Int. J. Oral Maxillofac. Surg.

2008; 37: 10321038

doi:10.1016/j.ijom.2008.05.013, available online at http://www.sciencedirect.com

Research Paper
Osteosynthesis

Local effect of titanium implant D. G. Olmedo1, G. Duffo2,

R. L. Cabrini1,3, M. B. Guglielmotti1
1
Department of Oral Pathology, School of

corrosion: an experimental Dentistry, University of Buenos Aires, National

Research Council (CONICET), Marcelo T. de
Alvear 2142 28 A Buenos Aires C1122 AAH,
Argentina; 2Department of Materials, National

study in rats Atomic Energy Commission, National

Research Council (CONICET), Av. Gral. Paz
1499, San Martn (1650), Buenos Aires,
Argentina; 3Department of Oral Pathology,
School of Dentistry, University of Buenos
D. G. Olmedo, G. Duffo, R. L. Cabrini, M. B. Guglielmotti: Local effect of titanium Aires and Department of Radiobiology,
implant corrosion: an experimental study in rats. Int. J. Oral Maxillofac. Surg. 2008; National Atomic Energy Commission, Marcelo
T. de Alvear 2142 28 A Buenos Aires C1122
37: 10321038. # 2008 International Association of Oral and Maxillofacial AAH, Argentina
Surgeons. Published by Elsevier Ltd. All rights reserved.

Abstract. The aim of this study was to evaluate histologically the biological effect of
pitting corrosion and to contribute clinically relevant data on the permanence of
titanium metal structures used in osteosynthesis in the body. Commercially pure
titanium laminar implants (control) and commercially pure titanium laminar
implants with pitting corrosion (experimental) were implanted in the tibiae of rats.
At 14 days post-implantation the animals were killed. The tibiae were resected,
fixed, radiographed and processed for embedding in methyl methacrylate.
Percentage of bone-implant contact and peri-implant bone volume were evaluated.
The histological study of the titanium implants submitted to pitting corrosion
showed scarce boneimplant contact, it was only present in the areas with no pitting
and/or surface alterations. There was a statistically significant lower percentage of
boneimplant contact in the experimental group (6%  4) than in the control group
(26%  6) (p < 0.001). Products of corrosion in the peri-implant bed, especially
Keywords: titanium corrosion; metal ion re-
around the blood vessels and areas of bone marrow in the metaltissue interface,
lease; pitting; macrophage; oral surgery; os-
were observed. The microchemical analysis of corrosion products revealed the teolysis.
presence of titanium. The adverse local effects caused by pitting corrosion suggest
that titanium plates and grids should be used with caution as permanent fixation Accepted for publication 21 May 2008
structures. Available online 7 July 2008

The discovery of relatively inert metals
and alloys has led to the increasingly
widespread use of metal implants in ortho-
pedics and dentistry. Pure titanium and
titanium alloys are the most frequently
used materials for osseointegrated dental
and orthopedic implants because of their
biocompatibility13. Biocompatibility is
attributed to the formation of a protective
layer of titanium dioxide (TiO2) that
avoids direct contact between the implant
and its milieu16. This protective layer
reduces the reactivity of the metal.
Titanium is widely used in implants in
oral and maxillofacial surgery in the form
of grids, plates, screws and distractors.
The use of reduction plates for fractures
of maxillary bones and other bones is
becoming increasingly widespread. The
removal of titanium miniplates following
completion of the process of bone repair is
generally considered unnecessary owing
to the excellent biocompatibility of tita-
nium and its resistance to corrosion. This
is beneficial for the patient who does not
have to undergo surgery again29. Some
authors recommend removal of the mini-
plates only if they cause complications
and in cases of wound dehiscence or infec-
tion29. No metal or alloy is completely

0901-5027/1101032 + 07 $30.00/0 # 2008 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
 Local effect of titanium implant corrosion 1033

inert in vivo. When the implant is placed, a

considerable surface area might initially
be in intimate contact with organic fluids.
The resulting electrochemical processes
lead to corrosion and the release of metal
ions to the milieu14,35.
The in situ degradation of a metal
implant is detrimental because the process
of corrosion alters the structural integrity of
the implant and causes metal ions to be
released that remain in the peri-implant
milieu and/or migrate systemically8,2226.
Some authors therefore claim that titanium
miniplates should be removed, to allow for
physiological bony adaptation and avoid a
foreign body reaction17,21,29,37. The need
for removing titanium miniplates and grids
once bone repair has been completed is a Fig. 1. Experimental titanium implant (pitting corrosion). Scanning electron microscopy image
controversial issue18. showing pits (arrowed) along the surface cracks. 85.
BESSHO et al.4 examined 113 titanium
miniplates that had been retrieved after
miniplate fixation of mandibular fractures, 6  1  0.1 mm (control) (Implant-Vel, (SEM) (Einhoven, The Netherlands).
and identified surface depressions appar- Buenos Aires, Argentina). A further 20 The control laminar implants exhibited a
ently caused by pitting corrosion. Pitting c.p. titanium laminar implants were predominantly smooth surface with irre-
corrosion is a form of localized corrosion in degreased in acetone and placed in an gularities that are characteristic of the
which pits form on the metal surface. It electrolytic cell with a 1M sodium chlor- lamination process. The laminar implants
usually occurs on base metals, which are ide solution at an anodic potential of 15 submitted to the induction of pitting cor-
protected by a film of an oxide or other volts for 1 minute. In this way, implants rosion showed irregular pitting (approxi-
protective surface compound. In the pre- with pitting corrosion (experimental), as mately 100 m in diameter) that usually
sence of certain ions in the environment, evidenced by the circulating high density surrounded surface irregularities such as
such as chlorides, the film breaks down current, were obtained. After the in vitro surface cracks (Fig. 1). Conglomerates of
locally and rapid dissolution of the under- corrosion process, the samples were suc- titanium oxide were observed at the bot-
lying metal occurs in the form of pits5,10. cessively washed with tap water, deio- tom of the irregular pits (Fig. 2).
ZAFFE et al.38 evaluated the pre- and post- nized water, ethyl alcohol and acetone,
implantation surface features and surface then dried with hot air. The control group
Surgical procedure
alterations of titanium grids and plates in was treated in the same way. This proce-
patients. They reported the presence of pit- dure guarantees the removal of potential The animals were anesthetized intraperi-
ting on the surface of one of the grids among surface contaminants that might affect a toneally with a solution of 8 mg ketamine
other alterations. biological response. chlorhydrate (Fort Dodge1 - Argentina)
The aim of the present study was to The sample surfaces (control and and 1.28 mg xylazine (Bayer Argentina
evaluate histologically the biological experimental) were examined in a 515 S.A.) per 100 g body weight. The skin
effect of pitting corrosion in the peri- Philips scanning electron microscope of both tibiae was shaved before a
implant milieu in rat tibiae. The results
will contribute clinically useful data on the
permanence of titanium metal structures
used in osteosynthesis in the body.

Materials and methods

Experimental animals
Throughout, 20 male Wistar rats, 90 g body
weight were used; they were fed ad libitum.
The guidelines of the National Institute of
Health (NIH) (NIH Publication No 85-23,
Rev. 1985) and the Statement of Ethics
Principles of the Faculty of Dentistry, Uni-
versity of Buenos Aires (Res (CD) 352/02 y
Res (CD) 694/02) for the use and care of
laboratory animals were observed.

Laminar implants
Fig. 2. Experimental titanium implant (pitting corrosion). Scanning electron microscopy image
The authors used 20 commercially pure of a growing pit. The bottom of the pit is irregular and contains conglomerates of titanium
(c.p.) titanium laminar implants of oxides. 640.
1034 Olmedo et al.

1.5 cm incision was made along the tibial

crest. The subcutaneous tissue, muscles
and ligaments were dissected to expose
the lateral external surface of the diaphy-
seal bone. An end-cutting bur was used to
drill a hole 1.5 mm in diameter with man-
ual rotating movements to avoid over-
heating and necrosis of the bone tissue7.
No cooling with NaCl was required. A
titanium laminar implant previously sub-
mitted to pitting corrosion was placed in
the hematopoietic bone marrow compart-
ment of the right tibia (experimental
group). A control titanium laminar
implant was placed in the left tibia (con-
trol group). A separate-stitch suture was
performed. No antibiotic therapy was
administered. At 14 days post-implanta- Fig. 3. Control: 14 days post-implantation. Ground section. The presence of lamellar bone in
tion the animals were killed by ether over- close contact with the titanium implant surface (boneimplant contact) is observed (toluidine
blue 1%; original magnification 400).
dose, the tibiae were resected, fixed in
formalin and radiographed. At 14 days
post-implantation the experimental of the implant and the percentage involved the implant was evaluated (peri-implant
model employed in the present study in direct bone-to-implant contact were bone volume). Statistical analysis was
exhibits unequivocal evidence of peri- determined (percentage of bone implant performed using Students t-test
implant laminar bone tissue formation contact). The total volume of bone around (P < 0.05).
7,11,28
.

Histological processing
The tibiae were processed for embedding
in methyl methacrylate, and sectioned
with a saw at the level of the metal implant
to obtain 3 cross-sections transversal to the
central long axis of the tibia. The sections
were ground with a polishing machine and
completed manually with sandpaper.
Fifty-micrometer sections were stained
with 1% toluidine blue to allow for ade-
quate observation and identification/dis-
crimination of the tissues (bone and
bone marrow), in particular at the
metaltissue interface, an area of particu-
lar relevance in terms of histomorpho-
metric evaluation.

Microchemical analysis
The peri-implant products of corrosion
were chemically identified by energy dis-
persive X-ray spectrometry (EDX) in a
515 Philips SEM (Einhoven, The Nether-
lands) equipped with an EDX system
(EDAX Falcon PV 8200 [3.0], Mahwah,
NJ).

Histomorphometric analysis
Histomorphometric determinations were
performed on sections using a light micro-
scope (Zeiss Axioscop 2 MOP, Carl Zeiss,
Jena, Germany) at 160 magnification, on
line with an image analysis system (Kon- Fig. 4. Experimental: 14 days post-implantation. Ground section. Note the presence of products
tron KS300 v. 2, Kontron Elektronik, of corrosion (arrowed) in the bone marrow between the implant surface and the bone tissue
Munich, Germany). The total perimeter (toluidine blue 1%; original magnification 400).
 Local effect of titanium implant corrosion 1035

Results
Animals
No immediate or intermediate postopera-
tive complications were observed in any of
the control or experimental animals.

Histological study
The histological analysis of the control
animals revealed the presence of large
areas of lamellar bone in close contact
with the metal surface (boneimplant con-
tact) (Fig. 3). In other areas the bone tissue
was separated from the metal implant by
bone marrow. None of the animals exhib-
ited an inflammatory response.
The histological study of the implants
submitted to pitting corrosion revealed
scarce boneimplant contact, only present
in the areas with no pitting and/or surface
alterations. Peri-implant products of cor-
rosion and large areas of bone marrow
were observed in the metaltissue inter-
face (Fig. 4). The surface of the metal
implants was irregular, with uneven and
indented edges. Crystalline-like structures
were occasionally found on the surface
(Fig. 5). The position of the corrosion
products in the bone marrow, migrating
and surrounding peri-implant blood ves-
sels, is noteworthy (Fig. 6).

Microchemical analysis
The chemical analysis of the crystalline-
like products (EDX) in the peri-implant
milieu revealed the presence of titanium in
the spectrum (Fig. 7). Given the con-
straints of the technique (EDX), the
authors failed to detect C, O or N. It
was not possible to identify the type of
titanium compound present. The Au peaks
corresponded to the metal employed for
sample coating.
Histomorphometric study
The histomorphometric study revealed a
statistically significant lower percentage
of boneimplant contact in the experimen-
tal group (6%  4) than in the control
group (26%  6) (p < 0.001). No statisti-
cally significant differences in peri-
Table 1. Histomorphometric study of peri-implant bone
Histomorphometric Parameters Control n:20 x
Bone-implant contact (%)
Peri-implant bone volume (cm2*)
: standard deviation.
n.s: statistically not significant.
x : mean.
*
projection values. Magnification 160.
Fig. 5. Experimental: 14 days post-implantation. Higher magnification of Fig. 4. Note the
crystalline-like structures scattered in the bone marrow of the interface corresponding to
corrosion products (arrowed) (toluidine blue 1%; original magnification 1000).
implant bone tissue volume were found fixation, but they failed to assess the pre-
between the control and experimental sence of pitting corrosion on the mini-
groups (10  2 cm2 and 8  3 cm2, pro- plates before implantation. This is a
jection values) (Table 1). process that may occur in vivo over long
periods of time. Within this context, ZAFFE
et al.38 demonstrated that the surface of
titanium grids from patients 6 months
Discussion
post-implantation had been modified by
Corrosion of the metals used to manufac- corrosion. They showed how a fragment
ture implants is an issue of great relevance at the cut end of a grid was reduced in
in the science of biomaterials. The present thickness, its edge rounded, the flat surface
study describes the histological evaluation no longer smooth but uneven and pitted38.
of the effect of titanium pitting corrosion The experimental model used in the
in the peri-implant milieu. present study is a suitable method to study
BESSHO et al.4 detected pitting corrosion newly formed bone around laminar
on titanium miniplates used for fracture implants under local and/or systemic con-
ditions7,1113,28.
Pitting corrosion produces local attack,
Experimental n:20 x p especially on isolated spots of the pro-
26  6 64 <0.001 tected metal surface, propagating into
10  2 83 n.s. the metal. Craters, pits, surface cracks
and depressions may appear during the
preparation of the sheets used to manu-
facture miniplates18, and be potential sites
for the initiation of corrosion. The authors
1036 Olmedo et al.
Fig. 6. Experimental: 14 days post-implantation. Note the presence of a blood vessel in the bone
marrow near the implant surface and products of corrosion (arrowed) in the vicinity (original
magnification 1000).
observed by SEM the initiation of pitting
in areas with surface cracks. Titanium
exhibits the greatest resistance to general-
ized corrosion, pitting corrosion and cre-
vice corrosion compared with other metals
or alloys, such as stainless steel or chro-
mium cobalt, used in oral surgery18. Cre-
vice corrosion is a form of local corrosion
Fig. 7. EDX spectrum evidencing the titanium content of the particles found around the
implants.
that results from differences in oxygen
concentration of electrolytes or changes
in pH in a confined space, such as the
crevices between a screw and a plate6,10.
The severity of corrosion and the quantity
of corrosion products released may
depend on the susceptibility to corrosion
of the implant material, and on the tissue
response to the implant and to the surgical
procedures used during implantation20.
In the present study, corrosion was
induced artificially in the plates in condi-
tions that exceed the aggressiveness of the
biological microenvironment the metal
structure would be exposed to in vivo.
The aim was to study the effect of surface
changes of treated plates on biological
response rather than the effect of the che-
mical changes that occur locally during
the propagation of pitting corrosion.
The authors observed the presence of
corrosion products histologically around
the implant, both free or phagocytosed by
macrophages. In some cases the products
of corrosion were found around the blood
vessels, in keeping with the findings of
MEACHIM and WILLIAMS19 and TORGERSEN
et al.33, in a histological study of soft
tissue adjacent to titanium implants. The
observation of metal particles located
intracellularly or in association with ves-
sels may represent a biological response
aimed at eliminating the foreign mate-
rial19,30,32.
The implants submitted to pitting corro-
sion and the control implants were sub-
mitted to different lavages before
implantation in vivo to guarantee the
removal of potential surface contaminants
that might affect the biological response.
The implants submitted to pitting corro-
sion exhibited a significantly smaller per-
centage of boneimplant contact than
control implants. Boneimplant contact
was only observed in areas with no pitting
and/or surface alterations. Boneimplant
contact was not observed in areas with
pitting in any of the cases. Although a
layer of oxide is formed spontaneously
when the plate is exposed to air after
pitting corrosion, the absence of bone
implant contact might be associated with
a change in the chemical composition and/
or structure (e.g. crystallography) of the
oxide grown on the pit surface. Further
studies are warranted to address this issue.
The presence of particulate corrosion and
wear products in the tissue surrounding the
implant may ultimately result in a cascade
of events leading to periprosthetic bone
loss15,34.
The properties and quality of the
implant material, the shape of the implant
and the handling and surgical procedure
are of crucial importance for an optimal
biological performance of any implant
device. Unstable conditions in the fracture
area after osteosynthesis lead to continu-
ous fretting at the screwplate interface.
Removal of the protective surface oxide
and oxygen depletion in the crevices
between plate and screws increase the risk

of both crevice corrosion and fretting
attack36. It is speculated that increased
mechanical stability during healing may
reduce the fretting component, and
thereby the corrosion.
Titanium dioxide is generally consid-
ered to be of low toxicity, although its
metabolism and biological behaviour are
not clearly understood21,29. The formation
of metal particles increases the surface
area available for oxidation and ion
release9,27. Owing to the lack of consistent
information on the long-term effects of
metal implants on the human body, an
international study group has suggested
that all non-functional implants should
be evaluated for removal31,32.
The present study shows that the surface
changes induced by artificial pitting cor-
rosion caused a reduction in bone apposi-
tion. Particles were found in peri-implant
tissues. The release of particles from the
metal structure of the implant to the sur-
rounding biological compartment, their
biodistribution in the organism and their
final destination are issues that lie at the
center of studies of biocompatibility and
biokinetics.
The adverse local effects caused by
pitting corrosion observed in the present
study suggest caution in the use of tita-
nium plates and grids as permanent fixa-
tion structures. These data must also be
considered in orthopedic reconstructions
and fixations. The risk of clinical compli-
cations related to corrosion of implants in
place today must be understood and
requires further study.
Acknowledgements. This study was sup-
ported by Grants: BID 1728/OC-AR -
PICT 33493 from the National Agency
for the Promotion of Science and Tech-
nology, O-020 from University of Buenos
Aires, CONICET PIP 6042 and Roem-
mers Foundation, Argentina.
Grants: BID 1728/OC-AR - PICT
33493 from the National Agency for the
Promotion of Science and Technology, O-
020 from University of Buenos Aires,
CONICET PIP 6042 and Roemmers Foun-
dation, Argentina.
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