FORMATION OF SELF-ORGANISING INTERFACE
BETWEEN THE BONE AND IMPLANTS
WITH NANOSTRUCTURED BIOACTIVE COATINGS: PHYSICS,
CHEMISTRY AND MECHANICS
A.I. Mamaev, V.A. Mamaeva
Institute of Strength Physics and Materials Science, Siberian Branch of the Russian
Academy of Science, Tomsk, Russian Federation
D.A. Malanin
Volgograd Scientific Centre of the Russian Academy of Sciences and Volgograd
State Medical University, Volgograd, Russian Federation
V.I. Kalita, A.G. Gnedovets, D.I. Komlev
A.A. Baikov’s Institute of Metallurgy and Materials Science of the Russian Academy
of Sciences, Moscow, Russian Federation
A. Yerokhin and A. Matthews
Department of Engineering Materials, University of Sheffield, Sheffield, U.K.
Abstract. The paper discusses effects of novel nanostructured composite coatings on
mechanical properties of bone-implant systems. The composite coatings comprise
thick Ti underlayer featured by 3-dimentional capillary-porous morphology and thin
top ceramic layer with enhanced biological activity. The Ti layer is produced by
plasma spraying under low incident angles and the bioceramic layer is produced by
plasma electrolytic oxidation. The coated Ti samples were implanted into animals and
resided there up to 2 years. Tensile tests were performed to evaluate shear strength at
the bone-implant interface. It was found that the composite coatings allowed faster
and better integration of Ti implants into bone tissue. The coatings provided 24%
increase in the interfacial shear strength. It was suggested that the composition of the
bioactive layer is principally responsible for the shear strength growth rate.
INTRODUCTION
To facilitate osseointegration of intrabone prosthetic implants they should possess a
specific porous surface structure, with porosity ranging between 50 and 500 m and
stiffness being intermediate between that of the bone and the implant material. These
characteristics of the porous structure promote osteoconductivity at the bone-implant
interface and ensure its high adhesion strength. However, none of the known
conventional porous structures satisfy these criteria in full. A preferable bioactive
compound for prosthetic implants is hydroxyapatite (Ca10(PO4)6(OH)2, HA). These
considerations are put into the base of development of principally new 3-dimensional
capillary-porous (3DCP) composite coating deposited by plasma spraying of Ti wire
or powder [1] followed by surface conversion by plasma electrolytic oxidation (PEO)
[2,3]. The 3D structure of Ti coating comprises alternating hills and valleys,
beginning at the coating-substrate interface. The region of the highest porosity
dedicated for bone ingrowth is located in the valleys and smaller capillary pores – in
the bulk of the hills and on their surfaces. The original 3DCP structure allowed
obtaining high shear strength, about 250 MPa, which is up to 6 times of that for
conventional porous structures [1]. Surface conversion of Ti results in formation of 5
to 50 m thick bioactive ceramic (BC) layer with titania matrix. The layer is featured
by fine porosity, ranging between 0.1 and 10 m and comprising 10 to 40% of its
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volume. Such structure of the top BC layer promotes formation of new bone material
and retain its bioactivity during desorption since titania matrix is thermodynamically
stable in the bone. Generally, the composite 3DCP + BC-PEO coatings are capable to
adapt easily to bone systems of live bodies and can therefore be categorised as healing
promoters.
The main purpose of this work was to study effects of the nanostructured composite
coatings on mechanical properties of the bone-implant system during medium-term
in-vivo residence.
MATERIALS AND METHODS
The studies were carried out in vivo using Ti wire implants. The wire samples of 2
mm in diameter were coated with 3DCP Ti layer using arc plasma spray method [1].
The mean average thickness of the 3DCP coating was 650 m. BC top layers
containing hydroxyapatite (HA), either alone or in the mixture with calcium
phosphates (CP), were deposited in electrolyte solutions by pulsed current PEO
methods [2, 3].
Integration of implants with bone were studied using 12 mature underbred dogs (24
knee joints), 3 to 4 years old, weighted 9 to 11 kg. The test protocol in parts of
experimental design, animal selection, keeping and bringing out of the experiment
was agreed with local ethical committee. The animals were randomly split into 3
groups to implant samples with (i) 3DCP Ti, (ii) 3DCP Ti + BC (HA) and (iii) 3DCP
Ti + BC (HA + CP) coatings respectively. At the first stage, on the side of joint
surface, some channels were formed in distal epiphyses of femoral bones of the
animals. The coated wire implants with length of 7 mm were subchondrically tight-fit
inserted in these channels. Biopsy of the samples was carried out after 24, 48, 72 and
96 weeks of implantation. The samples were taken off in such way that it is fully
surrounded by >1 cm thick bone tissue. To prevent subsequent changes in bone tissue
the samples were kept in physiological NaCl solution at 4oC.
Fig. 1. Typical appearance of the bone-implant sample for shear tests.
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At the second stage, within 24 to 48 hours after the biopsy, mechanical testing of the
samples was carried out to evaluate shear strength of the bone-implant interface. The
samples were coaxially placed inside Al cylinders of 20 mm in diameter, with
surrounding space filled in by epoxy resin (Fig. 1). Each time, 2 to 5 samples of each
type of coating were tested. The tests were carried out using ‘Instron’ model 1115
tensile tester at 0.5 mm min-1 strain rate.
Finally, implant surfaces after the shear tests were analysed using a binocular
microscope under x30 magnification. Polished cross-sections of the bone-implant
system and implants taken out of the bone were additionally studied by optical
microscopy under x1000 magnification.
RESULTS
Shear strength of bone-implant system with different types of coatings is collated in
Table 1. Visual observations of implants tested after 24 weeks (0.5 yrs) of
implantation showed that fracture always occurred in the bone and shear strength
represent that of the new bone formed at the interface. For 3DCP Ti and 3dCP Ti +
BC (HA) coatings the fracture in some cases proceeded via tops of the coating hills
whereas a presence of transparent fibrous structures of different density was observed
in valleys.
Table 1. Mean average shear strength (MPa) in bone-implant system.
Coating type
3DCP Ti
3DCP Ti + BC (HA)
3DCP Ti + BC (HA + CP)
Implantation time (yrs)
0.5
1.0
1.5
1.3
1.6
7.6
1.2
9.8
9.4
2.0
5.1
5.5
2.0
3.1
4.5
6.2
Mean
strength
3.4
6.2
4.7
average
In 48 weeks (1 year) after implantation, all groups fractured via highest tops of the
hills. Porous bone constituents with lamellar morphology remained between the hills.
Similar behaviour was observed for 3DCP Ti + BC (HA) samples after 72 weeks (1.5
yrs) , whereas for other groups the fracture occurred via the surrounding bone tissue.
In the latest tests (96 weeks or 2 yrs), the fracture always occurred through the bone,
on some distance from the interface.
At 24 weeks (0.5 yrs) after implantation, the shear strength of implants with 3DCP Ti
and 3DCP Ti +BC (HA) coatings was similar (1.3 and 1.2 MPa respectively) and
3DCP Ti +BC (HA + CP) coating showed a higher shear strength of 2 MPa (Fig. 2).
During the following 24 weeks, the value of shear strength of the samples with 3DCP
Ti +BC (HA) coating increased significantly and became 9.8 MPa, exceeding that of
other groups. At 72 weeks (1.5 yrs), the maximum strength was also shown by 3DCP
Ti +BC (HA) coatings; the strength of 3DCP Ti coating increased from 1.6 to 7.6
MPa and 3DCP Ti +BC (HA + CP) increased slightly, reaching 5.5 MPa.
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3DCP Ti + BC (HA)
Shear Strength (MPa)
10
8
3DCP Ti + BC (HA + CaP)
6
4
2
3DCP Ti
0
0.5
1
1.5
2
Implantation Time (Yrs)
Fig. 2. Effect of implantation time on shear strength in bone-implant systems with
different types of composite coatings.
Fig. 3. Typical surface morphology of implants pulled out from the bone during shear
tests. Left to right: 3DCP Ti; 3DCP Ti +BC (HA) and 3DCP Ti +BC (HA + CP). x30.
At the latest stage (96 weeks or 2 yrs) the shear strength for 3DCP Ti and 3DCP Ti +
BC (HA) coatings decreased to 3.1 and 4.5 MPa respectively but increased for 3DCP
Ti + BC (HA + CP) coating to 6.2 MPa.
Visual observations at x16 to x32 magnifications did not reveal any additional surface
films that could be formed on the implant surface during its residence in the animal
body (Fig. 3). However, some white matter was observed on the surfaces of 3DCP Ti
+BC (HA) and 3DCP Ti +BC (HA + CP) samples, which could be relatively easily
removed by scribing with a needle. Additionally, relatively thick non-transparent
globular features (probably grown in bone tissue) were present on the surface of
3DCP Ti +BC (HA + CP) coating, covering up to 85% of the surface area. The above
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surface morphologies were characteristic for each type of coating regardless the
implantation time.
The presence of bone tissue in the coating pores was also confirmed by the crosssectional analysis of implants both remaining in the bone and pulled out of it. The
latter provided better interfacial observations since the coating hills were free of the
bone tissue and relatively hard epoxy resin engaged tightly with the surface. In this
case a 10 to 25 m thick BC film was clearly observed. Thus it can be deduced that
BC coatings do not decompose fully in the body during at least 2 years, while forming
surface products that are dissimilar from those formed on 3DCP Ti coating.
DISCUSSION
According to the literature data, implant integration with bone tissue is mainly
determined by its surface profile or porosity. These requirements have been fully
obeyed in all experimental groups. This is supported by the fact that bare Ti implants
could be removed from the bone with much lower force event at the sampling stage
[1].
Important role in ensuring high interfacial adhesion strength in the bone-implant
system is also played by the bioactivity of the implant surface that enhances
osseoinduction and osseointegration. The samples with BC coatings (i.e. of 3DCP Ti
+BC (HA) and 3DCP Ti +BC (HA + CP) groups) studied in this work exhibited better
mechanical integration with the bone and therefore better shear strength, indicating
good osseoinductive and osseoconductive characteristics. Histological and immunohistochemical justification of this was provided elsewhere [1].
Current results are in agreement with data of interfacial shear strength of Ti- and HAcoated implants [4] in unloaded (0.63 MPa) and loaded (0.73 MPa) state. However, in
our case, the shear strength is almost an order of magnitude higher, probably due to
the highly convoluted surface morphology of 3DCP coating. Comparing data for
3DCP Ti +BC (HA) and 3DCP Ti +BC (HA + CP) coatings, it should be noted that at
24 weeks the former showed relatively low shear strength, making only a half of that
for the latter. However at 48 and 72 weeks, the situation reversed. This is probably
associated with differential coating desorption rate and corresponding formation of
the new bone. It is interesting that at these particular times the fracture of samples
with 3DCP Ti +BC (HA) coatings occurred via highest tops of the hills, whereas for
3DCP Ti +BC (HA + CP) coatings it went on through the surrounding bone. The
same argument can be put forward to explain increased shear strength of 3DCP Ti
+BC (HA + CP) coatings at 96 weeks, while further verification is required for 3DCP
Ti +BC (HA) coating data as there are some concerns regarding sample keeping in
this batch.
Due to the limited amount of samples available for the tests, it made a sense to
evaluate time-averaged shear strength for each coating group (Table 1). In regard to
this characteristic, the coatings can be ranked in the following ascending order:
3DCP Ti
(3.4 MPa)
<
3DCP Ti +BC (HA+ CP)
(4.7 MPa)
<
3DCP Ti +BC (HA)
(6.2 MPa)
Thus the account for bioactive properties of the coatings allows explaining implant
behaviour during the period of its residence, in particular differential rate of increase
in shear strength for 3DCP Ti +BC (HA) and 3DCP Ti +BC (HA + CP) coatings.
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CONCLUSIONS
The results of in vivo studies have shown that composite 3DCP Ti + BC coatings
allowed faster and better integration of Ti implants into bone tissue. In average, the
composite coatings provide 24% higher shear strength of the bone-implant interface.
A composition of the bioactive top layer appears to be the main factor determining the
rate of increase the shear strength.
ACKNOWLEDGEMENTS
The work was supported by the Russian State contract #02.523.11.3007. International
collaboration was supported by the Royal Society and is acknowledged with thanks.
REFERENCES
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Mamaev AI, Mamaeva VA and Vybornova SN: ‘Method of surface
modification of medical devices’. Patent No RU 2206642, 2000.
Yerokhin A and Matthews A: ‘Method for forming a bioactive coating’. UK
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Mouzin O, Soballe K, Bechtold JE: J. Biomed. Mater. Res. (Appl Biomater)
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