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Schaechter’s Mechanisms of
Microbial Disease
Schaechter’s Mechanisms of
Microbial Disease
SIXTH EDITION
N. Cary Engleberg
Professor Emeritus Department of Internal Medicine
Division of Infectious Diseases
Department of Microbiology and Immunology
University of Michigan Medical School
Ann Arbor, Michigan
Victor J. DiRita
Rudolph Hugh Endowed Chair in Microbial Pathogenesis and
Department Chair
Department of Microbiology & Molecular Genetics
Michigan State University
East Lansing, Michigan
Michael J. Imperiale
Arthur F. Thurnau Professor
Department of Microbiology and Immunology
University of Michigan Medical School
Ann Arbor, Michigan
Acquisitions Editor: Lindsey Porambo
Product Development Editor: Robyn Alvarez
Editorial Coordinator: Remington Fernando
Marketing Manager: Phyllis Hitner
Senior Production Project Manager: Alicia Jackson
Manager, Graphic Arts & Design: Stephen Druding
Prepress Vendor: Straive
Sixth Edition
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copies, or utilized by any information storage and retrieval system without written permission from
the copyright owner, except for brief quotations embodied in critical articles and reviews. Materials
appearing in this book prepared by individuals as part of their official duties as U.S. government
employees are not covered by the above-mentioned copyright. To request permission, please contact
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The publisher does not provide medical advice or guidance and this work is merely a reference tool.
Healthcare professionals, and not the publisher, are solely responsible for the use of this work
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Given continuous, rapid advances in medical science and health information, independent
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dosages, and treatment options should be made and healthcare professionals should consult a variety
of sources. When prescribing medication, healthcare professionals are advised to consult the product
information sheet (the manufacturer's package insert) accompanying each drug to verify, among other
things, conditions of use, warnings and side effects and identify any changes in dosage schedule or
contraindications, particularly if the medication to be administered is new, infrequently used or has a
narrow therapeutic range. To the maximum extent permitted under applicable law, no responsibility is
assumed by the publisher for any injury and/or damage to persons or property, as a matter of products
liability, negligence law or otherwise, or from any reference to or use by any person of this work.
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Sixth Edition
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transmitted in any form or by any means, including as photocopies or scanned-in or other electronic
copies, or utilized by any information storage and retrieval system without written permission from
the copyright owner, except for brief quotations embodied in critical articles and reviews. Materials
appearing in this book prepared by individuals as part of their official duties as U.S. government
employees are not covered by the above-mentioned copyright. To request permission, please contact
Wolters Kluwer at Two Commerce Square, 2001 Market Street, Philadelphia, PA 19103, via email at
[email protected], or via our website at shop.lww.com (products and services).
987654321
Printed in Mexico
This work is provided “as is,” and the publisher disclaims any and all warranties, express or implied,
including any warranties as to accuracy, comprehensiveness, or currency of the content of this work.
This work is no substitute for individual patient assessment based upon healthcare professionals'
examination of each patient and consideration of, among other things, age, weight, gender, current or
prior medical conditions, medication history, laboratory data and other factors unique to the patient.
The publisher does not provide medical advice or guidance and this work is merely a reference tool.
Healthcare professionals, and not the publisher, are solely responsible for the use of this work
including all medical judgments and for any resulting diagnosis and treatments.
Given continuous, rapid advances in medical science and health information, independent
professional verification of medical diagnoses, indications, appropriate pharmaceutical selections and
dosages, and treatment options should be made and healthcare professionals should consult a variety
of sources. When prescribing medication, healthcare professionals are advised to consult the product
information sheet (the manufacturer's package insert) accompanying each drug to verify, among other
things, conditions of use, warnings and side effects and identify any changes in dosage schedule or
contraindications, particularly if the medication to be administered is new, infrequently used or has a
narrow therapeutic range. To the maximum extent permitted under applicable law, no responsibility is
assumed by the publisher for any injury and/or damage to persons or property, as a matter of products
liability, negligence law or otherwise, or from any reference to or use by any person of this work.
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Contributors
C. Alan Anderson, MD
Professor of Neurology, Psychiatry, and Emergency Medicine
Department of Neurology
University of Colorado School of Medicine
Aurora, Colorado
Elliot J. Androphy, MD
Kampen-Norins Professor
Chair, Department of Dermatology
Indiana University School of Medicine
Indiana University Health
Indianapolis, Indiana
Jeffrey M. Bergelson, MD
Professor of Pediatrics, Emeritus
Division of Infectious Diseases
The Children’s Hospital of Philadelphia
University of Pennsylvania Perelman School of Medicine
Philadelphia, Pennsylvania
William J. Britt, MD
Charles A. Alford Professor of Pediatrics
Department of Pediatrics and Microbiology
University of Alabama School of Medicine
Attending Physician
Children’s Hospital of Alabama
University of Alabama Hospital
Birmingham, Alabama
Sandro K. Cinti, MD
Clinical Professor of Internal Medicine
Division of Infectious Diseases
University of Michigan Medical School
Michigan Medicine
Ann Arbor VA Healthcare System
Ann Arbor, Michigan
Kathleen L. Collins
Associate Dean for Physician Scientist Education and Training
Director, Medical Scientist Training Program
Professor of Internal Medicine and Microbiology and Immunology
University of Michigan Medical School
Ann Arbor, Michigan
Toni Darville, MD
Distinguished Professor of Pediatrics and Microbiology & Immunology
Chief, Division of Pediatric Infectious Diseases
North Carolina Children’s Hospital
University of North Carolina at Chapel Hill
Chapel Hill, North Carolina
Terence S. Dermody, MD
Vira I. Heinz Distinguished Professor and Chair of Pediatrics
Professor of Microbiology and Molecular Genetics
University of Pittsburgh School of Medicine
Physician-in-Chief and Scientific Director
UPMC Children’s Hospital of Pittsburgh
Pittsburgh, Pennsylvania
Shira Doron, MD
Attending Physician
Hospital Epidemiologist
Director, Antimicrobial Stewardship
Division of Geographic Medicine and Infectious Diseases
Associate Professor of Medicine
Tufts University School of Medicine
Boston, Massachusetts
Roman Dziarski
Professor Emeritus of Microbiology and Immunology
Indiana University School of Medicine–Northwest
Gary, Indiana
Barry I. Eisenstein, MD
Chief Medical Officer, CARB-X
Boston University
Washington, District of Columbia
N. Cary Engleberg, MD, DTM&H
Professor Emeritus
Departments of Internal Medicine
Division of Infectious Diseases
Department of Microbiology and Immunology
University of Michigan Medical School
Ann Arbor, Michigan
James M. Fleckenstein, MD
Professor of Medicine & Molecular Microbiology
School of Medicine
Washington University in Saint Louis
Attending Physician
Infectious Diseases
Veterans Affairs Health Care System, St. Louis
St. Louis, Missouri
David W. Haas, MD
Professor of Medicine, Pharmacology, and Pathology, Microbiology &
Immunology
Vanderbilt University School of Medicine
Adjunct Professor of Internal Medicine
Meharry Medical College
Nashville, Tennessee
Adolf W. Karchmer, MD
Professor of Medicine
Division of Infectious Diseases
Beth Israel Deaconess Medical Center
Harvard Medical School
Boston, Massachusetts
David W. Kimberlin, MD
Professor and Vice Chair for Clinical and Translational Research
Department of Pediatrics
The University of Alabama at Birmingham
Birmingham, Alabama
Roshni Mathew, MD
Clinical Associate Professor
Pediatric Infectious Diseases
Stanford University School of Medicine
Stanford, California
Associate Medical Director of Infection Prevention and Control
Lucile Packard Children’s Hospital at Stanford
Palo Alto, California
Peter Palese
Horace W. Goldsmith Professor and Chair
Department of Microbiology
Professor
Department of Medicine
Icahn School of Medicine at Mount Sinai
New York, New York
Moselio Schaechter
Distinguished Professor Emeritus
Tufts University
Boston, Massachusetts
Adjunct Professor
San Diego State University and University of California, San Diego
San Diego, California
Patrick M. Schlievert, PhD
Professor, Microbiology and Immunology and Internal Medicine
University of Iowa Hospital and Clinics
University of Iowa Carver College of Medicine
Iowa City, Iowa
David R. Snydman, MD
Emeritus Chief
Division of Geographic Medicine and Infectious Disease
Emeritus Hospital Epidemiologist
Division of Geographic Medicine and Infectious Diseases
Tufts Medical Center
Professor of Medicine
Tufts University School of Medicine
Boston, Massachusetts
Breanna J. Turman, BS
Graduate Student
Department of Microbiology and Immunology
University of North Carolina at Chapel Hill
Chapel Hill, North Carolina
Kenneth L. Tyler, MD
Louise Baum Endowed Chair and Chairman of Neurology
Professor of Medicine and Microbiology & Immunology
University of Colorado School of Medicine
Aurora, Colorado
Ken B. Waites, MD, F(AAM)
Professor of Pathology
University of Alabama at Birmingham
Birmingham, Alabama
David H. Walker, MD
The Carmage and Martha Walls Distinguished University Chair in Tropical
Diseases
Professor
Department of Pathology
Executive Director
Center for Biodefense and Emerging Infectious Diseases
The University of Texas Medical Branch
Galveston, Texas
Jason B. Weinberg, MD
Associate Professor of Pediatrics
Associate Professor of Microbiology and Immunology
Division of Pediatric Infectious Diseases
C.S. Mott Children’s Hospital
Michigan Medicine
The University of Michigan
Ann Arbor, Michigan
Jeffrey N. Weiser, MD
Professor and Chair
Department of Microbiology
New York University Grossman School of Medicine
New York, New York
John V. Williams, MD, FPIDS
Professor of Pediatrics, Microbiology & Molecular Genetics
Chief, Pediatric Infectious Diseases
Henry L. Hillman Chair in Pediatric Immunology
Director, i4Kids
University of Pittsburgh School of Medicine
UPMC Children’s Hospital of Pittsburgh
Pittsburgh, Pennsylvania
PAST CONTRIBUTORS
We acknowledge several individuals who contributed to previous editions
of this book and whose work formed a basis for many of the updated
chapters in this edition:
David W.K. Acheson
George M. Baer
Neil Barg
Michael Barza
Karen C. c
Jenifer Coburn
John M. Coffin
Laurie Comstock
James E. Crowe, Jr.Richard T. D'Aquila
Christoph Dehio
Mark R. Denison
Peter Dull
John R. Ebright
Kathryn M. Edwards
Roger G. Faix
Bernard N. Fields
Kevin Flaherty
George Fogg
Vance G. Fowler
Donald E. Ganem
Janet Gilsdorf
Sherwood L. Gorbach
Richard K. Groger
Phillip C. Hanna
Penelope J. Hitchcock
Mollie Jewett
Gary Ketner
Gerald T. Keusch
George S. Kobayashi
Donald Krogstad
Michael A. Lane
David W. Lazinski
John Leong
Zell A. McGee
Gerald Medoff
Roger W. Melvold
Cody Meissner
Roger Melvold
Melissa Miller
Joseph J. Nania
James Nataro
Lindsay E. Nicolle
E. Turner Overton
Timothy G. Palzkill
Jeffrey Parsonnet
Charles G. Prober
Vincent R. Racaniello
Rasmus Vedby Rasmussen
Jane E. Raulston
Julie E. Reznicek
Edward N. Robinson Jr
David Schlessinger
Robert T. Schooley
Daniel S. Shapiro
Jack D. Sobel
Arnold L. Smith
Patricia Spear
John Spitznagel
David Stephens
Gregory A. Storch
Stephen E. Straus
Francis P. Tally
Debbie S. Toder
Joseph G. Tully
Carl Waltenbaugh
Ellen Whitnak
Priscilla B. Wyrick
Victor L. Yu
Preface
The previous editions of this book were designed by its original editor-in-
chief, Moselio Schaechter, to present major concepts in microbiology and
infectious diseases in a pathobiological framework and within the context
of clinical cases. This format lends itself to an active form of studying and
is easily adaptable to problem-based learning. It is particularly appropriate
for use in revised medical curricula that feature a synthesis of basic
microbiology and clinical infectious diseases or those that follow an “organ
system” approach to the basic sciences.
N. Cary Engleberg
Victor J. DiRita
Michael J. Imperiale
Acknowledgments
Many colleagues and friends have helped us in the past in preparing this
book. Their names appear in the previous editions. For this revision, we
received invaluable advice from Terry Dermody concerning the
organization of the virology section, from Alexander Engleberg for review
of illustrations from a student perspective, and from David Friedman for
advice concerning quiz items. Our heartfelt thanks go to them for their kind
and thoughtful suggestions. We also express our appreciation to the students
and faculty members who provided helpful insights and reviews on the last
edition that helped focus our improvements for this one.
We are particularly grateful to Cory Adams, Robyn Alvarez, Remington
Fernando, Linda Cristina, and Andrea Vosburgh who provided expert
editorial assistance and helped greatly in organizing the diverse elements in
the book. Their support, hard work, patience, and persistence were
instrumental in bringing this book to completion. We thank Lindsey
Porambo, acquisitions editor, for helping to formulate the framework of the
sixth edition and for her support through the course of the project. We offer
special thanks to art director Jennifer Clements and artist Matt Chansky for
optimizing the color artwork and maintaining a style that is both coherent
and visually pleasing.
A special debt of gratitude is owed to the members of the Old Orchard
Philosophical Society for their engaging biweekly reflections and
contributions of spirit and fellowship. Finally, our appreciation and love go
to Kathleen, Victor, Amalia, Chris, Jenny, Amanda, Roderick, and Suzy for
their support and indulgence through the arduous task of making this book a
reality.
Figure Credits
Cover (C): Graphical abstract from Hurdis DL, Frank M, Snowden JS, et al.
The structure of an infectious human pyomavirus and its interactions with
cellular receptors. Structure. 2018;26(6):839.
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DiRienzo JM, Nakamura K. The outer membrane proteins of the Gram-
negative bacteria: biosynthesis, assembly, and function. Ann Rev Biochem.
1978;47:481-532; permission conveyed through Copyright Clearance
Center, Inc.
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Microbiology, from Blumberg PM, Strominger JL. Interaction of penicillin
with the bacterial cell: penicillin-binding proteins and penicillin-sensitive
enzymes. Microbiol Mol Biol Rev. 1974;38(3):291-335.
Figure 3-9. Adapted by permission from Springer: Kaback HR. Active
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Hoffman JS, Sanastil DD, et al., eds. Physiology of Membrane Disorders.
New York, NY: Plenum Publications; 1986:387-407.
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Sunderland, MA: Sinauer Associates, Inc.; 1990, with permission.
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Aging and Development. Faseb Monographs, vol 3. Boston, MA: Springer;
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Federation of American Societies.
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Cundliffe E, Reynolds PE, et al. The Molecular Basis of Antibiotic Action.
2nd ed. New York, NY: John Wiley & Sons; 1981; permission conveyed
through Copyright Clearance Center, Inc.
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Molecule of the Month (2011) under a CC-BY-4.0 license.
https://creativecommons.org/licenses/by/4.0/.
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AW, et al. Analogous interactions in initiating complexes of the classical
and lectin pathways of complement. J Immunol. 2009;182(12):7708-7717.
Copyright © 2009 by The American Association of Immunologists, Inc.
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complement C6 suggests a mechanism for initiation and unidirectional,
sequential assembly of membrane attack complex (MAC). J Biol Chem.
2012;287(13):10210-10222. Copyright © 2012 The American Society for
Biochemistry and Molecular Biology, Inc. All rights reserved.
https://creativecommons.org/licenses/by/4.0/
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JL. Pathology. 3rd ed. Baltimore, MD: Lippincott Williams & Wilkins;
1999:fig 2-30.
Table 7-1. Adapted by permission from Nature: Vivier E, Malissen B.
Innate and adaptive immunity: specificities and signaling hierarchies
revisited. Nat Immunol. 2005;6:17-21.
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Figure 11-1. Reprinted with permission from Koneman EW, et al.
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Wilkins; 1997:color plate 11-1C.
Figure 12-4. From Public Health Image Library-PHIL, CDC/Dr. Edwin P.
Ewing Jr.
Figure 13-1. Courtesy of Dr. Stuart S. Sagel.
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SD. Direct Smear Atlas: A Monograph of Gram-Stained Smear
Preparations of Clinical Specimens. Baltimore, MD: Lippincott Williams &
Wilkins; 2001.
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Microbiology, from Kim JO, Romero-Steiner S, Skov Sørensen UB, et al.
Relationship between cell surface carbohydrates and intrastrain variation on
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1999;67(5):2327-2333.
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SD. Direct Smear Atlas: A Monograph of Gram-Stained Smear
Preparations of Clinical Specimens. Baltimore, MD: Lippincott Williams &
Wilkins; 2001.
Figure 14-1. Reprinted with permission from McClatchey KD, Alkan S,
Hackel E, et al. Clinical Laboratory Medicine. 2nd ed. Philadelphia, PA:
Lippincott Williams & Wilkins; 2001.
Figure 15-2. Courtesy of Dr. Craig Hill.
Figure 15-3. Courtesy of A. Tzianabos.
Figure 17-1. Adapted with permission of John Wiley & Sons, from Taussig
MJ. Processes in Pathology and Microbiology. 2nd ed. Oxford, UK:
Blackwell Scientific Publications; 1984; permission conveyed through
Copyright Clearance Center, Inc.
Figure 17-2. Reprinted with permission from Rubin E, Farber JL.
Pathology. 3rd ed. Baltimore, MD: Lippincott Williams & Wilkins;
1999:fig 9-21.
Figure 17-3A. Courtesy of Dr. Stanley Falkow.
Figure 17-3B. Panel B reprinted with permission of Rockfeller University
Press, from Jones BD, Ghori N, Falkow SJ. Salmonella typhimurium
initiates murine infection by penetrating and destroying the specialized
epithelial M cells of the Peyer’s patches. J Exp Med. 1994;180(1):15-23;
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Figure 18-1. Reprinted with permission from McClatchey KD, Alkan S,
Hackel E, et al. Clinical Laboratory Medicine. 2nd ed. Philadelphia, PA:
Lippincott Williams & Wilkins; 2001.
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hamster tracheal organ cultures infected with Bordetella pertussis. J Infect
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Figure 20-2. From Schering Slide Library, Schering Corp., Kenilworth, NJ,
copyright owner. All rights reserved.
Figure 23-2. Redrawn after Centers for Disease Control and Prevention
(CDC). Trends in tuberculosis—United States, 2018. MMWR Morb Mortal
Wkly Rep. 2019;68(11):257-262.
Figure 24-1. Courtesy of Dr. E. M. Walker, Department of Microbiology
and Immunology, UCLA School of Medicine, Los Angeles, CA.
Figure 24-3. Reprinted with permission from Goodheart HP. A Photoguide
of Common Skin Disorders: Diagnosis and Management. Baltimore, MD:
Lippincott Williams & Wilkins; 1999.
Figure 25-2. Courtesy of James Gathany, Centers for Disease Control.
Figure 25-3. Courtesy of Dr. Mollie Jewett, Dr. Cristina Fernandez-Valle,
Angelika Linowski, and Stephanie Kurhanewicz, Burnett School of
Biomedical Sciences, University of Central Florida.
Figure 25-4A. Courtesy of Kent Loeffler, Dr. Laura Harrington, Renee
Anderson, Cornell Department of Entomology.
Figure 25-4B. Courtesy of Dr. Nancy Hinkle, Department of Entomology,
University of Georgia.
Figure 25-5. Adapted with permission from a figure from the Web site of
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Figure 25-6. Courtesy of the Centers for Disease Control.
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Lippincott Williams & Wilkins; 2003.
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Hackel E, et al. Clinical Laboratory Medicine. 2nd ed. Philadelphia, PA:
Lippincott Williams & Wilkins; 2001.
Figure 29-1. Courtesy of Dr. Gary Shackleford.
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Diagnostic Microbiology. 5th ed. Baltimore, MD: Lippincott Williams &
Wilkins; 1997:color plate 16-1B.
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virology. In: Knipe DM, Howley PM, eds. Fields Virology. 6th ed.
Philadelphia, PA: Lippincott Williams & Wilkins; 2013:21-51.
Figure 31-1. Used with permission from Dr. Linda M. Stannard, University
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Murphy, DVM, PhD, University of California-Davis, Davis, California.
Influenza virus: Courtesy of Pete Palese, PhD, Mount Sinai School of
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ed. New York, NY: Churchill Livingstone; 2000:1536-1552. Copyright ©
2000 Elsevier. With permission.
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MJ. Processes in Pathology and Microbiology. 2nd ed. Oxford, UK:
Blackwell Scientific Publications; 1984; permission conveyed through
Copyright Clearance Center, Inc.
Figure 31-4. Redrawn with permission of John Wiley & Sons, from Taussig
MJ. Processes in Pathology and Microbiology. 2nd ed. Oxford, UK:
Blackwell Scientific Publications; 1984; permission conveyed through
Copyright Clearance Center, Inc.
Figure 32-1. Adapted with permission from Knipe DM, Howley PM, eds.
Field’s Virology. 4th ed. Philadelphia, PA: Lippincott Williams & Wilkins;
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Baltimore, MD: Lippincott Williams & Wilkins; 1999:fig 12-32.
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Figure 34-1B. Reprinted with permission from Knipe DM, Howley PM,
Griffin DE, et al. Fields Virology. Philadelphia, PA: Lippincott Williams &
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Figure 34-3. Courtesy CDC/Cynthia S. Goldsmith and A. Tamin, 2020.
Public domain.
Figure 34-9A. From Public Health Image Library, Centers for Disease
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Figure 35-1. Courtesy of A. Kapikian.
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New York, NY: Raven Press; 1990.
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Philadelphia, PA: Lippincott Williams & Wilkins; 2001:ch 86, fig 2.
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Contents
Contributors
Preface
Acknowledgments
Figure Credits
PART I: PRINCIPLES
1 Establishment of Infection
Barry I. Eisenstein and Moselio Schaechter
6 Innate Immunity
Roman Dziarski
7 Adaptive Immunity
Marcela F. Pasetti and Jose M. Lemme-Dumit
31 Biology of Viruses
Terence S. Dermody and Jeffrey M. Bergelson
D URING all this time the fleet of yachts had gone clear of
misfortune. In fog and mist and blackness they were banging up
and down the rock-bound Breton coast amid ragged reefs and
pinnacles, through crooked passages, and over German mine-fields.
Offshore they dodged collisions by a hair or steered where the “Allo,
Allo,” of the wireless submarine warnings indicated that the enemy
was active. Good luck and good seamanship had saved them from
disaster. It seemed as though these yachts bore charmed lives, but
the pitcher can go too often to the well and the Alcedo was fated to
be the victim. She had often cruised with the Corsair on escort duty,
and between them there was bound to be a feeling of
companionship. In port the officers and men had become
acquainted, either visiting aboard or meeting ashore. And together
they had stood by to aid the people of the Antilles and the Finland at
the risk of destruction by torpedo attack.
CHIEF YEOMAN PAULSON GUNNER’S MATE WILEY