Review

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Improving osseointegration of
dental implants
Expert Rev. Med. Devices 7(2), 241256 (2010)

Carlos Nelson Elias

and Luiz Meirelles
Author for correspondence
Instituto Militar de Engenharia,
Biomaterials Laboratory, Pr. Gen.
Tiburcio 80, 22290-270 Rio de
Janeiro, RJ, Brazil
Tel.: +55 212 546 7244
elias@ime.eb.br

In the beginning of implantology, the procedures adopted for treating patients were performed
in two surgical phases with an interval of 36 months. Nowadays, it is possible to insert and
load a dental implant in the same surgical procedure. This change is due to several factors, such
as improvement of surgical technique, modifications of the implant design, increased quality of
implant manufacturing, development of the surgical instruments quality, careful patient
screening and adequate treatment of the implant surface. The clinical results show that adequate
treatment of surfaces is crucial for reducing healing time and treating at-risk patients. The surface
properties of dental implants can be significantly improved at the manufacturing stage, affecting
cells activity during the healing phase that will ultimately determine the host tissue response,
a fundamental requirement for clinical success. This review focuses on different types of dental
implant surfaces and the influence of surface characteristics on osseointegration.
KEYWORDS : bone formation dental implant nanostructure osseointegration surface properties

Modern dental implantology began almost

half a century ago. A review of the current
literature shows great evolution not only on
implant design and surgical techniques, but
also on the classification of clinical success,
failure and different surface treatments [13] .
Brnemark coined the term osseointegration,
which defines success and failure of dental
implants [4] . Osseointegration was originally
defined at the light microscopic level as a
direct structural and functional connection
between ordered, living bone and the surface
of a load-carrying implant [4] . Later, a more
clinically oriented definition was devised for
osseointegration as a process in which clinically asymptomatic rigid fixation of alloplastic
materials is achieved and maintained in bone
during functional loading. According to this
revised definition, clinical osseointegration
implies histologic osseointegration, it is necessary [there is] a contiguous contact between the
alveolar bone and the implant surface [5] . The
conventional protocol proposed by Brnemark
for treatment with dental implants establishes
that implant procedures should be carried out
in two phases. In the first, the surgical phase,
the alveolus is prepared and the implant is
installed. Furthermore, during the prosthetic
phase, the prosthesis is molded, prepared and
inserted. A 3-month interval between the surgical and prosthetic phase is recommended to
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10.1586/ERD.09.74

allow proper healing of mandibular implants,

whereas a 6-month interval is required for maxillary implants. During the healing period, the
patient may experience discomfort and, in some
cases, installation of provisional prosthesis
becomes difficult.
Primary stability and a healing time of
36 months before loading have been considered essential to allow osseointegration of
dental implants [6] . However, the need of the
healing time to load a dental implant was not
scientifically determined, but was only a clinical observation. Consequently, the original
Brnemark protocol has been modified over
the years. Today, there are protocols describing installation conditions with early implant
loading or even immediate implant loading
[7] . Immediate implant loading is defined as
an implant loaded within the first 2448 h
after surgical implant placement, whereas early
loading has been defined as loading performed
less than 14 days after the surgical implant
placement [8] . Previous results suggest that
there is no difference in implant failure rate
between early and conventional implant loading [9] . Changes in the implant protocol can
be attributed to the improvement of surgical
procedures, biomechanical understanding of
the implants, modifications of the implant
design and development of new surface treatments to obtain optimal biological response of

2010 Expert Reviews Ltd

ISSN 1743-4440

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Elias & Meirelles

titanium implants. To submit implants to masticatory load it

is necessary to take into consideration that the body requires a
minimum time to promote reactions leading to osseointegration. The strategy consists of altering titanium implant surface
properties, modifying the surgical technique and selecting the
most adequate implant design for a given situation. The implant
design has an influence on both primary stability and load distribution, and there is no standardization of implant shapes.
FIGURE 1 shows examples of available dental implants with different designs. Among the various designs, the original cylindrical
screwed implants with an external hexagon are still largely in use
after approximately 50 years of clinical success.
The osseointegration of dental implants is critically dependent on their surface properties. Several investigations have
analyzed the influence of implant surface properties for osseointegration [1015] . It has been shown that surface morphology,
topography, roughness, chemical composition, surface energy,
chemical potential, strain hardening, the presence of impurities, thickness of titanium oxide layer and the presence of
metal and non-metal composites have a significant influence on
bone tissue reactions. The goal is to improve tissue response,
decreasing the conventional waiting time for implant loading
and allowing immediate-early loading protocols. However, the
boneimplant interface of immediate-early loaded implants
must have similar mechanical strength compared with the
interface of a dental implant restored by the conventional protocol, where the host tissue has 36 months of healing time and
the bone biomineralization process is likely to be completed,
resulting in a tissue strong enough to resist oral forces. All
biomaterials trigger biological responses from the body when
they are implanted. During implant insertion and further cell
adsorption on the material surface, cells activate mechanisms
that can identify the material chemical composition and induce
different reactions. There are three classes of biocompatible
materials: bioinert, bioresorbable and bioactive [16] . With bioinert materials (e.g., stainless steel, cobaltchromium alloy,
zirconium, aluminum and polyamides), the organism induces
formation of fibrous-tissue capsules surrounding the foreign
body (scar tissue). Bioresorbable materials dissolve in contact

Figure 1. Examples of commercially available dental

implant designs.

242

with body fluids, such as polyglycolic acid and poly-l-lactic

acid. Bioactive materials stimulate a biological response from
the body, such as bonding to tissue. Hench and Jones suggested that there are two classes of bioactive materials: osteoconductive and osteoproductive [16] . Osteoconductive materials
(e.g., synthetic hydroxyapatite [HA] and tricalcium phosphate)
bond to hard tissue. Osteoproductive materials stimulate the
growth of new bone on the biomaterial surface (unalloyed titanium and tantalum) and spontaneously bind to living bone if
they have been previously subjected to a treatment involving a
soak in NaOH solution, followed by a subsequent heat treatment. Therefore, these metals can be called bioactive metals [17] .
Bioactive materials are those that elicit positive bone response,
which could ultimately results in bone growth. They can bind
to bone through a bone-like apatite layer on the implant surface,
where a chemical bonding along the boneimplant interface
is observed. There are similar biomaterial classifications discussing the different aspects of biomaterial celltissue interaction [18,19] . According to Yan, biomaterial may be described by
representing the tissues responses: biotolerant (e.g., stainless
steel and polymethyl-methacrylate ), bioinert (e.g., alumina
and zirconia) and bioactive (e.g., tricalcium phosphate and bioglass) [19] . Biotolerant materials release substances in nontoxic
concentrations, which may lead to the formation of a fibrous
connective tissue capsule. Bioinert materials exhibit minimal
chemical interactions with adjacent tissue, and a fibrous capsule
can form around bioinert materials.
Osseointegration of dental implants

Osseointegration was defined initially as a direct bone-toimplant contact and later considered, on a more functional
basis, as a direct bone-to-implant contact under load [6] . In
these definitions, the dynamic cellular and acellular processes
that occur at the interface on the micro- or nano-scale level
are not elucidated. Albrektsson et al. highlighted six factors
that are especially important for the establishment of reliable
osseointegration: implant material, implant design, surface
conditions, status of the bone, surgical technique and implant
loading conditions [20] .
Osseointegration can occur only if the cells adhere to the biomaterial surface. At this phase, reorganization of the cytoskeleton
and information exchange between cells and the extracellular
matrix at the cellbiomaterial interface occur, generating gene
activation and specific tissue remodeling. Both the morphology
and roughness of the biomaterials surface have an influence on
cell proliferation and differentiation, extracellular matrix synthesis, local factor production and even cell morphology [10] .
Adhesion of osteoblasts onto implant surfaces is not enough to
ensure osseointegration; it is necessary for cells to receive signals
inducing them to proliferate. For example, coating the titanium
surface with bone morphogenic protein-2 induces osteoblastic
cell division after adhesion. The presence of fibronectin during the interaction between these cells and the implant surface,
or the presence of protein, increases the cell division of human
osteoblasts. This phenomenon is associated with the fact that
Expert Rev. Med. Devices 7(2), (2010)

Improving osseointegration of dental implants

fibronectin has an amino acid sequence (RGD) signaling activation of cell cycles, resulting in cell division of osteoblasts [21,22] .
Silva and Menezes cited that the success in the integration of
biomaterial implants depends on responses such as cell attachment
and cell adhesion [23] . Cell adhesion must be regarded as a condition sine qua non for the effective application of the modern bioengineering, particularly in those cases that involve implantation
of 3D matrices colonized by the patients own cells. Therefore,
one should analyze adsorption, adhesion and behavior of cells
on the implant surfaces in order to speed up cell division, while
seeking to prevent apoptosis or cell death during contact with
implant surface.
During the initial healing phases, the complex 3D structure
of the fibrin network with attached adhesive proteins provides a
substrate for cell adhesion and migration [24] . The composition
and conformation of proteins adsorbed on surfaces provide signals or ligands for the adhesion of cells. The protein film on the
biomaterial surface has an influence on the adjacent host tissue,
which may lead to changes in coagulation time, cell absorption
and tissue repair [24] .
Interaction between cells & the surface of the
dental implants

Implant surface morphology affects attachment, proliferation,

extracellular matrix synthesis, growth factor release and cytokine production. Boyan et al. analyzed the role of material surfaces in regulating bone and cartilage cell response [21] . Initial
events at the surface include the adsorption of molecules from
the surrounding fluid, creating a conditioned interface to which
the cell responds. The surface morphology, as well as the microtopography and chemistry, determines the cell adsortion and
how cells will attach and align themselves [21] . It was suggested
that distinct alterations in cell adhesion structures related to
the surface topography are responsible for differences in cell
signaling, which lead to changes in cellular functions, such as
mineralization [25] . The attachment mechanisms used by the
cells on the biomaterial surface determine cell shape, which
is transmitted via the cytoskeleton to the nucleus, resulting
in expression of specific phenotypes. Insertion of biomaterials
into the human body and their contact with body fluids triggers several events. The body fluids contain ions, as well as
lipids, carbohydrates and proteins, that can be adsorbed at the
biomaterial surface. In this process, proteins play an important
role in inducing the desired response. In the past, it was thought
that cells identifying the presence of a foreign body induced
inflammatory reactions that resulted in encapsulation of the
biomaterial, thus isolating the organism. Today, it is possible
to select the desired protein reaction by choosing the correct
biomaterial and treating the biomaterials surface. It is also possible to obtain adsorption of a specific type of cell, or even avoid
adhesion of organic material. For example, the surface of dental
prosthetic components may have properties controlling biofilm
formation. In a similar way, the surfaces of dental implants
should allow specific proteins to be adsorbed in order to trigger
the mechanisms of osseointegration [26] .
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After the initial protein reaction to the foreign body at the physiological level, the ensuing responses are controlled by a sequence
of events that lead to acceptance or rejection of the material. These
responses involve recruitment of various types of cells existing
at the materials surface, all accounting for activities such as the
remodeling of the extracellular matrix [27] . With regard to dental
implants, it is not desirable for cell recruitment to lead to encapsulation of the material and consequent isolation from body fluids.
Changes in the implant surface, as well as control of both load and
micromovements, are crucial for preventing formation of fibrous
tissue at the boneimplant interface. The commercially pure titanium implant under overloading and higher micromovement does
not present any osseointegration.
Based on the concepts above, one can conclude that the surface
topography is one of the key parameters influencing cellular reactions towards artificial materials. The properties of dental implant
surfaces are extremely important for controlling the reactions
that lead to osseointegration and optimal implant performance.
Surfaces with defined microstructures may be useful for enhancement of the stable anchorage of transcutaneous implants in connective tissue or for prevention of epithelial down growth and
subsequent exfoliation [28] . The surface morphology modulates
the response of cells to a dental implant [2931] . These observations
suggest that specific interactions of bone cells with the implant
surface will result in altered phenotypic expression [32] .
Surface properties, such as morphology, roughness, oxide layer
thickness, impurity level and oxide types, depend on the treatment
process of the implants. The difficulty in analyzing the individual
influence of these parameters stems from the impossibility of altering only one parameter without affecting others. For instance,
it is not viable to modify the type or chemical composition and
crystal structure of titanium oxide while keeping the roughness
unchanged. When an implant is inserted into a tissue it would
be expected to create an adhesive gradient [32] . Irrespective of the
type of implant material, a general sequence of inflammatory and
repair events take place in the surrounding tissue after implantation [33] . After implant insertion, the surface comes immediately
into contact with blood. When in contact with the physiological
environment or blood plasma, titanium absorbs molecules, factor
I, factor III, IgG and CIq. A few seconds after the insertion, it
is possible to find platelets and polymorphonuclear granulocytes
adhered to the titanium surface. Adhesion of mature granular
leukocytes, neutrophils, acidophils and basophils occurs later.
The polymorphonuclear granulocytes are the first leukocytes to
be recruited to adhere to the titanium surface. Depending on the
preparation of the surface, there is a difference in cell adsorption
and reaction caused by the titanium exposed to human blood [33] .
The adhesion of monocytes (mononuclear leukocytes characterized by high phagocytic activity, representing 37% of
the circulating leukocytes) is sensitive to the thickness of the
titanium oxide layer [30] . Polymorphonuclear granulocytes are
more dependent on the surface roughness of the implant, whereas
macrophages prefer smoother surfaces.
A few months after insertion, treated implants show a greater
amount of bone tissue covering their surface compared with
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Elias & Meirelles

machined implants. Despite this finding, it is not clear how the

implant surface promotes or inhibits osteogenesis. It is possible
that a successful implantation depends on how quickly osteogenesis occurs around the implant that is, rapid adhesion of
osteoblasts to the surface of the implant and extracellular matrix
synthesis. So far, there are not enough data regarding how the
initial osteoblast adhesion occurs; cell behavior depends on both
interaction and triggering activities by cells and molecules.
Biomaterials in contact with the biological environment
experience dynamic changes in their surface properties, which
involve a cascade of reactions at the interface between host and
biomaterial, thus forming a conditioning film that modulates
cell responses [34] . Cells possess mechanical receptive properties
capable of identifying whether the implant surface has adequate
characteristics favoring the initial process of differentiation and
formation of bone matrix. The proteins adhering to implant surfaces induce adsorption of osteoblastic and pre-osteoblastic cells.
Studies show that surface treatments change interface forces, wettability, roughness, energy and capacity of adsorption of molecules
that recognize osteoblasts [30] . Cell adhesion is one of the initial
events, and is essential to subsequent proliferation and differentiation of bone cells before bone tissue formation [35] . It has been
demonstrated that cell adhesion to the surrounding extracellular matrix can influence many fundamental cellular processes,
including cell growth and differentiation [36] .
Wettability and surface energy influence the adsorption of proteins, and increase osteoblast focal adhesion on the implant surface.
The cell behavior on a hydrophilic surface is completely different
from that on a hydrophobic one. The expressions of bone-specific
differentiation factors for osteoblasts, such as type I collagen and
osteoprotegerin, are higher on hydrophilic surfaces [37] . Cells on
hydrophilic surfaces may generate an osteogenic environment by
producing more cytokines, such as TGF- 1 and PGE-2. Animal
research compared hydrophilic with hydrophobic dental implants
with equally rough surfaces. The results showed that a hydrophilic
surface presents a significantly higher bone-to-implant contact at 2
and 4 weeks of healing compared with a hydrophobic surface [38] .
A study analyzed and compared differences in the initial adhesion of osteoblasts on two groups of titanium substrates differing
only in surface energy. The results showed that higher implant
surface energy enhances cellular adhesion owing to wettability;
more cells bind directly to the surface [39] . Understanding the
influence of surface topography and chemical functionality on
the growth and adhesion of cells to biomaterials is important
for improving tissueimplant interfacial strength. Ismail et al.
analyzed the influence of surface chemistry and topography on
the contact guidance of MG63 osteoblast cells [40] . When bone
cells are attached to a solid substrate, their behavior and function
depends on the physicochemical and morphological properties of
the biomaterial surface. These surface characteristics determine
how biological molecules will adsorb on the surface and, more
particularly, determine the orientation of adsorbed molecules [41] .
The insertion of dental implants in low-density bone is a problem and the probability of failure increases during the treatment.
An example is the treatment of patients with a systemic disorder,
244

such as osteoporosis, or after being exposed to radiotherapy.

Patients submitted to irradiation demand new approaches to
implant osseointegration [42] . Such circumstances imply a challenging bone healing situation. Under these conditions, the survival rate of dental implants may decrease. The development of
surface modifications may increase the success of dental implants
in compromised patients. Patients with medical conditions, such
as diabetes, radiation treatment for cancer, xerostomia and osteoporosis, do not exhibit the optimum bone conditions for placement
of dental implants and the establishment of osseointegration.
Implant surface topography

Although commercially pure titanium is the prime material of dental

implants, there is a different rate of success among available dental
implant systems. The exact explanation of the difference between
success or failure among commercial implants is not clear. The process of osseointegration depends on several factors and is not yet fully
understood. The effect of implant surface topography, chemical
composition and surface roughness on the process of bone formation are the most studied factors. Studies have shown that titanium
implants with adequate roughness may enhance bone-to-implant
contact [43] and may increase removal torque force [4446] .
In addition, the roughness of implant surfaces also affects
the primary stability of dental implants [47] . Some mechanisms
involved in the osseointegration vary depending on whether the
implant surface is smooth or rough, since cells react differently
to these conditions. Fibroblasts and epithelial cells adhere more
strongly to smooth surfaces, whereas osteoblastic proliferation and
collagen synthesis are increased on rough surfaces [48] .
Several authors have tried to quantify the influence of roughness
on osseointegration in order to obtain optimal surface conditions
[11,13,49] . Despite the importance of roughness for osseointegration,
there is no ideal pattern of roughness regarding dental implants.
Buser et al. observed a tendency for increased bone-to-implant
contact with increasing implant surface roughness [50] . London
et al. could not confirm this observation [51] . Another study suggested that only dental implants with Ra value between 1 and
1.5 m induce an optimal surface for bone integration, so-called
moderately rough implants [52] .
In TABLE 1, one can observe that Ra has a significant influence on
the torque needed to remove the implant. Other parameters are
used to quantify the degree of roughness, such as quadratic average roughness (Rq), peak to valley roughness (Rz), and maximum
roughness height (Rmax). Among the space descriptive parameters used were highest peak (Rpkx), highest valley (Rvkx), peak
area (A1) and valley area (A2). Although the parameter Ra will
not always be useful to characterize the morphology of a given
surface, it has been used because no other variable of roughness
is known to better describe and predict the implant behavior.
Doubts exist as to whether the height of surface irregularities
is more important than the distance between them, and which
combination of these factors could improve osseointegration.
Although the increase in surface roughness promotes greater
mechanical anchorage, the implantbone interface strength will
not increase with the continuous increase of surface roughness
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Improving osseointegration of dental implants

values. Wennerberg et al. analyzed machined and Al 2O3-blasted

implants (particles sized 25 and 250 m) [53] . They observed a
better bone response for implant blasted with 25-m particles
compared with an as-machined surface (MS); however, no differences were found between the implant blasted with 25-m particles (Ra = 0.82 + 0.2 m) and the implant blasted with 250-m
particles (Ra = 2.11 + 0.1 m). Additionally, implants blasted
with 25-m particles of Al2O3 exhibited a greater boneimplant
contact area (46.4%) compared with those blasted with 250-m
particles (39.2%), despite the lower Ra values. The results indicated that there is an optimal range regarding surface roughness
for bone formation, and an average height deviation parameter
between 1 and 2 m is recommended for dental implants [54] .
Takeuchi et al. [55] and Brunette [32] have observed that the morphology and composition of a surface affect both shape and function
of the cells. The cell shape regulates growth, gene expression, protein
secretion, differentiation and apoptosis, while increased roughness
influences differentiation of osteoblasts and osteoclasts [32] .
Osteoblasts become flattened on smooth surfaces and they tend
to grow towards the machined grooves (FIGURE 2) . Grooves having
a depth of 0.5 m and a width ranging from 4.9 to 200 m allow
cells to grow along them. This cell behavior is different for surfaces exhibiting homogenous roughness. Cells present haptotaxis,
rugophobia and rugopholy. Regardless of the situation, there is
no direct contact between implant surface and bone because of
the existence of a thin layer of adsorbed proteins (fibronectin and
vitronectin) [56] .
The production of extracellular matrix is sensitive to roughness. Cell proliferation on implant surfaces is different because
the cells can identify rough surfaces. Cells cultivated on a rough
surface increase production of osteocalcin and alkaline phosphatase. These parameters are, therefore, indicative of osteoblastic
differentiation and consequent increases in osteoblast number [48] .
Production of growth factors, such as TGF- 1, is increased on
rough surfaces, and this is known to stimulate collagen formation
and prostaglandin production. There is a relationship between
osteogenic differentiation and increases in both roughness and
production of PGE-1 and -2 [48] . Inhibition of prostaglandin production depends on a decrease in cell proliferation and an increase
in phenotypic expression, as well as on the production of TGF- 1,
which suggests that the production of prostaglandin involved with
the mechanism of surface roughness depends on the stimulation
of osteogenic differentiation [29] .

Review

Nanotopography

Nanotopography modifications are commonly described in the

literature both as nanoroughness and nanofeatures. It is important
to understand that the overall surface roughness of the sample will
be modified when features are added to the surface, that is, by
adding nanofeatures the surface roughness will also be modified.
Moreover, the nanorough material will also possess nanofeatures;
however, the modifications commonly used to produce the socalled nanorough materials (e.g., acid etching) did not intentionally produce such nanofeatures, and from the usual surface
roughness parameters alone in use, is not possible to evaluate the
dimension of each individual feature at the surface. By contrast,
nanofabricated samples have well-defined dimensions that aim
to modulate cell activity, such as migration, attachment, proliferation and differentiation. FIGURE 3 shows an example of dental
implant surface submitted to a nanotopography modification.
Nanoroughness

Webster et al. evaluated osteoblast adhesion in vitro on alumina and titania discs prepared by compacting powders with
different sized particles onto the surface [57] . The discs were
sintered at different temperatures to obtain different nanoroughness parameters of alumina and titania. Higher osteoblast
adhesion was observed on both alumina and titania discs with
increased mean root square deviation (Sq) and larger surface
area. Additionally, discs prepared with an identical method
consisting of Ti, Ti6Al4 and CoCrMo was tested. As previously
reported on alumina and titania discs, increased osteoblast
adhesion was found on the discs from the different groups
with increased mean root square deviation [58] . Webster et al.
investigated osteoblast adhesion and concentration of different
proteins adsorbed on alumina, titania and HA, with different nanoroughnesses [59] . Pore diameter and porosity (%) were
also calculated. Once again, the osteoblast adhesion was greater
on the discs that exhibited increased nanoroughness, independently of the surface chemistry. Surface porosity was higher and
pore diameter decreased in discs with increased nanoroughness.
Protein adsorption revealed a greater amount of vitronectin
associated with increased osteoblast adhesion on the rougher
discs. Osteoblast proliferation and alkaline phosphatase synthesis on these surfaces was evaluated in another study from the
same group; alkaline phosphatase synthesis was higher after 21
and 28 days on the discs with increased nanoroughness values.

Table 1. Dental implant roughness and torque required to remove from rabbits tibia.
Surface

Ra (m)

Machined

Rq (m)

Rz (m)

Rmax
(m)

Rpkx (m) Rvkx

(m)

A1 (m2)

A2 (m2)

Torque
(N.cm)

0.65 0.11 0.81 0.17 6.09 0.37 7.76 1.37

21.6 0.41

3.14 0.52 24.71 5.42 70.66 16.20

Acid etched 0.51 0.10 0.71 0.07 5.09 0.46 6.78 1.33

1.77 0.37

2.74 0.42 34.76 7.35 103.86 14.80 75.4 10.5

Sandblasted 0.75 0.05 0.98 0.04 5.55 0.21 12.44 9.7

6.75 0.76

9.91 1.71 99.75 6.76 190.13 4.90

72.1 14.9

0.87 0.14 1.12 0.18 5.14 0.69 19.84 2.13 16.71 2.47 6.25 1.23 97.67 11.43 215.37 1.67

83.1 12.7

Anodized

57.0 18.6

A1: Peak area; A2: Valley area; Ra: Roughness average; Rmax: Maximum roughness height; Rpkx: Highest peak; Rq: Quadratic average roughness; Rvkx: Highest
valley; Rz: Peak to valley roughness.
Data taken from [13].

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cells observed on the nanogrooved substrata, which indicates cell activation.

Moreover, cell adhesion increased gradually from plain substrata with shallow
(30 nm) grooved substrata to higher values
observed on deeper (282 nm) grooved substrata. Similar results were found for cell
orientation; the deeper the grooves, the
more orientated the cells became. Another
approach to optimize cell activity with
20 m
10 m
nanofeatures includes the so-called islands
[65] or hemispherical pillars [66] obtained by
the polymer demixing process or colloidal
Figure 2. Surface morphology influences the osteoblast shape.
lithography. Dalby et al. compared fibroblast activity on flat surface and surface
De Oliveira and Nanci cultured bone rat calvaria cells on tita- with 13-nm high islands with a diameter of 263 nm [65] . After
nium discs etched with H2SO4 and H2O2 [60] . They observed 3 days, increased fibroblast spreading, more focal contacts assothat the acid-etched surface revealed nanopits, whereas the con- ciated to vinculin, upregulation of genes involved with cell sigtrol failed to show such features, although the surface roughness naling and collagen precursors were observed on the surface with
was not numerically evaluated. The results indicated an overex- nanoislands compared with the flat surface. In another study,
pression of osteopontin and bone sialoprotein, both intra- and endothelial cell activity was tested on surfaces with islands with
extra-cellularly, on cells seeded on the nano-modified group. In heights of 13, 35 and 95 nm [67] . Similar to fibroblasts, endotheaddition, a higher proportion of cells with peripheral cytoplasmic lial cells on the surface with 13-nm islands exhibited the largest
distribution of osteopontin were observed as early as 6 h.
cell areas (longer and wider axes) and well-defined cytoskeletons,
Larlsson et al. evaluated turned plus anodized, electropolished, compared with the flat, and the 35- and 95-nm surface islands.
and electropolished plus anodized implants on a rabbit model Contrary to the increased activity of the fibroblast and endoafter 16 weeks [61] . The electropolished implant investigated with thelial cells, surfaces with similar features (18-, 35- and 95-nm
atomic force microscope (AFM) showed the smoothest surface. islands) did not influence rat calvaria bone cells [68] . In a recent
After 6 weeks, the electropolished implants showed decreased paper, by Dalby et al., cell activity was compared on surfaces
bone formation compared with the rougher implants. In an identi- with different nanofeatures, including 35- and 45-nm islands
cal study, similar implants were investigated after 712 weeks of with diameters of 2.2 and 1.7 m, respectively [69] . Features
healing [62] . After 7 weeks, the results were similar to the previ- with columns 10-nm high and 144-m in diameter were also
ous study, which indicated higher bone formation to implants added on the flat (control) substrata. The human bone marrow
with increased surface roughness values (anodized) compared cells showed increased cell spreading in the three groups, with
with the smooth implants (electropolished). After 12 weeks, the cells extending filopodia towards the nanofeatures. It also demvalues for the rough implants were steady and the values for the onstrated a well-defined cytoskeleton, enhanced expression of
electropolished implants increased to approximately the same level stress fibers with clear focal contacts and increased expression of
as that found for the rougher implants. Long-term evaluation of osteocalcin and osteopontin on the substrata with nanofeatures.
these implants for 1 year did not reveal any difference in bone
Mendes et al. demonstrated higher bone formation with
formation [63] . It is concluded by in vitro and in vivo experiments nano-CaP coated cpTi and Ti6Al4V compared with uncoated
that cell activity and bone healing may be optimized by modulat- cpTi and Ti6Al4V groups placed in rats [70] . Nano-CaP features
ing surface roughness on the nanometer level of resolution.
were analyzed by field-emission scanning electron microscopy, and
the size varying from 20100 nm was estimated by high magnificaNanofeatures
tion analysis of the samples. Similar implant surface modification
The literature cited in the following section includes nanofeature with nano-CaP was also evaluated in a human study. Gone et al.
modifications that exhibit at least one dimension below 100 nm. placed microimplants into human posterior maxilla, and higher
The first commonly investigated design with controlled dimen- bone contact was observed to nano-CaP-coated compared with
sions on the surfaces was the parallel groove and ridge arrange- uncoated implants after 4 and 8 weeks of healing [71] .
ment at the microscale [32] . Cell orientation was related to the
In a series of studies, nanostructures of different sizes and chemgroove/ridge, and this phenomenon was described as contact ical composition were evaluated both on smooth and moderately
guidance. Approximately 10 years later, cell activity was also rough implants inserted in a rabbit model [72] . Turned cylindrical
related to nanofeatures. Wojciak-Stothard et al. investigated smooth implants were electropolished or mechanically polished to
murine macrophages on flat and nanogrooved surfaces with control the effect of microstructures, that is the bone response evaldifferent depth [64] . By 15 min after plating, most cells remained uated depended only on the nanomodification. In one experiment,
in the vicinity of the plain substrata, compared with well-spread electropolished implants were compared with electropolished
246

Expert Rev. Med. Devices 7(2), (2010)

Improving osseointegration of dental implants

implants modified with nano-HA [73] . AFM characterization

revealed an increase of 7 nm in size and 5 nm in diameter of the
detected nanofeatures present at the nano-HA surface, and similar
feature density compared with electropolished implants; while
both nano- and micro-roughness were similar. After 4 weeks of
healing, significantly higher bone formation was observed around
the nano-HA implant. Later, in an identical model, nano-HA and
nano-titania implants were compared for 4 weeks, an alternative
to differentiate the influence of nanometer features and chemical
composition [74] . AFM characterization showed larger features
with remarkably lower density on the nano-HA surface compared
with the nano-titania. Histological analyses demonstrated a tendency for enhanced bone formation to nano-titania compared
with nano-HA implants. The influence of nanofeatures was also
evaluated on moderately rough screw-shaped implants [75] . The
moderately rough blasted implant group was the control group
of the experiment and the underlying substrate for the two test
groups included in the experiment: nano-HA modified and acidetched with fluoride. Field-emission scanning electron microscope
ana lysis revealed particular nanofeatures at the fluoride-treated
and nano-HA implants, whereas the blasted implants failed to
show such small features. The microroughness ana lysis with an
interferometer showed similar values (surface roughness [Sa]
1.3 m). After 4 weeks, screw-shaped moderately rough implants
that exhibited particular nanostructures showed higher removal
torque values compared with blasted control implants that lacked
such structures. The presence of nanostructures, irrespective of
varying surface chemistry, resulted in evidence of supported bone
formation. The next step for continuous development of biomaterial surfaces may focus on the ideal nanostructure dimension and
distribution at the implant surface [72] .
Influence of the implant surface morphology
on osseointegration

Doubts exist about the optimal procedure for obtaining the best
biological response to dental implants. When the importance the
implant surface properties have for osseointegration is analyzed,
one should separate the influence of implant design and the morphology of surface. Analysis of implant design involves dimensions (length, diameter and wall thickness), shape (cylindrical,
conical and hybrid), screw thread type (triangular, squared, trapezoidal, rounded, microscrew and grooved), paths of screw threads,
angle of screw threads and type of prosthesis connection (e.g.,
external hexagonal, internal hexagonal connection, Morse cone
and star grip). Some of those parameters influence the primary
stability [47] and mechanical strength of the implant. With regard
to the surface morphology, one should analyze the macro-, micro-,
and nano-structures, as well as the surface homogeneity, chemical
and physical properties, type of oxide and its crystal structure.

Review

The differences between commercially available implants can

involve roughness, chemical composition, surface energy, chemical
potential, presence of hydrates and nitrates, layer with residual stress,
impurities resulting from manufacturing or handling procedures,
type of titanium oxide, crystal structure of oxide and thickness of
oxide layer. Analysis of these differences is important, as proteins
interact with the oxides existing on implant surfaces. The surface
roughness of dental implants can be assessed at three scales: macroscopically, microscopically and nanoscopically [87] . Each roughness determines different contacts with cells and biomolecules, thus
being responsible for intensity and types of biological bonds individually. Initially, one could expect that increasing the surface area
of the implant should result in more sites for cell attachment, facilitating tissue growth and improving mechanical stability. However,
this is not a general rule and may vary depending on the cell type.
Fibroblasts avoid rough surfaces and accumulate on smooth ones.
On the other hand, macrophages exhibit rugophilia, that is, they
prefer rough surfaces, whereas epithelial cells are more attracted to
rough surfaces than to smooth ones. Osteoblastic cells adhere to
rough surfaces more easily, a finding also observed in commercially
available implants with chemically treated surfaces [27,56,88] .
Besides the surface topography and roughness, surface chemistry has been investigated. Chemical composition of the surface
has an influence on the secondary stability and reactivity of the
implant. Schneider et al. reported the effect of surface chemistry
on the cell behavior of osteoblasts using a variety of cell cultures and animal models [89] . Schwarz et al. analyzed the effects
of surface hydrophilicity and microtopography on early stages
of soft- and hard-tissue integration at nonsubmerged titanium
implants [90] . The results indicated that titanium surfaces with
a higher surface energy may possess higher potency to promote
differentiation of osteoblasts by a higher expression of cell differentiation and cell activity markers, such as ALP, OC and TG
II. Their results confirm data from other authors [91,92] .
The morphology of dental implant surfaces may be modified by
chemical, mechanical, electrochemical and laser beam treatments.
By treating the implant surface, it is possible to reduce the loading

Dental implant surface modification

Several techniques to modify the implant surface have been proposed to improve the success rate of oral rehabilitation with osseointegrated implants [13,38,49,7686] . The results provide guidelines
for the development of implant surfaces.
www.expert-reviews.com

Figure 3. Example of dental implant surface submitted to

nanotopography modification.

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Elias & Meirelles

time following surgery [49] , accelerate bone growth and maturation [44] , increase primary stability [47] and ensure a successful
implantation [2] . There are numberless variables, combinations
of parameters related to surface treatment and factors influencing
osseointegration (material, implant design, implant surface, bone
quality and quantity, surgical technique and loading conditions).
However, researchers have established no consensus on which
surface, roughness and even implant design would be optimal.
The manufacturers adopt a variety of techniques for treating
implant surfaces. Such treatments increase the implant surface
area, improve primary stability, modify wettability, increase the
bone-to-implant contact area and increase the boneimplant
interface strength.
Selection of the methodology to be used for implant surface treatment is initiated by choosing the desirable roughness, since macro-,
micro- and nano-roughness are differently achieved. Today, there is a
tendency of obtaining hybrid surfaces morphologically characterized
by micro- and nano-structures [72,75] .
In some cases, the manufacturers change the chemical composition of the implant surfaces by adding calcium, phosphorus
and fluoride [80,93] .
Nowadays, the dental implant surface modifications can be
imparted by different methods, including ion beam, laser etching, acid etching, anodization and biomimetic coatings. For
study purposes, the surface modifications can be divided into
seven groups: machined, plasma spray and laser, acid etching,
grit blasting follow acid etching, laser etching, anodizing and
biomimetic coatings.
Machined dental implants

Machined or turned implants were used in early implantology,

introduced by Brnemark [4] . After being manufactured, these
implants are submitted to cleaning, decontamination and sterilization procedures. Scanning electron microscopy analysis shows that
the surfaces of machined implants have grooves, ridges and marks
of the tools used for their manufacturing (FIGURE 4) . These surface
defects provide mechanical resistance through bone interlocking.
The disadvantage regarding the morphology of nontreated
implants (machined) is the fact that osteoblastic cells are rugophilic that is, they are prone to grow along the grooves existing
on the surface, as shown in FIGURE 2 . This characteristic requires
a longer waiting time between surgery and implant loading. The use of these implants follows a protocol suggested by
Brnemark: 36-month healing or waiting time prior to loading.

100 m

100 m

Owing to morphological characteristics and lower resistance to

removal torque (TABLE 1) , machined dental implants are becoming
commercially unavailable.
Plasma spraying & laser treatments

An alternative surface treatment is laser ablation and plasma spraying a metal or ceramic onto an implants surface. The surface
treatment processes using laser and plasma spraying induce high
values for roughness parameters, which may be characterized as
macrorugosities. FIGURE 5 shows the morphology of the implant surface treated with laser. The surface exhibits macroroughness at low
magnification, whereas melting structures can be observed at high
magnification. At higher magnification, a laser-treated surface is
smoother than others. Interestingly, surfaces with layers deposed
by plasma spraying have similar characteristics, macroroughness
and melting structures.
Plasma spraying and laser treatments are no longer being used,
because the resulting macrorugosities have greater effects on primary stability than secondary stability. It is expected that surface
characteristics exhibit biological influence during implant installation and interaction with cells by modifying the mechanisms
involved in cell adsorption and differentiation.
The osseointegration of the dental implant with plasma-sprayed
HA is faster than uncoated implants. However, studies have
shown that these coatings may be partially dissolved/resorbed
after long periods of function [94] . In addition, the HA coating
is chemically unstable and bonds weakly to the implant surface.
Considering the potential of the association between laser ablation and smaller scale HA coatings to create a stable and bioactive
surface on titanium dental implants, Faeda et al. analyzed the
effects of a surface treatment created by laser-ablation (neodymium-doped yttrium aluminum garnet [Nd:YAG]) and, later, thin
deposition of HA particles by a chemical process [95] . They compared the removal torque of implants treated with laser followed
by acid etching, implants with only laser-ablation and implants
with MS. After 4, 8 and 12 weeks of healing, the removal torque
was measured. Average removal torque in each period was 23.3,
24.0 and 33.9 Ncm to MS, 33.0, 39.9 and 54.6 Ncm to lasermodified surface (LMS), and 55.4, 63.7 and 64.0 Ncm to HA.
The difference was statistically significant (p < 0.05) between
the LMS-MS and HA-MS surfaces in all periods of evaluation,
and between LMS-HA to 4 and 8 weeks of healing. The surface
characterization showed a deep, rough and regular topography
provided by the laser conditioning that was followed by the HA
coating. They conclude that the implants
with laser surface modification associated
with HA biomimetic coating can shorten
the implant healing period by the increase
of bone implant interaction during the first
2 months after implant placement [95] .
20 m

Figure 4. Machined dental implant surface morphology. It is possible to observe

tool irregularities from the machining process.

248

Acid-etched dental implants

Every manufacturer has its own acidetching method regarding concentration,

time and temperature for treating implant
Expert Rev. Med. Devices 7(2), (2010)

Improving osseointegration of dental implants

Review

terms of internal distribution. Atoms located

at the surface are surrounded by a smaller
number of neighbors compared with those
atoms in the inner regions, which increases
the level of atomic energy at the implant
surface. As a result, there is a greater tendency of adsorption of foreign atoms and
molecules. The greater the surface energy
per unit area is, the greater the possibility of
10 m
reactions between body and material. When
5 m
the implant is blasted, its surface suffers plastic microdeformation, in which a layer with
Figure 5. Dental implant surface treated with a laser. It is possible to observe
compressive residual stress is created. Part of
macroroughness and morphology with melting characteristics.
the kinetic energy of the particles is stored in
the form of crystal defects, such as dislocasurfaces. In general, acid treatment is performed by immersing tions, twins and grain boundaries, and these modifications increase
the implants into solutions of HCl + H2SO4, HF + HNO3 and the material surface energy [97] , as well as the possibility of modiHNO3. After acid attack, the implant is again immersed into an fication in the interaction between cells and implant. The residual
aqueous solution of HNO3 for passivation of titanium oxide and stress values obtained from blasting procedures depend on both
formation of a stable oxide layer. An example of the morphology hardness and granulometric distribution of the particles used. The
of an acid-etched surface of a commercially available implant is greater the granulometric distribution, the more heterogeneous the
strain distribution. Although acid treatment after blasting removes
shown in FIGURE 6.
Acid treatment provides homogeneous roughness, increased some atomic layers of the titanium surface deformed by the blasting
active surface area and improved bioadhesion. The morphology procedure, part of the residual strain remains at the implant surface.
Surfaces with Ra equal to 1 m have a good performance [11] .
of the implant surface shown in FIGURE 5 is isotropic and exhibits
micro-cavities with defined edges. This type of surface not only This level of roughness can be obtained by blasting followed by
facilitates retention of osteogenic cells, but also allows them to acid treatment (FIGURE 8) . The blasting procedure allows control
migrate towards the implant surface. Implants having surface mor- of the size of microcavities, but particles may be encrusted and
phology similar to that shown in FIGURE 5 induce fibrin retention, then contaminate the surface of the implant (FIGURE 7B) .The grit
favor adsorption of fibronectin and facilitate osseointegration [96] . blasting or sandblasting technique is normally made with titania
Despite the high success of dental implants with treated sur- or alumina. After the grit blasting procedure, performed particles
faces, complications can occur, such as loss of integration, peri- remain on the surface of implants and must be removed with acid
implantitis and mucositis, prothesis screw loosening and fracture and ultrasonic bath.
The influence of surface roughness on bone formation on titaof the implant itself. FIGURE 7 shows the apical part of a dental
implant fractured 4 years after the surgery. The broken implant nium-blasted surfaces was evaluated [53] . The samples were blasted
was removed surgically and the implant presented acid etching with Al2O3 particles. After surface preparation, the samples were
surface morphology characteristics. The failure occurred after the passivated, washed with distilled water and dried. The results
healing period due to implant overloading. The dental implant from animal experiments showed higher values for removal torque
presented a good osseointegration. Scanning electron microscopy and bone-to-implant contact for samples blasted with 25- and
observations showed, in
n some areas, the presence of organic mate- 75-m sized particles compared with those machined or blasted
with 250-m particles.
rial, which was present directly on the implant surface.
Acid etching yields low surface energy
and reduces the possibility of contamination since no particles are encrusted in the
surface. Among the commercially available acid-treated implants, one can cite the
Master Porous System (Conexo Sistema
de Prteses, Brazil), Osseotite (Biomet 3i,
USA), Friadenty Plus (Friadent GmbH,
Germany), Defcon TSA (Impladent SL,
3 m
Spain) and BlackFix (TitaniumFix, Brazil).
20 m
Blasted implants & etching

The atomic arrangement at the external surface of bulk metallic materials is different in
www.expert-reviews.com

Figure 6. Typical dental implant surface morphologies with acid etching treatment.
Image courtesy of Conexo Sistemas e Proteses, Brazil.

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Elias & Meirelles

25 m

Figure 7. Apical part of broken osseintegrated dental

implant with acid etching treatment. The fracture occurred
4 years after the surgery. It is possible to observe the adhesion of
organic material on the implant surface.

Alumina particles in the size range 2550 m are used to

sandblast the Sand-blasted, Large grit, Acid-etched (SLA)
implant (Straumann ITI, Germany). The sandblasting is followed by an acid etch in hot HCl/H 2SO4 acid solution. These
processes create micropits superimposed on the rough-blasted
surface. The pits have an average diameter of 1 m, and coalesce
to form larger craters with an average diameter of 10 m.
Sandblasting surfaces have Ra equal to 1.19 m and the total
roughness (Rt) equal to 10.53 m. Jarmar et al. measured the
roughness on SLA and Sa and found it to be 1.98 0.08 m [98] .
The dental implant denominate TiOblast (Astra Tech AB,
Sweden) made of commercially pure titanium is another example
of a gritblasted and then acid-etched treated implant. TiOblast
is gritblasted with 25-m titanium oxide particles, which create
small pits of predetermined size and shape.
The OsseoSpeed (Astra Tech AB, Sweden) dental implant
surface is fluoride-modified (hydrofluoric acid-treated surface).
The implant surface is blasted and later etched with diluted
hydrofluoric acid, which slightly reduces the high peaks. The
final surface structure has an isotropic roughness that is, there
is no preferred direction of the surface irregularities [93] . During
the blasting procedure, the surface roughness is increased. The
OsseoSpeed surface has Sa = 0.91 0.14 m and the TiOblast
surface has Sa = 1.12 0.24 m. The hydrofluoric acid treatment does not only change the microstructure, but also the
surface chemistry. According to the authors [93,99] , the surface
fluoride incorporated in the oxide acts as a precipitation site for
calcium and phosphorus, and also allows covalent bonding to
the phosphate to create fluoridated HA and fluorapatite.
Anodized implants

Titanium has a high surface energy following the machining

procedure, which facilitates adsorption of oxygen molecules.
Approximately 10 ns after oxygen adsorption, the molecules
250

dissociate to form the first atomic monolayer of oxygen. The

adsorbed oxygen transforms into titanium oxide within a few
milliseconds. Therefore, direct contact between pure titanium
and the host bone is very unlikely because the presence of the
titanium oxide layer and the properties of titanium oxide are
more important in terms of biocompatibility than those of pure
titanium. Based on this principle, researchers have modified both
the morphology and the crystal structure of the titanium oxide
of the implant surfaces. One of the methods consists of increasing the thickness of the oxide layer by anodization. This can be
achieved by several electrochemical procedures [13,44,100] .
Anodization is an electrochemical process where the implant is
immersed in an electrolyte while a current is applied, which will
make the implant the anode in an electric cell. Commercial dental implants, such as TiUnite (NobelBiocare, Switzland) and
Vulcano Actives (Conexo Sistemas de Prtese, Brazil), are
anozided. The electrolyte and the current used in the implants
treatment process create a porous surface structure (FIGURE 9) .
The high chemical stability and biocompatibility of titanium
are due the formation of titanium oxide on its surface. Titanium
oxide has three crystalline structures: anatase (tetragonal), rutile
(tetragonal) and brookite (orthorhombic) [101] . Crystallinity will
increase as the oxide layer thickness increases. Rutile and anatase
forms are the most important oxide structures for osseointegration
of implants. In addition to the increase in oxide layer thickness,
the titanium oxide film obtained from electrochemical anodization incorporates calcium and phosphorus as a heritage from
the electrolyte. The surface has more than 7% phosphorus in
the oxide layer, the highest percentage of amorphous hydroxides
compared with other implants assessed by x-ray photoelectron
spectroscopy (XPS). As a result, the titanium oxide existing on
the implant surface shows changes in its morphology and crystal
structure [102] .
By characterizing anodized implant surfaces with x-ray diffraction, Raman and XPS, it was found that a predominance of
anatase forms on anodized surfaces compared with MS, where
the rutile form is predominant (FIGURE 9A) . The results showed
that the differences between commercial implants depend on
the method used for surface treatment. Blasted and acid-treated
surfaces exhibit predominantly rutile forms, although their morphologies are different. On the other hand, anodized surfaces
have a predominance of anatase forms (FIGURE 10) and micropores
measuring 0.53.0 m (FIGURE 9) . The XPS spectra indicate that
the chemical composition of the outermost surface oxide layer on
the anodized implant surface contains calcium and phosphorus
electrochemically incorporated from the mixed electrolyte solution during the oxidation process (FIGURE 10B) .
The tissue healing process around anodized or acid etched
implants, inserted in bone sites with and without defects, is
quicker than in machined implants. In order to assess the efficiency of anodized implants, Gurgel el al. used dog teeth, and
3 months after extraction, they produced defects measuring 5 mm
high and 4 mm wide before inserting the implants [103] . The animals were sacrificed 3 months after the implant insertion. The
researchers found that the percentages of bone-to-implant contact
Expert Rev. Med. Devices 7(2), (2010)

Improving osseointegration of dental implants

Review

exhibit an apatite-forming ability and integrate with living bone. The apatite-forming ability of the metal is attributed to the
amorphous sodium titanate that is formed
during the NaOH and heat treatment [106] .
The bioactivity of a material depends especially on the structure and the amount of
functional groups such as amino (NH3)
and hydroxyl (OH) groups. The pres10 m
15 m
ence of hydroxide groups on the surface of
implant materials plays an important role
with respect to biointeraction with bone
Figure 8. Typical titanium dental implant surface sandblasted. (A) Clean surface.
cells and can stimulate cell attachment to
(B) Surface with alumina particle contamination.
the artificial hydroxyl-containing surface.
It was also observed that the basic titanium
and bone density of anodized implants were 57.03 21.86% and hydroxide groups induce apatite nucleation and crystallization
40.86 22.73%, whereas machined implants had 37.39 23.33% in simulated body fluid. Titanium oxides derived using some
and 3.52 4.87%, respectively.
techniques, such as a sol-gel process and treatment of metallic
Sul et al. compared mechanical strength and osseous-con- titanium with H2O2 or alkali, have abundant titanium hydroxide
ductivity of anodized implants containing magnesium, TiUnite groups on the surface, and bone-like apatite is formed on the
(anodized) and Osseotite (double acid attack) [104] . The implants surface. However, the apatite is not biomimetically formed on
were inserted into rabbit tibia, and 36 weeks later removal single crystal titanium oxide (anatase).
torques and the percentage of bone-to-implant contact were
measured. Magnesium implants demonstrated significantly Conclusions
greater removal torque values and more new bone formation Various processes exist to treat the surface of commercially
than Osseotite at 3 and 6 weeks. Magnesium implants also
available implants. Most of these surfaces have been analyzed
showed higher removal torque values at 3 weeks and new bone
by in vivo and in vitro studies, showing high clinical success
formation at 6 weeks than TiUnite. The results indicate that
rates. However, the methodologies used to prepare these sursurface chemistry facilitated more rapid and stronger osseoinfaces are mostly empirical, requiring a great number of assays.
tegration of the magnesium implants. This suggests potential
Moreover, the tests are not standardized and this makes it
advantages of magnesium implants for reducing high implant
difficult to compare the results;
failure rates in the early postimplantation stage and in compromised bone, making it possible to shorten bone healing time The results from in vivo and in vitro studies show that the surface
characteristics of the dental implants influence cell activity;
from surgery to functional loading, and enhancing the possibility
of immediate/early loading. The anodized surface implant has The dental implant surface treatment influences the way cells
a higher polarity compared with that of acid-treated samples,
adhere to the surface, which influences differentiation, prolifwhich causes adsorption of water and molecules. Adsorption of
eration, differentiation and formation of extracellular matrix;
these molecules creates an electric field along the oxide thickness.
This electric field induces titanium oxidation and, at the same
time, the oxide layer thickness increases, thus decreasing both
potential difference and the driving force for dissolution [104] .
In this way, taking into account that surface structure as well
as morphology are correlated with wettability, changes in their
properties affect adsorption of proteins needed for cell adhesion on the implant surface. Consequently, the performance of
a given treated surface depends on the biological response of the
implants used.
Mechanisms of bioactive dental implants

Bioactive materials form bioactive bonding with the living

bone by growing an apatite layer on their surfaces after they are
implanted in the bony site [17,105] . Titanium oxide has a tendency
to adsorb water at the surface, resulting in the formation of titanium hydroxide groups. Experimental results showed that titanium metal and its alloys subjected to NaOH and heat treatments
www.expert-reviews.com

20 m

Figure 9. Anodized dental implant surface morphology.

251

Review

250

30
25
20

+C 1s

0 1s

Ca 2p

35

15
10
5

0
100

200

300 400 500 600

Raman shift cm-1

700

800

P 2s
S1 2s
P 2p
S1 2p
Ca 3p, 0 2s

397

500

637

750

40

T1 2p
Ca 2s

1000

45

C KLL

1250

515

Intensity (a.u.)

1500

0 KLL
Ca LMM

50

Intensity/counts 1000

1750

55

146

2000

Elias & Meirelles

1100 1000 900 800 700 600 500 400 300 200 100

Binding energy/eV

Figure 10. Anodized dental implant spectra. (A) Raman spectrum. (B) x-ray photoelectron spectroscopy spectrum.

Topographic characteristics, roughness, energy and chemical

composition modify cell growth and change cell function at
the initial stages of osseointegration;
Further studies are needed to improve and describe the interaction between cells and implant surfaces, as well as to assess
the influence of different parameters involved, such as proteins, bone formation stimuli and individual therapy, for
compromised patients.
Expert commentary & five-year view

The development of dental implant surfaces over the past years

has improved oral rehabilitation in terms of patient inclusion criteria and overall tissue response. Bone and soft-tissue
responses to dental implants and attached prosthesis have
become more predictable, fulfilling the higher expectations
from the patients and also from the dentists. There is a general
agreement regarding material selection and which elements
should be avoided at the implant surfaces, reducing the possibility of failures, despite the constant increase of inserted dental
implants worldwide.
Current standards for surface characterization of dental
implant-related materials commonly focus on limited surface
properties and evaluation techniques that may not represent what
has really changed on the material surface. A so-called chemical modification, for example, will probably add new structures

on the surface and, at the same time, change the wettability of

the material. These three surface properties (among others) are
known to modify celltissue interactions. Thus, a specific surface
ana lysis protocol could be established, providing guidelines for
future developments.
The recent focus on nano-based modifications has given one
extra alternative to improve tissue response. In addition, the possibility to investigate the celltissue interaction on the nanoscale
will provide results for better understanding the mechanism
behind implant success or failure. At this stage, it is difficult to
determine the ideal size and configuration of the nanostructures
for dental implant surfaces, but preliminary results indicate that
solely the presence of specific nanostructures will improve bone
formation. The clinical follow-up of these modifications will indicate the potential benefits for the patients, with special attention
to tissue preservation and costs.
Financial & competing interests disclosure

The work was financially supported by the Brazilian Government (CNPq

Process 472449/2004-4, 400603/2004-7 e 500126/2003-6 and FAPERJ
Process E-26/151.970/2004). The authors have no other relevant affiliations
or financial involvement with any organization or entity with a financial
interest in or financial conflict with the subject matter or materials discussed
in the manuscript apart from those disclosed.
No writing assistance was utilized in the production of this
manuscript.

Key issues
Titanium dental implant success is increasing because the surgery technique has changed, implant manufacturing improved and implant
surface treatments are used.
Titanium surface treatments change cell activities.
Surface roughness changes the cells behavior.
Dental implant surface treatment is essential to reduce the implant loading time, and for the treatment of patients with a systemic disorder.
To improve the dental implant osseointegration, the surface treatment is the most important procedure.

252

Expert Rev. Med. Devices 7(2), (2010)

Improving osseointegration of dental implants

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Affiliations

Carlos Nelson Elias

Instituto Militar de Engenharia,
Biomaterials Laboratory, Pr. Gen. Tiburcio
80, 22290-270 Rio de Janeiro, RJ, Brazil
Tel.: +55 212 546 7244
elias@ime.eb.br

Luiz Meirelles
Department of Prosthetic Dentistry,
Institute of Odontology and Department of
Biomaterials, Institute of Clinical Science
at the Sahlgrenska Academy, University of
Gothenburg. Medicinaregatan 12, 41390,
Gothenburg, Sweden
luiz.meirelles@odontologi.gu.se

Expert Rev. Med. Devices 7(2), (2010)

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