Jan Lindhe. Clinical Periodontology

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SUPPORTIVE PERIODONTAL THERAPY (SPT) • 805

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IMPLANT CONCEPTS

CHAPTER 33

Historic Background and

Current Concepts

TOMAS ALBREKTSSON, TORD BERGLUNDH AND JAN LINDHE

Development of the osseointegrated implant

Early tissue response to osseointegrated

implants

Osseointegration from a mechanical and

biologic viewpoint

Osseointegration in the clinical reality

Future of osseointegrated oral implants

DEVELOPMENT OF THE

OSSEOINTEGRATED IMPLANT

In the early 1960s, Branemark and co-workers at the

University of Goteborg started developing a novel

implant that for clinical function depended on direct

bone anchorage – termed osseointegration. Osseoin-

tegration was certainly not an accepted phenomenon

at the time. Instead, the notion was that an oral im-

plant was embedded in soft tissue whether one liked

it or not. Therefore, the implanted device was never

as strongly anchored in the host tissues as immedi-

ately after its insertion. Animal experiments per-

formed at BrAnemark's laboratory clearly indicated

that it was possible to establish a direct bone anchor-

age, provided that a number of defined guidelines

were followed (Branemark et al. 1969). This was fur-

ther documented in the first clinical report published

few years later (Branemark et al. 1977).

Even though Branemark's team was the first to

suggest a direct bone anchorage and the potential

clinical advantages of such osseointegration, the sci-

entific community remained unconvinced of osseoin-

tegration and its potentials. The reason for this reluc-

tance to accept the new ideas was partly a methodo-

logical shortcoming: in the 1970s there were no meth

ods available to section intact bone to metal speci-

mens. Therefore, the histologic evidence of osseointe-

gration remained indirect (Fig. 33-1). Only after re-

Fig. 33-1. In the past there were only indirect methods

for verifying osseointegration. In this formalin-fixed

and thereby slightly shrunk specimen, one sees bone

tissue with a Haversian (H) system in close relation to

the titanium (Ti) threaded implant.

moval of the implant with potential simultaneous

removal of some soft interfacial tissues was it possible

to inspect and analyze the interface. The first investi-

gator to clearly demonstrate osseointegration was

Schroeder from Switzerland. Schroeder worked from

810 • CHAPTER 33

the mid 1970s, quite independently from Branemark,

with research on direct bone anchored implants.

Schroeder's team used newly developed techniques

cut through undecalcified bone and implant with-

out

previous separation of the anchorage. In, for their

time,

excellent illustrations, a direct bone to implant

contact was proved beyond doubt (Schroeder et al.

1976, 1978, 1981). Other pioneering work on osseoin

tegration was conducted at roughly the same time by

the German clinical scientist Schulte (1978).

Albrektsson et al. (1981) presented information on

series of background factors that needed control in

order for a reliable osseointegration of an implant to

ensue. These factors involved (1) the biocompatibility,

(

2) design and (3) surface conditions of the implant,

(4)

the status of the host bed, (5) the surgical technique

insertion, and (6) the loading conditions applied

afterwards. All these factors needed more or less si-

multaneous control in order to result in osseointegra

tion of the implanted device. Albrektssons laboratory

has since been devoted to learning more about these

various background factors. Twenty-eight PhD theses

on these topics have been published at the laboratory.

Ossseointegration, once looked upon with scepti-

cism, is now even regarded by some investigators as

frequently occurring, primitive foreign body reac

tion

to an implanted material. A biomechanical factor

alone

is thought to determine whether a fibrous en-

capsulation or a bone covering will develop around

implanted device. Indeed, the authors behind these

statements have demonstrated that even amalgam

compounds will be embedded in bone (Donath et

al.

1992). However, opposed to this view of osseointegra-

tion as simply a foreign body reaction is the docu-

mented evidence of the bone response being quanti-

tatively different depending on the type of biomaterial

and its surface roughness (Johansson 1991, Gottlander

1994, Wennerberg 1996).

EARLY TISSUE RESPONSE TO

OSSEOINTEGRATED IMPLANTS

The site in the edentulous alveolar ridge that is se-

lected for implant insertion is lined with a mucosa, in

most situations a keratinized mucosa, which guards

the hard tissue compartment. The surface of the bony

part of the ridge – the compact bone – is lined with the

periosteum, below which a layer of cortical bone can

be found. The cortical bone serves as an envelope for

the spongious or trabecular bone and the bone mar-

row that are included in the central portion of the ridge

(Fig. 33-2)

In order to acquire proper conditions for healing,

the implant following installation must exhibit good

mechanical stability. It has been assumed that proper

stability can be achieved when the marginal and/or

apical" portion of the site harbors sufficient amounts

compact bone and/or when the spongious (cancel-

Fig. 33-2.

Fig. 33-3.

lous) bone contributes with sufficient amounts of tra-

beculae.

The various steps used in the surgical procedure –

e.g. the incision in the mucosa, the elevation of the

mucoperiosteal flaps, the careful preparation of a ca-

nal in the cortical and spongy bone, and finally the

insertion of the titanium device – bring to bear a series

of mechanical insults which result in injury to both the

mucosa and the bone tissue. To the above described

injury must be added the adverse effects obtained by

the so called "press fit", namely the collapse of the

vasculature which occurs in the cortical portion of the

bone wall when the slightly wider implant is inserted

in the canal prepared in the hard tissue.

The damage to the soft and hard tissue initiates the

process of wound healing which ultimately allows (1)

the implant to become "anchylotic" with the bone, i.e.

osseointegrated, and (2) the establishment of a deli-

cate mucosal attachment or barrier to the titanium

device, which serves as a seal that prevents products

from the oral cavity reaching the anchoring bone tis-

sue.

The healing of the severed bone tissue is a compli-

cated process and apparently involves different steps

MPLANT PLACEMENT

compact bone

bleeding

tissue necrosis

resorption

new

bone

formation

bone marrow

bleeding

new

bone

formation

OSSEOINTEGRATION: HISTORIC BACKGROUND AND CURRENT CONCEPTS • 811

Fig. 33-4.

in the cortical and spongious parts of the surgical site.

In the cortical bone region resorption of mineralized,

avascular necrotic tissue must occur before new bone

can form on the implant surface. In the spongious

region of the site, on the other hand, woven bone

formation and osseointegration occur early in the

process of healing.

Some important features of the early wound, that

occur in the bone at the recipient site, can be observed

in Fig. 33-3 (ITI solid screw), which illustrates an

implant with surrounding tissues 24 hours after in-

stallation surgery. The implant has proper mechanical

stability, achieved by the "press-fit", i.e. the minute

lateral displacement of bone tissue and the tight con-

tact that was established following installation be-

tween the metal screw and the avascular cortical bone

in the marginal two-thirds of the site. This zone of

press-fit" has been calculated to be about 1 mm wide.

During site preparation and fitting of the implant,

bone trabeculae were in the apical portion of the site,

dislocated into the marrow space, blood vessels were

severed and bleeding occurred (Fig. 33-4) (ITI implant,

apical part). In Fig. 33-3 blood clot formation can also

be observed between the implant body and the host

bone. During the course of the following days, the

blood clot will mature and become substituted with a

granulation tissue, rich in neutrophils and macro-

phages. The leucocytes will start to decontaminate the

wound, and from the marrow spaces of the peripheral

vital bone, vascular structures will proliferate into the

newly formed granulation tissue.

Reparative macrophages and undifferentiated me-

senchymal cells will about one week after implant

insertion start to produce and release growth factors,

which stimulate

fibroplasias

through which an undif-

ferentiated

provisional connective tissue

forms in (1) the

apical, trabecular regions of the implant site, and (2)

the "furcation sites" (F) of a screw-shaped implant. A

"furcation site" (F) may be defined as the inner parts

of the threaded regions of the implant which, follow-

ing insertion, are without contact with the surround-

ing bone.

Osteoclasts will at this stage start to appear in the

bone marrow spaces more remote from the implant

surface, and the necrotic bone will gradually be resor-

Fig. 33-5.

Fig. 33-6.

bed. The provisional connective tissue is rich in (1)

newly formed vessels, (2) fibroblasts, and (3) undiffer-

entiated mesenchymal cells and will gradually mature

into an osteoid from which (4)

woven bone

(primary

osteons) will form to fill the void with bone tissue. This

phase of wound healing and early bone formation is

called

modeling.

Fig. 33-5 (Astra implant) illustrates an implant site

2 weeks after installation surgery. Note that woven

bone with primary osteons has formed at the base of

the surgical site and that newly formed bone has been

laid down not only in the apical part of the implant,

but also in the "furcation sites" of the implant surface

(

Fig. 33-6, enlargement of Fig. 33-5).

A further examination of the bone tissue next to the

implant documents the presence of so called reversal

lines (Fig. 33-7) (enlargement of a 3I implant), which

indicate the level, lateral to the titanium screw, to

812 • CHAPTER 33

Fig. 33-7.

Fig. 33-8a.

Fig. 33-8b.

Fig. 33-9.

Fig. 33-11.

Fig. 33-10.

Fig. 33-12.

OSSEOINTEGRATION: HISTORIC BACKGROUND AND CURRENT CONCEPTS • 813

Fig. 33-13. Osseointegration represents a direct bone to

implant contact at the resolution level of the light mi

croscope, but is still best defined based on maintained

stability of the implant. Retrieved clinical specimen

showing a high degree of bone to implant direct con-

tact.

which resorption of the necrotic tissue has occurred.

In the "furcation sites" of the implant, new bone for-

mation — osseointegration — is at this stage of healing

the dominating feature, while at the peaks of the

threads of the screw-type implant, discrete areas of

bone resorption can be seen, since the newly-formed

woven bone has poor loading capacity — implant sta-

bility is at this interval still maintained through the

press-fit" upheld in the necrotic part of the cortical

bone.

Fig. 33-8 (ITI solid screw) presents an implant site

after 4 weeks of wound healing. In this particular

implant the distance between the threads is about 1

mm. The bone tissue within a zone — about 1 mm wide

— lateral to the implant contains remnants of old bone

that have been partly replaced by newly formed

woven bone. The non-mineralized part of the bone

tissue (primary bone marrow) contains at this stage no

adipocytes. Note the presence of newly formed woven

bone that lines most parts of the implant surface. This

newly formed bone represents the first phase of true

osseointegration.

The phase of modeling is followed by a phase of

remodeling

during which the woven bone is substi-

tuted with lamellar bone with a good potential to take

up and distribute load. The woven bone is through a

process of osteoclastic activity gradually removed and

replaced by lamellar bone and bone marrow. Figs. 33-9

and 33-10 (ITI screw; different enlargements) illustrate

an implant site 8 weeks after the insertion of the

titanium screw. The titanium surface is lined with a

thin rim of lamellar bone, lateral of which a bone

marrow rich in adipocytes can be observed. Typical

secondary osteons with concentric lamellae and a cen

tral Haversian canal can be observed in the lamellar

bone within the zone of "press-fit", and in the adjacent

bone tissue.

As healing continues, all portions of the original

bone become replaced with new bone. Fig. 33-11 (ITI

solid screw) illustrates a site 4 months after implant

installation. The newly formed lamellar bone, next to

the implant, is continuous with the more lightly-

stained old bone tissue. In the apical, bone marrow

part of the site (Fig. 33-12), a thin rim of lamellar bone

can be seen in contact with the implant surface.

OSSEOINTEGRATION FROM A

MECHANICAL AND BIOLOGIC

VIEWPOINT

Osseointegration represents a direct connection be-

tween bone and implant without interposed soft tis-

sue layers (Fig. 33-13). However, 100% bone connec-

tion to the implant does not occur. Problems in iden-

tifying the exact degree of bone attachment for the

implant to be termed osseointegrated have led to a

definition of osseointegration based on stability in-

stead of on histologic criteria: "A process whereby

clinically asymptomatic rigid fixation of alloplastic

814 • CHAPTER 33

Fig. 33-14. Post mortem specimen of a titanium screw

implant showing a high degree of bone to implant con

tact after 4 years of clinical loading.

Fig. 33-15. Post mortem specimen of a maxillary im-

plant inserted together with a bone graft, immediately

prior to planned second stage surgery. Note the poor

bone to implant contact percentage in this specimen

that was basically similar to five other implants from

the same maxilla.

Fig. 33-16. Even if complete

bone tissue with cells and

ground substance requires a

minimum of 100 µm thickness

for ingrowth, ground substance

alone may invade pores of

much

smaller sizes, leading to

the

establishment of

biomechanical

bonds typical for

properly

osseointegrated im

plants. Bone

ground substance

invasion of

nm-sized irregulari

ties is only

hypothetical and

without any

proven significance

for implant

stabilization.

materials is achieved, and maintained, in bone during

functional loading" (Zarb & Albrektsson 1991). From

different retrieval studies of implants removed from

human jaws, despite maintained stability some infor-

mation regarding bone to metal contact percentage has

become available. Investigating more than 100

retrieved Nobelpharma type implants we have expe-

rienced more than 60% bone to implant contact for

implants loaded between 1 and

years (Fig. 33-14).

With increasing time of loading, there is a clear ten-

dency for there to be more bone in contact with

mandibular implants than with maxillary ones (Al-

brektsson et al. 1993). In some grafted cases we found

very sparse amount of bone to implant contact,

despite

the implants being clinically stable (Fig. 33-15)

(

Nystrom et al. 1993).

It has been suggested that the nature of the osseoin

tegrated bond is related to physical and chemical

forces acting over the interface (Albrektsson et al.

1983). However, even if such forces may act over the

bone to c.p. titanium interface, there is no evidence

that they play any dominant role in the strength of the

OSSEOINTEGRATION: HISTORIC BACKGROUND AND CURRENT CONCEPTS • 815

Fig.

33-17.

The optimal surface

roughness in experimental studies

is of an s

of about 1.4. s

repre-

sents the arithmetic mean of the

absolute values of the surface de-

partures (i.e. peaks and valleys)

from the mean plane within the

sampling area.

osseointegrated bond. The bond is in all probability

predominantly biomechanical. Having said this, sur-

face modified titanium implants may indeed show

bioactive properties. NaOH/heat-treated titanium

plates have been found to resist much higher failure

loads than non-treated controls (Yan et al

1997,

Skripitz & Aspenberg

1998,

Nishiguchi et al

1999).

Sul

(

2002)

has presented some evidence that titanium im-

plants oxidized in a calcium hydroxide solution like-

wise become bioactive.

It is known that complete bone ingrowth does not

occur in spaces much smaller than 100 microns (Al-

brektsson

1979).

However, bone ground substance

will adapt to surface irregularities in the 1-100 microns

range, explaining why changing the surface topogra-

phy at this level will result in a profound impact on

the holding power of the implant (Wennerberg

1996).

There is no scientific evidence that irregularities even

in the nm range will affect the bone response, though

this has been suggested by some investigators (Fig.

33-16).

Commercially available oral implants have

average surface irregularity values (s

) beween 0.5

and

2.5 microns. In animal experiments there is a

significantly stronger bone response to surfaces with

sa values of 1.0-1.5 microns (Fig.

33-17).

Surface ir-

regularities in the 2.0

microns range or greater will

show a diminished bone response, possibly because

of increasing ionic leakage from these relatively rough

surfaces.

Osseointegration is a time-related phenomenon.

Johansson & Albrektsson

(1987)

demonstrated that

during the first few weeks after implant insertion

there were no signs of proper osseointegration. Three

months after implant insertion there was a relatively

high proportion of bone to implant direct contact (Fig.

33-18)

and a clearly increased resistance to torque

removal. The amount of bone and resistance to torque

increased further, in the rabbit model used, at 6 and

months of follow-up. Yamanaka et al.

(1992)

investi-

Fig.

33-18. A

few weeks after implant insertion there is

very sparse bone to implant contact. The bone tissue

(B) contact with the implant (Ti) increases with time,

represented by this rabbit tibial implant at three

months after insertion. ST= Soft tissue.

gated the holding power of temporal bone implants

humans and found a gradually increasing removal

torque up to

3 years after implant insertion. Taken

together these results imply that c.p. titanium im-

816 • CHAPTER 33

Fig.

33-19.

hollow basket implant made from

Ti-6A1-

4V that was demonstrated to fail clinically in many

cases due to ongoing bone saucerization. This implant

was launched without any published clinical long-term

follow-up results, yet was at one time the most fre-

quently used oral implant in the

USA.

Stricter attitudes

from authorities and more critical analyses from den-

tists will, hopefully, prevent human experimentation

with untested products in the future.

plants are not very stable in bone during the first

weeks after their insertion. Despite this observation

primary loading of implants seems possible at least in

the mandible, mainly dependent on the previously

described "press-fit" (for review see Albrektsson &

Sennerby 2000). This does not prevent the possibility

that there may a slightly increased failure rate for early

loading even in mandibular sites. Furthermore, since

the implants are dependent on "press-fit" for main-

tained stability, the surgical technique must be care-

fully controlled. In the maxilla, there is as yet sparse

information about early loading. These data point to

the importance of diagnosing the stability of implants

which may differ considerably, e.g. in mandibles be-

tween the mental foraminae compared to in maxillae

of poor bone quantity and quality.

Previous attempts to measure implant stability and

thereby assess its degree of osseointegration have in-

cluded Periotest measurements (Schulte & Lukas

1993). The Periotest uses a metal probe accelerated by

an electromagnet. The contact duration of the probe

on the implant is measured by an accelerometer. Con

tact time is then related to implant mobility. Despite

being frequently used, the Periotest approach results

in widely different data, and individual measure-

ments have failed to reveal whether an implant is

osseointegrated or not. The device cannot be recom-

mended for clinical decisions on implant stability.

Meredith and co-workers (1994, 1996) have described

a different approach to assess bone formation around

an implant, measuring the resonance frequency of a

small transducer attached to an implant fixture. In a

Fig.

33-20.

solid cylinder implant removed because of

pain

3 years after its insertion. There is not one single

study documenting steady state bone levels around

solid cylindrical implants without special retention ele

ments such as threads. Since numerous studies of this

design have documented an ongoing gradual loss of

anchoring bone tissue, responsible dentists should

avoid working with cylindrical implant designs.

clinical application of this new so-called RFA tech-

nique (Resonance Frequency Analysis), Meredith et al.

(1996) investigated one group of nine patients with 56

Branemark implants during their first year of inser-

tion. They found the resonance frequency to rise from

an average of 7473 Hz at implant placement to an

average of 7915 Hz, 8 months later. In contrast, two

implants that failed to integrate showed clearly low-

ered frequency data. Furthermore, the authors col-

lected data obtained with 52 other Branemark im-

plants in nine patients examined 5 years after implant

placement and compared those with radiograms with

special reference to the exposed threads and the length

of each abutment. The findings indicated a clear cor-

relation (r = -0.78) between the length of the non-

osseointegrated part of the implant pillar and reso-

nance frequency. Resonance frequency of an im-

plant/transducer system was found to be related to

the height of the implant not surrounded by bone and

the stability of the implant/tissue interface. The inno

vative work by Meredith has resulted in clearly im-

proved ways of measuring implant stability in clinical

routine.

Once established, the osseointegrated interface is

relatively resistant but certainly not immune to vari-

ous types of outer stimuli. Whereas the healing bed

around an implant is highly sensitive to irradiation or

heat injuries, once osseointegration has occurred, the

same trauma levels will seemingly not affect the bond

(

Eriksson 1984, Jacobsson 1985). However, prolonged

adverse conditions may result in breakage of

osseointegration and subsequent implant failure (Fig.