Microbial Inhabitants of Humans
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1 Microbial Inhabitants of Humans The indigenous microbiota (or normal microflora ) comprises those microbes that inhabit the healthy human body. Many of these organisms (e.g., Streptococcus pyogenes, Staphylococcus aureus, Neisseria meningitidis, Haemophilus influenzae, and Escherichia coli) are responsible for common, and sometimes life-threatening, infections of healthy individuals, whereas others cause disease only when the body s defenses are impaired. This advanced textbook provides a unique overview of the microbial communities inhabiting those regions of the human body that are exposed to the external environment; these include the skin, eyes, oral cavity, and the respiratory, urinary, reproductive, and gastrointestinal tracts. To understand why particular organisms are able to colonize an anatomical region and why the resulting microbial community has a particular composition, an ecological approach is essential. Consequently, the key anatomical and physiological characteristics of each body site are described to show how these influence the nature of the environment at that site. The crucial roles of the indigenous microbiota in protecting against exogenous pathogens, regulating the development of our immune system and mucosae, and providing nutrients are also discussed. The involvement of these organisms in infections of healthy and debilitated individuals are described throughout, and methods of manipulating the composition of the indigenous microbiota for the benefit of human health are discussed. Microbial Inhabitants of Humans is a core textbook for advanced students taking courses in microbiology, medical microbiology, microbial ecology, and human biology. is Professor of Microbiology in the Faculty of Clinical Sciences and Head of the Department of Microbiology at the Eastman Dental Institute at University College London. He is the Editor-in-Chief of the journal Biofilms and has coauthored or edited several books, including Bacterial Disease Mechanisms (2002), Bacterial Adhesion to Host Tissues (2002), and Medical Implications of Biofilms (2003). i
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3 Microbial Inhabitants of Humans Their ecology and role in health and disease University College London iii
4 32 Avenue of the Americas, New York ny , USA Cambridge University Press is part of the University of Cambridge. It furthers the University s mission by disseminating knowledge in the pursuit of education, learning and research at the highest international levels of excellence. Information on this title: / This publication is in copyright. Subject to statutory exception and to the provisions of relevant collective licensing agreements, no reproduction of any part may take place without the written permission of Cambridge University Press. First published 2005 A catalogue record for this publication is available from the British Library Library of Congress Cataloguing in Publication data Wilson, Michael, Microbial inhabitants of humans : their ecology and role in health and disease /. p. cm. Includes bibliographical references and index. ISBN Body, Human Microbiology. 2. Medical microbiology. 3. Microbial ecology. I. Title. QR46.W dc isbn Hardback Cambridge University Press has no responsibility for the persistence or accuracy of URLs for external or third-party internet websites referred to in this publication, and does not guarantee that any content on such websites is, or will remain, accurate or appropriate.
5 For Andrew, Bernie, Caroline, Fionn, Margaret, Mike, Pippa, Richard, Sarah, and Wil Long may your symbionts protect you v
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7 Contents Preface Abbreviations used for microbial genera xvii xix Chapter 1 An introduction to the human microbe symbiosis page Overview of the distribution and nature of the indigenous microbiota of humans Difficulties associated with determining microbial community composition Structural aspects of residential microbial communities Communication between members of microbial communities Environmental determinants affecting the distribution and composition of the indigenous microbiota Nutritional determinants Physicochemical determinants Mechanical determinants Biological determinants Host characteristics affecting the indigenous microbiota Effect of age Effect of host genotype Effect of gender Analytical methods used in characterising the indigenous microbiota Microscopy Culture Molecular approaches Metabolic approaches The epithelium site of host microbe interactions Structure of epithelia The epithelium as an excluder of microbes Mucus and mucins Innate and acquired immune responses at the mucosal surface Further reading 47 Chapter 2 The skin and its indigenous microbiota Anatomy and physiology of human skin Antimicrobial defence mechanisms of the skin Environmental determinants at different regions of the skin The indigenous microbiota of the skin Main characteristics of key members of the cutaneous microbiota Corynebacterium spp Propionibacterium spp Staphylococcus spp Micrococcus spp Malassezia spp. 73 vii
8 viii CONTENTS Acinetobacter spp Brevibacterium spp Dermabacter hominis Acquisition of the cutaneous microbiota Community composition at different sites Scalp Forehead Toe interspace Perineum Axillae Sole of the foot Forearm and leg Hands Outer ear Interactions among members of the cutaneous microbiota Dissemination of organisms from the skin Effect of antibiotics and other interventions on the indigenous microbiota of the skin Antibiotics Occlusion Skin cleansing Diseases caused by members of the cutaneous microbiota Acne Intravascular catheter-associated infections Infections associated with implanted prosthetic devices Wound infections Urinary tract infections Infective endocarditis Diseases caused by Malassezia spp Erythrasma Odour Pitted keratolysis Trichomycosis Further reading 104 Chapter 3 The eye and its indigenous microbiota Anatomy and physiology of the eye Antimicrobial defence mechanisms of the eye Environmental determinants at different regions of the eye The indigenous microbiota of the eye Main characteristics of key members of the ocular microbiota Acquisition of the ocular microbiota Composition of the indigenous microbiota of the eye Interactions among members of the ocular microbiota Dissemination of organisms from the eye Effect of antibiotics and other interventions on the ocular microbiota Antibiotic administration Contact lens wear 121
9 CONTENTS ix 3.5 Diseases caused by members of the ocular microbiota Conjunctivitis Blepharitis Keratitis Endophthalmitis Orbital cellulitis Dacryocystitis Further reading 125 Chapter 4 The respiratory system and its indigenous microbiota Anatomy and physiology of the respiratory tract Nose Pharynx Larynx Trachea Bronchi and bronchioles Alveolus Antimicrobial defence mechanisms of the respiratory tract Nasal cavity Conducting portion of respiratory tract other than the nasal cavity Respiratory portion Environmental determinants at different regions of the respiratory tract Composition of nasal fluid Composition of airway surface liquid Composition of alveolar lining fluid Contribution of microbial residents of the respiratory tract to nutrient availability Indigenous microbiota of the respiratory tract Main characteristics of key members of the respiratory microbiota Neisseria spp Haemophilus spp Streptococcus spp Streptococcus pyogenes Streptococcus pneumoniae Viridans group streptococci Moraxella catarrhalis Staphylococcus aureus Mollicutes Acquisition of the respiratory microbiota Community composition at different sites within the respiratory tract External nares Nasal cavity Nasopharynx Oropharynx Lower respiratory tract 166
10 x CONTENTS Interactions among members of the respiratory microbiota Dissemination of organisms from the respiratory tract Effects of antibiotics and other interventions on the respiratory microbiota Antibiotics Vaccination Intubation Radiation therapy Diseases caused by members of the respiratory microbiota Meningitis Pneumonia Sinusitis Otitis media Epiglottitis Diseases due to Staph. aureus Diseases due to Strep. pyogenes Further reading 178 Chapter 5 The urinary system and its indigenous microbiota The urinary system of females Anatomy and physiology Antimicrobial defence mechanisms of the urinary system Environmental determinants within the urethra The indigenous microbiota of the female urethra Main characteristics of key members of the urethral microbiota Acquisition of the urethral microbiota Community composition within the female urethra Dispersal of organisms from the urethra Effect of antibiotics and other interventions on the urethral microbiota Antibiotics Catheterisation Diseases caused by members of the urethral microbiota of females Infections due to Gram-positive anaerobic cocci Urethral syndrome The urinary system of males Anatomy and physiology Antimicrobial defence mechanisms Environmental determinants within the male urethra The indigenous microbiota of the male urethra Main characteristics of key members of the microbiota Acquisition of the microbiota of the male urethra Community composition of the microbiota of the male urethra Dispersal of organisms from the urethra Effect of antibiotics and other interventions on the urethral microbiota 201
11 CONTENTS xi Antibiotic use Catheterisation Diseases caused by members of the urethral microbiota of males Urethritis Prostatitis Balanitis Further reading 203 Chapter 6 The reproductive system and its indigenous microbiota Anatomy and physiology of the female reproductive system Antimicrobial defence mechanisms of the female reproductive system Innate defence mechanisms of the female reproductive system Acquired immune defence mechanisms of the female reproductive system Environmental determinants at different regions of the reproductive system Vagina Cervix Vulva Contribution of microbial residents of the reproductive system to nutrient availability The indigenous microbiota of the female reproductive system Main characteristics of key members of the microbiota Lactobacillus spp Ureaplasma urealyticum Gardnerella vaginalis Candida albicans Streptococcus agalactiae (Group B streptococcus) Acquisition of the microbiota of the female reproductive system Community composition at different sites within the female reproductive system Vagina Microbiota of post-menarchal/pre-menopausal women Microbiota of pre-menarchal girls Microbiota of post-menopausal women Cervix Vulva Dissemination of organisms from the female reproductive system Effect of antibiotics and other interventions and events on the indigenous microbiota of the female reproductive system Antibiotics Contraceptives Sexual intercourse 240
12 xii CONTENTS Pregnancy Douching Diseases caused by members of the indigenous microbiota of the female reproductive system Infections of the vagina Bacterial vaginosis Vaginal candidiasis Infections at sites other than the vagina Pelvic inflammatory disease Endometritis Chorioamnionitis Pre-term birth Neonatal infections Bartholinitis Further reading 248 Chapter 7 The gastrointestinal tract and its indigenous microbiota Anatomy and physiology of the gastrointestinal tract Antimicrobial defence mechanisms of the gastrointestinal tract Innate defence systems Acquired immune defence system Environmental determinants within different regions of the gastrointestinal tract Oesophagus Stomach Small intestine Large intestine The indigenous microbiota of the gastrointestinal tract Main characteristics of key members of the intestinal microbiota Bacteroides spp Eubacterium spp Clostridium spp Bifidobacterium spp Enterococcus spp Helicobacter pylori Enterobacteriaceae Ruminococcus spp Methanogenic bacteria Desulphovibrio spp Acquisition of the intestinal microbiota Community composition at different sites Oesophagus Stomach Small intestine Large intestine Microbial interactions in the gastrointestinal tract Positive interactions Negative interactions 296
13 CONTENTS xiii Dissemination of organisms from the gastrointestinal tract Effect of antibiotics and other interventions on the microbiotas of the gastrointestinal tract Antibiotics Artificial nutrition Probiotics and prebiotics Diseases caused by members of the intestinal microbiota Diseases due to Helicobacter pylori Irritable bowel syndrome Inflammatory bowel disease Diseases due to Clostridium spp Intra-abdominal infections Diseases due to Enterobacteriaceae Urinary tract infections Urinary tract infections in females Urinary tract infections in males Colorectal cancer Systemic infections resulting from bacterial translocation Contaminated small bowel syndrome Further reading 313 Chapter 8 The oral cavity and its indigenous microbiota Anatomy and physiology of the oral cavity Antimicrobial defence mechanisms of the oral cavity Environmental determinants at the various sites within the oral cavity Mechanical determinants Nutritional determinants Physicochemical determinants The indigenous microbiota of the oral cavity Main characteristics of key members of the oral microbiota Oral streptococci and other Gram-positive cocci Actinomyces spp Veillonella spp Anaerobic Gram-negative bacilli Spirochaetes Facultatively anaerobic Gram-negative bacilli Acquisition of the oral microbiota Community composition at different sites Supragingival plaque Gingival crevice Tongue Other mucosal surfaces Dissemination of organisms from the mouth Effect of antibiotics and other interventions on the oral microbiota Antibiotics Mechanical oral-hygiene measures Prosthetic devices Immunosuppressive chemotherapy 363
14 xiv CONTENTS 8.5 Diseases caused by members of the oral microbiota Dental caries Periodontal diseases Chronic gingivitis Acute necrotising ulcerative gingivitis Periodontitis Bacterial endocarditis and other extra-oral infections Denture stomatitis Halitosis Endodontic infections Actinomycosis Further reading 372 Chapter 9 Role of the indigenous microbiota in maintaining human health Colonisation resistance Exclusion of exogenous microbes Mechanisms involved in colonisation resistance Occupation of adhesion sites Alteration of the physico-chemical environment Production of antagonistic substances Utilisation of the available nutrients within a site Disruption of colonisation resistance Role of microbial factors Role of host factors Host development Host nutrition Short-chain fatty acids Vitamins Detoxification Further reading 392 Chapter 10 Manipulation of the indigenous microbiota Probiotics Probiotics and gastrointestinal health Probiotics and vaginal health Prevention of dental caries using probiotics Prebiotics Inhibition of microbial adhesion Inhibition of adhesion using antibodies Inhibition of adhesion using adhesins or adhesin analogues Inhibition of adhesion using receptors or receptor analogues Prevention of medical-device-associated infections Replacement therapy Prevention of infections due to Staphylococcus aureus Prevention of pharyngeal colonisation and infection Prevention of dental caries 410
15 CONTENTS xv Prevention of otitis media Prevention of urinary tract infections Treatment of infections due to Clostridium difficile Localised modification of the host environment Further reading 416 Index 421
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17 Preface The Guiness Book of Records and the Hitch Hikers Guide to the Galaxy are both books that document many astounding facts concerning life, the universe, and everything else. However, as far as I am aware, in neither of these eminent publications is there any mention of two truly amazing observations: an adult human being consists of ten times as many microbial cells as mammalian cells, and he or she carries around approximately 1.25 kg of microbes. Knowing this, who could fail to be intrigued by the microbial component of that mammal microbe symbiosis known to us as a human being. The immediate questions prompted by this knowledge are usually along the lines of: (1) Which microbes are present? (2) How do they manage to survive? (3) What are they doing there? (4) Are they dangerous? Each of these questions about our indigenous microbiota is addressed in this book, and some of the answers will be surprising. The complexity of the microbial communities found at many body sites is truly astounding; it has been estimated that we provide a home for at least 1,500 different microbial taxa that collectively contain more than 200 times as many genes as the human genome. Most of these organisms have not yet been grown in the laboratory, and so we know very little about them. However, modern molecular approaches are not only enabling us to detect their presence but, thanks to gene sequencing, also to gain some idea of their physiology and virulence potential. In order to try to understand how members of the indigenous microbiota manage to survive on our body and what they are up to while living there, an ecological approach has been adopted in this book motivated by Pasteur s statement that, The germ is nothing. It is the terrain in which it is found that is everything. As for the question of the ability of such microbes to cause disease the answer is a resounding yes. Some of the deadliest diseases of humankind are caused by microbes that are normal inhabitants of various body sites of healthy individuals (e.g., Neisseria meningitidis, Streptococcus pyogenes, Haemophilus influenzae, Staphylococcus aureus, and Streptococcus pneumoniae). Amazingly, for most of our lives, the majority of individuals suffer no ill effect from harboring such organisms. Less virulent members of the indigenous microbiota are also a frequent cause of less life-threatening but nevertheless debilitating diseases. In fact, the most common infectious diseases of mankind caries, periodontal diseases, and urinary tract infections are all caused by microbes indigenous to humans. Furthermore, advances in medicine and surgery have resulted in the increasing use of various devices and immunosuppressive therapies which have provided opportunities for many indigenous microbes to cause a variety of serious infections. However, all is not doom and gloom, and it is important also to consider a question that is not often asked about our indigenous microbiota: Are they of any benefit? The answer, undoubtedly, is yes. Not only do our indigenous microbiota protect us against exogenous pathogenic microbes, but they also provide us with as much as 10 percent of our energy requirements, supply a range of vitamins, and play a key role in the development of our immune system and mucosal surfaces. xvii
18 xviii PREFACE Disappointingly, but not surprisingly, the attention that has been given to most members of the indigenous microbiota (other than disease-inducing species) by microbiologists and immunologists is insignificant compared with that directed toward exogenous pathogens. This has left us remarkably ignorant of the most intimate relationship that any of us will ever experience during our lifetime. The exhortation to know thyself must surely extend to that part of the human microbe symbiosis (i.e., our symbionts) that can justifiably be termed microbial self. It is the author s hope that this book will inspire others to take a greater interest in, as well as to cherish, our indigenous microbiota.
19 Abbreviations used for microbial genera A. Actinomyces Ab. Abiotrophia Acin. Acinetobacter Act. Actinobacillus Aer. Aeromonas All. Alloiococcus B. Bacteroides Bac. Bacillus Bif. Bifidobacterium Brev. Brevibacterium C. Corynebacterium Camp. Campylobacter Can. Candida Cap. Capnocytophaga Chlam. Chlamydia Cit. Citrobacter Cl. Clostridium Col. Collinsella Des. Desulphovibrio E. Escherichia Eg. Eggerthella Eik. Eikenella Ent. Enterococcus Enter. Enterobacter Eub. Eubacterium F. Fusobacterium G. Gardnerella Gem. Gemella H. Haemophilus Hel. Helicobacter K. Klebsiella Kyt. Kytococcus L. Lactobacillus Lac. Lactococcus Leg. Legionella Lep. Leptotrichia Lis. Listeria M. Micrococcus Mal. Malassezia Mor. Moraxella Myc. Mycoplasma Mycob. Mycobacterium N. Neisseria P. Propionibacterium Pep. Peptostreptococcus Por. Porphyromonas Pr. Proteus Prev. Prevotella Ps. Pseudomonas Roth. Rothia Rum. Ruminococcus Sac. Saccharomyces Sal. Salmonella Sel. Selenomonas Ser. Serratia Sh. Shigella Staph. Staphylococcus Strep. Streptococcus T. Treponema Tr. Trichomonas Tur. Turicella U. Ureaplasma V. Veillonella Y. Yersinia xix
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