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MEDICAL MICROBIOLOGY

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Medical
Microbiology
NINTH EDITION

Patrick R. Murray, PhD, F(AAM), F(IDSA)

Vice-President, Microbiology
Sparks, Maryland;
Adjunct Professor, Department of Pathology
University of Maryland School of Medicine
Baltimore, Maryland

Ken S. Rosenthal, PhD

Professor of Immunology
Augusta University/University of Georgia Medical Partnership
Athens, Georgia;
Emeritus Professor,
Northeastern Ohio Medical University
Rootstown, Ohio

Michael A. Pfaller, MD, F(CAP), F(AAM), F(IDSA)

Consultant
JMI Laboratories
North Liberty, Iowa
Professor Emeritus
University of Iowa College of Medicine
Iowa City, Iowa

Edinburgh London New York Oxford Philadelphia St Louis Sydney 2021

iii
© 2021, Elsevier Inc. All rights reserved.

First edition 1990

Second edition 1994
Third edition 1998
Fourth edition 2002
Fifth edition 2005
Sixth edition 2009
Seventh edition 2013
Eight edition 2016

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(other than as may be noted herein).

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using any information, methods, compounds or experiments described herein. Because of rapid advances
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Printed in the USA

Last digit is the print number: 9 8 7 6 5 4 3 2 1

 Contents
Preface, vii 19 Streptococcus and Enterococcus, 191
Acknowledgments, ix
Dedication, xi 20 Bacillus, 210
21 Listeria and Related Gram-Positive Bacteria, 217
SECTION 1
Introduction, 1 22 Mycobacterium and Related Acid-Fast
Bacteria, 226
1 Introduction to Medical Microbiology, 2
23 Neisseria and Related Genera, 241
2 Human Microbiome in Health and Disease, 6
24 Haemophilus and Related Bacteria, 250
3 Sterilization, Disinfection, and Antisepsis, 12
25 Enterobacteriaceae, 257
SECTION 2
26 Vibrio and Related Bacteria, 271
General Principles of Laboratory
Diagnosis, 17 27 Pseudomonas and Related Bacteria, 278
4 Microscopy and In Vitro Culture, 18 28 Campylobacter and Helicobacter, 286
5 Molecular Diagnosis, 24 29 Miscellaneous Gram-Negative Rods, 293
6 Serologic Diagnosis, 30 30 Clostridium, 307

SECTION 3 31 Non–Spore-Forming Anaerobic Bacteria, 318

Basic Concepts in the Immune Response, 37 32 Treponema, Borrelia, and Leptospira, 327
7 Elements of Host Protective Responses, 38 33 Mycoplasma, 340
8 Innate Host Responses, 49 34 Rickettsia, Ehrlichia, and Related Bacteria, 343
9 Antigen-Specific Immune Responses, 64 35 Chlamydia, 353
10 Immune Responses to Infectious Agents, 83
SECTION 5
11 Antimicrobial Vaccines, 104 Virology, 361

SECTION 4 36 Viral Classification, Structure, and

Replication, 362
Bacteriology, 113
37 Mechanisms of Viral Pathogenesis, 378
12 Bacterial Classification, Structure, and
Replication, 114 38 Role of Viruses in Disease, 388
13 Bacterial Metabolism and Genetics, 127 39 Laboratory Diagnosis of Viral Diseases, 396
14 Mechanisms of Bacterial Pathogenesis, 142 40 Antiviral Agents and Infection Control, 403
15 Role of Bacteria in Disease, 152 41 Papillomaviruses and Polyomaviruses, 411
16 Laboratory Diagnosis of Bacterial Diseases, 161 42 Adenoviruses, 421
17 Antibacterial Agents, 169 43 Human Herpesviruses, 428
18 Staphylococcus and Related Gram-Positive 44 Poxviruses, 450
Cocci, 178
v
vi Contents

45 Parvoviruses, 456 65 Opportunistic Mycoses, 649

46 Picornaviruses, 461 66 Fungal and Fungal-Like Infections of Unusual or
Uncertain Etiology, 675
47 Coronaviruses and Noroviruses, 472
48 Paramyxoviruses, 478 SECTION 7
Parasitology, 685
49 Orthomyxoviruses, 490
67 Parasitic Classification, Structure, and
50 Rhabdoviruses, Filoviruses, and Replication, 686
Bornaviruses, 500
68 Pathogenesis of Parasitic Diseases, 693
51 Reoviruses, 507
69 Role of Parasites in Disease, 697
52 Togaviruses and Flaviviruses, 515
70 Laboratory Diagnosis of Parasitic Disease, 699
53 Bunyaviridae and Arenaviridae, 527
71 Antiparasitic Agents, 708
54 Retroviruses, 533
72 Intestinal and Urogenital Protozoa, 716
55 Hepatitis Viruses, 550
73 Blood and Tissue Protozoa, 729
56 Prion Diseases, 565
74 Nematodes, 750
SECTION 6 75 Trematodes, 768
Mycology, 571
76 Cestodes, 779
57 Fungal Classification, Structure, and
Replication, 572 77 Arthropods, 791
58 Pathogenesis of Fungal Disease, 578 SECTION 8
59 Role of Fungi in Disease, 587 78 Microbial Connections by Body System
60 Laboratory Diagnosis of Fungal Disease, 589 and Disease
BONUS electronic-only chapter. Access via your
61 Antifungal Agents, 600 included activation code

62 Superficial and Cutaneous Mycoses, 612 Answers

63 Subcutaneous Mycoses, 622 Index, 809

64 Systemic Mycoses Caused by Dimorphic
Fungi, 632
 Preface
Our knowledge about microbiology and immunology is to choose the most important information and explana-
constantly growing, and by building a good foundation of tions for inclusion in this textbook. Each chapter has been
understanding in the beginning, it will be much easier to carefully updated and expanded to include new, medically
understand the advances of the future. relevant discoveries. In each of these chapters, we have
Medical microbiology can be a bewildering field for the attempted to present the material that we believe will help
novice. We are faced with many questions when learning the student gain an interest in as well as a clear understand-
microbiology: How do I learn all the names? Which infec- ing of the significance of the individual microbes and their
tious agents cause which diseases? Why? When? Who is at diseases.
risk? Is there a treatment? However, all these concerns can With each edition of Medical Microbiology we refine and
be reduced to one essential question: What information update our presentation. There are many changes to the
do I need to know that will help me understand how ninth edition, both in the print and e-versions of the book.
to diagnose and treat an infected patient? The book starts with a general introduction to microbiol-
Certainly, there are a number of theories about what a ogy and chapters on the human microbiome and epidemi-
student needs to know and how to teach it, which suppos- ology of infectious diseases. The human microbiome (that
edly validates the plethora of microbiology textbooks that is, the normal population of organisms that populate our
have flooded the bookstores in recent years. Although we do bodies) can now be considered as another organ system
not claim to have the one right approach to teaching medi- with 10 times as many cells as human cells. This micro-
cal microbiology (there is truly no one perfect approach to biota educates the immune response, helps digest our food,
medical education), we have founded the revisions of this and protects us against more harmful microbes. Additional
textbook on our experience gained through years of teach- chapters in the introductory section introduce the tech-
ing medical students, residents, and infectious disease fel- niques used by microbiologists and immunologists and are
lows, as well as on the work devoted to the eight previous followed by chapters on the functional immune system.
editions. Recent developments in rapid microbial identification are
We have tried to present the basic concepts of medi- highlighted. The immune cells and tissues are introduced,
cal microbiology clearly and succinctly in a manner that followed by an enhanced chapter on innate immunity and
addresses different types of learners. The text is written updated chapters on antigen-specific immunity, antimi-
in a straightforward manner with, it is hoped, uncompli- crobial immunity, and vaccines. Each of the sections on
cated explanations of difficult concepts. In this edition, bacteria, viruses, fungi, and parasites is introduced by the
we challenged ourselves to improve the learning expe- relevant basic science chapters and then a summary chap-
rience even more. We are using the new technology on ter that highlights the specific microbial diseases before pro-
StudentConsult.com (e-version) to enhance access to the ceeding into descriptions of the individual microbes, “the
material. In the previous edition, we added chapter sum- bug parade.”
maries and learning aids in the beginning of each of the Each chapter on the specific microbes begins with a
microbe chapters, and on the e-version these are keyed to summary (including trigger words), which is keyed to the
the appropriate sections in the chapter. In the e-version appropriate part of the chapter in the e-version. As in previ-
of the ninth edition, we added an infectious disease ous editions, there are many summary boxes, tables, clini-
chapter that lists the microbes by organ system and cal photographs, and original clinical cases. Clinical Cases
disease with hyperlinks to the appropriate chapter are included because we believe students will find them
in the text. This will facilitate access to the microbes for particularly interesting and instructive, and they are a very
those in organ-system or disease/case-based curricula. efficient way to present this complex subject. Each chapter
As in previous editions, there are new and enhanced fig- in the “bug parade” is introduced by relevant questions to
ures to assist learning. Details are summarized in tabular excite students and orient them as they explore the chap-
format rather than in lengthy text, and there are colorful ter. Finally, students are provided with access to the new
illustrations for the visual learner. Clinical Cases pro- Student Consult website, which provides links to additional
vide the relevance that puts reality into the basic science. reference materials, clinical photographs, animations, and
Important points are emphasized in boxes to aid stu- answers to the introductory and summary questions of
dents, especially in their review, and the study questions, each chapter. Many of the figures are presented in step-by-
including Clinical Cases, address relevant aspects of each step manner to facilitate learning. A very important feature
chapter. Each section (bacteria, viruses, fungi, parasites) on the website is access to more than 200 practice exam
begins with a chapter that summarizes microbial diseases, questions that will help students assess their mastery of
and this also provides review material. the subject matter and prepare for their course and licen-
Our understanding of microbiology and immunology is sure exams. In essence, this edition provides an under-
rapidly expanding, with new and exciting discoveries in standable text, details, questions, examples, and a review
all areas. We used our experience as authors and teachers book all in one.

vii
viii Preface

To Our Future Colleagues: The What are all the disease characteristics and conse-
quences?
Students What is the epidemiology of infection?
How can you prevent its disease?
On first impression, success in medical microbiology would What is its treatment?
appear to depend on memorization. Microbiology may seem What social issues are caused by the microbial infection?
to consist of only innumerable facts, but there is also a logic Answering the DIVIRDEPTS questions will require that
to microbiology and immunology. Like a medical detective, you jump around in the chapter to find the information, but
the first step is to know your villain. Microbes establish a this will help you learn the material.
niche in our bodies; some are beneficial and help us to digest Get familiar with the textbook and its bonus materials and
our food and educate our immune system, while others may you will not only learn the material but also have a review
cause disease. Their ability to cause disease, and the disease book to work from in the future. For each of the microbes,
that may result, depend on how the microbe interacts with learn three to five words or phrases that are associated with
the host and the innate and immune protective responses the microbe—words that will stimulate your memory (trig-
that ensue. ger words, provided in the chapter summary) and organize
There are many ways to approach learning microbiology the diverse facts into a logical picture. Develop alternative
and immunology, but ultimately the more you interact with associations. For example, this textbook presents organ-
the material using multiple senses, the better you will build isms in the systematic taxonomic structure (frequently
memory and learn. A fun and effective approach to learn- called a “bug parade,” which the authors think is the easi-
ing is to think like a physician and treat each microbe est way to introduce the organisms). Take a given virulence
and its diseases as if it were an infection in your property (e.g., toxin production) or type of disease (e.g.,
patient. Create a patient for each microbial infection meningitis) and list the organisms that share this property.
and compare and contrast the different patients. Pretend that an imaginary patient is infected with a specific
Perform role-playing and ask the seven basic questions as agent and create the case history. Explain the diagnosis to
you approach this material: Who? Where? When? Why? your imaginary patient and also to your future professional
Which? What? and How? For example: Who is at risk for colleagues. In other words, do not simply attempt to mem-
disease? Where does this organism cause infections (both orize page after page of facts; rather, use techniques that
body site and geographic area)? When is isolation of this stimulate your mind and challenge your understanding of
organism important? Why is this organism able to cause the facts presented throughout the text and it will be more
disease? Which species and genera are medically impor- fun. Use the summary chapter at the beginning of each
tant? What diagnostic tests should be performed? How is organism section to review and help refine your “differen-
this infection managed? Each organism that is encountered tial diagnosis” and classify organisms into logical “boxes.”
can be systematically examined. No textbook of this magnitude would be successful without
Use the following acronym to create a clinical case the contributions of numerous individuals. We are grate-
and learn the essential information for each microbe: ful for the valuable professional help and support provided
DIVIRDEPTS. by the staff at Elsevier, particularly Jeremy Bowes, Joanne
How does the microbial disease present in the patient and Scott and Andrew Riley. We also want to thank the many
the differential diagnosis? students and professional colleagues who have offered their
How would you confirm the diagnosis and identify the advice and constructive criticism throughout the develop-
microbial cause of disease? ment of this ninth edition of Medical Microbiology.
What are the virulence properties of the organism that
cause the disease? Patrick R. Murray, PhD, F(AAM), F(IDSA)
What are the helpful and harmful aspects of the innate
Ken S. Rosenthal, PhD
and immune response to the infection?
What are the specific conditions or mechanisms for Michael A. Pfaller, MD, F(CAP), F(AAM), F(IDSA)
replicating the microbe?
 Acknowledgments
We would like to acknowledge all the editors and staff who helped in the development
and production of this text.

ix
This page intentionally left blank

     
To all who use this textbook, that they may benefit from
its use as we did in its preparation
This page intentionally left blank

     
SECTION 1
Introduction

SECTION OUTLINE 1 Introduction to Medical Microbiology

2 Human Microbiome in Health and Disease
3 Sterilization, Disinfection, and Antisepsis

1
Discovering Diverse Content Through
Random Scribd Documents
 NOTICE BIOGRAPHIQUE[2]

Le Père Louis Marie Sinistrari, de l'Ordre des Mineurs Réformés de

l'étroite Observance de Saint-François, naquit à Ameno, petite ville
du district de Saint-Jules, dans le diocèse de Novare, le 26 Février
1622. Il reçut une éducation libérale et fit ses humanités à Pavie, où
il entra, en 1647, dans l'Ordre des Franciscains. Se consacrant alors
à l'enseignement, il fut d'abord professeur de Philosophie; puis il
enseigna dans la même ville la Théologie pendant quinze années
consécutives, au milieu d'un concours nombreux d'étudiants que sa
réputation avait attirés de tous les pays de l'Europe. Ses prédications
dans les principales villes de l'Italie, en même temps qu'elles firent
admirer son éloquence, produisirent pour la piété les meilleurs
résultats. Également cher au Siècle et à la Religion, il avait reçu de la
nature les dons les plus brillants: stature carrée, haute taille, visage
ouvert, front large, œil vif, teint coloré, conversation agréable et
pleine de saillies;[3] mais ce qui était plus précieux, il possédait
aussi les dons de la grâce, qui lui faisait supporter avec une
résignation invincible les attaques d'une maladie arthritique à
laquelle il était sujet; remarquable d'ailleurs par son humilité, sa
candeur et sa soumission absolue aux règles de son Ordre. Homme
de toutes sciences,[4] il avait appris sans maître les langues
étrangères, et souvent, dans les Comices généraux de son Ordre,
tenus à Rome, il soutint des thèses publiques de omni scibili.
Toutefois, il s'adonna plus particulièrement à l'étude des Droits Civil
et Canonique. Il occupa à Rome le poste de Consulteur au Tribunal
suprême de la Sainte Inquisition; fut pendant près de deux ans
Vicaire-Général de l'Archevêque d'Avignon, et ensuite Théologien
attaché à l'Archevêque de Milan. En 1688, chargé par les Comices
généraux des Franciscains de compiler les statuts de l'Ordre, il
s'acquitta de cette tâche dans son traité intitulé Practica criminalis
Minorum illustrata. Il mourut l'an de grâce 1701, le 6 Mars, à l'âge
de soixante-dix-neuf ans.[5]
 TABLE DES MATIÈRES

PAG
E
Avant-propos VII
Démonialité: origine du mot—En quoi ce crime diffère de ceux
de Bestialité et de Sodomie.—Opinion de Saint Thomas. Nos 1
à 8. 1
Le commerce matériel avec les Incubes et les Succubes n'est
pas imaginaire; témoignage de Saint Augustin. Nos 9 et 10. 15
Sorciers et Sorcières; leurs rapports avec le Diable; cérémonies
de leur profession. Nos 11 à 23. 21
Artifices employés par le Diable pour se donner un corps. No
24. 31
Les Incubes ne s'attaquent pas seulement aux femmes. No 26. 35
Esprits Follets: n'ont aucune frayeur des exorcismes. No 27. 37
Histoire plaisante de la signora Hieronyma: le repas enchanté.
No 28. 39
Hommes procréés par les Incubes: Romulus et Rémus, Platon,
Alexandre le Grand, César-Auguste, Merlin l'Enchanteur,
Martin Luther.—C'est d'un Incube que doit naître l'Antechrist.
No 30. 57
Les Incubes ne sont pas de purs esprits: ils engendrent, donc
ils ont un corps qui leur est propre.—Observation sur les
Géants. Nos 31 à 33. 59
Les Anges ne sont pas tous de purs esprits: décision conforme
du deuxième Concile de Nicée. No 37. 77
Existence de créatures ou animaux raisonnables, autres que
l'homme, et ayant comme lui un corps et une âme. Nos 38 à
43. 79
En quoi ces animaux diffèrent-ils de l'homme? Quelle est leur
origine? Descendent-ils, comme tous les hommes d'Adam,
d'un seul individu? Y a-t-il entre eux distinction de sexes?
Quelles sont leurs mœurs, leurs lois, leurs habitudes sociales?
Nos 44 à 50. 93
Quelles sont la forme et l'organisation de leur corps?
Comparaison tirée de la formation du vin. Nos 51 à 56. 101
Ces animaux sont-ils sujets aux maladies, aux infirmités
physiques et morales, à la mort? Nos 57 et 58. 115
Naissent-ils dans le péché originel? Ont-ils été rachetés par
Jésus-Christ, et sont-ils capables de béatitude et de
damnation? Nos 61 et 62. 127
Preuves de leur existence. Nos 65 à 70. 133
Histoire d'un Incube et d'une jeune nonne. No 71. 151
Histoire d'un jeune diacre. No 72. 155
Les Incubes sont affectés par des substances matérielles: donc
ils participent de la matière de ces substances. No 73. 161
Exemple tiré de l'histoire de Tobie: expulsion de l'Incube qui
tourmentait Sara; guérison du vieux Tobie. Nos 74 à 76. 163
Saint Antoine rencontre un Faune dans le désert: leur
conversation. Nos 77 à 84. 173
Autres preuves de la corporéité des Incubes, notamment la
Manne des Hébreux ou Pain des Anges. Nos 90 à 95. 193
Comment il faut entendre ces paroles du Christ: «J'ai d'autres 205
brebis qui ne sont pas de cette bergerie».—Discours d'Apollon
 à l'Empereur Auguste: la fin des Dieux. Nos 96 à 101.
«Le Grand Pan est mort», ou la mort du Christ annoncée aux
Faunes, Sylvains et Satyres; leurs lamentations. No 102. 217
Solution du problème: Comment une femme peut être
fécondée par un Incube.—Comparaison des Géants avec les
mulets. Nos 104 à 105. 224
En quoi consiste la vertu génératrice; pourquoi il ne naît plus
de Géants. Luxuria in humido. Nos 106 à 111. 224
Appréciation du crime de Démonialité: 1o commis avec le
Diable; 2o commis avec l'Incube. Nos 112 à 114. 234
La Démonialité est-elle plus grave que la Bestialité?—
Conclusion. No 115. 238
Appendice. 243
Notice Bibliographique. 261
 LETTRE
du
R. P. PROVINCIAL DES CAPUCINS
POUR LA PROVINCE DE P....
P..., vendredi [8 octobre 1875].
†
Pax
Monsieur Isidore Liseux,
5, rue Scribe, Paris.
J'ai parcouru l'ouvrage que vous m'avez envoyé hier et, vraiment,
j'ai été content de l'édition; ce n'est pas encore le moment de
donner mon avis sur la valeur de l'œuvre en elle-même. Ici vous
n'auriez trouvé, en fait d'ouvrages du R. P. Louis-Marie d'Ameno, que
son livre: Practica criminalis Minorum; le De Delictis et Pœnis se
trouve, je crois, dans un autre de nos couvents; mais vous auriez
reçu un excellent accueil. Je crois que Des Grieux n'a guère habité le
Saint-Sulpice actuel, qui ne date que de 1816.
J'ai remarqué, à la page 132–133, une erreur de traduction assez
grave: vous rendez Carthusia Ticinensis par Chartreuse du Tessin,
quand il s'agit de la fameuse Chartreuse de Pavie, fort connue de
tous les voyageurs en Italie. Il y a aussi, autant qu'un coup d'œil
superficiel m'a permis de m'en rendre compte, quelques autres
erreurs; mais, en somme, l'œuvre est bonne, et vous pouvez
recevoir les félicitations de
Votre tout petit serviteur,
Fr. A.....
o. m. c.
m. p.
Couvent des Capucins, rue...
Paris.—Typographie Motteroz, 31, rue du Dragon.
 NOTES
[1]
Poppysmatum. Cette expression étant peu usitée, il
n'est pas inutile de consigner ici la définition qu'en donne
le Glossarium eroticum linguæ Latinæ (auctore P. P.,
Paris, 1826):
POPPYSMA.—Oris pressi sonus, similis illi quo
permulcentur equi et canes. Obscene vero de susurro
cunni labiorum, quum frictu madescunt.
Le P. Sinistrari, très-versé dans la littérature classique,
avait fait son profit de l'épigramme suivante de Martial (l.
VII, 18):
IN GALLAM
Quum tibi sit facies, de qua nec fœmina possit
Dicere, quum corpus nulla litura notet;
Cur te tam rarus cupiat, repetat que fututor,
Miraris? Vitium est non leve, Galla, tibi.
Accessi quoties ad opus, mixtisque movemur
Inguinibus, cunnus non tacet, ipsa taces.
Di facerent, ut tu loquereris, et ipse taceret!
Offendor cunni garrulitate tui.
Pedere te mallem: namque hoc nec inutile dicit
Symmachus, et risum res movet ista simul.
Quis ridere potest fatui poppysmata cunni?
Quum sonat hic, cui non mentula mensque cadit?
Dic aliquid saltem, clamosoque obstrepe cunno:
Et si adeo muta es, disce vel inde loqui.
 (Note de l'éditeur.)
[2]
Cette Notice est extraite du tome Ier des Œuvres
complètes du P. Sinistrari (Romæ, 1753).
[3]
«Quadrato corpore, statura procera, facie liberali,
fronte spatiosa, oculis rutilantibus, colore vivido, jucundæ
conversationis, ac lepidorum salium.»
[4]
«Omnium scientiarum vir.»
[5]
Les Œuvres complètes du P. Sinistrari (Romæ,
Giannini, 1753–1754, 3 vol. in-folio), comprennent les
livres suivants: Practica criminalis Minorum illustrata,—
Formularium criminale,—De Incorrigibilium expulsione ab
Ordinibus Regularibus,—De Delictis et Pœnis, auxquels il
convient d'ajouter le présent ouvrage: De Dæmonialitate,
publié pour la première fois en 1875.
 *** END OF THE PROJECT GUTENBERG EBOOK DE LA
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