and Effacing Escherichia coli'' Infection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99

M. Sueyoshi, M. Nakazawa, and S. Tanaka

17. Immunological Cross Reactivity ofEAEA (Intimin) from E. coli that Cause Attaching and Effacing Lesions in Humans and Rabbits . . . . . . . . . . . . . . . I 03

Tonia S. Agin and Marcia K. Wolf

18. Characterization of the EAEA Protein of Attaching and Effacing Escherichia coli 045 from Pigs Using Monoclonal Antibodies . . . . . . . . . . . . . . . . . . . 105

Chengru Zhu and John M. Fairbrother

19. Interactions between the Enteric Pathogen and the Host: An Assortment of Bacterial Lectins and a Set ofGlycoconjugate Receptors . . . . . . . . . . . . . . 109

Michele Mouricout

20. Virus-Receptor Interactions in the Enteric Tract: Virus-Receptor Interactions . . . 125 K. V. Holmes, D. B. Tresnan, and B. D. Zelus

21. Characterization of a Porcine Enterocyte Receptor for Group A Rota virus 135 Mark S. Kuhlenschmidt, Mark D. Rolsma, Theresa B. Kuhlenschmidt, and

Howard B. Gelberg

22. A 50 kDa Membrane Protein from Bovine Kidney Cells Is a Putative Receptor for Bovine Viral Diarrhea Virus (BVDV) . . . . . . . . . . . . . . . . . . . . . . . . . . . 145

H. C. Minocha, W. Xue, and J. R. Reddy

23. Fimbria! Adhesins of Salmonella typhimurium: Role in Bacterial Interactions with Epithelial Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 149

A. J. Baumler, R. M. Tsolis, and F. Heffron

Contents ix

24. Phenotypic and Genotypic Profiles of Human, Canine, and Porcine Spirochetes Associated with Colonic Spirochetosis Correlates with in Vivo Brush Border Attachment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 159

N. Muniappa and G. E. Duhamel

25. A Three-Receptor Model for the Interaction of the K88 Fimbria! Adhesin Variants of Escherichia coli with Porcine Intestinal Epithelial Cells 167

Alan K. Erickson, Lloyd 0. Billey, Geetha Srinivas, Diane R. Baker, and David H. Francis

26. Fimbria! Colonisation Factors FI8AB and FI8AC of Escherichia coli Isolated from Pigs with Postweaning Diarrhea and Edema Disease . . . . . . . . . . . . . 175

H. Imberechts, H. U. Bertschinger, B. Nagy, P. Deprez, and P. Pohl

27. Plasminogen Receptors: Turning Salmonella and Escherichia coli into Proteolytic Organisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 185

T. K. Korhonen, K. Liihteenmaki, M. Kukkonen, R. Pouttu, U. Hynonen, K. Savolainen, B. Westerlund-Wikstrom, and R. Virkola

28. Evaluation of DNA "Fingerprinting" for Predicting the Potential of E. coli 0157:H7 Isolates to Cause Hemolytic Uremic Syndrome (HUS) . . . . . . . . 193

Kelly K. McAdoo and C. A. Carson

29. Fermentation and Growth Response of a Primary Poultry Isolate of Salmonella typhimurium Grown under Strict Anaerobic Conditions in Continuous Culture and Amino Acid-Limited Batch Culture . . . . . . . . . . . . . . . . . . . . . 20 I

K. G. Maciorowski, D. J. Nisbet, S.D. Ha, D. E. Corrier, J. R. DeLoach, and S.C. Ricke

30. Distribution ofK88-Adhesive and Non-Adhesive Phenotypes among Four Popular Breeds of Pigs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 209

Diane R. Baker, Lloyd 0. Billey, and David H. Francis

3 I. Elucidating the Cell Entry Mechanisms of Porcine Rota viruses . . . . . . . . . . . . . . 213 Rafael A. Garduno, Andrew Brevik, and David A. Benfield

32. Adherence and Invasion of Aeromonas caviae to Monolayer Cells: Adherence and Invasion of Aeromonas caviae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 217

Jonathan Shaw, Jonathan Thomley, and Adrian Eley

33. FI07-Binding Immunoassay Detects Porcine Intestinal Receptors for FI07 Fimbriae of Escherichia coli . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 221

Margrit Stamm, Evelyn A. Dean-Nystrom, and BradT. Bosworth

34. Intracellular Transport and Processing of Protein Toxins Produced by Enteric Bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225

K. Sandvig, 0. Garred, and B. van Deurs

35. Murine Model ofRotavirus Infection................................... 233 Ningguo Feng, Manuel A. Franco, and Harry B. Greenberg

X Contents

36. Cloning of the RDEC-1 Locus ofEnterocyte Effacement (LEE) and Functional Analysis of the Phenotype on Hep-2 Cells . . . . . . . . . . . . . . . . . . . . . . . . . . 241

D. K. R. Karaolis, T. K. McDaniel, J. B. Kaper, and E. C. Boedeker

37. Characterization of the Agfba Fimbria) Operon Encoding Thin Aggregative Fimbriae of Salmonella enteritidis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 247

S. Karen Collinson, Sharon C. Clouthier, James L. Doran, Pamela A. Banser, and William W. Kay

38. Cell Membrane Permeability- and Mitochondrial Dysfunction-Inducing Activities in Cell Free Supernatants from Serpulina hyodysenteriae Serotypes 1 and 2 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 249

N. A. Witters and G. E. Duhamel

39. C02 Regulation of Virulence Genes in Enteropathogenic Escherichia coli 253 R. D. Haigh and P. H. Williams

40. Binding of Human Enterotoxigenic Escherichia coli Expressing Coli Surface Antigen 6 to Rabbit Intestinal Enterocytes and Glycoproteins ..... , . . . . 257

Anna Helander, Gunnar C. Hansson, and Ann-Mari Svennerholm

41. Functional Analysis of Serpulina hyodysenteriae Hemolysin Lytic Activity 259 D. R. Hyatt and L. A. Joens

42. Cloning, Sequencing, and Expression of a Campylobacter jejuni Peri plasmic Binding Protein (P29) Involved in Histidine Transport . . . . . . . . . . . . . . . . 263

S. G. Garvis, G. J. Puzon, and M. E. Konkel

43. Norepinephrine-Induced Growth and Alteration of Molecular Fingerprints in Escherichia coli 0 157:H7 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 265

Kien T. Nguyen and Mark Lyte

44. AF/R2 Adhesin and Cytopathic Effect as Virulence Traits of Diarrhea-Inducing Escherichia coli 0103 in European Rabbit . . . . . . . . . . . . . . . . . . . . . . . . . 269

C. Chalareng, F. Pillien, M. Boury, C. Tasca, J. De Rycke, and A. Milon

45. Apoptosis of Crypt Cells and Inflammatory Reactions in the Small Intestine of Mice Challenged with Staphylococcal Enterotoxin B . . . . . . . . . . . . . . . . . 273

Yiran Qiao, Ludmila Asher, and Wallace Baze

46. Serovar Specific Differences in Salmonella Survival within Macrophage Cells 277 W. R. Schwan and D. J. Kopecko

47. Genetics of Virulence of Enteropathogenic E. coli . . . . . . . . . . . . . . . . . . . . . . . . 279 James B. Kaper, Timothy K. McDaniel, Karen G. Jarvis, and

Oscar Gomez-Duarte

48. Interactions of Enteric Pathogens with Human Epithelial Cells: Bacterial Exploitation of Host Processes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 289

B. Brett Finlay

Contents xi

49. Hemolysin Phenotypes and Genotypes of EAEA-Positive and EAEA-Negative Bovine Verotoxigenic Escherichia coli . . . . . . . . . . . . . . . . . . . . . . . . . . . . 295

K. S. Sandhu, R. C. Clarke, and C. L. Gyles

50. Regulators of Escherichia coli K99 Region I Genes . . . . . . . . . . . . . . . . . . . . . . . 303 Thomas Lo-Tseng, John Lee, and Richard E. Isaacson

51. Pathotypes of Bovine Verotoxigenic Escherichia coli Isolates Producing Attaching/Effacing (AE) Lesions in the Ligated Intestinal Loop Assay in

Rabbits . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 311 B. China, V. Pirson, E. Jacquemin, P. Pohl, and J. G. Mainil

52. Pathogenicity and Sequence Analysis Studies Suggest Potential Role of Gene 3

in Virulence of Swine Enteric and Respiratory Corona viruses . . . . . . . . . . 317 Prem S. Paul, Eric M. Vaughn, and Patrick G. Halbur

53. Studies of the Astrovirus Signal that Induces (-1) Ribosomal Frameshifting 323 Terry L. Lewis and Suzanne M. Matsui

54. Norepinephrine Induced Growth and Expression of Virulence Associated Factors in Enterotoxigenic and Enterohemorrhagic Strains of Escherichia coli . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 331

M. Lyte, B. Arulanandam, K. Nguyen, C. Frank, A. Erickson, and D. Francis

55. Unique Salmonella choleraesuis Surface Protein Affecting Invasiveness: Possible inv Related Sequence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 341

C. W. Maddox, K. Kasemsuksukul, W. H. Fales, C. Besch-Williford, C. A. Carson, and K. Wise

56. A Novel Regulatory Mechanism for a Novel Phase-Variable Outer Membrane

Protein of Escherichia coli . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 349 Ian R. Henderson, Mary Meehan, and Peter Owen

57. Adhesion of K88AB Fimbriated E. coli in Piglet Small Intestines in Relation

with Iron Transport Molecules . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 357 Philippe Grange, Bruno Vedrine, and Michele Mouricout

58. Interaction of Escherichia coli Producing Cytotoxic Necrotizing Factor with Hela Epithelial Cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 363

Jean De Rycke, Jean-Philippe Nougayrede, Eric Oswald, and Philippe Mazars

59. Adherence Patterns of Bacterial Diarrheal Agents in AIDS . . . . . . . . . . . . . . . . . 367

Yury Polotsky, James P. Nataro, Donald P. Kotler, and Jan M. Orenstein

60. In Defense of Mucosal Surfaces: Regulation and Manipulation of the Mucosal Immune System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 373

C. 0. Elson

61. Virus-like Particle Vaccines for Mucosal Immunization . . . . . . . . . . . . . . . . . . . . 387 Mary K. Estes, Judith M. Ball, Sue E. Crawford, Christine O'Neal,

Antone A. Opekun, David Y. Graham, and Margaret E. Conner

xii Contents

62. Comparative Studies ofthe Pathogenesis, Antibody Immune Responses, and Homologous Protection to Porcine and Human Rotaviruses in Gnotobiotic Piglets . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 397

L. Saif, L. Yuan, L. Ward, and T. To

63. Maternal Immunization of Pregnant Cattle with Recombinant VP8* Protein of Bovine Rotavirus Elicits Neutralizing Antibodies to Multiple Serotypes: Colostral Neutralizing Antibody by Rotavirus VP8* . . . . . . . . . . . . . . . . . . 405

Dongwan Yoo, Joongbok Lee, Richard Harland, Elaine Gibbons, YoussefElazhary, and Lome A. Babiuk

64. Immunoprophylaxis of Salmonella gallinarum Infection by Salmonella enteritidis-Immune Lymphokines in Broiler Chicks . . . . . . . . . . . . . . . . . . 413

Michael Kogut, Guillermo Tell~z, Edward McGruder, Billy Hargis, and John DeLoach

65. Current Concepts of Competitive Exclusion Cultures for the Control of Salmonellae in Domestic Poultry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 421

Charles M. Scanlan

66. Selection of Swine Resistant to F4-Positive Escherichia coli . . . . . . . . . . . . . . . . 427 A. Bertels, J. Jourquin, N. Buys, A. Van Zeveren, H. De Greve,

J.P. Hemalsteens, andY. Bouquet

67. Hemagglutinin-Esterase Glycoprotein Gene of Bovine Coronavirus Delivered by Adenovirus Vector Induces Mucosal Immunity in Cotton Rats . . . . . . . 431

M. E. Baca-Estrada, L. A. Babiuk, and D. Yoo

68. Role of Metabolic Products Produced by Competitive Exclusion Cultures for the Control of Salmonellae in Domestic Poultry . . . . . . . . . . . . . . . . . . . . . . . . 435

Charles M. Scanlan

Index 437