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Characteristics of bone ingrowth and

interface mechanics of a new porous


tantalum biomaterial
J. D. Bobyn, G. J. Stackpool, S. A. Hacking, M. Tanzer, J. J. Krygier
From the Montreal General Hospital and McGill University, Montreal, Canada

e have studied the characteristics of bone This porous tantalum biomaterial has desirable
W ingrowth of a new porous tantalum biomaterial
in a simple transcortical canine model using
characteristics for bone ingrowth; further studies are
warranted to ascertain its potential for clinical
cylindrical implants 510 mm in size. The material reconstructive orthopaedics.
was 75% to 80% porous by volume and had a J Bone Joint Surg [Br] 1999;81-B:907-14.
repeating arrangement of slender interconnecting Received 9 July 1998; Accepted after revision 5 March 1999
struts which formed a regular array of
dodecahedron-shaped pores. We performed
histological studies on two types of material, one with In the last 20 years a variety of porous surfaces and
a smaller pore size averaging 430 µm at 4, 16 and 52 materials has been used to obtain fixation of bone ingrowth
weeks and the other with a larger pore size averaging in total hip and knee prostheses. The most common include
650 µm at 2, 3, 4, 16 and 52 weeks. Mechanical titanium and cobalt-chrome-alloy sintered beads, diffusion-
1-8
push-out tests at 4 and 16 weeks were used to assess bonded titanium, fibre metal, and titanium plasma spray.
the shear strength of the bone-implant interface on Based on the clinical outcome and histological evidence
implants of the smaller pore size. from retrieved implants, it is clear that porous surfaces
The extent of filling of the pores of the tantalum support tissue ingrowth or ongrowth and are generally
material with new bone increased from 13% at two effective for supplementing the stability of the implant by
9-15
weeks to between 42% and 53% at four weeks. By 16 biological fixation.
and 52 weeks the average extent of bone ingrowth Nevertheless, conventional porous materials each have
ranged from 63% to 80%. The tissue response to the certain deficiencies or weaknesses. For instance, sintered
small and large pore sizes was similar, with regions of beaded and fibre metal coatings have a porosity which is
contact between bone and implant increasing with limited to 30% to 50% by volume, a factor which directly
time and with evidence of Haversian remodelling limits the maximum interfacial strength that can develop by
within the pores at later periods. Mechanical tests at bone ingrowth. Conventional metallic porous materials are
four weeks indicated a minimum shear fixation best suited for use as coatings on implants since they do not
strength of 18.5 MPa, substantially higher than has readily have the required mechanical and processing char-
been obtained with other porous materials with less acteristics which would allow them to be used as bulk
volumetric porosity. structural materials for implants, bone augmentation, or
substitutes for bone graft.
A new porous biomaterial made of tantalum has recently
been developed for potential application in reconstructive
16-18
J. D. Bobyn, PhD, Associate Professor orthopaedics and other surgical disciplines. The materi-
Departments of Surgery and Biomedical Engineering, Montreal General
Hospital, Rm A2-156, 1650 Cedar Avenue, Montréal, Québec, Canada al has an unusually high and interconnecting porosity with
H3G 1A4. a very regular pore shape and size. It can be made into
G. J. Stackpool, MD complex shapes and used either as a bulk implant or as a
S. A. Hacking, MEng surface coating. Our aim in this study was to characterise
J. J. Krygier, CET
Jo Miller Orthopaedic Research Laboratory, Montreal General Hospital this porous tantalum material in terms of the extent and rate
Research Institute, RMLs 1-409, 1650 Cedar Avenue, Montréal, Québec, of bone ingrowth as well as the strength of fixation at the
Canada H3G 1A4.
interface.
M. Tanzer, MD, FRCS C, Clinical Associate Professor
Division of Orthopaedic Surgery, Montreal General Hospital, Rm A2-144,
1650 Cedar Avenue, Montreal, Québec, Canada H3G 1A4.
Materials and Methods
Correspondence should be sent to Dr J. D. Bobyn.
©1999 British Editorial Society of Bone and Joint Surgery Implants. The manufacture of the porous tantalum begins
0301-620X/99/59283 $2.00 with the pyrolysis of a thermosetting polymer foam pre-
VOL. 81-B, NO. 5, SEPTEMBER 1999 907
908 J. D. BOBYN, G. J. STACKPOOL, S. A. HACKING, M. TANZER, J. J. KRYGIER

Fig. 1a Fig. 1b

Figure 1a – Scanning electron micrograph of porous tantalum showing the cellular


structure formed by the tantalum struts. There is the occasional smaller opening or portal
which interconnects with the larger pores or cells. Figure 1b – Higher power scanning
electron micrograph of a single pore illustrating the surface microtexture on the struts
caused by crystal growth during the process of tantalum deposition. Figure 1c –
Photographs showing transcortical implants with small and large pore sizes.

Fig. 1c

cursor to obtain a low-density vitreous carbon skeleton tion, Allendale, New Jersey) for use in a canine model as a
which has a repeating dodecahedron array of pores inter- transcortical implant (Fig. 1). They had two different pore
connected by smaller openings or portals. Commercially sizes. The mean pore size was determined using two tech-
pure tantalum is deposited into and about the carbon skele- niques in each of which the data were expressed as a mean
ton using chemical vapour deposition/infiltration (CVD/ with 95% confidence intervals (CI). The first involved
CVI) to create a porous metal construct. Because of the measuring the diameter of 100 dodecahedron-shaped pores,
crystallographic growth and orientation of the tantalum excluding the smaller connecting portals, based on second-
during deposition, the process results in a surface with a ary electron SEM images of the two pore sizes. This
distinct microtexture as shown in Figure 1. Thin CVD/CVI method gave a mean pore diameter of 547 µm (95% CI 537
films of 10 to 100 µm can impart very high mechanical to 557) for implants of smaller pore size and 710 µm (95%
properties because the deposit is typically 100% dense, CI 696 to 724) for those of the larger. The second technique
with grain sizes of less than 1 to 5 µm and impurities of used the line intercept method based on the digital meas-
<0.05%. The typical thickness of the tantalum coating is urement of 1000 pore openings on SEM images of ten
19
approximately 50 µm. An increase in thickness of the different implants. It included all pore lengths inter-
tantalum deposition can affect the pore size and mechanical cepting the grid lines, not just the full diameters of the
properties. pores, and therefore gave smaller mean pore sizes with
Cylindrical implants 5 mm in diameter and 10 mm in larger CIs. By this method the mean pore size was found to
length were made from porous tantalum (Implex Corpora- be 430 µm (95% CI 413 to 447) in implants with the small
THE JOURNAL OF BONE AND JOINT SURGERY
CHARACTERISTICS OF BONE INGROWTH AND INTERFACE MECHANICS OF A NEW POROUS TANTALUM BIOMATERIAL 909

pore size and 650 µm (95% CI 629 to 679) in those with


the larger size. The volume porosity of all implants ranged
from 75% to 80%.
Experimental study. We used skeletally mature mongrel
dogs weighing between 25 and 35 kg. Under standard
aseptic surgical techniques a lateral approach was made to
the femoral diaphysis. A specially designed C-shaped
adjustable jig was clamped to the femur to ensure accurate
and reproducible alignment and sizing of perpendicular
20
drill holes. Bushings which fitted into the jig were used to
guide pilot (2.5 mm) and final (4.95 mm) drills. All the
implant sites were prepared using slow drill speeds and
copious saline irrigation to minimise mechanical and ther-
mal trauma to cortical bone. The final drill hole gave a
Fig. 2
slight press-fit of the transcortical implants which were
inserted into the holes with 2 to 3 mm left proud of the Diagram of the test arrangement used for the mechanical
push-out tests.
periosteal surface. Four implants were inserted into each
femur of each animal. After surgery the animals were
allowed to recover without limitation of diet or activity. The end of the plunger was brought into contact and
Implants with a large pore size were the first to be aligned with the intramedullary end of the implant. The
manufactured and supplied for evaluation. This precluded a bone was supported in a metal cradle with the implant
direct comparison of the two pore sizes in the same ani- centred over a hole 5.5 mm in diameter to provide room for
mals. Three animals with implants of large pore size (24 push-out (Fig. 2). Gaps in the curvature between the femora
implants) were studied at each period of 2, 3, 4, 16 and 52 and the metal cradle were filled with cold-curing dental
weeks and three (24 implants) with implants of small pore acrylic cement to give uniform support during mechanical
size at 4, 16 and 52 weeks. At the end of each study, the testing. The cradle was mounted to a support on a universal
femora were removed and prepared for either undecalcified joint which allowed alignment of the plunger with the
thin-section histology or mechanical testing. implant. Load was applied to the implant at a cross-head
Histological examination. Histological preparation includ- speed of 0.05 cm/min, a rate which was selected based on
1,20 1
ed dehydrating, defatting, and embedding in acrylic. previous studies. Load was applied until the bone-implant
The implants were sectioned either longitudinally through interface ruptured or there was compressive collapse of the
the centre or transversely. All sections were polished and implant as defined from the peak on the load-deformation
sputter-coated for analysis by backscattered SEM. The curve.
1
longitudinal sections were created as close to the centre of Following the design of a previous study, after comple-
the implant as possible because only central sections gave a tion of each push-out test, the remaining femur was divided
true impression of the extent of penetration of the ingrowth into halves through the implant site to allow measurement
of new bone across the full diameter of the implant. We of the cortical thickness. This was done at four equidistant
used computerised image analysis on the longitudinal sec- locations to obtain a mean thickness which was used for
tions to determine the extent of bone ingrowth, which was calculation of the bone interfacial area. The shear strength
defined as the percentage of available porosity filled with of fixation was calculated by dividing the peak load by this
new bone. Some sections were subsequently mounted on area. In instances when the implant underwent compressive
slides, ground, polished, and stained with paragon for failure before rupture of the bone-implant interface, a value
qualitative examination by transmitted light microscopy. for shear strength could not be calculated but it was
Mechanical testing. We performed mechanical testing only assumed to be at least as great as those obtained from
on implants of small pore size. Twelve specimens from the implants which were successfully tested.
four-week and six from the 16-week periods had a push-out Statistical analysis. Each implant in each femur was trea-
test. Femora from each of the three animals in each group ted independently for statistical analysis. Sample independ-
were randomly selected for mechanical testing. They were ence was not verified in separate experiments since in
stripped of soft tissue and the proximal and distal femoral previous studies this has always been presumed for the
1-7,20
metaphyses excised, thus leaving the diaphyseal segment transcortical implant model. The data from all
containing the implants. This was divided longitudinally implants of a given pore size at a given time were tested for
into two halves with a band saw to give access to the normality using the Kolmogorov-Smirnov and the Marti-
implant inside the intramedullary canal. Each implant was nez-Iglewicz tests. For each data set the mean and 95% CI
pushed out of the femur with a cylindrical plunger of were calculated. When data were normally distributed,
4.8 mm diameter attached to the cross-head of a servo- differences in the extent of bone ingrowth between the two
hydraulic Instron test apparatus (Canton, Massachusetts). types of implant at various times were compared using
VOL. 81-B, NO. 5, SEPTEMBER 1999
910 J. D. BOBYN, G. J. STACKPOOL, S. A. HACKING, M. TANZER, J. J. KRYGIER

Table I. Extent of mean bone ingrowth (%) as a function of pore size and time
Bone ingrowth
Time 95% CI
(weeks) Small pore Large pore for difference p value
2* - 13.3 (n = 24) - -
(95% CI 10.8 to 15.8)
3* - 23.0 (n = 24) - -
(95% CI 20.0 to 26.0)
4 41.5 (n = 12) 52.9 (n = 23)† 6.9 to 15.9 0.00003
(95% CI 37.3 to 45.8) (95% CI 50.4 to 55.4)
16 63.1 (n = 18) 69.2 (n = 24) 1.5 to 10.8 0.01
(95% CI 58.2 to 68.0) (95% CI 67.0 to 71.5)
52 79.7 (n = 24) 70.6 (n = 23)† -12.9 to -5.4 0.000008
(95% CI 76.9 to 82.5) (95% CI 68.3 to 73.0)
* implants of small pore size were not studied at two and three weeks
† 1 implant at four and 52 weeks was not included because of a sectioning error

unpaired Student’s t-tests at the 95% CI to assess sig- extent of bone ingrowth increased to a mean of 52.9% for
nificance. Data for shear strength from the successful the large pore size compared with 41.5% for the small pore
mechanical tests at four weeks were expressed as a mean size, a difference which was statistically significant. At 16
with 95% CI. An unpaired Student’s t-test was used to weeks, the difference in mean ingrowth between the large
compare these with data from an earlier four-week mechan- pore size (69.2%) and the small pore size (63.1%) was also
ical study in which the dimensions of the implant, the significant. By 52 weeks, the mean extent of ingrowth of
animal model, surgical technique, mechanical test protocol, implants with a small pore size (79.7%) was significantly
1
and sample size were virtually identical. greater than that of those with the large size (70.6%).
Backscattered SEM showed a clear pattern of formation
Results of new bone within the porous tantalum material. At two
weeks, the primary source of the initial formation of bone
Histological analysis. All the groups of data from the was the intramedullary canal and the edges of the drill hole
histological analyses were found to have a normal distribu- (Fig. 3). Ingrowth was generally scant and only small
tion and were evaluated by Student’s t-tests. Table I gives regions of close apposition of bone to the struts of the
details of bone ingrowth and the results of statistical analy- porous tantalum were observed. At three weeks it appeared
sis on differences between means. In implants of large pore that more new bone arose from, or was continuous with, the
size, the mean extent of ingrowth at two and three weeks drilled edges of the cortex (Fig. 4). In some sections there
was 13.3% and 23.0%, respectively. At four weeks, the was a slight periosteal reaction and new bone seemed to be

Fig. 3 Fig. 4
Backscattered scanning electron micrograph of a two-week implant with a Backscattered scanning electron micrograph of a three-week implant with
large pore size showing bone growth of 13%. New bone appears to arise a large pore size showing bone ingrowth of 21%. Compared with the
from the intramedullary canal and the edges of the drill hole, with little implant at two weeks (Fig. 3) there is increased continuity of new bone
bone on the periosteal surface. The bony trabeculae are immature and with the drilled cortical edges, additional new bone arising from the
slender. periosteal surface and a general thickening of the bony trabeculae.

THE JOURNAL OF BONE AND JOINT SURGERY


CHARACTERISTICS OF BONE INGROWTH AND INTERFACE MECHANICS OF A NEW POROUS TANTALUM BIOMATERIAL 911

Fig. 5 Fig. 6

Figure 5 – Transmitted light photomicrograph of an interface region of a four-week implant with a small pore size. The reversal line from
the original drill hole is evident and the microtexture of the tantalum struts is apparent (paragon15). Figure 6 – Backscattered scanning
electron micrograph of a 16-week implant of small pore size showing ingrowth of 76%. There are many regions of contact between new
bone and the tantalum struts. A pronounced periosteal reaction has resulted in additional incorporation of the implant by new bone.
Haversian remodelling is evident within the porous network.

there was very dense ingrowth and extensive bone-implant


apposition although there were regions of porosity that
were not filled with bone and tantalum struts which
remained incompletely surrounded by new bone. The
ingrowth often extended abundantly above the periosteal
aspect of the femur and showed cortical remodelling within
the pores into Haversian systems. In some sections, partic-
ularly at four and 16 weeks, there was noticeable intra-
cortical porosity adjacent to the implants, suggestive of a
remodelling phenomenon associated with increased blood
flow and bone turnover during the repair process (Figs 5
and 6).
Mechanical testing. Six of the four-week implants with
small pore sizes were successfully tested mechanically in
that the interface ruptured before mechanical collapse of
the implant. The mechanical test data were found to have a
Fig. 7 normal distribution. The mean shear strength was calcu-
Backscattered scanning electron micrograph of a transverse section lated to be 18.5 MPa (95% CI 17.4 to 19.6). The remaining
through a 52-week implant with a small pore size with ingrowth of 84%. six implants at four weeks and all six implants tested at 16
There is some residual porosity around the tantalum struts but relatively
complete incorporation of the implant. weeks had compressive failure before rupture of the bone-
implant interface. For both time periods, this suggested that
the values of shear strength were higher than those calcu-
partly generated from the periosteal surface. Overall, there lated from the successful tests at four weeks.
was more ingrowth than at two weeks and hence more
regions of apparent contact of bone with tantalum struts. Discussion
The four-week implants showed more complete ingrowth
and many regions of apparent contact between new bone Our study has given an initial characterisation of the
and the porous material in all histological sections (Fig. 5). response of bone to a new porous tantalum biomaterial in a
Ingrowth of bone across the full diameter of the implant canine transcortical model. Substantial filling of the pores
was common. At 16 (Fig. 6) and 52 weeks (Figs 7 and 8) with new bone to 40% to 50% occurred by four weeks with
VOL. 81-B, NO. 5, SEPTEMBER 1999
912 J. D. BOBYN, G. J. STACKPOOL, S. A. HACKING, M. TANZER, J. J. KRYGIER

Fig. 8a Fig. 8b
Transmitted light micrographs of a transverse section through a 52-week implant with small pore size. There are multiple regions of intimate bone-strut
contact and evidence of a vascular supply throughout the ingrown bone (paragon; a)11, b)27).

implants of both pore sizes. This resulted in a mean shear porosity of porous tantalum. The latter, however, has a high
fixation strength of at least 18.5 MPa (2700 PSI). Com- strength:weight ratio and overall mechanical properties
17
pared with previous studies using porous-coated trans- which would be adequate for most clinical applications.
cortical implants, high fixation strength occurred much The bulk properties of the porous tantalum can be con-
earlier with porous tantalum. The data from this investiga- trolled by the manufacturing process; additional strength
tion are best compared with those of an earlier study in can be obtained simply by additional deposition of tantalum
which sintered, beaded cobalt-chrome transcortical on to the struts. This indicates the need for supplementary
implants spanning similar pore sizes were used because characterisation of the mechanical properties of the materi-
1
both had equivalent protocols. The maximum mean shear al with different processing parameters.
strength obtained at four weeks with the beaded cobalt- The pore sizes of both types of implant which we
chrome implants was 9.3 MPa (95% CI 8.3 to 10.3), a evaluated were at the upper limit of the characteristics of
difference of 9.2 MPa (95% CI 7.8 to 10.6) which was pore size of conventional porous materials. Nevertheless,
significant (Student’s t-test; p=0.004). Studies using other the rates of bone ingrowth and the overall extent of filling
porous metals and different implants and testing techniques of the porosities with new bone were very high. There were
have reported fixation strengths to cortical bone at four statistical differences in the mean extent of bone ingrowth
3,21
weeks ranging from 1.2 MPa to 13.1 MPa. between the two pore sizes at the different time periods.
The increased rate of development of the interfacial Implants with the large pore size initially had greater
shear strength with porous tantalum can best be attributed ingrowth, but by 52 weeks those with the small pore size
to the higher volume fraction available for ingrowth. While were more completely ingrown. These differences may
fibre metal coatings have a porosity of 40% to 50% and have resulted from the slight inherent variations in pore
sintered-beaded coatings of the type studied by Bobyn et characteristics between the two types of implant or from
1
al of only 30% to 35%, the porous tantalum material interanimal variability in the healing response. In any case,
examined in this study had a substantially higher porosity the relative differences were not large and unlikely to result
of 75% to 80%. This meant that for any given percentage in any practical or meaningful clinical consequence. The
filling, a greater volume of bone was present within the material of small pore size, by virtue of its higher density of
porous tantalum, thus giving a proportionate increase in struts per unit volume, inherently has stronger mechanical
interface strength. The end result was a faster rate of properties and hence would probably be preferred for most
development of strength. The higher porosity of the porous clinical applications.
tantalum also theoretically allowed a higher ultimate It is possible that the surface microtexture of the struts
strength to develop. Clinically, however, the rate of fixation forming the porous material contributed to the overall
may be more important since the time required for second- osteogenic response. Cell-culture studies and studies in
ary stabilisation of an implant by bone ingrowth can influ- animals with both unloaded and dynamically loaded
ence the load-bearing after operation. implants have shown that microtextured surfaces such as
The measured strength of the interface probably repre- those produced by grit blasting or acid etching are highly
22-25
sents a lower bond since half of the implants at four weeks osteophilic. The histological studies clearly showed
and all at 16 weeks failed in compression before rupture of that the porous tantalum served as an effective scaffold for
the interface. The compressive failure indicated a certain relatively complete incorporation with new bone by 16
reduction in mechanical properties associated with the high weeks, with little change after 52 weeks of implantation.
THE JOURNAL OF BONE AND JOINT SURGERY
CHARACTERISTICS OF BONE INGROWTH AND INTERFACE MECHANICS OF A NEW POROUS TANTALUM BIOMATERIAL 913

Although not as realistic as a fully-functional load- One or more of the authors have received or will receive benefits for
personal or professional use from a commercial party related directly or
bearing model, the transcortical model is very useful for the indirectly to the subject of this article.
initial characterisation of new porous biomaterials. It
allows control of several parameters which influence the References
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