Periodontology 2000, vol.
17, 1998, 22-35
Printed in Denmark • All rights reserved
Osseointegration: a reality
ROBERT K. SCHENK & DANIEL
BUSER
Bone healing is certainly a fascinating biological
accomplishment of the skeletal tissues and one of
the rare examples in which regenerative processes
fully restore the original structure and function. This
is achieved by a sequence of cellular activities that
closely resemble the development and growth of
bone during embryonic and postnatal life. In
intramembranous (or direct) ossification, bone is
formed directly in the mesenchyme. The majority of
bones in the trunk and the extremities, however, are
preformed as cartilaginous models and substituted
later on by bone in the process of endochondral (or
indirect) ossification. Bone regeneration follows
similar pathways: in direct (or primary) healing, a
scaffold of woven bone, closely associated with an
expanding vascular net, invades the granulation
tissue that organizes the initially formed blood clot.
In indirect (or secondary) healing, connective tissue
and/ or fibrocartilage differentiates within the
fracture gaps and is replaced by bone as in
endochondral ossification.
Osseointegration clearly belongs to the category of
direct or primary healing. Originally, it was defined
as direct bone deposition on the implant surfaces (9),
a fact also called "functional ankylosis" (48). In a
more comprehensive way, osseointegration is
characterized as "a direct structural and functional
connection between ordered, living bone and the
surface of a load-bearing implant" (39).
Osseointegration can be compared with direct
fracture healing, in which the fragment ends become
united by bone, without intermediate fibrous tissue or
fibrocartilage formation. A fundamental difference,
however, exists: osseointegration unites bone not to
bone, but to an implant surface: a foreign material.
Thus the material plays a decisive role for the
achievement of union.
Prerequisites for osseointegration
Material and surface properties
Osseointegration shares many prerequisites with
primary fracture healing, such as precise fitting (ana-
tomical reduction), primary stability (stable fixation)
and adequate loading during the healing period. In
addition, osseointegration requires a bioinert or
bioactive material and surface configurations that are
attractive for bone deposition (osteophilic).
Bioinert materials do not release any harmful
substances and therefore do not elicit adverse tissue
reactions. Titanium, either commercially pure or in
certain alloys, is generally recognized as being
bioinert and used extensively in both dental and
orthopedic surgery. A bioactive material is thought to
cause a favorable tissue reaction, either by
establishing chemical bonds with tissue components
(hydroxyapatite) or by promoting cellular activities
involved in bone matrix formation. Bioactivity is
currently restricted to compounds of poor mechanical
quality and can only be applied as a coating
(hydroxyapatite, carriers for inductors and growth
factors).
The notion that surface properties of implants
might influence the elaboration of a bone-implant
contact is relatively new. It could be anticipated that
rough surfaces will improve adhesive strength
compared with smooth ones. This assumption is now
confirmed by numerous animal experiments that
measured the push- and pull-out strength or removal
torque values (17—19, 34, 51, 57). The observation
that a rough surface favors bone deposition and thus
gradually increases the extent of the boneimplant
interface was somewhat surprising (12). It is now
supported by numerous experimental studies (29, 30,
54-56). Roughness can be further characterized by
the shape and dimension of the surface irregularities.
The degree of mechanical interlock increases with the
roughness of the substrate. At the same time, the
structure and function of the boneimplant contact
changes. A smooth surface only transmits
compressive forces, with little resistance against
shear, and apparently none against traction. A mild
roughness (<10 pm) augments the resistance against
shear. Adhesion, however, requires either a chemical
bond or a microporosity (microprotrusions and
microundercuts of 20—50 um) that leads to a
microindentation between bone and metal.
Macroporosity (pore size 100-500 um) favors bony
ingrowth and is widely used as porous coatings
(beads, sintered wire mesh, multilayered lattices) in
orthopedic implants (4, 7, 15, 16, 46). Finally, the
macro-design or shape of an implant has an important
bearing on the bone response: ongrowing bone
concentrates preferentially on protruding elements of
the implant surface, such as ridges, crests, teeth, ribs
or the edge of threads, that apparently act as stress
risers when load is transferred (42).
Primary stability and adequate load
The tissue response to a freshly installed implant
greatly depends on the mechanical situation. As in
direct fracture healing, it requires perfect stability if
bone is expected to be formed. In a fracture, a stable
fixation is obtained by exact adaptation and
compression of the fragments. The primary stability
of implants depends on their appropriate design and
precise press fitting at surgery.
Primary stability must counteract all forces that
could create micromotion between the implant and
the surrounding tissues. Or, in other words, it should
build up enough preload to compensate for functional
load. It thus determines not only the size but also the
direction of the forces that are considered to remain
adequate. All these parameters must be specified, and
this makes it understandable why immediate
functional loading may be adequate for such systems
as bar-connected screws, whereas others require a
prolonged, unloaded healing period before a
supraconstruction can be installed.
Stages of osseointegration
Direct bone healing, as it occurs in defects, primary
fracture healing and in osseointegration is activated
by any lesion of the pre-existing bone matrix. When
the matrix is exposed to extracellular fluid,
noncollagenous proteins and growth factors are set
free and activate bone repair. Attracted by
chemotaxis, osteoprogenitor cells of the bone marrow
and from the endocortical and periosteal bone
envelopes migrate into the site of the lesion. They
proliferate and differentiate into osteoblast precursors
and osteoblasts and start bone deposition on the walls
of the defect, the fragment ends and possibly on the
implant surface. At this time osteoclasts are rarely
seen and apparently not involved in the process of
activation.
Once activated, osseointegration follows a common,
biologically determined program that is
subdividedinto 3 stages:
incorporation by woven bone formation;
adaptation of bone mass to load (lamellar
and parallel-fibered bone deposition); and
adaptation of bone structure to load (bone
remodeling).
Incorporation by woven bone formation
The first bone tissue formed is woven bone (Fig. IA).
It is often considered as a primitive type of bone
tissue and characterized by a random, felt-like
orientation of its collagen fibrils, numerous,
irregularly shaped osteocytes and, at the beginning,
a relatively low mineral density. But it has an
outstanding capacity: it grows by forming a scaffold
of rods and plates and thus is able to spread out into
the surrounding tissue at a relatively rapid rate. The
formation of the primary scaffold is coupled with the
elaboration of the vascular net and results in the
formation of a primary spongiosa that can bridge
gaps of less than 1 mm within a couple of days.
Woven bone is the ideal filling material for open
spaces and for the construction of the first bony
bridges between the bony walls and the implant
surface. Woven bone usually starts growing from the
surrounding bone towards the implant, except in
narrow gaps, where it is simultaneously deposited
upon the implant surface. Woven bone formation
clearly dominates the scene within the first 4 to 6
weeks after surgery.
Adaptation of bone mass to load
(deposition of parallel-fibered and lamellar bone)
Starting in the second month, the microscopic
structure of newly formed bone changes, either
towards the well-known lamellar bone, or towards an
equally important but less known modification called
parallel-fibered bone. Lamellar bone is certainly the
most elaborate type of bone tissue. Packing of the
collagen fibrils into parallel layers with alternating
course (comparable to plywood) gives it the highest
ultimate strength. Parallel-fibered bone is an
intermediate between woven and lamellar bone: the
collagen fibrils run parallel to the surface but without
a preferential orientation in that plane. This is clearly
seen in polarized light: lamellar bone is strongly
birefringent (anisotropic), and parallel-fibered bone
is not (isotropic). Another important difference is
found in the linear apposition rate: for human
lamellar bone, this amounts to only 1-1.5 gm/day; for
parallel-fibered bone it is 3—5 times larger. As far as
the growth pattern is concerned, both types cannot
form a •scaffold like woven bone, but merely grow
by apposition on a preformed solid base.
Considering this last condition, three surfaces are
qualified as a solid base for deposition of
parallelfibered and lamellar bone: woven bone
formed in the first period of osseointegration, pre-
existing or pristine bone surface and the implant
surface.
Schenk & Buser

Fig. l. Stages one and two of osseointegration. All sections are ground and
polished, and surface-stained with toluidine blue. A. Stage l: woven bone
incorporation. The 150- to 400-pm-wide gap between the pre-existing bone
(PB) and the implant is filled with a scaffold of newly formed woven bone
(dark staining). Sulmesh-coated press-fit cup, retrieved at autopsy 33 days
after total hip replacement from an 82-year-old woman, x 60. B. Stage 2:
reinforcement of initially formed woven bone (darker staining) with lamellar
bone. Femoral revision stem made of commercially pure titanium with a
corundum-blasted surface, retrieved 5 months after revision surgery from a
65year-old man, x60. C. Stage 2: reinforcement of pre-existing bone
(brighter). This femoral stem was inserted in a 65-year-old woman who died
4 months later from a hypertonic crisis. Lamellar bone is deposited upon the
devitalized remnants of the trabeculae and has established contact with the
corundum-blasted titanium surface, x60. D. Stage 2: enlargement of bone-
implant contact by direct lamellar bone deposition upon the rough titanium
surface. A cross-sectioned wire (diameter 700 gm) of a sulmesh-coated
acetabular cup is concentrically surrounded by lamellar bone. Specimen
retrieved at autopsy of a 92-year-old woman 21 months after total hip replace-
ment, x 74.

Woven bone formed in the first period of
osseointegration (Fig. 1B). Deposition of more
mature bone on the initially formed scaffold results
in reinforcement and often concentrates on the areas
where major forces are transferred from the implant
to the surrounding original bone
Pre-existing or pristine bone surface. This
becomes obvious in sites where implants are
surrounded by cancellous bone (Fig. IC). Quite
frequently, the trabeculae become necrotic due to the
temporary interruption of the blood supply at
surgery. Reinforcement by a coating with new,
viable bone compensates for the loss in bone quality
(fatigue), and again may reflect the preferential
strain pattern resulting from functional load.
The implant surface. Bone deposition in this site
increases the bone-implant interface and thus
enlarges the load-transmitting surface (Fig.
ID).Extension of the bone-implant interface and
reinforcement of pre-existing and initially formed
bone compartments are considered to represent an
adaptation of the bone mass to load. Dental implants
are less suitable for the demonstration of this
interrelationship than prostheses such as artificial
hips, which are preferentially surrounded by
cancelIous bone that responds almost predictably and
rapidly to changes in magnitude and direction of load.
This justifies the inclusion of some samples taken
from our studies dedicated to orthopedic implants in
this chapter that otherwise deals with the dental
aspects of osseointegration.Adaptation of bone
structure to load(bone remodeling and modeling)
Bone remodeling characterizes the last stage of
osseointegration. It starts around the third month and,
after several weeks of increasingly high activity,
slows down again, but continues for the rest of life.
In cortical, as well as in cancellous bone, remodeling
occurs in discrete units, often called a bone
multicellular unit, as proposed by Frost (25, 26).
Remodeling starts with osteoclastic resorption,
followed by lamellar bone deposition. Resorption and
formation are coupled in space and time. In cortical
bone, a bone multicellular unit consists of a squad of
osteoclasts (cutting cone) that form a sort of drill-
head and produce a cylindrical resorption canal with
a diameter equal to an osteon, that is, 150—200 pm
(43— 45). The cutting cone advances with a speed of
about 50 gm per day, and is followed by a vascular
loop, accompanied by perivascular osteoprogenitor
cells. About 100 um behind the osteoclasts, the first
osteoblasts line up upon the wall of the resorption
canal and begin to deposit concentric layers of
lamellar bone. After 2—4 months, the new osteon is
completed. In the healthy skeleton, resorption and
formation are not only coupled, but also balanced,
thus maintaining the skeletal mass over a longer time
period. If formation does not match resorption, a local
deficit in bone mass occurs that accumulates with
time and may cause osteoporosis.
The bone multicellular unit concept is also valid
for cancellous bone. On the trabecular surface
remodeling starts with an accumulation of osteoclasts
that produce an erosion cavity (43—45). Some days
later, osteoblasts appear and refill the eroded space
with new lamellar bone in a couple of weeks. The
structural unit that results from this remodeling ac
tivity is called a lamellar packet, or simply packet.
Coupling of resorption and formation is also valid for
trabecular bone multicellular units, which are
described in this context only in their cross-sectional
appearance.Whereas the underlying mechanism of
coupling and balance has been extensively studied,
little is known about the local activation of bone
remodeling. When bone is deprived of its blood
supply, it undergoes a series of changes, but bone dies
slowly (43). Osteocytes disintegrate — often not
totally, leaving DNA residues in the otherwise
"empty lacunae". Important matrix constituents are
degraded and breakdown products may be released
via lacunae and canaliculi. In any case, recruitment
and activation of osteoclasts, and thus the onset of
remodeling becomes effective only after a lag time of
3 or more weeks. Cyclical load stimulates cortical
remodeling. Functional adaptation of cancellous
bone, however, is based on shape-deforming,
uncoupled or unbalanced resorption and formation.
Its control and regulation is still an unsolved problem.
Remodeling in the third stage of osseointegration
contributes to an adaptation of bone structure to load
in two ways:
It improves bone quality by replacing pre-existing,
necrotic bone and/or initially formed, more
primitive woven bone with mature, viable lamellar
bone.
It leads to a functional adaptation of the bone
structure to load by changing the dimension and
orientation of the supporting elements.
It has been mentioned already that bone remodeling
continues throughout life and thus becomes
important for the longevity of implants. Continuous
replacement of old bone by new bone prevents
accumulation of microdamage and fatigue as one
possible cause of aseptic implant loosening.
Osseointegration of
dental implants
Orthopedic joint replacement and dental implants
share many common features, such as material,
surface configuration, or measures for primary
stabilization. As far as failure is concerned, dental
implants face the main complication by piercing the
mucosa, thereby evoking the risk of infection. In joint
replacement, the articulating surfaces are subjected to
wear the resulting particulate may cause foreign body
reactions and possibly aseptic loosening.
Schenk & Buser
The tissue response to both categories of implants is
modified by the structure of the surrounding bone.
The rather bulky components of artificial joints are
mainly supported by cancellous bone. Initial contact
with cortical bone is marginal. In the jaw bones, the
coronal part of the dental implants becomes firmly
anchored within compact bone, whereas the apical
segment is exposed to cancellous bone and bone
marrow. These local differences influence profoundly
the histological aspects of osseointegration in all
stages.
Histological observations in animal research
The canine mandible is frequently used in
experimental studies of dental implant incorporation.
After extraction of all premolars (PI-P4) and the first
molar teeth (Ml) and a healing period of 3—5
months, the alveolar crest presents sufficient and
healthy bone that allows placement of several
implants. Fig. 2A-C are taken from a study in
foxhounds, where osseointegration of unloaded and
loaded commercially pure titanium implants with a
sandblasted and acidetched surface were compared
with those of titanium plasma-sprayed controls (20).
Histology and histomorphometric analysis of bone-
implant contact was made at 3 months of healing
(unloaded implants) and compared with 6 months (3
months loaded), and 15 months of healing (12 months
loaded).
Osseointegration in cortical bone areas. Primary
stability is obtained by congruency and press-fitting,
which leads to direct bone-implant contact. Press
fitting often causes local overload, with plastic
deformation of the lamellae and even fissures and
microcracks (Fig. 2D).
The local blood supply is disturbed by rupture and
compression of vessels. The bone becomes avascular
and necrotic but still provides stability. In this
experiment, primary contact was found at 3 months
in about 20% of the implant surface. It was reduced
by bone ongrowth and remodeling to 8—9% at 6
months and 5-6% at 15 months.
When screw-type implants are inserted into
cortical bone, a bur is recommended with a diameter
that is somewhat larger then the core of the thread.
The wall of the bore-hole is then often detectable in
the sections and separated from the screw thread by a
50- to 100-gm-wide gap (Fig. 2E). At 3 months, it is
partially or completely filled by lamellar bone,
formed in the second stage of osseointegration. Bone
remodeling, as the dominant mechanism in stage
three, finally replaces the avascular areas by mature
living bone (Fig. 2F). Cortical remodeling
substantially contributes to the increase in interface
between implant and living bone that amounts to
60—70% after 15 months in this material.
Osseointegration in cancellous bone areas. The
volume density of bone matrix in cortical bone is
about 80—90%, in cancellous bone only 20—25%.
Cancellous bone, therefore, contributes much less to
the primary stability. Sites where direct contact
between implant and trabeculae was forced by
compression are rather rare (Fig 2G, H). On the other
hand, a large compartment of implant surface is
exposed to bone marrow, with its ample vascularity
and abundance of precursor cells for osteoblasts.
Secondary bone-implant contact is achieved by
bridging the intertrabecular marrow space. In the first
stage, scaffolds of woven bone accomplish this goal.
Prominent structures on either side, that is, free ends
of trabeculae, or edges and threads of the implant,
serve as a sort of bridgehead and narrow the span to
be covered. Once established, these bony anchors are
reinforced by lamellar bone and finally subjected to
continuous remodeling, which improves bone quality
as well as the orientation and dimension of the
supporting elements.
In-between the bony anchors a large surface remains
exposed to bone marrow only. Bone ongrowth also
spreads out from neighboring anchors along this
surface and covers it with a bony coating often less
than 50 gm wide (Fig. 21). This is seen in later stages
of osseointegration, when the structure of the bone
marrow has matured to the red and/or fatty type.
Bony coating can be considered as a reaction of the
bone marrow stroma cells to the rough titanium
surface that produces bone also in sites that do not
participate in weight-bearing. Bone marrow is a
delicate tissue that is physiologically encased by
bony walls. The bony coating of the implant surface
thus may represent an attempt to replace the missing
parts of the protective bony envelope. If the bony
coating in-between the bony anchors is or becomes
involved in load transfer, it is reinforced by additional
bone deposition. The thin, mechanically unimportant
bony coating is usually included in the morphometric
measurements. Therefore, the percentage of bone-to-
implant contact in the cancellous part of the implant
site reaches the same or even higher values as for the
cortical lining. In this study, about two thirds of the
rough titanium surface was covered by bone in all
specimens examined (20).
Histological observations in removed human
implants
Compared with animal experiments, the retrieved
implants represent a heterogeneous selection of
cases, and the results have to be generalized with
caution. Information about the patient, the case
history, the quality of the host bone, and last but not
least the skill of the surgeon are usually scanty, and
in most cases the cause for removal is implant
failure.
As far as osseointegration is concerned, retrieved
implants are indispensable for long-term evaluation
of implants subjected to functional load. With this
aim, the histological examination of explanted ITI@
(Institut Straumann, Waldenburg, Switzerland)
implants was started 2 years ago. The following
examples are taken from the first set of 10 cases. All
specimens were retrieved with a trephine that
preserves a thin but coherent bone sheath around the
implant and thus allows quantification of the
interface.
Measurements of the percentage of bone-implant
contact had to be restricted to the implant surface
that was retrieved together with the surrounding
bone. It was calculated as percentage of this
reference surface. The mean value in the 10 explants
was 78.1%. The lowest value of 54.1% was found at
7 years in an old type F hollow cylinder with peri-
implantitis. A titanium plasma-sprayed screw that
had functioned over 12 years reached the maximum
of 94.1%. The histology confirms most observations
made in the animal experiments: contact is
established by mature, viable lamellar bone that
adheres to the rough, microporous titanium plasma-
sprayed surface and undergoes remodeling at a
remarkably high rate.
Schenk & Buser
Fig. 2. Osseointegration of rough-surfaced, loaded and
unloaded titanium implants in the canine mandible (20).
All specimens were ground and polished and surface-
stained with toluidine blue and basic fuchsin. A.
Nonsubmerged commercially pure titanium implant with a
sandblasted and acid-etched surface at 15 months (12
months loaded). The lingual side is in contact with cortical
bone, the buccal aspect mainly with spongiosa. Hollow-
screw design, outer diameter 4.1 mm, total length 9 mm,
endosseous portion 6 mm (Institut Straumann,
Waldenburg, Switzerland), x8. B. Same section,
osseointegration in cortical bone, x30. C. Same section,
bone anchorage in the cancellous bone part, x30. D.
Primary contact with cortical bone. Press-fitting led to local
overload and plastic deformation of the lamellae. Some
fissures originate from the edge of the thread. Remodeling
in the otherwise devitalized bone has started at the lower
margin of the micrograph. Sandblasted and acid-etched
surface, 3 months unloaded, x 75. E. Secondary bone-
implant contact by bone apposition. A straight cement line
delineates the wall of the former drill hole from the bony
filling in the thread. TWO large vascular spaces are lined
by osteoblasts and osteoid, indicating ongoing bone
deposition. Titanium plasma-sprayed surface, 3 months
unloaded, x 75.
F. Secondary bone-implant contact achieved by cortical
bone remodeling. Three cortical bone remodeling units
have evolved in direct contact with the implant surface. At
3 months, they are in an early stage of bone formation.
Sandblasted and acid-etched surface, 3 months unloaded, x
80, G. Formation of bony anchors in the cancellous part of
the implant site. The apical and the middie thread are
connected to pre-existing trabeculae (brighter) by newly
formed bone bridges. The coronal thread is shown at higher
magnification in H. Sandblasted and acid-etched surface, 3
months unloaded, x 25. H. The middle thread exhibits
primary, punctate contact with pre-existing bone. Lamellar
bone apposition has completed the bony anchor that
resembles a pair of pliers. Sandblasted and acidetched
surface, 3 months unloaded, x50. I. The groove between the
coronal and the middle thread is covered by a less than 50-
gm-thin bony coat, deposited by the red bone marrow on
the sandblasted and acid-etched surface. 3 months
unloaded, x80.
Schenk & Buser
The small number of cases does not allow for a
comparative evaluation of implant types. It shows,
however, some remarkable peculiarities. The basket of
most hollow cylinders exhibits a bone fill that is
connected to the outside bone via the perforations (Fig.
3A). Support by the bone plug may become less
important for hollow screw implants, where the
threaded part transfers the major part of the load to the
outside bone (Fig. 3B). In case of an infection,
however, the perforations also serve as preformed
pathways for the invasion of granulation tissue (Fig.
3C). The bone around screw-type implants presents
similar findings as in experimental animals: in
cancelIous compartments, the bony anchors
concentrate upon the protruding ridges, whereas in
contact with cortical bone, the threads become almost
completely filled with bone, except for the space
required for vascular supply (Fig. 3E). Bony coating is
also regularly observed along surfaces that are exposed
to bone marrow, but not engaged in load transfer (Fig.
3F).
Histological observations in human implants
retrieved at autopsy
Microscopic examination of retrieved implants is
limited by the small diameter of the trephine and the
lack of connections to the bony walls of the implant site.
Intact specimens of human cadavers, however, are rare
for obvious ethical reasons (27, 36, 50). A recent study
(38) reported the histological findings in four bar-
connected and immediately loaded titanium plasma-
sprayed screws that were functioning for 12 years in the
edentulous mandible of a 95-year-old patient. In his
will, the patient donated his body to the Institute of
Anatomy, University of Berne. Following perfusion
with a formaldehyde solution, the anterior segment of
the mandible was retrieved, including the four implants
with surrounding tissues. For further details of the case
history, histological preparation, and detailed
documentation of the findings, we refer to the original
publication (38). This summary is restricted to some
selected histological aspects of osseointegration.
As far as histology and histomorphometry are
concerned, the four implants are almost
interchangeable. At least two thirds of the screw length
are directly lined by cortical or cancellous bone. The
percentage of direct contact was calculated in the 4
specimens as 73.4, 82.9, 68.7 and 80.4, the mean being
76.4%.
In the orofacial, midaxial sections, the lingual
aspects of the implants are in contact with dense
compact bone, the facial surface borders on cancellous
bone and bone marrow (Fig. 4A). In contact with
cortical bone, the thread of the screws are filled with
28
compact bone and some vascular canals (Fig. 4B).
Cortical remodeling takes place in immediate contact
with the plasma-sprayed titanium surface, and only a
few sites with primary initial contact have escaped
remodeling and are still detectable at 12 years.
Adjacent to cancellous bone, the implant surface is
covered almost completely by a 100- to 200-gmv,ide
layer of lamellar bone (Fig. 4C). The remaining parts of
the surface abut on bone marrow or are, to a lesser
extent, lined by thin bony coatings. Bony anchors
connect the tips of surrounding, rather thick trabeculae
with the ridges of the thread. The bone marrow is
mostly of the fatty type and well vascularized, without
any signs of inflammation or foreign body reaction.
In two of the four implants, the tip of the screws were
firmly anchored in the inferior cortex of the mandible.
The other two screw tips ended in the medullary
spongiosa. In the latter case the surface of the screw
ends are sheathed by bone that is continuous with the
surrounding trabeculae that finally merge with the
cortical bone (Fig. 4D).
In view of the high age of these patients, the bone
remodeling activity is of particular interest. Cortical
bone remodeling steadily produces new secondary
osteons. Interstitial lamellae fill the interspace between
these cylindrical units. A large number of osteocytes
within the interstitial compartment lose their
connections to the endocortical surface and die. The
avascular matrix in these areas continues to accumulate
mineral, and finally the empty lacunae and canaliculi
become filled with calcium salts. Compared to viable
bone, the avascular bone matrix is hypermineralized,
harder and more brittle. This state was called
"micropetrotic" by Frost (24). At the age of 80 and
more, about 50—70% of the cortex in long bones is
micropetrotic, and this holds true also for the mandible
in the case under investigation. In the vicinity of the
implant, however, the remodeling activity is much
higher. Active remodeling sites and newly formed
osteons are often found in direct contact with the
titanium surface (Fig. 4B, E).
This indicates, that when forming a resorption cavity,
osteoclasts may clean thoroughly the titanium
plasmasprayed surface from adhering old bone.
Subsequently, osteoblasts appear and deposit new,
mineralizing bone on and into the microporosities,
thereby reconstructing the microindentations at the
interface.

Fig. 3. Osseointegration of explanted IT] e implants (Institut Straumann,
Waldenburg, Switzerland) retrieved. A. Hollow-cylinder 'IYpe F implant,
retrieved at 4 years. Bone-implant contact is at 78.1%, x8. B. Hollow screw
implant, retrieved at 5 years. Bone-implant contact is at 83.2%, x8. C.
Hollow-cylinder 'IYpe F implant, retrieved at 4 years because of peri-
implantitis. The infection hasentered the internal portion of the basket. Bone-
implant contact was not determined, x 10. D. Titanium plasmasprayed screw,
retrieved at 9 years, bone-implant contact is at 77.4%, x 2. E. Titanium
plasma-sprayed screw, filling of thread with cortical bone, F. Titanium
plasmasprayed screw, bony coating of thread, x 30.
The bone coverage of the screw thread in the cancellous
compartments is also subject to remodeling. As
mentioned before, trabecular bone remodeling is
initiated again by osteoclasts digging out an erosion
cavity, which is then filled up again by osteoblasts.
Lamellar packets are clearly separated by cement lines
Osseointegration: a reality
from the pre-existing bone (Fig. 4F). Since newly
formed bone stains more intensely because of its
somewhat lower mineral density, lamellar packets can
easily be identified along the bone-implant interface
(Fig. 4E). The perfect reconstruction of the bone-
implant interface merits special attention: it restores
microindentation that ensures adhesion of bone to the
metal, an indispensable prerequisite for successful and
long-lasting osseointegration.
Discussion and clinical
considerations
In the past 20 years, the utilization of dental implants
became a scientifically accepted treatment modality for
the rehabilitation of fully and partially edentulous
patients.
Schenk & Buser
Fig. 4. Osseointegration of an immediately loaded,
barconnected titanium plasma-sprayed screw after 12 years
of function in a 95-year-old patient. All specimens are ground
and polished, and surface-stained with toluidine blue and
basic fuchsin (38). A. Mid-axial, orofacial section of one of
the four implants. The buccal aspect points to the right and is
in contact with spongiosa, while the lingual side is covered
by cortical bone, x 3.2. B. The thread on the lingual side is
filled by compact bone still undergoing remodeling. A newly
formed osteon is seen in the upper thread (darker staining)
and a resorption space in the lower one, x40. C. Anchorage
in cancellous bone on the oral aspect is secured by a
continuous bone layer covering the thread. Recently formed
30
lamellar packets (darker staining, arrows) indicate ongoing
trabecular remodeling, x40. D. The tip of the self-tapping
screw protrudes into the marrow cavity. It is covered by a
bone plate and supported by trabeculae that are connected to
the cortical layer, x 15. E. Cortical bone remodeling is shown
by a secondary osteon (darker staining) in direct contact with
the titanium plasma-sprayed surface, x80. F. CancelIous
bone remodeling resulted in a lamellar packet (darker
staining) inserted into the bone plate previously deposited on
the titanium plasma-sprayed surface. It is delineated by
cement lines from the bone deposited earlier on the thread,
x80.

This progress in implant dentistry is clearly based on
the discovery that endosseous dental implants can be
anchored in jaw bone with direct bone-implant contact.
This phenomenon was first described by Brånemark et
aL (8), who examined submerged titanium implants
with a machined surface in dogs and later called this
osseointegration (9). Similar findings were described
by Schroeder et al, (47) in histological nondecalcified
sections of nonsubmerged titanium implants with a
titanium plasma-sprayed surface in monkeys. He
termed this type of implant anchorage later as being
functional ankylosis (4B). As outlined above in detail,
osseointegration is achieved and maintained after
implant insertion with a cascade of three different
maturation steps, starting with the incorporation of the
implant by woven bone formation, followed by the
adaptation of bone to load by lamellar and parallel-
fibered bone deposition, and finally the ongoing
structural adaptation of bone to load by bone
remodeling.
Since the early 1980s, experimental and clinical
research has focused on the various factors that
influence the osseointegration of endosseous dental
implants. These efforts were in part necessary to
improve implant anchorage in bone, since a significant
widening of implant indications took place in implant
dentistry in the late 1980s. The original documentation
of osseointegrated implants was based on
retrospective studies in fully edentulous patients. In
the past 10 years, partially edentulous patients were
increasingly treated with dental implants. Today, this
group of patients clearly dominates the daily routine.
As a consequence, many implants are inserted in areas
of reduced vertical bone height and high functional
load, such as in posterior segments of both jaws. In
addition, implants are also placed in clinical situations
with implant-supported single crowns or short-span
bridges with the lack of cross-arch stabilization. Based
on experimental studies and clinical experience,
certain trends became apparent in recent years, which
are discussed here with regard to implant material,
implant placement modality, implant shape, and
implant surface.
Implant material
As described above, bioinert or bioactive materials can
achieve osseointegration as long as certain guidelines
are respected. Among the clinically tested implant
materials, commercially pure titanium is recognized
today as a material of choice, since it is not only
characterized by excellent biological but also good
mechanical properties (49). Alternative implant
materials could not provide enough evidence for
longevity and satisfying success rates. For example,
Osseointegration: a reality
aluminum oxide (A1203) implants completely
disappeared from the market in the late 1980s, since
this implant material was not strong enough to
withstand high masticatory forces and demonstrated an
increased risk for fatigue fractures under long-term
function,
Implant placement modality
TWO modalities for implant placement are known in
implant dentistry: the submerged and the
nonsubmerged approach. For years, emotional
discussions took place at conferences as to which
approach should be chosen in patients. Today, it is
generally accepted that both modalities are applicable
in implant patients and offer predictable bone and soft
tissue integration, as demonstrated both in animal (13,
23, 28, 52) and in clinical studies (3, 5, 14, 22). Hence,
clinical considerations are of primary importance today
which approach should be chosen by the clinician. Most
recently, a strong trend towards a nonsubmerged
implant placement is apparent, since it helps the
clinician to avoid a second surgical procedure and to
reduce the treatment time and related costs.
Implant shape. A tremendous variety of different
implant shapes have been developed and clinically
tested in the past 20 years, In general, a titanium
implant of any shape can achieve osseointegration, if
primary stability is obtained by a low-trauma surgical
procedure and precise fitting, The implant shape,
however, will influence the predictability, how often
osseointegration is achieved after implant insertion and
how osseointegration is maintained over time under
long-term functional load. Today, screwtype implants
are highly preferred in implant dentistry, since threaded
implants offer two major advantages compared with
press-fit cylindrical implants. First, the implant threads
improve primary implant stability, which is important
in avoiding micromovements of the implant until
osseointegration is achieved. This is primarily
important for implants inserted in a nonsubmerged
fashion or in areas of low bone density. Second, the
threads seem to play an important role for the load
transfer from the implant to the surrounding bone. This
aspect is not yet fully understood, but it is a striking
observation that bone trabeculae most often point to
and are attached on the edge of the threads as
demonstrated by several histological sections of
osseointegrated implants in this chapter (Fig. 2c, g, h).
Implant surface
The implant surface is one of the six factors described
by Albrektsson et al. (l) to be important for bone
Schenk & Buser
integration of endosseous dental implants. In the past
10 years, surface modifications have received a lot of
attention by several research teams. The two best
documented titanium surfaces in implant dentistry are
the machined titanium surface and the titanium plasma-
sprayed surface. Since screw-type implants with a
machined surface have demonstrated an increased
failure rate for short implants and for implants inserted
in sites with poor bone density (31-33, 41), several
attempts have been made to improve implant anchorage
in bone by modifying the surface characteristics of
titanium implants. One attempt was made with a
hydroxyapatite coating of titanium implants. This
coating offers an improved bone adhesion, as shown in
several experimental studies (12, 21, 51, 58). The long-
term efficacy of hydroxyapatite-coated implants,
however, is still under dispute. Whereas some
publications (6, 10, 11) presented long-term results
well comparable to results with threaded titanium
implants, other authors (35, 40, 53) reported a clearly
increased failure rate for hydroxyapatite-coated
implants, some with severe complications. Probably
due to these negative reports in the dental literature,
hydroxyapatite-coated implants play only a marginal
role in implant dentistry today.
Another attempt was made by roughening titanium
surfaces to improve implant anchorage in jaw bone.
The titanium plasma-sprayed surface was the first
rough titanium surface that was introduced into implant
dentistry more than 2 decades ago (47). It demonstrated
satisfying long-term results in fully and partially
edentulous patients (2, 14, 37). Alternatively, rough
titanium surfaces can be produced by noncoating
techniques such as sand- or grit-blasting, Ti02-blasting,
acid etching, or combinations of the above. Based on
numerous studies in the past decade, there is
overwhelming scientific evidence that rough titanium
surfaces offer significantly better bone anchorage than
do machined titanium surfaces. This was evaluated
both by histomorphometric evaluation of the bone-
implant interface, and by biomechanical studies
measuring either pull-out, push-out or removal torque
forces (12, 17—20, 29, 30, 34, 54—58). It is not
surprising, therefore, that rough titanium implants have
become increasingly popular in implant dentistry in
recent years and are now offered by most implant
manufacturers. From a clinical point of view, rough
titanium surfaces offer a significantly better implant
anchorage in bone with shorter healing periods and the
option to utilize shorter implants with a good long-term
prognosis. It has to be kept in mind, however, that
differences in roughness characteristics do exist and
that these newly introduced surfaces need to be
evaluated very carefully and compared critically with
the clinically very well documented titanium surfaces
32
such as the machined and titanium plasma-sprayed
surface.
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