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1/11
Periodontology
2000 Vol.
17 1998 36-46
Printed in Denm ark. All rights reserved
C o p y r i g h t M u n k s g a a r d 1 9 9 8
PERIODONTOLOGY 2000
I SSN 0906-6713
Surface configurationsof
dental implants
JAN
EIR IKELLINGSEN
The use and development of implants for restoring
single or multiple loss of teeth has been through sev-
eral phases to reach the optimal goal of having a per-
manent, artificial anchoring of fixed bridges or
crowns in the upper and lower jaw. This period,
mainly based on trial-and-error approaches, has led
to the development of different implant materials,
designs and treatment techniques that have not al-
ways led to the results expected or desired.
More needs to be known about the optimal situ-
ation of the connection between an artificial ma-
terial and the tissues what type of material that
gives the best tissue response and what type of sur-
face is preferred by the bone cells or the cells in the
soft tissue.
If
this is known, the response of the bone
or soft tissue can be predicted when the implants are
installed into the jaws.
Today's implant materials function well when the
bone quality is good and especially when there is
bicortical anchorage. However, in many cases the
situation is not optimal and regions have cancellous
bone and a thin cortical lamellae. Although some re-
Table 1. Different types of materials used in the
body as biomaterials
Gold
Cobalt-chromium alloys
Stainless steel
Titanium
Zirconium
Niobium
Tantalum
Hydroxyapatite
Bioglasses
Tricalcium phosphate
Carbon
Polymers
A 1 2 0 3
cent reports (52, 66,
72,
85) indicate that good clin-
ical results can be achieved even after shorter heal-
ing time using the conventional implants, most re-
search (1, 2, 4 18-21) shows that a relatively long
healing period without any stress is needed to
achieve a tight bony contact with the implant ma-
terial. The healing time, however, depends on the
bone quality, and one aspect of current research is to
try to determine the best treatment modalities with
reduced bone quality, particularly in the maxillary
region.
Another aim of biomaterial research is to improve
the bone quality after implantation by introduction
of active bone-inducing substances. Structures on
the implant surface or in the tissues may also have
such an effect.
The current situation concerning the clinical use
of implants is based on basic research and animal
and clinical trials that have been performed at many
institutions worldwide during the last
3
decades. The
result of this activity is that treatment with implants
is now generally accepted in dentistry if the treat-
ment is done according to some accepted principles:
cylindrically shaped implants, preferably with
threads, and the surgical and the subsequent pros-
thodontic procedures performed according to an ac-
cepted protocol.
However, with all respect to the research per-
formed in this field, the state of the art today is
mainly a result of trial-and-error approaches to op-
timizing already known materials and methods.
Scientifically based engineering of new materials to
reach a specific goal is rare. Most biomaterials used
in implantology are not specifically developed for
this purpose but were available before they were
used as biomaterials. Examples of these materials
are listed in Table
1.
The materials form a heterogen-
eous group consisting of metals, precious and non-
precious, oxide forming, corrosive, more or less non-
corrosive, ceramics and non-metals and non-cer-
amics. The effects of these materials in bone
36
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Ellinasen
sults obtained with this type of implants and is not
based to the same extent on systematic biomechan-
ical research and knowledge of the optimal bio-
mechanical connection between the implants and the
bony structures. Following an implantation, the im-
plant goes through several phases in which stability
and the transfer of loads are important. To obtain op-
timal healing of the bone close to the implant surface,
stability of the implant bed is important
(22, 73,
88).
Introduction of threads to the cylindrically implant
improves the implant stability significantly
(41).
Threaded cylindrical implants help the surgeon in
placing the implant exactly in the pre-drilled cavity,
and due to the threads the implant is stable and fixed
during the healing process. This probably has clinical
consequences. Screw-shaped implants have been
found to be in closer contact with bone than are cylin-
drical implants without threads
(24).
The observation
of improved bone healing around screw-shaped im-
plants has also been confirmed by Albrektsson et al.
(5)
in a long-term clinical trial. Different types of
thread profiles have been used on the cylindrical im-
plants but all with the same goal: to establish a stable
fixation between the implant and the bony tissue and
to improve load transfer.
Introduction of threads on cylindrical implants
leads to a change in the distribution of the stress ap-
plied to the implant compared with cylindrically
shaped implants (80).A cylindrically shaped implant
will largely transfer the stress to the apical part with
axially directed loads and probably to the neck and
apical part with horizontally directed loads. When
bone implants are designed, attention should be di-
rected towards distributing the loads evenly in the
bone. This will reduce the possibilities for overloading
the bone, and according to Wolff's law, induce bone
remodeling
or
bone formation. Both excessive and in-
sufficient stress have been suggested to promote bone
resorption at the neck region (30,811.
Overloading was suggested as a main causal factor
behind loss of Brinemark (Nobel Biocare AB, Gote-
borg, Sweden) implants (68). The same group found
improved results with longer implants compared
with shorter ones, further indicating that over-
loading is a major factor in the loss of dental im-
plants.
An
even distribution of loads in the bone thus
increases the load-carrying capacity of the implant.
Although the bone structure differs between differ-
ent types of cancellous bone and cortical bone areas,
studies have been performed to identify an optimal
thread profile. Frandsen et al. (41) observed an in-
creasing retention with increasing screw diameter
and increasing thread length when testing the hold-
ing power of four different screws implanted in can-
cellous bone of cadaveric femoral heads.
Most cylindrically threaded implants have a
thread profile similar to machined screws. It has
been argued that this is not an optimal profile in
bone. Other groups have therefore constructed im-
plants with different thread profiles and a different
angle of the thread flank (Fig.
2)
(82). It is debated
whether these changes in thread profiles have any
real clinical significance. Both systems with different
thread types have demonstrated long-term clinical
success
(1, 20).
In a recent thesis, Hansson et al. (50) present an-
other threading profile with minute threads with a
depth of only 0.1 mm (Fig. 3). These authors argue
that this type of threads have improved capacities to
carry load compared with the regular type of threads,
such as those on Branemark implants
(50).
These findings are in accordance with recent
findings by Wong et al. (94) that demonstrated im-
proved push-out strength for implant surfaces with
many small peaks compared with a surface with
high, but few peaks.
Surface microstructure
Fig.
3.
Example of an implant with a combination
of
microthreads and conventional threads: Astra Tech ST
Molndal, Sweden)
Another important factor of the surface configur-
ation is the microstructure of the implant surface.
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Surface configurations of dental implants
This can vary considerably depending on the surface
treatment of the implant. Variation of the surface
microstructure has been reported to influence the
stress distribution, retention of the implants in bone
and cell responses to the implant surface.
Gross et al. (45) investigated the in vivo responses
to pellet-blasted or flame-sprayed cylinders made of
titanium and Ti,+414V lloy, and furthermore to ti-
tanium rods flame sprayed with hydroxyapatite,
which were implanted into rabbit femurs. The
authors concluded that, independent of the implant
chemistry, each implant should have a micro-rough-
ness that
allows
fixation of trabeculae and conse-
quently a transmission of forces. The implants with
rough surfaces had improved bone response, with
bone trabeculae growing in a perpendicular direc-
tion to the implant surface.
An improved retention in bone has also previously
been reported after implantation of rough-surfaced
implants.
Several authors have discussed the dimension of
the ideal roughness that would provide increased re-
tention and an improved bone response. The rough-
ness can be considered on different levels: macros-
tructural, microstructural and ultrastructural, and
roughness on these different levels probably has dif-
ferent effects on the living tissues. It has been estab-
lished in the literature based on several studies that,
to gain complete growth of bone into a materials
irregularities, these need to be at least
100
pm in size.
Growth of bone into cavities or pores of this size will
give a mechanical interlocking of the material with
bone. This was demonstrated by Bobyn et al. (12) in
studying cobalt-based alloys with pore sizes of 50-
400 pm, Bone ingrowth was also observed by Cle-
mow
et al.
(29)
when this group studied porous coat-
ed
Ti l,V
femoral implants with pore sizes ranging
from 175 to 235 pm.
The optimal pore size to obtain bone ingrowth
might also depend on the material. Breme et al. (14)
stated that titanium alloy implants had an optimal
pore size of 100 pm. Increased removal torque values
were, however, also found when
using
titanium
po-
rous-coated screws of stainless steel with a pore size
of 10-40 pm. These small pores do not allow a maxi-
mal ingrowth of bone but may give increased reten-
tion based on mechanical interlocking. This has
also
been stated by Predecki et al. (67) in a study of bone
ingrowth to titanium and aluminum implants with
channels with diameters of 95-1000 pm. This group
reported the fastest bone ingrowth into channels
with diameters of 500-1000 pm, and no ingrowth
smaller scale was, however, found to be important
for integration of the bone with the implant surface.
These findings indicate that other mechanisms, not
purely based on mechanical interlocking, determine
the reactions between bony tissue and biomaterials.
Although surface roughness on a micrometer scale
gives some retention due to bone ingrowth,
in vitro
cell studies indicate that this property of the surface
influences the function of the cells, the matrix depo-
sition and the mineralization (13, 64, 78). Cells seems
to be sensitive to microtopography and appear to be
able to use the morphology of the material for orien-
tation and migration
116,
25 , 2 6 . The maturation of
the cells also affects the response to the surface
roughness, which is in agreement with earlier obser-
vations that indicated that chondrocytes are affected
differently by local factors such as vitamin
D
and
transforming growth factor
p
depending on the
stages of maturation of the cells
13,
76-78, 84).
Microtopography may therefore be one factor that
influences the differentiation of mesenchymal cells
into fibroblasts, chondrocytes or osteoblasts. Based
on these studies, the authors hypothesized that
osteogenesis may be favored by vascular ingrowth,
whereas a limited vascular ingrowth may induce
chondrogenesis.
Implants exhibiting a micro-roughness on their
surface have been tested and used both in animal
studies and in human patients. Buser et al.
(20)
in-
vestigated the correlation between different surface
structures and the bone response, as measured by
bone-to-implant contact. The surfaces investigated
in that study included titanium plasma-sprayed ti-
tanium, sandblasted and acid-etched titanium as
Fig.
4.
Scanning electron micrograph
with
high resolution
x503) of the surface of a machined, threaded implant
fNobel Biocare Mark 111
nto the 95-pm channels. Surface roughness on a
.~
_
39
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Fig. 5. Scanning electron micrograph with high resolution
x503) of the surface
of
a titanium plasma-sprayed
threaded implant
IT1
Bonefit)
well as hydroxyapatite-coated titanium. The authors
reported a positive correlation between increased
roughness and bone contact measured by histologi-
cal techniques. Titanium surfaces may also be blas-
ted with T i 0 2 particles to give micro-roughness. In
a clinical study in dogs, the biological response to
implants with this surface was compared with ma-
chined titanium. The authors reported significantly
higher removal torque values for the blasted im-
plants
(44)
(Fig.
4-6).
The ideal surface roughness for bone implants on
a micrometer scale probably depends on the distri-
bution of cortical or cancellous bone and on the
level of loading to the implants. Nevertheless, an op-
timal surface roughness has been proposed based on
experimental studies. In a series of studies, Wenneb-
erg et al. systematically investigated the effect of sur-
face roughness of implants and the response in rab-
bit bone (90-93). The implant surfaces were char-
acterized by profilometry as well as with a three-
dimensional laser technique. Titanium implants
with four different surface structures were created by
blasting with A12 3or Ti02 in addition to the ma-
chined surface. The surfaces were blasted with 25-
pm particles of
T i 0 2
or 25-pm, 75-pm or 250-pm par-
ticles of A1203.The authors concluded that implants
with a surface roughness of Sa 1 to 1.5 pm seemed
to be at an optimal roughness with regard to reten-
tion in bone as well as bone-to-implant contact as
measured by histomorphometry. This optimal sur-
face was created by blasting with 25- to 75-pm par-
ticles and resulted in surface roughness of Sa=0.83
and Sa=1.29 respectively.
A
rougher surface as
created by 250-pm particles led to a surface rough-
ness of Sa=2.11 and did not result in an improved
bone response. Implants treated with the 25-pm par-
ticles had significantly more bone-to-implant con-
tact than implants treated with the 250-pm particles
when the three best threads were considered.
No
sig-
nificant differences could, however, be detected
when the authors recorded the bone-to-implant
contact to all threads on the screw implants. Blasting
the titanium implants with 250-pm particles did not
improve the retention of the implants in bone.
Al-
most identical removal torque values were recorded
when the implants blasted with 25-pm particles and
250-pm particles were removed. The observation of
an improved response of bone to implants with a
surface roughness of Sa 1.0-1.5 pm is also in accord-
ance with observations by von Recum van Kooten
(89) that reported excellent tissue attachment with-
out signs of inflammation when implanting filter
membranes with pore sizes of 1-3 pm. Based on
these results, it seems that the benefit of increasing
roughness on a micrometer scale reaches a maxi-
mum level between 1.0 and 1.5 pm. Above this level
no further positive response in the bone can be ex-
pected. This observation indicates that the findings
from in
vitro
cell experiments that bone cells are ru-
gofile and respond positively with increased matrix
deposition and mineralization are also true in an in
vivo situation. This may be because the less rough
surfaces to a certain extent stimulate the bony tissue
through loading, which in return responds with in-
creased bone growth. Another, or additional inter-
pretation of the findings of Wennerberg et al. (90-
93) could be that the rugofile bone cells recognizes
the surface prepared by the course particle, as a
Fig.
6.
Scanning electron micrograph with high resolution
X503) of the surface of a titanium dioxide-blasted
threaded implant Astra Tech TiO-blast)
40
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urface configurationsof dental implants
smooth surface, whereas the 25-pm particles creates
a rough surface that is identified by the osteoblasts
(Fig.
7).
Surface ultrastructure
Although micro-roughness seems to be an important
characteristic for tissue response to biomaterials,
there are also observations that indicate a biological
response to irregularities on the nanometer level.
Larsson et al. 59-61) studied the biological effect of
changing the oxide thickness of titanium implants
from an electropolished level, to thick oxide layers
formed by anodization. By this treatment the surface
changes from an amorphous metal surface with a
noncrystalline oxide to a polycrystalline metal sur-
face with a crystalline oxide layer. Analysis of these
surface at a high resolution level demonstrated that
the new surface was heterogeneous with mainly
smooth areas of thick oxide but separated with po-
rous regions on a nanometer level. This observation
of an increased roughness after anodization of ti-
tanium was in line with earlier transmission electron
microscopic studies demonstrating increased pore
sizes with increased oxide thickness (58). Implants
with this thick, heterogeneous oxide seemed to have
a slightly improved response in bone, particularly in
the first weeks after implantation. This difference
could, however, not be observed after longer healing
periods. This is in accordance with earlier obser-
vations by Ellingsen Videm
36)
that did not show
any significant correlation between oxide thickness
on titanium implants and the bony response. The
latter observation was measured by push-out experi-
ments and histomorphometry, after 8-week healing
of titanium implants in rabbits. These authors ar-
gued that the outermost molecular layers of the bio-
material are the important part for the bone re-
sponse, because the surface chemistry
of
these
layers is exposed to the tissue. Morphological
changes on a nanometer level may introduce ad-
ditional effects to the tissue response which, in turn,
can further improve the bone healing.
The surface chemistry of the
implants
The chemical properties
of
the biomaterial surface
play an important role for the tissue responses
elicited by the material. This is at least one main rea-
Fig. 7. Bone cells exposed to a medium rough and a very
rough surface. The rugofile bone cells may recognize the
very rough surface right) as
a
smooth surface, whereas
the medium rough surface left) is recognized as a trough
rough surface by the osteoblasts.
son why the tissues responds differently to different
materials. A material with a surface that is accepted
by the tissue seems to exhibit improved integration
with bone, either due to passive growth, leading to a
tight connection between implants and bone, or by
stimulation that probably leads to a bone-implant
bonding. This is probably the case with the two main
materials used in dental implants, hydroxyapatite
and titanium. The calcified parts of the bone con-
sists of hydroxyapatite (or rather carbonated apa-
tite), and introducing this substance as an implant
material often gives favorable responses in the bone.
The chemical structure of the hydroxyapatite is,
however, important, and small changes in this sur-
face chemistry may have biological consequences.
This was observed in a recent study 11) investigat-
ing the osteoblastic responses to synthetic hydroxy-
apatite powders supplied by different manufac-
turers. Although both powders was shown to have a
phase-pure hydroxyapatite structure as indicated by
X-ray diffraction analysis, the calcium-to-phosphate
ratio deviated significantly from the stoichiometric
value for hydroxyapatite; one was rich in calcium
and the other slightly calcium deficient. There were
also small differences in impurities of carbon, so-
dium, silica and alumina. The authors observed that
one material seemed to be inferior to the other
based on the way that the osteoblasts reacted. The
cells cultured on this material had half the amount
of alkaline phosphatase and DNA as the cells cul-
tured on the other hydroxyapatite material. It seems
justified to do similar experiments
in
viva
In some elegant studies, Hanein et al.
(47-49)
demonstrated that cell adhesion
is
sensitive to vari-
41
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Ellingsen
ations in the surface organization of the material on
the atomic level. This group has tested the adhesion
of epithelial A6 cells to chemically equivalent but
structurally distinct phases or surfaces of calcium
(R,R)-tartrate tetrahydrate crystals. The observations
demonstrated that the outermost molecular layers of
a surface influence the interaction between the cells
and the biomaterial.
The biological effects of modifying the biomaterial
surface have also been elaborated by our group
31,
35-38). In an attempt to study the effect of the oxide
layer of titanium on calcium-phosphate precipita-
tion, titanium-dioxide(TiOz) and powder of oxidized
and nonoxidized titanium were introduced into an
in uitro nucleation test system 31). In this system
we found that titanium powder enhances calcium-
phosphate nucleation only after prolonged pre-in-
cubation in an aqueous buffer, or after autoclaving.
These treatments enhance the growth of the oxide
layer. Calcium phosphate crystals could be identified
on the surface
of
the oxidized titanium powder.
X-
ray diffraction analysis of the precipitates revealed
the pattern of poorly crystalline hydroxyapatite. This
observation indicated that the oxide content, or
structure, is required for titanium to act as a nu-
cleation substrate. Even more effective nucleation
was observed when pure TiOZ was used as a nu-
cleation substrate. The presence of serum proteins,
as in the body, will probably mask the reaction sites
and interfere with the capacity of these substances
to induce nucleation. This effect was observed in the
present study, but to a lesser extent when pure TiOa
was present as nucleation substrate. The nucleation
capacity and formation of calcium phosphate pre-
cipitates is related to the biocompatibility of ti-
tanium, and enhanced nucleation capacity may in-
dicate improved biocompatibility.
The biological activity of the TiOZ probably also
influences the protein adsorption to titanium. In an
in uitro study, serum proteins seemed to adsorb to
titanium dioxide by the same mechanisms as to hy-
droxyapatite through calcium binding
35).
The
surface characteristics of TiOZprobably change from
an anionic to a cationic state by the adsorption of
calcium to the surface. This will subsequently in-
crease its ability to adsorb acidic macromolecules,
such as albumin, a property demonstrated for hy-
droxyapatite (9,
10).
Manipulation of the surface oxide layer of ti-
tanium results in modification of the surface prop-
erties of the biomaterial with consequences for its
biological properties. This was demonstrated in a
study in which TiOZwas pretreated with lanthanum
37).Lanthanum ions (La3+)are known to have high
affinity for binding sites usually occupied by cal-
cium. Lanthanum pretreatment of TiOz alters the
properties of this substance, as shown by both in ui
tro and in uiuo tests. The total capacity for adsorp-
tion of serum proteins increased, and the amount of
albumin adsorbed to TiOZ pretreated with lantha-
num was shown to be more than five times increased
compared with untreated TiOz. Marked effects by
this modification were also observed in uiuo when
TiOz was implanted subperiosteally on the rats
sculls. Untreated TiOZ resulted in no adverse reac-
tions from the tissues, as demonstrated by a tight
connection between the TiOz powder with new bone
formation after 4 weeks and no indication of bone
resorption. Implantation of the lanthanum-pre-
treated TiOz resulted in the formation of a layer of
fibrous tissue with mononuclear cells that separated
the implant material from the bone. A similar ten-
dency was also observed when metallic titanium im-
plants were pretreated with lanthanum and im-
planted in rabbits and evaluated by the use of a
push-out test. The lanthanum-pretreated implants
had a significantly looser fit than untreated titanium
implants.
The mechanisms that lead to bone-bonding or to
a firm connection between the biomaterial and bone
are not completely known. The increased adsorption
of proteins to lanthanum-treated TiOZ means that
these proteins may therefore well contain more in-
hibitors of mineralization than the proteins that ad-
sorb to pure TiOz. Proteoglycans are important
modulators in the mineralization of bone and may
interact with mineral crystallites as an important
stage in the control of mineral growth
33, 87).
Fluoride ions have documented activity in bone.
This element is known to form fluoridated hydroxy-
apatite or fluorapatite with improved crystallinity
and better resistance to dissolution than hydroxy-
apatite 8, 42). Fluoride also enhances the incorpor-
ation of newly formed collagen into the bone matrix
and increases the rate of seeding of apatite crystals
as well as increasing trabecular bone density and
stimulating osteoprogenitor cells number in uitro (6,
79). The alkaline phosphatase activity, which is an
indication of the bone formation, was also elevated
after introduction of fluoride in an in uitro study
40).Titanium fluoride forms a stable layer, a glaze,
when applied onto tooth surfaces
(86).
This stable
layer is assumed to consist of titanium, which shares
the oxygen atoms of phosphate on the hydroxyapa-
tite surface, giving a covalently bonding between ti-
tanium and the hydroxyapatite.
4
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Surface configurations of dental implants
titanium-bound oxygen and forms a titanium-fluor-
ide compound. When fluoride-modified titanium
implants are implanted into bone, the surfaces are
exposed to phosphate from the bone at a neutral pH.
This will make possible a reaction in which the oxy
gen in phosphate replaces the fluoride and binds to
titanium to create a covalently binding between
bone and titanium. The fluoride ions released by this
process may thus catalyze the new bone formation
in the surrounding tissue through the bone-stimu-
lating mechanisms discussed above (Fig.9). Fluoride
has also an inhibiting effect on the proteoglycan and
glycosaminoglycan adsorption to hydroxyapatite,
which may further improve the bonding to bone (34,
46, 71). ~~~~~~~l~~~~~nd
g~ycosam~nog~ycans
re
known to inhibit mineralization 39).
The surface qualities are
Of
utmost importance in
establishing of a reaction between the implant and
the tissues. This concerns the surface structure as
well as its chemical and biological properties. Much
attention has been focused on the importance of the
macrostructure of the implants for establishing re-
tention in the bone. More attention will probably be
focused in the future on the biological effects of the
surface structure on the microstructural and ultra-
structural levels as well as on the surface chemistry
of the implants. Progress in these fields based on
knowledge of the biological effects may provide im-
plants with improved tissue response and clinical
performance in the future.
Fig. 8. Scanning electron micrograph of a fluoride-modi-
fied implant after the push-out procedure. The implant is
partly right side) covered by bone that is firmly fixed to
the implant surface, which indicates bonding between the
titanium implant and bone.
References
Fig. 9. A possible mechanism between the fluoride-modi-
fied titanium and bone. Oxygen in phosphate may replace
the fluoride and bind to titanium to create a covalently
binding between bone and titanium. The fluoride ions
which are released by this process may thus catalyze the
new bone formation in the surrounding tissue.
When nonthreaded smooth surfaced titanium im-
plants with a fluoride-modified oxide layer were in-
stalled into rabbits, significantly increased retention
in the bone was observed after a push-out test pro-
cedure (38). This was observed after a 4-week heal-
ing period, but an even more pronounced effect was
observed after an 8-week healing period. Scanning
electron microscopic analyses of the retrieved im-
plants revealed that the fluoride-coated implants
were partly covered by bone that had fractured in-
ternally in the bone and was firmly k e d to the im-
plant surface (Fig. 8). By a surface modification of
TiOz
with fluoride, the fluoride probably replaces the
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