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Oral Wound Healing Cell Biology and Clinical Management Edited by Hannu Larjava Professor and Chair, Division of Periodontics Faculty of Dentistry University of British Columbia Vancouver BC, Canada A John Wiley & Sons, Ltd., Publication

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Page 1: Oral Wound Healing (Larjava/Oral Wound Healing) || Front Matter

Oral Wound HealingCell Biology and Clinical Management

Edited by

Hannu LarjavaProfessor and Chair, Division of PeriodonticsFaculty of DentistryUniversity of British ColumbiaVancouverBC, Canada

A John Wiley & Sons, Ltd., Publication

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Page 2: Oral Wound Healing (Larjava/Oral Wound Healing) || Front Matter

This edition fi rst published 2012 by John Wiley & Sons, Inc

© 2012 John Wiley & Sons, Inc

Wiley-Blackwell is an imprint of John Wiley & Sons, Inc formed by the merger of Wiley’s global Scientifi c,

Technical and Medical business with Blackwell Publishing.

Registered Offi ceJohn Wiley & Sons, Ltd, The Atrium, Southern Gate, Chichester, West Sussex, PO19 8SQ, UK

Editorial Offi ces2121 State Avenue, Ames, Iowa 50014-8300, USA

The Atrium, Southern Gate, Chichester, West Sussex, PO19 8SQ, UK

9600 Garsington Road, Oxford, OX4 2DQ, UK

For details of our global editorial offi ces, for customer services and for information about how to

apply for permission to reuse the copyright material in this book please see our website at

www.wiley.com/wiley-blackwell.

Authorization to photocopy items for internal or personal use, or the internal or personal use of specifi c clients,

is granted by Blackwell Publishing, provided that the base fee is paid directly to the Copyright Clearance Center,

222 Rosewood Drive, Danvers, MA 01923. For those organizations that have been granted a photocopy license

by CCC, a separate system of payments has been arranged. The fee codes for users of the Transactional

Reporting Service are ISBN-13: 978-0-8138-0481-1/2007.

Designations used by companies to distinguish their products are often claimed as trademarks. All brand names

and product names used in this book are trade names, service marks, trademarks or registered trademarks of

their respective owners. The publisher is not associated with any product or vendor mentioned in this book. This

publication is designed to provide accurate and authoritative information in regard to the subject matter covered.

It is sold on the understanding that the publisher is not engaged in rendering professional services. If professional

advice or other expert assistance is required, the services of a competent professional should be sought.

Library of Congress Cataloging-in-Publication Data

Oral wound healing : cell biology and clinical management / edited by Hannu Larjava.

p. ; cm.

Includes bibliographical references and index.

ISBN 978-0-8138-0481-1 (hardcover : alk. paper)

I. Larjava, Hannu.

[DNLM: 1. Periodontal Diseases–rehabilitation. 2. Mouth–injuries. 3. Oral Surgical

Procedures–rehabilitation. 4. Wound Healing. WU 240]

617.6′32–dc23

2011042663

A catalogue record for this book is available from the British Library.

Wiley also publishes its books in a variety of electronic formats. Some content that appears in print may not be

available in electronic books.

Set in 10/12pt Times by SPi Publisher Services, Pondicherry, India

1 2012

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Page 3: Oral Wound Healing (Larjava/Oral Wound Healing) || Front Matter

Contents

Contributors xiii

Preface xvii

1 Oral Wound Healing: An Overview 1 Hannu Larjava

Clotting and inflammation (chapters 2, 3 and 4) 1

Re-epithelialization and granulation tissue formation (chapters 5 and 6) 2

Angiogenesis (chapter 7) 3

Healing of extraction sockets (chapter 8) 4

Flap design for periodontal wound healing (chapter 9) 4

Regeneration of periodontal tissues (chapters 10 and 11) 5

Osteointegration and soft tissue healing around

dental implants (chapter 12) 6

The pulp healing process (chapter 13) 7

Dermal wound healing and burn wounds (chapter 14) 7

Healing of large dentofacial defects (chapter 15) 8

References 9

2 Hemostasis, Coagulation and Complications 11 Carol Oakley and Hannu Larjava

Introduction 11

Primary hemostasis 12

Secondary hemostasis and the coagulation system 13

Tertiary hemostasis 16

Tissue factor 16

Von willebrand factor 17

Other coagulation factors 17

Cell-centric model of hemostasis: from initiation to propagation 18

The procoagulant membrane 20

Membrane particles 22

Endothelium and hemostasis 22

Pro- and anticoagulant functions 22

Platelets 24

Coagulation and wound healing 26

Limitations of the waterfall cascade model and screening laboratory tests 26

Implications for laboratory tests 27

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vi Contents

Pre-surgical evaluation to prevent bleeding problems 27

Medical history 27

Diet and herbal supplements 29

Clinical examination 29

Presurgical planning 30

Control of intra-operative/primary bleeding 30

Post-operative/secondary bleeding 31

Conclusions 32

References 32

3 Inflammation and Wound Healing 39 Anna Turabelidze and Luisa Ann DiPietro

Introduction 39

The innate immune response in wounds 39

Inflammatory cell infiltration into wounds 40

Inflammatory cell function in wounds 41

Neutrophils 41

Mast cells 42

Macrophages 43

T lymphocytes 43

Gamma delta T-cells or dentritic epidermal T-cells (DETCs) 44

Cytokines and chemokines in wounds 44

Interleukin-1 (IL-1) 45

Interleukin-6 (IL-6) 45

Interleukin-8 (IL-8 or CXCL8) 45

Tumor necrosis factor (TNF alpha) 46

Macrophage chemoattractant protein (MCP-1 or CCL2) 46

Interferon inducible protein 10 (IP-10 or CXCL10) 46

Stromal cell-derived factor (SDF-1 or CXCL12) 46

Transforming growth factor-beta (TGF-b) 47

Inflammation in oral mucosal wounds 47

Inflammation in fetal wounds 48

Role of inflammation in keloids 49

Inflammation and diabetic wounds 49

Conclusions 50

References 50

4 Specialized Pro-resolving Lipid Derived Fatty Acid Mediators: Wiring the Circuitry of Effector Immune Homeostasis 57

Gabrielle Fredman and Charles N. Serhan

Inflammation: the cardinal signs 57

Complete resolution and tissue homeostasis is the ideal

outcome of acute inflammation 58

Lipoxins, resolvins, protectins and maresins: semper vigilantes

of anti-inflammation and pro-resolution 60

Lipoxins 62

Resolvins 62

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Contents vii

Protectins 65

Maresins 65

Resolution of inflammation is an actively regulated

process in vivo 66

Resolvins and protectins are protective in experimental

models of inflammatory diseases 67

Specialized pro-resolving lipid mediators in oral medicine:

restoration of tissue homeostasis in experimental periodontitis 70

Resolution and wound healing 72

Anti-inflammation vs. Pro-resolution 72

Resolution toxicity 73

Clinical implications and the development of stable analogs 74

Conclusions 74

Acknowledgments 75

References 75

5 Re-epithelialization of Wounds 81 Leeni Koivisto, Lari Häkkinen and Hannu Larjava

Introduction 81

Keratinocytes form a protective barrier between an organism

and its environment 81

Keratinocytes are activated rapidly to restore the epithelial

barrier after wounding 82

Many different factors contribute to re-epithelialization 84

Keratinocytes become exposed to novel extracellular matrix molecules in wounds 85

Integrins are signaling molecules that mediate cell adhesion to extracellular matrix and cell migration 87

Cytokines and growth factors are important mediators of wound healing 95

Serine proteases and matrix metalloproteinases modulate extracellular matrix and generate biologically active molecules 102

Levels of divalent cations in the wound fluid affect re-epithelialization 105

Wound-induced electrical field directs re-epithelialization 106

Final stages of re-epithelialization 106

Failure to re-epithelialize: chronic wounds 107

Conclusions 107

References 108

6 Granulation Tissue Formation and Remodeling 125 Lari Häkkinen, Hannu Larjava and Leeni Koivisto

Introduction 125

Overview of connective tissue response to wounding 126

Wound healing stages 129

Origin and identity of wound fibroblasts 129

Granulation tissue formation 134

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viii Contents

Activation of connective tissue cells 135

Cell proliferation 138

Cell migration 141

Matrix deposition and wound contraction 144

Transforming growth factor-b 149

Connective tissue remodeling 151

Downregulation of cell proliferation and cellularity 152

ECM degradation 152

ECM reorganization and increased stability by collagen cross-linking 154

Downregulation of ECM production 155

Re-emergence of quiescent fibroblast phenotype 156

Specific features of oral mucosal wound healing 157

Conclusions 159

Acknowledgments 159

References 159

7 Angiogenesis and Wound Healing: Basic Discoveries, Clinical Implications and Therapeutic Opportunities 175

Peter J. Polverini

Introduction 175

How blood vessels develop 175

Early mechanistic insights into the angiogenic response:

from solid tumors to chronic inflammation and wound healing 177

The role of other inflammatory cells in angiogenesis 179

Matrix molecules 180

Vascular endothelial growth factor and the modern era

of angiogenesis research 181

Signaling networks of potential importance in wound

neovascularization 182

Inhibitors of angiogenesis: important counterweights in wound

neovascularization 184

The role of aberrant wound angiogenesis in the pathogenesis

of diabetes mellitus 186

Conclusions 187

References 188

8 Wound Healing of Extraction Sockets 195 Roberto Farina and Leonardo Trombelli

Healing of extraction sockets 195

Histological aspects 195

Clinical aspects 199

Factors influencing the healing of extraction sockets 202

Smoking 202

Flapless tooth extraction 202

Location of the edentulous site 202

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Contents ix

Single versus multiple extractions 203

Chlorhexidine mouth rinse following tooth extraction 203

Healing of extraction sockets following immediate implant placement 203

Histological aspects 204

Clinical aspects 204

Healing determinants of extraction sockets after immediate implant placement 206

Does the use of reconstructive technologies alter the healing

of extraction sockets? 211

Graft materials 211

Barrier membranes 215

Bioactive agents 216

Combination of different reconstructive technologies 217

Conclusions 223

References 223

9 Flap Designs for Periodontal Healing 229 Leonardo Trombelli and Roberto Farina

Flap management, wound stability and periodontal regeneration 229

Flap designs to achieve primary closure 230

Techniques without preservation of the interdental supracrestal soft tissues and with double flap elevation 230

Techniques with preservation of the interdental supracrestal soft tissues and with double flap elevation 231

Techniques with preservation of the interdental supracrestal soft tissues and with a single flap elevation: the Single Flap Approach 233

Surgical treatment of periodontal intraosseous defects:

technical hints 237

Conclusions 240

References 241

10 Periodontal Regeneration: Experimental Observations – Clinical Consequences 243

Ulf M.E. Wikesjö, Cristiano Susin, Jaebum Lee,

Douglas P. Dickinson and Giuseppe Polimeni

Introduction 243

Wound healing 244

Periodontal wound healing 245

Periodontal regeneration – new attachment 247

Wound stability 248

Space provision 251

Wound closure for primary intention healing 256

Conclusions 256

Acknowledgment 257

References 257

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x Contents

11 Biological Agents and Cell Therapies in Periodontal Regeneration 261 Hannu Larjava, Yi Yang, Edward Putnins, Jyrki Heino

and Lari Häkkinen

Introduction 261

Adjunct growth factors in periodontal wound repair 261

PDGF and IGF-1 in periodontal regeneration 262

Platelet-rich plasma in periodontal therapy 265

FGF-2 in periodontal regeneration 265

Growth and differentiation factor-5 in periodontal regeneration 266

Other growth factors in periodontal regeneration 267

Bioactive collagen-derived peptide in periodontal

regeneration (PepGen P-15®) 267

Enamel matrix proteins in periodontal regeneration and

wound healing 269

Stem cells in periodontal wound healing 273

Conclusions 275

References 275

12 Wound Healing Around Dental Implants 287 Cristina Cunha Villar, Guy Huynh-Ba, Michael P. Mills

and David L. Cochran

Introduction 287

Historical development 287

Titanium – the metal of choice 290

Healing following implant placement 291

Peri-implant soft tissue healing 291

Implant/peri-implant mucosa interface 292

Peri-implant hard tissue healing 294

From healing to clinical application 296

Implant stability testing 297

Destructive methods 297

Non-destructive methods 298

Wound healing and loading protocols 302

Conclusions 303

References 304

13 The Pulp Healing Process: From Generation to Regeneration 313 Stéphane Simon, Anthony J. Smith, Philip J. Lumley,

Paul R. Cooper, and Ariane Berdal

From generation to regeneration 313

The dentine–pulp complex 314

The odontoblast: a key cell for regenerative endodontics 316

Pulpal responses to injury 320

At the molecular level 323

Reparative dentinogenesis and pulp capping 324

Conclusion 328

References 328

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Contents xi

14 Dermal Wound Healing and Burn Wounds 333 Anthony Papp

Introduction 333

Burn injury 333

Skin anatomy 334

Epidermis 334

Dermis 335

Skin vasculature 335

Skin appendages and subcutaneous fat 336

Burn depth 336

Epidermal burns 337

Dermal burns 337

Full thickness burns 338

Wound healing 338

Treatment 340

Conservative treatment 340

Surgical treatment 341

Special features in perioral burns 342

Conclusions 343

References 344

15 Healing of Large Dentofacial Defects 347 George K.B. Sándor, Robert P. Carmichael, Leena P. Ylikontiola,

Ahmed Jan, Marc G. DuVal and Cameron M.L. Clokie

Introduction 347

The need for bone 349

Bone healing 349

Primary bone healing 349

Secondary bone healing 349

Gap osseous healing and bone grafts 350

Growth factors 350

Blood supply and the soft tissue envelope 351

Vasculoendothelial growth factor (VEGF) effects 351

Angiogenesis 352

Surgical maneuvers to induce and promote healing of

large defects 355

Periosteal healing 355

Tent pole procedures 355

Sinus lifting/lateral ridge augmentation 359

Hyperbaric oxygen therapy (HBOT) 371

Distraction osteogenesis 372

The distracting dental implant 377

Guidance of implant placement 378

Tissue engineering with growth factors BMPs and VEGF 378

Tissue engineering with stem cells and growth factors 381

The field of tissue engineering 381

Sources of stem cells 381

Stimulating stem cells 381

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xii Contents

Manipulating the construct 382

Future directions 382

Specifically difficult wounds 383

Maxillectomy cavities 383

Wound infections necrotizing fasciitis 387

Conclusions 391

References 392

Index 397

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Page 11: Oral Wound Healing (Larjava/Oral Wound Healing) || Front Matter

Editor

Hannu Larjava, DDS, PhD, Dip Perio

Professor and Chair, Division

of Periodontics

Faculty of Dentistry

University of British Columbia

Vancouver, BC, Canada

Contributors

Ariane Berdal, DDS, MPhil, DSc

Centre de Recherche des Cordeliers

Physiologie Orale Moléculaire

Paris, France

Robert P. Carmichael, DMD, MSc,

FRCDC

Chief of Dentistry, Bloorview Kids Rehab

Director, Ontario Cleft Lip and Palate

Program

Co-ordinator of Prosthodontics, Hospital

for Sick Children

Assistant Professor, University of Toronto

Toronto, Ontario, Canada

Cameron M.L. Clokie, DDS, PhD,

FRCDC

Professor and Director of Graduate

Program in Oral and Maxillofacial

Surgery and Anaesthesia

University of Toronto

Toronto, Ontario, Canada

David L. Cochran, DDS, MS, PhD, MMSci

Chair and Professor

Department of Periodontics

University of Texas Health Science

Center at San Antonio

San Antonio, TX, USA

Paul R. Cooper, BSc, PhD

Senior Lecturer in Molecular Biology

Oral Biology

School of Dentistry

University of Birmingham

St Chad’s Queensway

Birmingham, UK

Douglas P. Dickinson, PhD

Associate Professor

Department of Oral Biology

Georgia Health Sciences University

College of Dental Medicine

Augusta, Georgia, USA

Luisa Ann DiPietro, DDS, PhD

Professor and Director

Center for Wound Healing

and Tissue Regeneration

College of Dentistry

University of Illinois at Chicago

Chicago, IL, USA

Marc G. DuVal, DDS

Chief Resident, Graduate Program

in Oral and Maxillofacial Surgery

and Anaesthesia

University of Toronto

Toronto, Ontario, Canada

Roberto Farina, DDS, PhD, MSc

Research Assistant

Research Centre for the Study

of Periodontal and Peri-implant Diseases

University of Ferrara

Ferrara, Italy

Contributors

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xiv Contributors

Gabrielle Fredman, PhD

Post Doctoral Fellow

Center for Experimental Therapeutics

and Reperfusion Injury

Department of Anesthesiology,

Perioperative, and Pain Medicine

Brigham and Women’s Hospital/Harvard

Medical School

Boston, Massachusetts, USA

Lari Häkkinen, DDS, PhD

Associate Professor

Laboratory of Periodontal Biology

Department of Oral Biological

and Medical Sciences

Faculty of Dentistry

University of British Columbia

Vancouver, BC, Canada

Jyrki Heino, MD, PhD

Professor

Department of Biochemistry

and Food Chemistry

University of Turku

Turku, Finland

Guy Huynh-Ba, DDS, Dr Med Dent, MS

Assistant Professor

Department of Periodontics

University of Texas Health Science

Center at San Antonio

San Antonio, TX, USA

Ahmed Jan, DDS

Chief Resident in Oral and Maxillofacial

Surgery and Anesthesia

University of Toronto

Toronto, Canada

Leeni Koivisto, PhD

Research Associate

Laboratory of Periodontal Biology

Department of Oral Biological

and Medical Sciences

Faculty of Dentistry

University of British Columbia

Vancouver, BC, Canada

Jaebum Lee, DDS, MSD, PhD

Chief Clinical Scientist

Laboratory for Applied Periodontal

and Craniofacial Regeneration

Departments of Periodontics

and Oral Biology

Georgia Health Sciences University

College of Dental Medicine

Augusta, Georgia, USA

Philip J. Lumley, DDS, PhD

Director and Head

The School of Dentistry

University of Birmingham

Birmingham, UK

Michael P. Mills, DMD, MS

Clinical Associate Professor

Department of Periodontics

University of Texas Health Science

Center at San Antonio

San Antonio, TX, USA

Carol Oakley, DDS, MSc, PhD

Clinical Associate Professor

Department of Oral Biological

and Medical Sciences

Faculty of Dentistry

University of British Columbia

Vancouver, BC, Canada

Anthony Papp, MD, PhD, FRCSC

Medical Director BC Professional

Firefi ghters’ Burn,

Plastic and Trauma Unit

Vancouver General Hospital

Vancouver, BC,

Canada

Giuseppe Polimeni, DDS, MS

Clinical Associate Professor, Senior

Clinical Scientist

Laboratory for Applied Periodontal

and Craniofacial Regeneration

Departments of Periodontics

and Oral Biology

Medical College of Georgia School

of Dentistry

Augusta, Georgia, USA

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Contributors xv

Peter J. Polverini, DDS, DMSc

Professor and Dean

University of Michigan

School of Dentistry

Ann Arbor, Michigan, USA

Edward Putnins, PhD, DMD, Dip Perio,

MSC, MRCD(C)

Associate Dean Research, Graduate

and Post Graduate Studies

University of British Columbia

Faculty of Dentistry

Department of Oral Biological

and Medical Sciences

Vancouver, BC, Canada

George K.B. Sándor, MD, DDS, PhD,

Dr Habil, FRCDC, FRCSC, FACS

Professor of Tissue Engineering

Regea Institute for Regenerative

Medicine

University of Tampere

Tampere, Finland

Professor of Oral and Maxillofacial

Surgery

University of Oulu

Oulu, Finland

Charles N. Serhan, PhD

The Simon Gelman Professor

of Anaesthesia (Biochemistry

and Molecular Pharmacology) Harvard

Medical School

Director, Center for Experimental

Therapeutics and Reperfusion

Injury

Department of Anesthesiology,

Perioperative, and Pain Medicine

Brigham and Women’s Hospital

Professor, Harvard School of Dental

Medicine, Oral Medicine, Infection

and Immunity

Boston, Massachusetts, USA

Stéphane Simon, DDS, PhD

Maitre de Conférence Hospitalo-

Universitaire

Department of Oral Biology

University of Paris Diderot

Paris, France

Groupe Hospitalier Pitié

Salpétrière

Paris, France

Associate Researcher

University of Birmingham

Birmingham, UK

Anthony J. Smith, PhD

Professor in Oral Biology

School of Dentistry

University of Birmingham

Birmingham, UK

Cristiano Susin, DDS, MSD, PhD

Associate Professor of Periodontics,

Oral Biology and Graduate Studies

Associate Director, Laboratory

for Applied Periodontal and

Craniofacial Regeneration

Director, Clinical Research

Georgia Health Sciences University

College of Dental Medicine

Augusta, Georgia, USA

Leonardo Trombelli, DDS, PhD,

Professor and Director, Research

Centre for the Study of Periodontal

and Peri-implant Diseases

Director, Dental Clinic,

University Hospital

University of Ferrara

Ferrara, Italy

Anna Turabelidze, BS

Center for Wound Healing and Tissue

Regeneration

College of Dentistry

University of Illinois at Chicago

Chicago, IL, USA

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xvi Contributors

Cristina Cunha Villar, DDS, MS, PhD

Assistant Professor

Department of Periodontics

University of Texas Health Science

Center at San Antonio

San Antonio, TX, USA

Ulf M.E. Wikesjö, DDS, DMD, PhD,

Diplomate ABP

Professor, Director

Laboratory for Applied Periodontal and

Craniofacial Regeneration

Departments of Periodontics and Oral

Biology

Georgia Health Sciences University

College of Dental Medicine

Medical College of Georgia School of

Dentistry

Augusta, Georgia, USA

Yi Yang, DDS, MSD, MSC, PhD

University of British Columbia

Vancouver, BC, Canada

Leena P. Ylikontiola, MD, DDS, PhD

Assistant Professor, Institute of Dentistry

University of Oulu

Co-ordinator of Cleft Lip and Palate

Surgery

Oulu University Hospital

Oulu, Finland

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Page 15: Oral Wound Healing (Larjava/Oral Wound Healing) || Front Matter

Our understanding about wound healing has vastly increased over the last decade. Currently,

the PubMed search with the words ‘wound healing’ results in almost a hundred thousand

citations. These publications range from basic science to clinical studies and cover multiple

disciplines in biology and medicine. Explosion of new knowledge makes it difficult to pro-

cess the information and condense it into meaningful concepts. The goal of this book was to

filtrate the massive information to summaries of wound healing topics that were written by

experts in the field. These experts covered not only their own endeavors but also the science

at large in their topic area.

At the time of planning this book, there was no comprehensive book covering recent

advancements in the field of oral wound care. Wound healing books covering healing of skin

and other organs existed and had been extremely successful for dermatologists, wound heal-

ing researchers and other health professionals. Wounds are common in oral cavity, ranging

from wounds on pulp tissue after tooth preparation to those caused by surgical procedures

on soft tissue and bone. Oral wound care has several special features and covers unique

processes such as soft tissue healing, healing of bone and extraction socket, regeneration of

periodontal structures and healing around dental implants. Although many of these pro-

cesses have been described in review articles over the years, there was no reference material

(book) that covered the entire topic of oral wound healing. This book is the first one that

focuses on wound healing in the oral cavity.

This book is intended for a diverse audience, from clinicians to wound healing students.

The topics of the book can be useful especially for residents and graduate students who are

in training programs aimed at surgical management of oral tissues (such as oral surgery,

periodontics, endodontics and oral medicine) and for oral biology or other researchers who

are investigating wound healing. In addition, undergraduate students and general practition-

ers who are advancing their training in surgical sciences would also benefit from the infor-

mation presented in this book.

Oral Wound Healing is divided into 15 chapters. The first seven chapters cover the fun-

damentals of wound healing and they are organized to reflect the sequence of wound healing

events, starting from blood clotting and ending with angiogenesis. The last eight chapters

cover more clinical aspects of wound healing, ranging from healing of extraction sockets to

large craniofacial defects.

I would like to express my deep gratitude to the contributors, without whom this book

would have never seen completion. I would also like to thank Ms Melissa Wahl for patiently

waiting for the final work and for John Wiley & Sons, Inc. for publishing the book.

Preface

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