AN INTRODUCTION TO

BIOCERAMICS
Second Edition

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AN INTRODUCTION TO

BIOCERAMICS
Second Edition

Editor

Larry L. Hench
University of Florida, USA

ICP

P884_9781908977151_tp.indd 2

Imperial College Press
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Published by
Imperial College Press
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Covent Garden
London WC2H 9HE
Distributed by
World Scientific Publishing Co. Pte. Ltd.
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British Library Cataloguing-in-Publication Data
A catalogue record for this book is available from the British Library.

AN INTRODUCTION TO BIOCERAMICS
Second Edition
Copyright © 2013 by Imperial College Press

All rights reserved. This book, or parts thereof, may not be reproduced in any form or by any means,
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b1486 An Introduction to Bioceramics 2nd Edition

DEDICATIONS

Dedicated to Gerry Merwin (1947–1992) and Bill Hall (1922–1992), clinicians
and scientists who pioneered use of new biomaterials.

A special dedication of this second edition is to Dr. June Wilson Hench, co-editor
of the first edition, who made so many important discoveries in the field of bioactive glasses and pioneered the technological transformation from the laboratory
to FDA-approved clinical products. Her lifetime of contributions to the field of
Bioceramics, her mentorship of many students and her creativity is a legacy that
will be never forgotten. June is greatly missed!
This volume is also dedicated to the memory and pioneering contributions of
Professor Raquel LeGeros, co-author of Chapter 17, who passed away during the
final stages of publication of the book. She will be remembered always for her
warm and gentle leadership in the field of calcium phosphate bioceramics.

Cover Ackowledgement
Colour enhanced scanning electron micrograph (SEM) of bone regeneration
(green and yellow areas) around S53P4 bioactive glass particle (grey areas).
Photo courtesy of Dr. Heimo Ylanen, Abo Akademi University, Turku, Finland.

v

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b1486 An Introduction to Bioceramics 2nd Edition

PREFACE

Since the 1970s, when it was first realized that the special properties of ceramic
materials could be exploited to provide better materials for certain implant applications, the field has expanded enormously. Initial applications depended on the
fact that smooth ceramic surfaces elicited very little tissue reaction and provided
wear characteristics suitable for bearing surfaces. Resultant orthopedic use has
enjoyed forty years’ clinical success, notably in Europe.
Today, as well as the so-called inert “bioceramics”, materials have been
developed that have properties which allow their use where bonding to soft or
hard tissues is needed, where controlled degradation is required, where loads are
to be borne, where tissue is to be augmented, or where the special properties of
ceramics can be allied with those of polymers or metals to provide implant materials with advantages over each.
In all of these applications, and many others described in this text, the tissue reactions to, and properties of, these bioceramics have been increasingly
carefully studied so that they can be controlled and, more importantly, predicted.
This is the information which must be understood before they are applied
clinically.
Assessment of the growth of the field of bioactive ceramics in the first
edition in 1993 showed that the number of presentations on that subject at the first
World Biomaterials Congress in 1980 formed 6% of the program. By the time of
the fourth such congress in 1992, that figure was 23% of the whole. In 1980
presentations came from 12 centers in 5 countries, in 1992 from 88 centers in 21
countries. Research is international and continues to expand worldwide, as indicated by the breadth of contribution in this second edition.
The breadth of bioceramics also continues to expand, as illustrated by the

addition of 21 additional chapters in this second edition. Much of the expanded
growth of subject matter is in the field of bioactive materials. Bioactive materials
can be divided into two major areas: one contains bioactive glasses and glassceramics, which develop biological hydroxyapatite at their surfaces after implantation; and the other, contains calcium phosphate-based ceramics, which are
usually developed from chemical precursors.

vii

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An Introduction to Bioceramics 2nd Edition

Materials from both groups have been used as powders and sometimes as
solids in applications where mechanical requirements are low, and as composites
and coatings where mechanical requirements are high. Some have been designed
specifically for high strength applications. As the behavior of bioceramics in both
short- and long-term applications has become increasingly predictable and reliable, their clinical application has increased, as indicted by the large number of
clinical applications chapters presented in the second edition.
The growth of bioceramics as a field and as a vital component of the
healthcare industry parallels the increasing need for affordable and improved
healthcare for an increasingly large and aging population. The chapters presented
in the second edition provide the latest understanding of this important field and

provide the basis for creating the next generation of biomaterials.
Please note the following regarding the contents of this second edition.
Several chapters of the first edition have been included without alteration. This is
based upon my judgment as Editor that these are “classic” reviews of the field and
merit inclusion “as is”. Some other chapters, of equal importance, however, have
been up-dated to include clinical results during the last twenty years in order to
represent the growing clinical significance of the field of bioceramics. A few
chapters have been greatly reduced in size because the content has not become
clinically important. Because of their historical significance a short, edited version of the chapters has been included with key references. This decision has
made it possible to keep within reasonable page limits for the second edition and
still include a comprehensive up-dating of the field. I greatly appreciate these
important new contributions from leaders of the field. I also hope that the authors
of the chapters reduced in size will understand the rationale of my decision.
Bioceramics has become one of the most important fields of the healthcare
industry and I am pleased that this second edition represents this growing
importance.
Larry L. Hench
Ft. Myers, FL
October 11, 2012

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b1486 An Introduction to Bioceramics 2nd Edition

CONTENTS


Preface

vii

Author Index

xiii

Chapter 1

Introduction
Larry L. Hench and June Wilson

Chapter 2

The use of Alumina and Zirconia
in Surgical Implants
Samuel F. Hulbert

1

27

Chapter 3

Bioactive Glasses
Larry L. Hench and Orjan Andersson

49


Chapter 4

Bioactive Glasses: Gene Activation
Larry L. Hench

71

Chapter 5

Angiogenic Potential of Bioactive Glasses
Alejandro A. Gorustovich, Luis A. Haro Durand,
Judith A. Roether and Aldo R. Boccaccini

87

Chapter 6

Bioactive Glasses: Clinical Applications — Historical
June Wilson, Antti Yli-Urpo and Risto-Pekka Happonen

95

Chapter 7

Clinical Applications of Bioactive Glasses: ENT
Larry L. Hench

Chapter 8


Clinical Applications of Bioactive Glasses:
Endosseous Ridge Maintenance
Larry L. Hench

115

Clinical Applications of Bioactive Glasses:
Periodontal Repair
Paul Robinson II

125

Clinical Applications of Bioactive Glasses:
Maxillofacial Repair
Ian Thompson

137

Chapter 9

Chapter 10

109

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Chapter 11

An Introduction to Bioceramics 2nd Edition

Clinical Applications of Bioactive Glass:
Orthopaedics
David M. Gaisser and Larry L. Hench

151

Chapter 12

Bioactive Glass in Spinal Repair
Janek Frantzén

159

Chapter 13

A/W Glass-Ceramic: Processing and Properties
Tadashi Kokubo

171


Chapter 14

A/W Glass-Ceramic: Clinical Applications
Takao Yamamuro

189

Chapter 15

Ceravital® Bioactive Glass-Ceramics
Ulrich M. Gross, Christian Müller-Mai and Christian Voigt

209

Chapter 16

Machinable and Phosphate Glass-Ceramics
Wolfram Höland and Werner Vogel

215

Chapter 17

Hydroxyapatites
Racquel Z. LeGeros and John P. LeGeros

229

Chapter 18


Silicon Substituted Hydroxyapatite
Robert J. Friederichs, William Bonfield and
Serena M. Best

279

Chapter 19

Porous Hydroxyapatite
Edwin C. Shors and Ralph E. Holmes

287

Chapter 20

Stability of Calcium Phosphate Ceramics
and Plasma Sprayed Coatings
C.P.A.T. Klein, J.G.C. Wolke and K. de Groot

305

Chapter 21

Hydroxyapatite Coatings
William R. Lacefield

331

Chapter 22


Bioactive Glass Coatings
Larry L. Hench and Orjan Andersson

349

Chapter 23

Bioactive HA Coatings by Ti Surface Activation
Tadashi Kokubo and Seiji Yamaguchi

355

Chapter 24

Pyrolytic Carbon Coatings
Reinhold H. Dauskardt and Robert O. Ritchie

367

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Introduction


xi

Chapter 25

Pyrolytic Carbon Prostheses: Clinical Results
Jonathan Shute

389

Chapter 26

Bioceramic Composites
Paul Ducheyne, Michele Marcolongo and Evert Schepers

397

Chapter 27

Design of Bioactive Ceramic-Polymer Composites
William Bonfield

403

Chapter 28

Calcium Phosphate Cements
Sanjukta Deb

409


Chapter 29

Radiotherapy Glasses
Delbert E. Day and Thomas E. Day

431

Chapter 30

Dental Glass-Ceramics and ZrO2-Ceramics
Wolfram Höland, Marcel Schweiger
and Volker M. Rheinberger

447

Chapter 31

Bioactive Glass for Tooth Remineralization
and Pain Desentization
David C. Greenspan and Larry L. Hench

455

Porous Bioactive Ceramic and Glass Scaffolds
for Bone Regeneration
Julian R. Jones

463


Treatment of Chronic Wounds with Bioactive
Borate Glass Fibers
Steven Jung

487

Chapter 32

Chapter 33

Chapter 34

Bioactive Glass-Ceramics for Load-Bearing
Applications
Oscar Peitl, Edgar D. Zanotto, Francisco C.
Serbena and Larry L. Hench

Chapter 35

Porous Wall, Hollow Glass Microspheres
George G. Wicks, Steven Serkiz, Shuyi Li
and William Dynan

Chapter 36

Molecular Modeling of Bioactive Glasses
and Reactions
Paul Robinson II and Larry L. Hench

495


505

511

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An Introduction to Bioceramics 2nd Edition

Chapter 37

Characterization of Bioceramics
Larry L. Hench

521

Chapter 38

Regulation of Medical Devices: Historical
Emanuel Horowitz and Edward Mueller


541

Chapter 39

Regulation of Medical Devices: Current Status
David C. Greenspan

549

Chapter 40

Technology Transfer of Bioceramics:
From Concept to Commerce
Larry L. Hench and Giuseppe Cama

561

Chapter 41

Ethical Issues
Larry L. Hench

573

Chapter 42

Summary and Future Directions
Larry L. Hench

583


Index

593

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b1486 An Introduction to Bioceramics 2nd Edition

AUTHOR INDEX

* Denotes affiliation from the first edition.
** Denotes current affiliation/affiliation of new authors to the second edition.

Editors
Hench, Larry L.
Chapters 1, 3, 4, 7, 8, 11, 22, 31, 34, 36, 37, 40, 41, 42
Advanced Materials Research Center, University of Florida, Gainesville, Florida,
USA*
University of Florida, Gainesville, Florida and University of Central Florida,
Florida, USA**
Wilson, June
Chapters 1, 6
Bioglass® Research Center, Advanced Materials Research Center, University of
Florida, Gainesville, Florida, USA*


Authors
Andersson, Orjan
Chapters 3, 22
Abo Akademi, Turku, Finland*
Best, Serena M.
Chapter 18
University of Cambridge, Cambridge, UK**
Boccaccini, Aldo R.
Chapter 5
University of Erlangen, Germany**

xiii

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An Introduction to Bioceramics 2nd Edition

Bonfield, William
Chapters 18, 27
IRC in Biomedical Materials Queen Mary and Westfield College London,

London, UK*
University of Cambridge, Cambridge, UK**
Cama, Giuseppe
Chapter 40
King’s College/Guy’s Hospital, London, UK**
Dauskardt, Reinhold H.
Chapter 24
University of California, Berkeley, California, USA*
Day, Delbert E.
Chapter 29
University of Missouri, Missouri, USA*
University of Missouri Science and Technology, Rolla, Missouri, USA**
Day, Thomas E.
Chapter 29
University of Missouri, Missouri, USA.*
MoSci Corp., Rolla, Missouri, USA**
Deb, Sanjukta
Chapter 28
King’s College/Guy’s Hospital, London, UK**
de Groot, Klaas
Chapter 20
University of Leiden, the Netherlands*
Ducheyne, Paul
Chapter 26
University of Pennsylvania, Philadelphia, USA*
Dynan, William
Chapter 35
Medical College of Georgia, Augusta, Georgia, USA**

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b1486 An Introduction to Bioceramics 2nd Edition

Author Index

xv

Frantzén, Janek
Chapter 12
Turku University, Turku, Finland*
Friederichs, Robert J.
Chapter 18
University of Cambridge, Cambridge, UK**
Gaisser, David M.
Chapter 11
NovaBone Products, Alachua, Florida, USA**
Gorustovich, Alejandro A.
Chapter 5
National Atomic Energy Commission CNEA Regional Noroeste, Argentina**
Greenspan, David C.
Chapters 31, 39
DSpinode Consulting, Gainesville, Florida, USA**
Gross, Ulrich M.
Chapter 15
University Hospital Steglitz, Free University of Berlin, Germany*

Happonen, Risto-Pekka
Chapter 6
Institute of Dentistry, University of Turku, Finland*
Haro Durand, Luis A.
Chapter 5
National Atomic Energy Commission CNEA Regional Noroeste, Argentina
National Research Council CONICET, A4408FTV, Argentina**
Höland, Wolfram
Chapters 16, 30
Otto-Schott-Institute for glass chemistry, Friedrich-Schiller-University Jena,
Germany*
Ivoclar Vivadent AG, Principality of Liechtenstein**

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An Introduction to Bioceramics 2nd Edition

Holmes, Ralph E.
Chapter 19
University of California at San Diego, USA*
Horowitz, Emanuel

Chapter 38
Johns Hopkins University, Baltimore, Maryland, USA*
Hulbert, Samuel F.
Chapter 2
Rose-Hulman Institute of Technology, Terre Haute, Indiana, USA*
Jones, Julian R.
Chapter 32
Imperial College London, London, UK**
Jung, Steven
Chapter 33
MoSci Corp., Rolla, Missouri, USA**
Klein, C.P.A.T.
Chapter 20
University of Leiden, the Netherlands*
Kokubo, Tadashi
Chapter 13, 23
Kyoto University, Japan*
Chubu University, Kasugai, Japan**
Lacefield, William R.
Chapter 21
University of Alabama at Birmingham School of Dentistry,
Alabama, USA*

Birmingham,

Li, Shuyi
Chapter 35
Medical College of Georgia, Augusta, Georgia, USA**

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b1486 An Introduction to Bioceramics 2nd Edition

Author Index

xvii

LeGeros, John P.
Chapter 17
New York University College of Dentistry, New York, USA.*
LeGeros, Raquel Z.
Chapter 17
New York University College of Dentistry, New York, USA*
Marcolongo, Michele
Chapter 26
University of Pennsylvania, Philadelphia, USA*
Mueller, Edward
Chapter 38
Food and Drug Administration Center for Devices and Radiological Health
Rockville, USA*
Müller-Mai, Christian
Chapter 15
University Hospital Steglitz, Free University of Berlin, Germany*
Peitl, Oscar
Chapter 34

Universidade Federal de São Carlos, Brazil**
Rheinberger, Volker M.
Chapter 30
Ivoclar Vivadent AG, Principality of Liechtenstein**
Ritchie, Robert O.
Chapter 24
University of California, Berkeley, California, USA*
Robinson II, Paul
Chapters 9, 36
University of Florida, Gainesville, Florida, USA**

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An Introduction to Bioceramics 2nd Edition

Roether, Judith A.
Chapter 5
University of Erlangen, Germany**
Schepers, Evert
Chapter 26
University of Leuven, Leuven, Belgium*

Schweiger, Marcel
Chapter 30
Ivoclar Vivadent AG, Principality of Liechtenstein**
Serbena, Francisco C.
Chapter 34
Federal University of San Carlos, San Carlos, Brazil**
Serkiz, Steven
Chapter 35
Medical College of Georgia, Augusta, Georgia, USA**
Shors, Edwin C.
Chapter 19
University of California at San Diego, USA*
Shute, Jonathan
Chapter 25
University of Florida, Gainesville, Florida, USA**
Thompson, Ian
Chapter 10
King’s College/Guy’s Hospital, London, UK**
Voigt, Christian
Chapter 15
University Hospital Steglitz, Free University of Berlin, Germany*

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b1486 An Introduction to Bioceramics 2nd Edition


Author Index

xix

Vogel, Werner
Chapter 16
Otto-Schott-Institute for glass chemistry, Friedrich-Schiller-University Jena,
Germany*
Wicks, George G.
Chapter 35
Savannah River National Laboratory, Aiken, South Carolina, USA**
Wolke, Joop G.C.
Chapter 20
University of Leiden, the Netherlands*
Yamaguchi, Seiji
Chapter 23
Chubu University, Kasugai, Japan**
Yamamuro, Takao
Chapter 14
Kyoto University, Japan*
Yli-Urpo, Antti
Chapter 6
Institute of Dentistry, University of Turku, Finland*
Zanotto, Edgar D.
Chapter 34
Federal University of San Carlos, San Carlos, Brazil**

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b1486 An Introduction to Bioceramics 2nd Edition

Chapter 1

INTRODUCTION
Larry L. Hench and June Wilson
1.1. OVERVIEW
Thousands of years ago humans discovered that clay could be irreversibly
transformed by fire into ceramic pottery. Ceramic pots stored grains for long
periods of time with minimal deterioration. Impervious ceramic vessels held
water and were resistant to fire, which allowed new forms of cooking. This discovery was a large factor in the transformation of human culture from nomadic
hunters to agrarian settlers. This cultural revolution led to a great improvement in
the quality and length of life.
During the last fifty years another revolution has occurred in the use of
ceramics to improve the quality of life of humans. This revolution is the development of specially designed and fabricated ceramics for the repair and reconstruction of diseased, damaged or “worn out” parts of the body. Ceramics used for this
purpose are called bioceramics. This book describes the principles involved in the
use of ceramics in the body. Most clinical applications of bioceramics relate to
the repair of the skeletal system, composed of bones, joints and teeth, and to augment both hard and soft tissues. Ceramics are also used to replace parts of the
cardiovascular system, especially heart valves. Special formulations of glasses
are also used therapeutically for the treatment of tumors.
Bioceramics are produced in a variety of forms and phases and serve many
different functions in the repair of the body, which are summarized in Fig. 1.1 and
Table 1.1. In many applications ceramics are used in the form of bulk materials
of a specific shape, called implants, prostheses, or prosthetic devices. Bioceramics
are also used to fill space while the natural repair processes restore function. In

other situations the ceramic is used as a coating on a substrate, or as a second
phase in a composite, combining the characteristics of both into a new material
with enhanced mechanical and biochemical properties.
Bioceramics are made in many different phases. They can be single crystals
(sapphire), polycrystalline (alumina or hydroxyapatite), glass (Bioglass®), glassceramics (A/W glass-ceramic) or composites (polyethylene-hydroxyapatite). The
phase or phases used depend on the properties and function required. For example, single crystal sapphire is used as a dental implant because of its high strength.
A/W glass-ceramic is used to replace vertebrae because it has high strength and
1

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b1486 An Introduction to Bioceramics 2nd Edition

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An Introduction to Bioceramics 2nd Edition

Fig. 1.1.

Clinical uses of bioceramics.

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b1486 An Introduction to Bioceramics 2nd Edition

Introduction

3

Table 1.1. Form, Phase and Function of Bioceramics.
Form

Phase

Function

Powder

Polycrystalline, Glass

Space-filling, therapeutic treatment,
regeneration of tissues

Coating

Polycrystalline, Glass
Glass-Ceramic

Tissue bonding, thromboresistance, corrosion
protection


Bulk

Replacement and augmentation of tissue,
Single Crystal
replace functioning parts
Polycrystalline, Glass
Glass-Ceramic
Composite
(Multi-Phase)

bonds to bone. Bioactive glasses have low strength but bond rapidly to bone, so
are used to augment the repair of boney defects.
Ceramics and glasses have been used for a long time outside the body for
a variety of applications in the health care industry. Eye glasses, diagnostic instruments, chemical ware, thermometers, tissue culture flasks, chromatography columns, lasers, and fiber optics for endoscopy are commonplace products in the
multi-billion dollar industry. Ceramics are widely used in dentistry as restorative
materials: gold porcelain crowns, glass-filled ionomer cements, endodontic treatments, dentures etc. Such materials, called dental ceramics, are reviewed by
Preston.1 However, use of ceramics inside the body as implants is relatively new:
alumina hip implants have been used for just over 40 years. (See Hulbert et al.,
1987, for a review of the history of bioceramics.2)
This book is devoted to the use of ceramics as implants. Many compositions of ceramics have been tested for potential use in the body but few have
reached human clinical application. Clinical success requires the simultaneous
achievement of a stable interface with connective tissue and an appropriate, functional match of the mechanical behavior of the implant with the tissue to be
replaced. Few materials satisfy this severe dual requirement for clinical use.

1.2. TYPES OF BIOCERAMICS–TISSUE INTERFACES
No material implanted in living tissues is inert; all materials elicit a
response from the host tissue. The response occurs at the tissue–implant interface
and depends upon many factors, listed in Table 1.2.
There are four general types of implant–tissue response, as summarized in

Table 1.3. It is critical that any implant material avoids a toxic response that kills

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b1486 An Introduction to Bioceramics 2nd Edition

4

An Introduction to Bioceramics 2nd Edition
Table 1.2. Factors affecting interfacial response.
Tissue Side

Implant Side

— Type of Tissue
— Health of Tissue
— Age of Tissue
— Blood Circulation in Tissue
— Blood Circulation at Interface
— Motion at Interface
— Closeness of Fit
— Mechanical Load
Table 1.3.
Implant–Tissue Reaction


— Composition of Implant
— Phases in Implant
— Phase Boundaries
— Surface Morphology
— Surface Porosity
— Chemical Reactions
— Closeness of Fit
— Mechanical Load

Implant–Tissue Interactions: Consequences.
Consequence

Toxic
Biologically nearly inert

Tissue dies
Tissue forms a non-adherent fibrous capsule around
the implant

Bioactive

Tissue forms an interfacial bond with the implant or
regenerates natural tissues

Dissolution of implant

Tissue replaces implant

cells in the surrounding tissues or releases chemicals that can migrate within tissue fluids and cause systemic damage to the patient.3 One of the main reasons for
the interest in ceramic implants is their lack of toxicity.

The most common response of tissues to an implant is formation of a nonadherent fibrous capsule. The fibrous tissue is formed in order to “wall off” or
isolate the implant from the host. It is a protective mechanism and with time can
lead to complete encapsulation of an implant within the fibrous layer. Metals and
most polymers produce this type of interfacial response; the cellular mechanisms
which influence this response are described in a later section.
Biologically inactive, nearly inert ceramics, such as alumina or zirconia,
also develop fibrous capsules at their interface. The thickness of the fibrous layer
depends on the factors listed in Table 1.2. The chemical inertness of alumina and
zirconia results in a very thin fibrous layer under optimal conditions (Fig. 1.2).
More chemically reactive metallic implants elicit thicker interfacial layers.
However, it is important to remember that the thickness of an interfacial fibrous
layer also depends upon motion and fit at the interface, as well as the other factors
indicated in Table 1.2.

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Introduction

5

Figure 1.2. Comparison of interfacial thickness of reaction layer of bioactive implants
or fibrous tissue of inactive bioceramics in bone. (Reprinted from L.L. Hench, 1991,
Bioceramics: From Concept to Clinic, J. Amer. Ceram. Soc., 74, 1487–570, with

permission.)

The third type of interfacial response, indicated in Table 1.3, is when a
bond forms across the interface between implant and the tissue. This is termed a
“bioactive” interface. The interfacial bond prevents motion between the two
materials and mimics the type of interface that is formed when natural tissues
repair themselves. This type of interface requires the material to have a controlled
rate of chemical reactivity, as discussed in Chapters 3–6. An important characteristic of a bioactive interface is that it changes with time, as do natural tissues,
which are in a state of dynamic equilibrium.
When the rate of change of a bioactive interface is sufficiently rapid the
material “dissolves” or “resorbs” and is replaced by the surrounding tissues.
Thus, a resorbable biomaterial must be of a composition that can be degraded
chemically by body fluids or digested easily by macrophages (see below). The
degradation products must be chemical compounds that are not toxic and can be
easily disposed of without damage to cells.

1.3. TYPES OF BIOCERAMIC–TISSUE ATTACHMENTS
The mechanism of attachment of tissue to an implant is directly related to
the tissue response at the implant interface. There are four types of bioceramics,

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