Oral Microbiology. Third edition. Philip Marsh PUb/IC Health Laboratory Service Centre for Applied Microbiology and Research Salisbury.

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1 Oral Microbiology

2 Oral Microbiology Third edition Philip Marsh PUb/IC Health Laboratory Service Centre for Applied Microbiology and Research Salisbury and Michael Martin Department of Clinical Dental SCiences UnIVersity of Liverpool m CHAPMAN &. HALL University and Professional DIvIsion London Glasgow New York Tokyo Melbourne Madras

3 Published by Chapman" Hall, 2-6 Boundary Row, London SE1 8HN Chapman & Hall, 2-6 Boundary Row, London SE1 BHN, UK Blackie Academic & Professional, Wester Cleddens Road, Bishopbriggs, Glasgow G64 2NZ, UK Chapman & Hall, 29 West 35th Street, New York NY10001, USA Chapman & Hall Japan, Thomson Publishing Japan, Hirakawacho Nemoto BUilding, 6F, Hirakawa-cho, Chiyoda-ku, Tokyo 102, Japan Chapman & Hall Australia, Thomas Nelson Australia, 102 Dodds Street, South Melbourne, Victoria 3205, Australia Chapman & Hall India, R. Seshadri, 32 Second Main Road, CIT East, Madras , India First edition 1980 Second edition 1984 Reprinted 1985, 1988, 1989 Third edition 1992 Reprinted ,1984,1992 P.O. Marsh and M.V. Martin Typeset in 10/12pt Palatino by Intype, London ISBN DOl / ISBN (ebook) Apart from any fair dealing for the purposes of research or private study, or criticism or review, as permitted under the UK Copyright Designs and Patents Act, 1988, this publication may not be reproduced, stored, or transmitted, in any form or by any means, without the prior permission in writing of the publishers, or in the case of reprographic reproduction only in accordance with the terms of the licences issued by the Copyright Licensing Agency in the UK, or in accordance with the terms of licences issued by the appropriate Reproduction Rights Organization outside the UK. Enquiries concerning reproduction outside the terms stated here should be sent to the publishers at the London address printed on this page. The publisher makes no representation, express or implied, with regard to the accuracy of the information contained in this book and cannot accept any legal responsibility or liability for any errors or omissions that may be made. A catalogue record for this book is available from the British Library Library of Congress Cataloging-in-Publication Data available

4 To Jane, Katherine, Thomas and Jonathan

5 Contents Preface to the third edition Preface to the second edition Preface to the first edition xi xiii xiv 1 Oral microbiology. Background and introduction 1 The role of the oral microflora in health and disease 1 Terminology 3 Summary 4 Further reading 5 2 The mouth as a microbial habitat 6 The mouth as a habitat 6 Factors affecting the growth of micro-organisms in the oral cavity 14 Summary 25 Further reading 25 3 The resident oral microflora 27 Principles of microbial taxonomy 27 Principles of microbial identification 28 Recent advances in microbial taxonomy 29 Gram-positive cocci 30 Gram-positive rods and filaments 39 Gram-negative cocci 43 Gram-negative rods 45 Mycoplasma 50 Fungi 50 Viruses 51 Protozoa 52 Summary 53 Further reading 54

6 VIIi Contents 4 Acquisition, adherence, distribution and functions of the oral microflora 56 Acquisition of the resident oral microflora 56 Ageing and the oral microflora 59 Methods of determining the resident oral microflora 60 Distribution of the resident oral microflora 66 Factors influencing the distribution of oral microorganisms 71 Factors involved in adherence 75 Functions of the climax community: colonization resistance 80 Metabolism of oral bacteria 82 Summary 96 Further reading 97 5~ Dental plaque 98 Development of plaque 98 Structure and function of dental plaque 101 Mechanisms of plaque formation 105 Bacterial composition of the climax community of dental plaque from different sites 113 Plaque fluid 121 Calculus 122 Microbial interactions in dental plaque 123 Microbial homeostasis in dental plaque 129 Summary 131 Further reading Dental caries 133 Specific and non-specific plaque hypotheses 133 Evidence for caries as an infectious disease 135 Aetiology of human enamel caries 136 Microbiology of enamel caries 137 Microbiology of root-surface caries 146 Bacterial invasion of dentine and root canals 149 Pathogenic determinants of cariogenic bacteria 151 Approaches for controlling dental caries 155 Summary 164 Further reading Periodontal diseases 167 Ecology of the periodontal pocket: implications for plaque sampling 167

7 Contents IX Evidence for microbial involvement in periodontal diseases 170 Microbiology of periodontal diseases 171 The habitat and source of periodontopathic bacteria 186 Treatment and prevention of periodontal diseases 187 Pathogenic determinants of periodontopathic bacteria 189 Pathogenic synergism and periodontal disease 194 Summary 196 Further reading The role of oral bacteria in other infections 198 Predisposing factors 198 Abscesses in the oral region 200 Dental abscesses 200 Abscesses associated with osseointegrated implants 203 Osteomyelitis 203 Dry sockets 204 Actinomycosis 204 Salivary gland infections 205 Infective endocarditis and bacteraemia 207 The use and misuse of antimicrobial agents in the control of micro-organisms 210 Summary 211 Further reading Yeasts and viral infections 212 Candidosis 212 Other fungal infections 218 The hepatitis viruses 218 Human immunodeficiency virus 221 Herpes 224 Hand, foot and mouth disease 224 Other viruses 225 Summary 225 Further reading Cross infection control 227 The routes and source of cross infection 227 The evidence for proven cross infection 229 Vaccination 231 Medical history 231 The risk areas 232 Summary 237

8 x Contents Further reading 237 Concluding remarks 238 Glossary 241 Index 245

9 Preface to the third edition Since the second edition of Oral Microbiology was published in 1984, there has been an enormous expansion in knowledge across the complete breadth of this subject area. This has resulted in the need to not just update but to totally rewrite the previous edition. In particular, there have been striking advances in the taxonomy of the oral microflora, which is enabling closer associations between certain organisms with health and disease to be discerned. These changes in classification have caused difficulties when comparing new studies with earlier work when a different nomenclature was in use. It is hoped that the comparisons of the past and present classification schemes presented in this edition will be of value to young and experienced researchers alike. The significance of the role of endogenous substrates to the nutrition of the resident oral microflora, and the complex relationship between the host defences and the normal flora is also discussed extensively in this edition. The last few years have seen renewed interest and progress in the understanding of dental caries, particularly of the root surface in the elderly. Advances have continued to be made in the microbial aetiology of periodontal diseases, while the precise role of specific bacterial species in tissue breakdown remains a contentious area. These advances in knowledge are being converted into improved methods of diagnosis, treatment, and prevention. New research into oral manifestations of AIDS, the control of cross infection and of other oral infections has made this an opportune time to write an enlarged, third edition of this book. It is intended that this new edition will continue to help science and clinical students of all levels, as well as research workers and teachers alike, to understand the microbial ecology of the oral cavity and its importance in health and disease. We would like to thank our colleagues who have helped and advised us, especially Else Theilade, Michael Pang, Jeremy Hardie, Rob Whiley, Saheer Gharbia, Haroun Shah, Roy Russell and Pauline Handley. We

10 XII Preface to the third edition would also like to thank the following individuals and publishers for granting permission to reproduce data or figures: Alan Dolby (Figure 6.2) and Pauline Handley (Figure 4.5, Table 4.6); American Society for Microbiology (Figure 4.5); Cambridge University Press (Figure 7.3, Table 7.7); Harwood Academic Publishers (Table 4.6); Journal of Dental Research (Tables 6.9 and 6.10); and MTP Press Ltd (Figures 2.6 and 4.2, Table 6.1). Particular thanks also go to our families who have put up with so much during the preparation of this book. P. D. Marsh, Salisbury M. V. Martin, Liverpool

11 Preface to the second edition Oral microbiology forms an important part of the curriculum of dental students while the multidisciplinary nature of the research in this area means that studies of the adherence, metabolism and pathogenicity of oral bacteria are equally relevant to microbiologists. The success of the first edition of Oral Microbiology stems in part from the fact that the book satisfies successfully the needs of both of these groups of students as well as those of general dental practitioners, medical students and senior scientists. Since the publication of the first edition there have been rapid advances in our knowledge of the mechanisms involved in dental plaque formation, in the metabolism of oral bacteria both in health and disease, and in the aetiology of periodontal disease. This knowledge is being applied to the development of specific measures to control the incidence and severity" of oral infections. Consequently, the second edition has been enlarged to include two comprehensive chapters on the current theories of the aetiology and prevention of these diseases. Elsewhere in the second edition, recent advances in our understanding of the colonization of the tooth surface by oral bacteria and in the biochemical basis of their pathogenicity have also been incorporated, while the glossary of microbiological and dental terms has been extended. The nomenclature of oral bacteria has been brought up to date, although this is an area in constant flux and the future will result in minor changes in the bacterial nomenclature as used in this text. We would like to thank Derek Ellwood, Bill Keevil, Ailsa McKee, Haroun Shah and Geoffrey Craig and all our colleagues who have helped and advised us in the preparation of the second edition. Especial thanks go to our wives, Jane and Anne, and our families for their patience, support and encouragement P. D. Marsh, Salisbury M. V. Martin, Liverpool

12 Preface to the first edition Micro-organisms in the mouth are responsible for a variety of infections including the most prevalent diseases affecting man today. A vast amount of pure and applied research in many disciplines is underway in an attempt to determine the aetiology of these oral infections with the hope that preventive measures can be developed. Results from such studies appear in a bewildering spectrum of journals and although review articles on specific topics have been published there have been only a few attempts to produce a text-book devoted solely to oral microbiology. The object of this book is to bridge this gap in the literature by providing a general introduction to the microbiology of the mouth both in health and disease. Oral Microbiology has been written deliberately to appeal also to students of dentistry who lack an inexpensive text dealing specifically with this important part of their syllabus. Naturally, terminology will have been used that is unfamiliar to students of either subject. I hope that the provision of glossary will overcome any problems that might arise. A book of this length produces severe constraints on the amount of material that can be included. Of necessity, a few topics have had to be omitted or treated superficially and some areas of current debate and controversy have been simplified for clarity. I am indebted to many colleagues for their constructive criticism and advice during the preparation of the manuscript, particularly Dr George Bowden, Dr Jeremy Hardie and Dr Paul Rutter. All the photographs were kindly provided by Mr Alan Saxton of Unilever Research. I would like to take this opportunity to thank the authors and publishers who gave their permission for me to reproduce tables and figures from their articles. In addition I want to express my gratitude to Mrs Mabel Cockerill for her excellent and accurate typing of the manuscript, to Dr Dominic Recaldin and his staff of Thomas Nelson and Sons Ltd., and to the series' editors for their help in making the writing of this, my first book, such a painless experience. Finally, I would like to thank my wife, Jane,

13 Preface to the first edition xv for her support and encouragement during all stages of the preparation of this book. London, 1979 P. D. Marsh

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