Abstract

We observed surfaces and cross sections of thin hydroxyapatite (HA)-coated implants produced by the thermal decomposition method in a patient attending our clinic who underwent implant removal at 80 months due to fracture of the implants. On the implant surfaces of the removed sample, most of the HA had dissolved, and extensive osseointegration was observed where Ti had closely bonded to bone. This indicated that the HA coated on the implant surfaces had disappeared and osseointegration had been established where Ti directly bonded to the bone. In addition, calcium titanate (CaTiO3) and HA layers formed by the thermal decomposition method showed no desorption. The results clearly indicate the positive clinical potential of thin HA-coating by the thermal decomposition method.

Introduction

Pure titanium is the standard material for oral implants. Various methods for treating the surface of such implants have been developed with the aim of enhancing bonding between implant and surrounding bone. Since the 1980s, coating the implant with hydroxyapatite (HA) in particular has drawn much interest, as so doing greatly enhances biocompatibility, which leads to early stage synostosis by osteoconduction.16 However, the advantages offered by HA remain to be fully exploited due to problems in its application. Maintaining a uniform thickness of 30–80 µm is crucial but difficult due to problems such as dissolution, desorption, and cracking.710 Recently, in order to overcome these problems and obtain the full benefits offered by HA-mediated osteoconduction, a method of coating implants with an HA layer only a few micrometers in thickness has been developed and applied.1115 

In this study, we observed thin HA-coated implants produced by the thermal decomposition method in a patient attending our clinic who underwent implant removal at 80 months due to fracture of the implants. We report our observations and analyses of the surfaces and cross sections of the removed implants.

Materials and Methods

Case

The patient was a 37-year-old man. At initial presentation, his chief complaint was masticatory disorder due to lack of bilateral molars in the mandible. He had no significant systemic disease or local problem, the bone quality of the region of implantation was D2 and D3, and implantation was planned in accordance with the patient's wishes.

On May 24, 2001, 2 thin HA-coated implants (Platon Implant, Bio Type I, Platon Japan, Tokyo, Japan) were inserted to replace the left mandibular first and second molars using a single-stage procedure. On August 29, 2001, a superstructure was attached by cementation. Implant therapy was then conducted to replace the right mandibular first and second molars. After attachment of the superstructure, a good clinical course was observed on regular examination. However, on November 17, 2007, the 2 implants on the left side broke and desorbed along with the superstructure. The implants broke at sites subjected to stresses exerted by the tips of the abutment screws, and no procedures other than implant removal were considered. The implants were removed on February 7, 2008. The surfaces and cross sections of the removed implants were observed with the patient's consent.

Analysis methods

One of the removed implants and its surrounding bone was fixed with 10% formalin solution, after which it was dehydrated in an increasing series of ethanol solutions and embedded with polyester resin to obtain a specimen. This specimen was cut across the implantation axis and its surface ground with waterproof grinding paper for use as a sample (removed sample). Reflection images obtained with a scanning electron microscope (SEM) (JSM-6340F, JEOL Ltd, Tokyo, Japan) and Ca and Ti surface analysis images obtained with the electron probe microanalyzer (EPMA) (JXA-8200, JEOL Ltd) were observed at 15 kV of acceleration voltage. An unused implant (control sample) was also observed for comparison with the removed sample.

The other removed implant was fixed on the sample table while unembedded. Next, Pt-Pd sputter coating was conducted for surface protection, and electrical conduction and cross sections were prepared by focused ion beam (FIB) treatment. Sections were observed with a SEM (S-4700, Hitachi, Tokyo, Japan) at 10 kV acceleration voltage. Carbon was deposited on the treated area as a local protective coating to reduce damage caused by gallium ion beam irradiation.

Results

Observation of SEM reflection electron images of the removed samples at low magnification revealed close and extensive bonding to bone (Figure 1). Partial magnification revealed that the implant and bone were light and slightly darker gray, respectively, and that the implant had bonded closely to the bone (Figure 2). At this site, percentage of bone-to-implant contact at the calcium titanate (CaTiO3) boundary was 99.1%. On the other hand, in the control sample, a few micrometers of slightly darker gray HA coating was observed on the surface of the light gray implant (Figure 3).

Figure 1

Reflection electron image of removed sample at low magnification: dense bone (Bo) formation was observed around the implant (Ti).

Figure 1

Reflection electron image of removed sample at low magnification: dense bone (Bo) formation was observed around the implant (Ti).

Figures 2–5

Figure 2. Reflection electron image of removed sample: implant (Ti) showed close bonding to bone (Bo). Figure 3. Reflection electron image of control sample: hydroxyapatite (HA) layers a few micrometers thick were observed on Ti surfaces. Figure 4. Ca surface analysis of the control sample by electron probe microanalyzer (same area as in Figure 3). Light area on Ti surfaces is Ca, which indicates HA layers. Figure 5. Ca surface analysis of removed sample by electron probe microanalyzer (same area as in Figure 2). Light area on Ti surfaces is Ca, which indicates bone (Bo).

Figures 2–5

Figure 2. Reflection electron image of removed sample: implant (Ti) showed close bonding to bone (Bo). Figure 3. Reflection electron image of control sample: hydroxyapatite (HA) layers a few micrometers thick were observed on Ti surfaces. Figure 4. Ca surface analysis of the control sample by electron probe microanalyzer (same area as in Figure 3). Light area on Ti surfaces is Ca, which indicates HA layers. Figure 5. Ca surface analysis of removed sample by electron probe microanalyzer (same area as in Figure 2). Light area on Ti surfaces is Ca, which indicates bone (Bo).

The Ca and Ti surface analysis conducted with the EPMA revealed Ca layers coated with HA on the implant surface in the control sample (Figure 4). In the removed sample, Ca showed distribution throughout the bone that had bonded to the implant (Figure 5). Ca showed an even distribution, and no increase in Ca density on the Ti surfaces made it impossible to clarify whether the Ca was present in the HA or the bone.

On the other hand, on the implant surfaces of the removed sample, the area where no bone formation had occurred was very small. In the magnified reflection electron images, the implant was light gray, and the area where no bone formation had occurred was dark gray (Figure 6). The EPMA analysis of the same area revealed no Ca distribution on the Ti surfaces of the implant (Figure 7).

Figures 6–9

Figure 6. Reflection electron image of area where no bone formation was observed. No hydroxyapatite (HA) layers were observed on Ti surfaces. Figure 7. Ca surface analysis of area where no bone formation was observed by electron probe microanalyzer in removed sample (same area as in Figure 6). No Ca was observed on Ti surfaces. Figure 8. Highly magnified scanning electron microscope (SEM) image of cross section of focused ion beam (FIB)-treated sample. Titanium dioxide (TiO2) (a) and calcium titanate (CaTiO3) (b) layers were observed on Ti surface layers. Figure 9. Highly magnified SEM image of cross section of FIB-treated sample. TiO2 (a), CaTiO3 (b), and HA (c) layers were observed on Ti surface layers.

Figures 6–9

Figure 6. Reflection electron image of area where no bone formation was observed. No hydroxyapatite (HA) layers were observed on Ti surfaces. Figure 7. Ca surface analysis of area where no bone formation was observed by electron probe microanalyzer in removed sample (same area as in Figure 6). No Ca was observed on Ti surfaces. Figure 8. Highly magnified scanning electron microscope (SEM) image of cross section of focused ion beam (FIB)-treated sample. Titanium dioxide (TiO2) (a) and calcium titanate (CaTiO3) (b) layers were observed on Ti surface layers. Figure 9. Highly magnified SEM image of cross section of FIB-treated sample. TiO2 (a), CaTiO3 (b), and HA (c) layers were observed on Ti surface layers.

When the cross sections of the surfaces of the removed implant treated with FIB were observed at high magnification with a SEM, a slightly darker gray layer considered to be titanium dioxide (TiO2) was observed on the Ti surface layer (Figure 8a), and a molding layer believed to be CaTiO3 was observed on top of that (Figure 8b).

In addition, a light gray Ti surface layer and a slightly darker gray layer considered to be a layer of TiO2 on top of the Ti layer (Figure 9a) were observed around the top of the thread. Another layer believed to be CaTiO3 overlapped these layers (Figure 9b), with a further layer considered to be HA (Figure 9c) on top of that.

Discussion

According to numerous studies, root form titanium oral implants, including those developed by Branemark et al,16 are highly predictable therapies. One of the drawbacks of implant therapy, however, is the long treatment period required, and a number of methods have been developed to resolve this problem. One method is to modify the titanium surfaces with HA, and many types of implant now include titanium surfaces coated with HA, which offers excellent biocompatibility and osteoconduction. However, implants coated with HA by plasma-spraying or flame-spraying suffer from problems related to the thickness of the HA film, uneven film composition, and rough inner structures, all of which can lead to loss of implant due to film breakage or desorption.4,610,17 

Recently, thin HA coatings of only a few micrometers in thickness have drawn much attention as a potential solution to this problem. In this study, the implants analyzed were coated with CaTiO3 and HA at the relatively low temperature of 600°–650°C by the thermal decomposition method, which allows high purity and HA layers of 3–5 µm in thickness. Moreover, the double-layered coating of CaTiO3 and HA provides strong adhesive strength.11,12,14 

Where no bone formation had occurred on the surfaces of the removed sample, observation by EPMA revealed no Ca distribution in contrast to the control sample. This indicated that the HA layers on the implants had disappeared. Where bone formation had occurred, Ca showed an even distribution and no increase in density on the titanium surface. This indicated the disappearance of HA from the Ti surfaces in the overall implant, suggesting a transition from biointegration to osseointegration.

Observation of the FIB-treated samples at high magnification revealed bonding of CaTiO3 layers to the TiO2 layers on the Ti surface layer, and layers considered to be HA were also partially observed. This indicated that, as reported by Kawamura et al,14 CaTiO3 layers and HA layers formed by the thermal decomposition method are thin with excellent adhesion, making desorption and breaking of the coating layers rare.

In thin HA-coated implants at 80 months after placement, most of the HA had dissolved, and osseointegration with close and extensive bonding of Ti was observed. In addition, CaTiO3 layers and HA layers formed by the thermal decomposition method showed no desorption, indicating the usefulness of the thin HA-coating method.

Abbreviations

     
  • CaTiO3

    calcium titanate

  •  
  • EPMA

    electron probe microanalyzer

  •  
  • FIB

    focused ion beam

  •  
  • HA

    hydroxyapatite

  •  
  • SEM

    scanning electron microscope

Acknowledgments

The authors would like to thank Associate Professor Jeremy Williams, Tokyo Dental College, for his assistance with the English of the manuscript.

References

References
1
de Groot
,
K.
Bioceramics consisting of calcium phosphate salts.
Biomaterials
1980
.
1
:
47
50
.
2
Jarcho
,
M.
Biomaterial aspects of calcium phosphates. Properties and applications.
Dent Clin North Am
1986
.
30
:
25
47
.
3
de Groot
,
K.
,
R.
Geesink
,
C. P.
Klein
, and
P.
Serekian
.
Plasma sprayed coatings of hydroxylapatite.
J Biomed Mater Res
1987
.
21
:
1375
1381
.
4
Cook
,
S. D.
,
J. F.
Kay
,
K. A.
Thomas
, and
M.
Jarcho
.
Interface mechanics and histology of titanium and hydroxylapatite-coated titanium for dental implant applications.
Int J Oral Maxillofac Implants
1987
.
2
:
15
22
.
5
Zablotsky
,
M. H.
Hydroxyapatite coatings in implant dentistry.
Implant Dent
1992
.
1
:
253
257
.
6
Kay
,
J. F.
Calcium phosphate coatings for dental implants. Current status and future potential.
Dent Clin North Am
1992
.
36
:
1
18
.
7
de Bruijn
,
J. D.
,
Y. P.
Bovell
,
J. E.
Davies
, and
C. A.
van Blitterswijk
.
Osteoclastic resorption of calcium phosphates is potentiated in postosteogenic culture conditions.
J Biomed Mater Res
1994
.
28
:
105
112
.
8
Wang
,
B. C.
,
T. M.
Lee
,
E.
Chang
, and
C. Y.
Yang
.
The shear strength and the failure mode of plasma-sprayed hydroxyapatite coating to bone: the effect of coating thickness.
J Biomed Mater Res
1993
.
27
:
1315
1327
.
9
Maxian
,
S. H.
,
J. P.
Zawadsky
, and
M. G.
Dunn
.
Mechanical and histological evaluation of amorphous calcium phosphate and poorly crystallized hydroxyapatite coatings on titanium implants.
J Biomed Mater Res
1993
.
27
:
717
728
.
10
Klein
,
C. P.
,
J. G.
Wolke
,
J. M.
de Blieck-Hogervorst
, and
K.
de Groot
.
Features of calcium phosphate plasma-sprayed coatings: an in vitro study.
J Biomed Mater Res
1994
.
28
:
961
967
.
11
Hasegawa
,
S.
Characterization and canine bone tissue reaction of hydroxyapatite-coated titanium using thermal decomposition method.
Bull Tokyo Med Dent Univ
1996
.
43
:
25
44
.
12
Zhou
,
P.
and
M.
Akao
.
Preparation and characterization of double layered coating composed of hydroxyapatite and perovskite by thermal decomposition.
Biomed Mater Eng
1997
.
7
:
67
81
.
13
Seno
,
T.
,
Y.
Izumisawa
,
I.
Nishimura
, et al
.
The interfacial strength in sputtering-hydroxyapatite-coating implants with arc-deposited surface.
J Vet Med Sci
2003
.
65
:
419
422
.
14
Kawamura
,
K.
,
H.
Matsubara
,
Y.
Nakanishi
,
Y.
Hirose
, and
M.
Ochi
.
Bone formation of Ultra-thin CaTiO3 and hydroxyapatite (HA) coated implant [in Japanese].
Dent J Health Sci Univ Hokkaido
2006
.
25
:
119
126
.
15
Ozeki
,
K.
,
Y.
Okuyama
,
Y.
Fukui
, and
H.
Aoki
.
Bone response to titanium implants coated with thin sputtered HA film subject to hydrothermal treatment and implanted in the canine mandible.
Biomed Mater Eng
2006
.
16
:
243
251
.
16
Branemark
,
P. I.
,
R.
Adell
,
U.
Breine
,
B. O.
Hansson
,
J.
Lindström
, and
A.
Ohlsson
.
Intra-osseous anchorage of dental prostheses. I. Experimental studies.
Scand J Plast Reconstr Surg
1969
.
3
:
81
100
.
17
Cook
,
S. D.
,
G. C.
Baffes
,
A. J.
Palafox
,
M. W.
Wolfe
, and
A.
Burgess
.
Torsional stability of HA-coated and grit-blasted titanium dental implants.
J Oral Implantol
1992
.
18
:
354
365
.