You are on page 1of 10

Surface Analysis of Failed Oral Titanium Implants

Marco Esposito,1,2 Jukka Lausmaa,3 Jan–M. Hirsch,2,4 Peter Thomsen1


1
Institute of Anatomy and Cell Biology, Göteborg University, Göteborg, Sweden

2
Department of Oral and Maxillofacial Surgery, Uppsala University Hospital, Uppsala, Sweden

3
Department of Chemistry and Materials Technology, Swedish National Testing and Research Institute SP, Borås, Sweden

4
Department of Oral and Maxillofacial Surgery, Göteborg University, Göteborg, Sweden

Received 18 February 1998; revised 25 August 1998; accepted 5 October 1998

Abstract: The aim of the present study was to investigate the surface topography, compo-
sition, and oxide thickness of consecutively failed, oral Brånemark implants in order to
determine possible causes for failure. The failure criterion was lack of osseointegration
manifested as implant mobility. Ten implants were retrieved before loading (early failures)
and 12 during a period of function up to 8 years (late failures). At retrieval, early losses did
not display any clinical sign of infection. All late failures were radiographically characterized
by peri-implant radiolucency and did not show infectious signs with one exception. No implant
seemed to be lost due to peri-implantitis (plaque-induced progressive marginal bone loss).
Twelve implants were analyzed by scanning electron microscopy (SEM), Auger electron
spectroscopy (AES), and depth profiling using a blind protocol. Two pristine fixtures, which
underwent the same preparation as the failed implants, were used as controls. In the SEM,
control samples were essentially free from macroscopic contamination, whereas failed im-
plants contained varying amounts of tissue residues. AES showed that all surfaces consisted of
Ti oxide and varying amounts of additional elements, with C dominating in most cases.
Nitrogen and sometimes Na, Ca, P, Cl, S, and Si were detected. The Si contamination was most
likely due to ion leaching from the glass vials used for storage. Depth profiles showed a typical
oxide thickness of 5– 8 nm for all samples. In conclusion, no significant changes in the oxide
layer composition or thickness as a result of implantation were observed. The results do not
indicate any material-related cause for the failures of these implants. Possible reasons for these
failures were impaired healing, asymptomatic infection, and overload. © 1999 John Wiley & Sons,
Inc. J Biomed Mater Res (Appl Biomater) 48: 559 –568, 1999

Keywords: dental implants; surface spectroscopy; medical device failure; osseointegration;


titanium

INTRODUCTION covered by a carbon-dominated contamination layer and trace


amounts of N, Ca, P, Cl, S, Na and Si.7,8
Based on the predictable results obtained by commercially pure Several authors have underscored the importance of
titanium (CP Ti) implants ad modum Brånemark,1–5 the reha- implant surface cleanliness. For instance, it has been re-
bilitation of edentulous patients with implants according to the ported that a small amount of fluorine contamination can
osseointegration concept is an accepted and expanding treatment dramatically alter the surface oxide of Ti implants during
modality. The integration of Ti implants in bone has been partly autoclaving.9 It has been hypothesized that surface con-
ascribed to the biocompatibility of the surface oxide layer.6 The taminants may be released from the implant surface, en-
surface of Ti consists of a thin (2–6 nm) oxide (mainly TiO2) hancing and perpetuating the inflammatory response, thus
altering the healing process and possibly provoking the
dissolution of Ti.10 –21 It has also been suggested that
Correspondence to: M. Esposito, Institute of Anatomy and Cell Biology, Göteborg single monolayers of contaminants from the environment
University, Box 420, SE-405 30 Göteborg, Sweden
Contract grant sponsor: Swedish Medical Research Council; contract grant number:
or bulk material can invalidate the utility of implants.22 It
9495 is, therefore, possible that some early implant failures
Contract grant sponsors: National Research Council of Italy (CNR); Einar and
Greta Asker Foundation; C. M. Lerici Foundation; Hjalmar Svensson Foundation; (when osseointegration fails to occur) may be caused by
Faculty of Medicine and the Faculty of Odontology, Göteborg University, Sweden the presence of contaminants on the implant surface,
© 1999 John Wiley & Sons, Inc. CCC 0021-9304/99/040559-10 whereas some late losses (when the achieved osseointe-
559
560 ESPOSITO ET AL.

TABLE I. Clinical Data of Patients with Failed Implants


Implant Positiond
Patient Implant Length and Primary Resorption Anatomy Implantation Possible Reason for Failure
Sample Datac and Diameter Stability and Bone Qualitye Time Patient’s Notes and Symptoms

Aa 46 m 7 mm L2 maxilla C T(6) 8 years Bruxist Overload


3.75 mm good 3 pain at percussion

B 48 m 13 mm L3 maxilla E T(7) 8 monthsf Bone graft Impaired healing


3.75 mm bad 4 Le Fort I pain at percussion

C — 10 mm — — 0 (control) — —
3.75 mm

D1 60 m 18 mm R1 maxilla E T(2) 18 months Overdenture Overload


3.75 mm good 3 pain at percussion

D2 18 mm L1 maxilla E 18 months Overdenture Overload


3.75 mm good 4 pain at percussion

Eb 77 m 15 mm L3 maxilla B T(6) 8 monthsf — Impaired healing


3.75 mm good 4 —

F1 56 m 10 mm L4 maxilla E T(7) 16 months Bone graft Overload/impaired healing


4 mm optimal 4 sinus lift pain at percussion

F2a 15 mm R3 maxilla E 16 months Bone graft Overload/impaired healing


3.75 mm optimal 4 sinus lift pain at percussion

F3a 13 mm R2 maxilla E 16 months Bone graft Overload/impaired healing


3.75 mm optimal 4 sinus lift pain at percussion

F4a 10 mm R1 maxilla E 16 months Bone graft Overload/impaired healing


3.75 mm optimal 4 nasal lift pain at percussion

F5 10 mm L1 maxilla E 18 months Bone graft Overload/impaired healing


3.75 mm optimal 4 nasal lift pain at percussion

F6 15 mm L2 maxilla E 18 months Bone graft Overload/impaired healing


3.75 mm optimal 4 nasal lift pain at percussion

F7 15 mm L3 maxilla E 18 months Bone graft Overload/impaired healing


3.75 mm optimal 4 sinus lift pain at percussion

G 54 f 10 mm R2 maxilla C T(6) 6 monthsg Thin bone Impaired healing


3.75 mm good 2 use of barrier pain at percussion

H 76 m 18 mm R2 mandible B T(5) 3 monthsf — Impaired healing/iatrogenic


3.75 mm optimal 3 —

I — 10 mm — — 0 (control) — —
3.75 mm

J1 68 m 13 mm R3 maxilla E T(6) 10 monthsf Bone graft Impaired healing/iatrogenic


3.75 mm bad 3 buccal onlay —

J2 10 mm L1 maxilla E 10 monthsf Bone graft Impaired healing/iatrogenic


3.75 mm bad 3 nasal lift —

(continued)

gration is lost after many years of function), could be due radicals liberated by cells undergoing metabolic processes
to progressive dissolution of Ti over time. at the interface.24,26 –28 These oxidative processes could be
It has been reported that, after implantation, a continu- responsible for the release of Ti ions (indeed negligible)
ous oxide growth occurs over the years (from 50 Å before observed in vivo29,30 and were considered to be indicative
implantation up to 2000 Å, after 6 years of function).23 of biological activity of Ti.23,26 –28
These preliminary findings were confirmed by others.24,25 Based on in vitro observations, it has also been hypothesized
According to Eliades,26 who referred to other studies, the that hydrogen peroxide (H2O2) released during an inflammatory
highest rate of oxide growth was found in areas of the process may react with the Ti surface, thus forming a Ti-
implant located in the bone marrow, whereas the lowest gel.28,31,32 The formation of this gel was suggested to be related
rate was observed in cortical bone. It has been hypothe- to the extensive oxide growth observed in vivo24 and was con-
sized that the oxide growth could be induced by oxidizing sidered to be an important factor for the biocompatibility of Ti.
SURFACE ANALYSIS OF FAILED ORAL TITANIUM IMPALNTS 561

TABLE I. (continued)
Implant Positiond
Patient Implant Length and Primary Resorption Anatomy Implantation Possible Reason for Failure
Sample Datac and Diameter Stability and Bone Qualitye Time Patient’s Notes and Symptoms

K 70 f 13 mm R1 maxilla E T(8) 12 monthsf — Impaired healing/iatrogenic


3.75 mm bad 3 —

La 52 m 10 mm R1 maxilla C P(3) 3 years — Overload


3.75 mm good 3 pain at percussion

M 37 m 15 mm L1 mandible B P(5) 8 months — Overload


3.75 mm optimal 2 pain at percussion

N 54 f 15 mm L3 maxilla B T(6) 6 monthsf — Impaired healing


3.75 mm good 3 —

O1 70 f 15 mm R2 maxilla B T(6) 6 monthsf — Impaired healing


3.75 mm good 4 —

O2a 15 mm R1 maxilla B T(6) 6 monthsf — Impaired healing


3.75 mm good 4 —
a
Implant accidentally dropped on the surgical sheet.
b
Implant handled with surgical gloves.
c
Age at implant installation; m ! male; f ! female.
d
R ! right; L ! left; 1, 2, 3, respectively ! mesial, medial and distal implant.
e
Jaw shape and quality39: A ! most of the alveolar ridge is present; B ! moderate residual jaw resorption; C ! only basal bone remains; D ! some resorption of the basal
bone has occurred; E ! extreme resorption of the basal bone; 1 ! almost the entire jaw is composed of homogeneous compact bone; 2 ! a thick layer of compact bone surrounds
a core of dense trabecular bone; 3 ! a thin layer of cortical bone surrounds a core of dense trabecular bone of favorable strength; 4 ! a thin layer of cortical bone surrounds a core
of low density trabecular bone of poor strength; T ! total and P ! partial edentulous, in parenthesis the total number of inserted implants.
f
Removed at abutment connection.
g
Removed 2 weeks after abutment connection.
Patient B lost another implant at the abutment connection which was accidentally lost.
Patient D (diabetes, high blood pressure and by-pass) refused bone grafting, therefore only 2 implants could be placed in the canine areas to support an overdenture. Two weeks
after the operation, dehiscences developed around both implants, which healed 2 weeks later. This complication was related to diabetes.
Patient F (2 heart attacks, high blood pressure and heavy smoker) was bone grafted and lost all implants (11) already twice.
Patient K (ankylosing spondylitis and high blood pressure) was bone grafted in the sinus and nasal cavity; however, the failed implant was not in graft.
Patient L was bone grafted in the sinus, but the failed implant was not in the graft. The provisional reconstruction fractured in the middle and the implant holding a cantilever
unit failed.

On the other hand, experimental and clinical studies have of Ti flame-sprayed IMZ implants was reported 1 year after
yielded contradictory results both in terms of surface contam- installation.36
ination and oxide growth. In fact, it was reported that, in The purpose of the present study was to analyze the
some of the early animal experiments, when the implant surface properties of consecutively retrieved Brånemark im-
surface was not chemically cleaned, there was a black or plants in order to determine the possible role of surface
grayish slight discoloration of the tissue adjacent the abut- contamination and oxide growth for the failure of Ti im-
ment.33 However, no relationship with implant losses was plants.
reported. Ameen et al.34 analyzed CP Ti plates as received
from the manufacturer. After “handling contamination” with
stainless steel tweezers, no obvious change in the surface MATERIALS AND METHODS
chemistry was detected. Thus, the authors questioned the
validity of rigorous protocols in handling Ti implants, and CP Ti implants (Brånemark System, Nobel Biocare AB,
concluded that the biological relevance of surface contami- Göteborg, Sweden) were inserted at the Department of Oral
nants for osseointegration (if any) could only be speculated and Maxillofacial Surgery, Uppsala University Hospital,
upon. Another experimental investigation21 did not demon- Sweden (with the exception of sample G), to support fixed
strate any statistical difference in bony contact between bio- prostheses according to the general principles given by Adell
logically contaminated implants and standard controls. How- et al.37 in partially and totally edentulous patients. Bone
ever, it was still recommended to avoid soft tissue contami- grafting procedures were implemented when the available
nation of implants in the clinical situation. bone volume was insufficient. After connection of the supra-
The chemical composition of 11 failed Brånemark fix- structure, patients were checked at 6 months, 1 year, and
tures, after cleaning and autoclaving, has previously been thereafter annually. Periodical radiographs were taken after
investigated.35 No substantial oxide thickness increase was fitting the suprastructure, at the 1, 3, and 5 year controls using
found (both test and control samples had an oxide thickness a standardized method with the parallel, long-cone tech-
in the range of 10 nm). In addition, reduced oxide thickness nique.38
562 ESPOSITO ET AL.

Patient and Implant Characteristics Methods of Surface Analysis

The criterion for implant removal was lack of osseointegra- Two control and 12 retrieved samples were analyzed with a
tion recorded as the slightest mobility tested by rotating scanning Auger microprobe (SAM, Physical Electronics, PHI
and/or moving every implant back and forward using instru- 660, USA), with facilities for scanning electron microscopy
ments. All fixtures were checked for mobility at abutment (SEM) and Auger electron spectroscopy (AES). SEM was
connection and at each visit before bridge insertion. How- used to investigate the implant surfaces with respect to sur-
ever, once the bridge was fitted, it was not removed unless face topography and the possible presence of macroscopic
radiographs showed peri-implant radiolucency or excessive films or particulates and also for selecting areas for AES
marginal bone loss. The implants were in such cases tested analysis. Auger survey spectra (30 –1030 eV) were acquired
for mobility. No implant had to be removed for progressive from at least 2 different locations on each sample. The
marginal bone loss during the study period (October 1996 – analysis areas were selected either at the tip, flank, or bottom
April 1997). All the retrieved implants were mobile and were of threads, the neck or the cylindrical portion of the implant,
surrounded by a radiolucent line on radiographs. Twenty-two or the apical cone (see Fig. 1). All survey spectra were
failed implants were consecutively removed from 13 patients measured using a beam energy of 5.0 keV, beam currents
(Table I). The mobile implants were retrieved under local around 200 nA, and a CMA resolution of 0.6%. The electron
anesthesia by gently unscrewing them with stainless steel beam was defocused to a diameter of 200 !m, which was the
forceps, which were carefully positioned on the cover screw survey analysis spot size. The survey spectra were evaluated
or on the abutment in order to avoid any possible contami- semi-quantitatively, by noting the relative peak heights of the
nation of the implant surface. The implants were rinsed with detected elements and dividing these into 3 different levels
sterile physiological saline (NaCl) solution and were imme- (see legend of Table II).
diately immersed in such a solution contained in plastic vials Overlayer thicknesses (organic films and surface oxide)
used for transporting tissue samples for histopathologic ex- were measured by depth profiling, using 1.5 keV argon ions
amination. Special care was taken to avoid any possible for sputtering. Alternating sputtering and analysis cycles
source of contamination. However, in 6 cases the implant (0.25 or 0.5 min of sputtering per cycle) were used. To ensure
dropped accidentally on the surgical sheet and, in one case, a uniform and reproducible sputter rate and to minimize
the implant was touched with gloves (Table I). The implant artifacts due to sample geometry and surface roughness, the
sites were carefully curetted from remaining soft tissue and analyzing electron beam was focused to 0.5 !m and posi-
flaps raised to achieve primary closure. tioned at an appropriate area on the sample, over which the
The failed implants were retrieved after an insertion time ion beam was rastered (1.5 " 1.5 mm2). Prior to each series
ranging from 3 months up to 8 years. The implants had of analyses, the sputtering rate was calibrated against anod-
different lengths (from 7–18 mm). Twelve fixtures had been ized Ti samples with known oxide (TiO2) thicknesses. Typ-
placed in bone of poor density (type 4)39 and 13 in extremely ical sputter rates for TiO2 were around 5 nm/min. The oxide
resorbed maxillas (type E).39 The majority of the losses (20) thickness was defined as the depth at which the oxygen signal
occurred in maxillas of totally edentulous (9) or bone grafted had decreased to 50% of that at the oxide surface. In those
patients (10). Pain at percussion was experienced at 14 sites. cases where a thick carbon overlayer was present, the thick-
With the exception of patient L, no signs of infection such as ness of the latter was subtracted.
marginal mucosal swelling, redness, or suppuration were
present at retrieval. In patient L, abundant plaque accumula-
tion, redness, and marked bleeding tendency were observed at RESULTS
the failed implant site.
Surface Composition

In the SEM, the control samples were essentially free from


Sample Preparation macroscopic contamination. Different degrees of organic res-
idues, appearing mainly as dark stains, were detected on most
The failed implants were immediately inspected for macro- of the retrieved samples (Figs. 2 and 3). The surface topog-
scopic soft tissue remnants, which were carefully removed raphy was dominated by grooves and ridges along the ma-
using CP Ti tweezers. All retrieved implants and 2 nonim- chining direction and appeared essentially unchanged on the
planted controls were ultrasonically cleaned, separately, for retrieved samples, as compared to the controls.
10 min in clean glass containers filled with sterile saline. No The AES analyses showed that all surfaces consisted of Ti
macroscopic contamination or discoloration was visible to the oxide, with varying amounts of additional elements. Table II
naked eye after this procedure. The failed and the 2 control gives the relative amounts, in 3 different levels, of the ele-
implants were placed in clean and sterile plastic or glass vials ments (except Ti and O) that were detected. All control
(for details see Table II), filled with saline solution. There- implants showed clear Ti signals, while for the retrieved
after, all vials were labeled with a code number and stored in samples only weak or no Ti signals were detected at the
a refrigerator prior to mail postage to the surface analyst, who outermost surface. Carbon was the dominant signal in the
did not have access to any clinical information. AES spectra for most cases. O, N, and sometimes Ca, P, Cl
SURFACE ANALYSIS OF FAILED ORAL TITANIUM IMPALNTS 563

TABLE II. Results from Surface Analyses of Retrieved Implants

Samplea Packaging Material Analysis Locationb Contaminantsc dox (nm)d SEM Observations and Other Notes
A Glass B1 C Na Cl Ca P (Si) Organic film on cylinder
6 weeks B2 C Na Cl (P) (Ca)
T2 C (Ca) (P) (S)
F2 C (Ca) (P) (S) (Na) (Cl)
Cyl C (Ca) (P) (S)
Cyl C Ca (P) (S) Analysis of bright stain
Cyl C N O (S) Analysis of dark stain
T2 6
B Glass B1 C Cl (P) (Si) Films on threads
3 weeks B3 C Cl (P) (Si)
T1 C Si (P)
T2 C Si (P) (Ca)
F1 C (Cl) (P) (Si) (S)
Cyl C Si P (Cl) Analysis of dark area
Cyl C Na Cl P Si Analysis of bright area
T3 C NO Analysis of dark area
T3 6
Cyl 6
C Glass T1 C Si (Cl) (Ca) No macroscopic contamination
Control T3 C Si
3 weeks B1 C Si Na Cl Ca (P)
B3 C Si Na Cl Ca (P)
T4 C Si Na Cl Ca
T3 6–7
T8 6–7
D1 Glass F2 C Si Cl S Thick films on threads
3 weeks T6 C Si Cl S
B2 C N O Na Cl S (Si) No Ti detected
T3 #15 Carbon overlayer
T8 #10 Carbon overlayer
E Glass B1 C Si Mg Na Cl Ca
36 weeks B2 C Si Mg Na Cl Ca
T3 C Si Mg Na Cl Ca
Cyl 7–8
T6 8–11 Carbon overlayer
F1 Glass B1 C Si Ca Na Cl Patchy surface
32 weeks B3 C Si Ca Cl (P)
T5 C Si Ca
T12 C Si S Na (Mg)
T5 5
F6 Plastic B1 C Cl Na P (Ca) (Si) No films, stains or particulates
36 weeks B4 C Cl Na P
T5 C Cl P (Si)
T7 C Cl P
T2 6
T7 6
F7 Plastic T3 C Cl Na P Bright stains, dark films on cylinder
36 weeks T6 C Cl Na P
B5 C Cl Na P (Si)
Cyl C N Na Cl Analysis of dark film
T2 6
T8 6
(continued)
564 ESPOSITO ET AL.

TABLE II. (continued)

Samplea Packaging Material Analysis Locationb Contaminantsc dox (nm)d SEM Observations and Other Notes

I Glass B1 C Na Cl Si Ca (P) (F) Drying stains, no films


Control B3 C Na Cl Si Ca P F
31 weeks T4 C Si Na Cl Ca P F
T5 C Na Cl Si Ca P F Analysis of drying stain
Cyl 5
T5 7
J1 Plastic B1 C (Na) (Cl) (Si) (Ca) (P) (F) Dark films
29 weeks B4 C (Na) (Cl) (S) (P)
T4 C (Si) (Cl) (P)
T3 C N O Cl S Analysis of dark film
Cyl 5
T5 5
K Plastic B2 C Na Cl (S) Dark films
29 weeks B4 C Na Cl P
T5 C Na Cl (Ca)
T5 C N Cl S Analysis of dark film
Cyl 7
T5 7
L Plastic B2 C S P (Ca) (Na) (Cl) Patchy surface, dark films
26 weeks B4 C Ca P S (Na) (Cl)
T4 C Ca P S (Na) (Cl)
T6 C Ca P (S)
Cone 5
T4 7
M Plastic B3 C Ca P Na Cl (S) No macroscopic contamination
20 weeks B5 C Ca P (S) (Na) (Cl)
T6 C Ca P (Si) (Na) (Cl)
Cyl 7–8
T3 7
T6 7
O1 Plastic B2 C Ca S P (Cl) No macroscopic contamination
18 weeks B5 C Ca P (S)
T4 C Ca P (S)
T2 7
T7 5–6
a
Time elapsed between retrieval and analysis (storage time).
b
Denotes the location on the implant where analysis was performed (B1 ! bottom of 1st thread; T2 ! tip of 2nd thread; etc.; F ! flank; Cyl ! cylindrical part of fixture; etc.;
see also Fig. 1).
c
Elements (except Ti and O) that were detected. Dominant elements ($10%) are written in bold type, intermediate levels (# 1–10%) in normal type, and trace amounts (%1%)
in parentheses.
d
Surface oxide thicknesses, based on depth at which oxygen signal has decreased to 50% of intensity at oxide surface and assuming sputtering rate calibrated against TiO2.

Na, S, and Si were detected in the organic overlayers. The D1 and E for which overlayer thicknesses up to 15 nm were
main difference in surface composition between the retrieved measured. However, both these samples were characterized
implants and the controls was that the former had signifi- by significant organic overlayers, which led to depth profile
cantly higher amounts of C at the surface. The only exception broadening and over-estimates of the oxide thickness.
was sample E, which displayed an unusual Mg contamina-
tion. As can be observed in Table II, the high Si levels are
strongly correlated to the material (glass) used for storing the DISCUSSION
implants prior to analysis.
Surface analysis investigations of failed implants have the
Surface Oxide Thickness Measurements
advantage that they do not provoke any additional discomfort
The depth profiles showed typical oxide thicknesses of 5– 8 for the patients in contrast to histological studies, where, in
nm for all samples (Table II), with the exception of samples order to obtain useful information, an adequate amount of
SURFACE ANALYSIS OF FAILED ORAL TITANIUM IMPALNTS 565

Figure 3. SEM micrograph of implant D1 showing an area with


pronounced organic residues (dark areas). The bright areas represent
parts of the surface with less organic material. Scale bar ! 500 !m.

ferred to other similar techniques such as XPS (X-ray photo-


emission spectroscopy), also called ESCA (electron spectros-
copy for chemical analysis), because it offers elemental anal-
ysis with high lateral resolutions (&0.1–1.0 !m) and precise
selection of the analysis area (by SEM).
The majority of failed implants were inserted in resorbed
maxillas, which in many cases had to be bone grafted prior to
Figure 1. Schematic illustration showing different analysis loca- implant placement. Pain at percussion was the only symptom
tions on the implants and the numbering of threads. in 14 cases. No macroscopic signs of infection or inflamma-
tion were observed, with exception of patient L. This patient
had not showed up at the scheduled controls, but was seen in
tissue has to be retrieved and properly oriented. In addition, the emergency room due to pain and bridge mobility. The
these failed implants, being surrounded by a soft tissue cap- failed implant site was characterized by abundant plaque
sule, could be efficiently cleaned to allow for reliable analy- accumulation, redness, and heavy bleeding tendency on prob-
ses, in contrast to failed implants that have previously been ing. Radiographically the implant was entirely surrounded by
embedded in plastic (unpublished observations) or successful a radiolucent line. At clinical inspection, the 4-unit provi-
implants integrated in bone, for which analysis is hampered sional maxillary bridge was found to be fractured in the
by plastic and/or tissue residues.23,24,40 AES was here pre- middle and the mesial implant, supporting 1 premolar and a
mesial cantilever, was clearly mobile. The patient referred
that the routine hygienic measures in the area had stopped not
to further compromise the situation. Such a clinical picture
may indicate a superficial infection superimposed to a failure
etiology due to overload. Therefore, the late failed Brånemark
implants analyzed in this study had clinical characteristics
similar to the late failures investigated in a recent immuno-
histochemical investigation.41 In addition, the failure charac-
teristics and patterns of these implants are in agreement with
those observed in a recent systematic overview on the same
implant system,42 and is in accordance with the etiologies
(overload in relation to nonoptimal bone characteristics) that
are believed to play a major role for the losses of this type of
implants.43
All the implant surfaces analyzed consisted of Ti oxide,
with varying amounts of contaminants or organic matter
(mainly C and N, but also traces of Ca, P, Na, Cl, S, and Si).
Figure 2. SEM micrograph of implant A showing no macroscopic
contamination and normal topography. The round dark areas were
The main difference observed between retrieved and control
caused by the electron beam during AES analysis. Scale bar ! 500 implants was that the former had significantly higher C lev-
!m. els, which is consistent with the thin organic films frequently
566 ESPOSITO ET AL.

TABLE III. Oxide Thicknesses of Nonimplanted and Implanted Brånemark Implants as Reported in the Literature

Implantation Time
Authors Nonimplanted (nm) Implanted (nm) (Range) Methodologyf
McQueen et al., 1982a,23 5 Af up to 200Bf (6 months–8 years) A and B
Sundgren et al., 1986c,24 3.5 up to 63b (6 months–8 years) C
Lausmaa et al., 1988d,25 2–6 up to 16b Not specified D and E
Klauber et al., 199014 2 — — D
Binon et al., 199248 17 Af; 10.8 Df — — A and D
Aparicio et al., 1992e,35 10 10–15b (3–20 months) D
Olefjord et al., 199317 4.2–4.6 — — E
Esposito et al., 1999 5–7 5–8 or 7–15b (3 months–8 years) D
a
No calibration of sputtering rate.
b
Organic overlayer on the implant probably leading to depth profile broadening.
c
Same material as in McQueen et al.23
d
Oxide thickness for nonimplanted samples depending on the sterilization procedure. Presented depth profile indicate similar oxide thicknesses for nonimplanted and retrieved
samples, if C overlayer is accounted for.
e
Failed implants cleaned and sterilized twice: before and after insertion by the authors.
f
A: Oxide thickness determined from the depth at which O signal has decreased to a concentration of 10% to 20%.
B: Oxide thickness determined from the depth at which S, P, and Ca profiles terminate.
C: Oxide thickness determined from O/Ti signal intensity ratio, taking into account escape depth and sputtering induced effects.
D: Oxide thickness determined from the depth at which the O signal has decreased to half its value in the bulk of the oxide.
E: Oxide thickness estimated from relative intensities of metallic and oxide contributions in XPS Ti2p spectra.

observed on retrieved samples44 and from samples exposed to marked increase of the oxide layer over time for functioning
serum solutions.45 Some contamination may also have orig- CP Ti implants.23–25 No significant oxide growth was ob-
inated from several sources, e.g., the fabrication process, as a served in the group of failed implants analyzed in the present
result of the cleaning and sterilization procedures, from the investigation, not even for the implant that had been in
environment during handling and storage,7,9,46,47 at implant function up to 8 years. It could be argued that the previous
insertion, or during retrieval and analysis preparation proce- studies were not dealing with failed implants and, conse-
dures. In particular, the Si contamination was observed only quently, that the lack of oxide layer growth could have
on the samples stored in glass vials (both tests and controls) conditioned the failure process. On the other hand, it should
and not for those placed in plastic vials. In order to confirm also be recognized that reliable depth profiling of screw-
this hypothesis, 2 additional pristine implants, as received shaped machined (rough) samples requires careful position-
from the manufacturer, were analyzed. No traces of Si were ing of the ion and electron beams to areas on the surface that
found. Therefore, Si being one of the major constituents of minimize artifacts due to sample geometry and roughness. In
glass, the observed Si contamination was mainly attributed to addition, in order to obtain reliable oxide thickness measure-
ion dissolution from the glass vials. ments, the area that is subjected to analysis must be free from
The only major exception in the surface composition of tissue or plastic remnants. It is noteworthy that in those cases
failed implants was sample E, where Mg was found to be a where increased oxide thicknesses were recorded,23,25 and for
dominant contaminant. The sample was incautiously handled sample D1 and E in the present investigation, the implant
with gloves. One possible source for this contamination surface was covered by a significant organic overlayer. Fail-
could, therefore, have been talc powder on surgical gloves. ure to respect these analysis conditions leads to severe profile
In view of the present and previous findings,34 it is prob- broadening and misleading results (i.e., over-estimated oxide
able that the slight surface contamination possibly induced by thicknesses). This may also explain the different oxide thick-
accidentally dropping six of the implants on the surgical sheet nesses reported by McQueen et al.23 and Sundgren et al.24
was not relevant for the analytical procedures used, because analyzing the same material. In fact, in the latter report, the
no differences could be detected comparing the “accidentally sputtering was calibrated and areas with less organic residuals
contaminated” sample to the remaining samples. This may were selected for analysis; see Table III for details. In addi-
indicate, as previously suggested,34 that the clinical validity tion, also the length of the alternating sputtering and analysis
of some rigorous protocols for handling Ti implants could be cycle was found to significantly affect the measurements of
carefully revisited. oxide thickness.7
With regard to surface contamination, the present findings, Instead, our results corroborate the finding of Aparicio and
for both test and control implants, are in good overall agree- Olive,35 who reported an essentially unchanged oxide layer
ment with other studies on unused7,14,25,48,49 and retrieved CP thickness. These authors, when discussing their findings in
Ti implants.23–25,35,36,44 However, this is clearly not the case relation to those of McQueen et al.,23 postulated that the
for the measured oxide thicknesses, for which contradictory differences could be due to the shorter implantation periods
results, based on retrieved functioning implants, have been of their own implants (between 3–20 months). However, it is
presented. In fact, some authors reported a constant and also true that the latter specimens were carefully cleaned and
SURFACE ANALYSIS OF FAILED ORAL TITANIUM IMPALNTS 567

not embedded, rendering the presence of macroscopic con- 2. Lekholm U, van Steenberghe D, Herrmann I, Bolender C,
tamination minimal, thus facilitating the analysis procedure. Folmer T, Gunne J, Henry P, Higuchi K, Laney WR, Lindén U.
Osseointegrated implants in the treatment of partially edentu-
Interestingly, other studies on retrieved Ti flame-sprayed
lous jaws: A prospective 5-year multicenter study. Int J Oral
implants (IMZ), after accurate cleaning, displayed a signifi- Maxillofac Implants 1994;9:627– 635.
cant decrease of the oxide layer thickness compared to un- 3. Jemt T, Chai J, Harnett J, Heath MR, Hutton JE, Johns RB,
used controls, which was interpreted as a loss of part of the McKenna S, McNamara DC, van Steenberghe D, Taylor R,
oxide layer in the surrounding tissues or during sample prep- Watson RM, Herrmann I. A 5-year prospective multicenter
follow-up report on overdentures supported by osseointegrated
aration.36
implants, Int. J Oral Maxillofac Implants 1996;11:291–298.
The difference in oxide thicknesses reported by several 4. Henry PJ, Laney WR, Jemt T, Harris D, Krogh PHJ, Polizzi G,
investigators (Table III) may also be partly attributed to Zarb GA, and Herrmann I. Osseointegrated implants for single-
different methodologies adopted to measure the Ti oxide tooth replacement: A prospective 5-year multicenter study. Int
layer, which might have led to different results. In fact, there J Oral Maxillofac Implants 1996;11:450 – 455.
is no absolute standardized means of measuring Ti oxide 5. Friberg B. Sterile operating conditions for the placement of
intraoral implants. J Oral Maxillofac Surg 1996;54:1334 –1336.
thickness on retrieved implants. 6. Kasemo B, Lausmaa J. Surface science aspects on inorganic
The present findings might have important consequences biomaterials. CRC Crit Rev Biocomp 1986;2:335–380.
for the hypothesis of oxide growth and the suggested Ti-gel 7. Lausmaa J, Kasemo B, Mattsson H. Surface spectroscopic char-
formation at the implant-tissue interface in vivo. Recently, acterization of clinical titanium implant materials. Appl Surf Sci
Eliades26 elaborated an intriguing hypothesis to explain the 1990;44:133–146.
8. Lausmaa J. Surface spectroscopic characterization of titanium
contribution of biological substances to the oxide growth, implant materials. J Electr Spectr Rel Phen 1996;81:343–361.
based on the postulate that the site of implantation affected 9. Lausmaa J, Kasemo B, Hansson S. Accelerated oxide growth on
the thickness of the oxide layer (i.e., Ti oxide thickness in titanium implants during autoclaving caused by fluorine con-
bone cortex was believed to be 3– 4 times thinner than in bone tamination. Biomat 1985;6:23–27.
marrow). However, no evidence of altered Ti oxide growth in 10. Baier RE, Meyer AE, Natiella JR, Natiella RR, Carter JM.
Surface properties determine bioadhesive outcomes: methods
relation to the anatomical location can be found in the liter- and results. J Biomed Mater Res 1984;18:337–355.
ature or in the present material. No evidence supporting 11. Kasemo B, Lausmaa J. Biomaterial and implant surfaces: A
directly or indirectly the hypothesis that Ti-gel formation may surface science approach. Int J Oral Maxillofac Implants 1988;
occur in vivo31,32 can be found either. The argument that the 3:247–259.
lack of Ti oxide growth was observed only for failed and not 12. Kasemo B, Lausmaa J. Biomaterial and implant surfaces: On
the role of cleanliness, contamination, and preparation proce-
for functioning implants may tentatively be used to explain dures. J Biomed Mater Res 1988;22:145–158.
the failure etiology. However, oxide thickness measurements 13. Baier RE, Meyer AE. Implant surface preparation. Int J Oral
on failed implants are more accurately performed. In addi- Maxillofac Implants 1988;3:9 –20.
tion, the same cell-derived oxidizing products that have been 14. Klauber C, Lenz LJ, Henry PJ. Oxide thickness and surface
used in the literature24,26 –28 to explain the oxide growth contamination of six endosseous dental implants determined by
electron spectroscopy for chemical analysis: A preliminary re-
around successfully bone-integrated implants are, in fact, port. Int J Oral Maxillofac Implants 1990;5:264 –271.
likely to be found in a higher concentration at a failed implant 15. Smith DC. Surface characterization of implant materials: bio-
interface due to the presence of inflammatory cells.41 There- logical implications. In: Davies JE, editor. The bone-biomaterial
fore, the hypotheses used to explain the Ti oxide growth in interface. Toronto: Univ Toronto; 1991. p 3–18.
vivo24,26 –28 need to be carefully revisited, because there 16. Smith DC. Dental implants: Materials and design consider-
ations. Int J Prosthodont 1993;6:106 –117.
might be no significant oxide growth occurring in vivo. The
17. Olefjord I, Hansson S. Surface analysis of four dental implant
presence of analysis artifacts may have induced some authors systems. Int J Oral Maxillofac Implants 1993;8:32– 40.
to reach erroneous conclusions. In order to clarify this issue, 18. Brånemark PI, Lausmaa J, Ericson L, Thomsen P, Brånemark
new surface analytical studies on retrieved successful im- R, Skalak R. Anatomy of osseointegration and the transfer of
plants are required. load. In: Fonseca RJ, Davis WH, editors. Reconstructive pre-
prosthetic oral and maxillofacial surgery. 2nd Ed. Philadelphia:
Since the clinical scenario and the results suggest that the
WB Saunders; 1995. p 165–224.
role of surface contamination and peri-implantitis41,43,50 may 19. Zöller GO, Zentner A. Initial attachment of human gingival
be excluded, the present findings support the assumption that fibroblast-like cells in vitro to titanium surfaces pretreated with
the failures hereby analyzed may be attributed to impaired saliva and serum. Clin Oral Implants Res 1996;7:311–315.
healing, asymptomatic infection, or disruption of a weak 20. Ericsson I, Persson LG, Berglundh T, Edlund T, Lindhe J. The
bone-to-implant interface51 (early losses) and to overload in effect of antimicrobial therapy on periimplantitis lesions. An
experimental study in the dog. Clin Oral Implants Res 1996;7:
relation to the host characteristics (late failures).41 320 –328.
Nobel Biocare Norden AB is acknowledged for donating the control 21. Ivanoff CJ, Sennerby L, Lekholm U. Influence of soft tissue
implants. contamination on the integration of titanium implants. An ex-
perimental study in rabbits. Clin Oral Implants Res 1996;7:
REFERENCES 128 –132.
22. Bjursten LM, Gould TRL, Skalak R, Baier RE, Beertsen W,
1. Adell R, Lekholm U, Rockler B, Brånemark PI. A 15-year study Ducheyne P, Kasemo B, Pilliar RE. Basic science committee.
of osseointegrated implants in the treatment of the edentulous In: van Steenberghe D, Albrektsson T, Brånemark PI, Henry PJ,
jaw. Int J Oral Surg 1981;10:387– 416. Holt R, Lidén G, editors. Tissue integration in oral and maxillo-
568 ESPOSITO ET AL.

facial reconstruction. Amsterdam: Excerpta Medica; 1986. p 1992;7:94 –103.


511–513. 36. Kuliralo M, Pireaux JJ, Caudano R, Dourov N. Surface studies
23. McQueen D, Sundgren JE, Ivarsson B, Lundström I, af Eken- on titanium IMZ implants. J Biol Buccale 1991;19:247–253.
stam B, Svensson A, Brånemark PI, Albrektsson T. Auger 37. Adell R, Lekholm U, Brånemark PI. Surgical procedures. In:
electron spectroscopic studies of titanium implants. In: Lee Brånemark PI, Zarb GA, Albrektsson T, editors. Tissue-inte-
AJC, Albrektsson T, Brånemark PI. editors. Clinical applica- grated prostheses. Chicago: Quintessence; 1985. p 211–232.
tions of biomaterials. Chichester: Wiley; 1982. p 179 –185. 38. Strid KG. Radiographic procedures. . In: Brånemark PI, Zarb
24. Sundgren JE, Bodö P, Lundström I. Auger electron spectro- GA, Albrektsson T, editors. Tissue-integrated prostheses. Chi-
scopic studies of the interface between human tissue and im- cago: Quintessence; 1985. p 317–327.
plants of titanium and stainless steel. J Colloid Interface Sci 39. Lekholm U, Zarb GA. Patient selection and preparation. In:
1986;10:9 –20. Brånemark PI, Zarb GA, Albrektsson T, editors. Tissue-inte-
25. Lausmaa J, Kasemo B, Rolander U, Bjursten LM, Ericson LE,
grated prostheses. Chicago: Quintessence; 1985. p 199 –209.
Rosander L, Thomsen P. Preparation, surface spectroscopic and
40. Lausmaa J, Linder L. Surface spectroscopic characterization of
electron microscopic characterization of titanium implant ma-
titanium implants after separation from plastic-embedded tissue.
terials. In: Ratner BD, editor. Surface characterization of bio-
materials. Amsterdam: Elsevier; 1988. p 161–174. Biomater 1988;9:277–280.
26. Eliades T. Passive film growth on titanium alloys: physico- 41. Esposito M, Thomsen P, Mölne J, Gretzer C, Ericson LE,
chemical and biologic considerations. Int J Oral Maxillofac Lekholm U. Immunohistochemistry of soft tissues surrounding
Implants 1997;12:621– 627. late failures of Brånemark implants. Clin Oral Implants Res
27. Kasemo B, Lausmaa J. Metal selection and surface character- 1997;8:352–366.
istics. In: Brånemark PI, Zarb GA, Albrektsson T, editors. 42. Esposito M, Hirsch JM, Lekholm U, Thomsen P. Biological
Tissue-integrated prostheses. Chicago: Quintessence; 1985. p factors contributing to failures of osseointegrated oral implants.
99 –116. (I) Success criteria and epidemiology. Eur J Oral Sci 1998;106:
28. Tengvall P, Lundström I. Physico-chemical considerations of 527–551.
titanium as a biomaterial. Clin Mater 1992;9:115–134. 43. Esposito M, Hirsch JM, Lekholm U, Thomsen P. Biological
29. Ducheyne P, Willems G, Martens M, Helsen J. In vivo metal- factors contributing to failures of osseointegrated oral implants.
ion release from porous titanium-fiber material. J Biomed Mater (II) Etiopathogenesis. Eur J Oral Sci 1998;106:721–764.
Res 1984;18:293–308. 44. Mouhyi J, Sennerby L, Pireaux JJ, Dourov N, Nammour S, Van
30. Osborn JF, Willich P, Meenen N. The release of titanium into Reck J. An XPS and SEM evaluation of six chemical and
human bone from a titanium implant coated with plasma- physical techniques for cleaning of contaminated titanium im-
sprayed titanium. In: Heimke G, Soltész U, Lee AJC, editors. plants. Clin Oral Implants Res 1998;9:185–194.
Clinical implant materials. Advances in biomaterials. Amster- 45. Healy KE, Ducheyne P. Hydration and preferential molecular
dam: Elsevier; 1990. p 75– 80. adsorption on titanium in vitro. Biomat 1992;13:553–561.
31. Tengvall P, Elwing H, Sjöqvist L, Lundström I, Bjursten LM. 46. Doundoulakis JH. Surface analysis of titanium after steriliza-
Interaction between hydrogen peroxide and titanium: a possible tion: role in implant-tissue interface and bioadhesion. J Prosthet
role in the biocompatibility of titanium. Biomat 1989;10:118 – Dent 1987;58:471– 478.
120.
47. Keller JC, Draughn RA, Wightman JP, Dougherty WJ, Meletiou
32. Tengvall P, Lundström I, Sjöqvist L, Elwing H, Bjursten LM.
SD. Characterization of sterilized CP titanium implant surfaces.
Titanium– hydrogen peroxide interaction: model studies of the
Int J Oral Maxillofac Implants 1990;5:360 –367.
influence of the inflammatory response on titanium implants.
Biomat 1989;10:166 –175. 48. Binon PP, Weir DJ, Marshall SJ. Surface analysis of an original
33. Brånemark PI, Breine U, Adell R, Hansson BO, Lindström J, Brånemark implant and three related clones. Int J Oral Maxil-
Ohlsson A. Intra-osseous anchorage of dental prostheses. I. lofac Implants 1992;7:168 –175.
Experimental studies. Scand J Plast Reconstr Surg 1969;3:81– 49. Edwards BN, Gold BR. Analysis of surface cleanliness of three
100. commercial dental implants. Biomat 1992;13:775–780.
34. Ameen AP, Short RD, Johns R, Schwach G. The surface anal- 50. Isidor F. Histological evaluation of peri-implant bone at im-
ysis of implant materials. 1. The surface composition of a plants subjected to occlusal overload or plaque accumulation.
titanium dental implant material. Clin Oral Implants Res 1993; Clin Oral Implants Res 1997;8:1–9.
4:144 –150. 51. Esposito M, Thomsen P, Ericson LE, Lekholm U. Histopatho-
35. Aparicio C, Olivé J. Comparative surface microanalysis of logical observations at early failed oral implants. Int J Oral
failed Brånemark implants. Int J Oral Maxillofac Implants Maxillofac Implants, to appear.