Tissue response to porous tantalum acetabular cups

The Journal of Arthroplasty Vol. 14 No. 3 1999

Tissue Response

to Porous Tantalum

Acetabular Cups A Canine Model J. Dennis Bobyn, PhD, Kai-Kai Toh, BA, MB, BS, S. A d a m H a c k i n g , M E n g , M i c h a e l Tanzer, M D , F R C S ( C ) , a n d J a n J. K r y g i e r , CET

Abstract: This study evaluated the osseous tissue response to a n o n c e m e n t e d metal-backed acetabular component made of a n e w porous tantalum biomaterial. Eleven dogs with bilateral total hip arthroplasties (22 acetabular implants) were studied for a period of 6 months. Thin section histology, high-resolution radiography, and backscattered scanning electron microscopy revealed that all 22 implants had stable b o n e - i m p l a n t interfaces. Regions of bone ingrowth were present in all histologic sections. The depth of bone ingrowth varied from 0.2 m m to the maximal limit of 2 mm. Analyzing contiguous regions of interest across the full b o n e - i m p l a n t interface, the m e a n bone ingrowth for all sections was 16.8% _+ 5.7%. In the peripheral regions of the cup where b o n e - i m p l a n t contact was most consistent, bone ingrowth averaged 25.1% -+ 10.1%. The data indicate that the porous tantalum material is effective for biologic fixation in the dog and may provide a suitable alternative to other porous materials used in acetabular cup design. K e y w o r d s : porous tantalum, acetabular cup, bone ingrowth, total hip arthroplasty, canine.

Noncemented acetabular implants were developed as a potential solution to the unacceptable aseptic loosening rates that occurred with cemented acetabular implants used in total hip arthroplasty. Some of the first-generation noncemented acetabular implants were poorly designed and led to problems such as dissociation of the polyethylene liner from the metal backing, excessive wear, and periimplant osteolysis [1,2]. Given appropriate linerbacking congruency, locking mechanism, and polyethylene thickness and quality, porous-coated, metal-backed acetabular implants of various designs

have shown excellent clinical function and durability of fixation 5 to I0 years after primary surgery [1,3-5]. Retrieval analyses have documented that bone ingrowth occurs reproducibly and to a sufficient extent to establish reliable biologic fixation {6-8]. Fundamental to the stabilization of noncemented cups is achieving a tight initial fit between implant and bone at the time of surgery. This fit provides the optimal conditions for secondary fixation by bone ingrowth. Apart from initial stability, several other factors have been identified as being crucial for the optimization of bone ingrowth. These include pore size, bone-implant apposition, and implant material [2,9-14]. Several materials have been used effectively in the manufacture of porous surfaces for the metal backing, the most common being titanium or cobalt-chrome alloy beads and titanium fiber metal bonded by high-temperature heat treatments.

From the Jo Miller Orthopaedic Research Laboratory, Division of Orthopaedics, Montreal General Hospital McGill University, Montreal Quebec, Canada. Submitted November 17, 1997; accepted August 24, 1998. Reprint requests: J. Dennis Bobyn, PhD, Montreal General Hospital, Room A2-156, 1650 Cedar Avenue, Montreal, Quebec, Canada H3G IA4. Copyright © i999 by Churchill Livingstone® 0883-540319911403-0014510.0010

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The d e v e l o p m e n t of a n e w porous tantalum biomaterial has created n e w opportunities for acetabular cup design. Its mechanical properties and processing characteristics enable the m a n u f a c t u r e of structural c o m p o n e n t s m o r e readily t h a n with conventional porous metals. An example is the fabrication of a one-piece acetabular cup design in which the polyethylene bearing surface is directly compression m o l d e d into a fully porous tantalum metal backing. Preliminary animal studies with transcortical porous t a n t a l u m implants have s h o w n the material to support rapid and extensive bone ingrowth [15]. The present study e x a m i n e d the bone tissue response to the porous t a n t a l u m material in a fully functional canine total hip arthroplasty model.

Materials and Methods

Implants The fabrication process of porous tantalum begins with the pyrolysis (thermal reduction) of a polyu r e t h a n e foam precursor to form a low-density vitreous carbon skeleton with an interconnected d o d e c a h e d r o n array of pores. T h r o u g h chemical vapor deposition and infiltration, commercially pure tantalum is deposited into and a r o u n d the vitreous carbon skeleton. For the present study, tantalum was deposited to a thickness of about 50 pm. This thickness resulted in an engineered structure with

Fig. 1. Scanning electron microscopic image of porous tantalum. The open interconnecting array of pores, the high porosity, and the slight surface texture on the tantalum struts resulting from the chemical vapor deposition process can be noted. (Inset) Scanning electron microscopic image of an interface region between compression-molded polyethylene (lower left) and open tantalum porosity (upper right) of an acetabular cup.

an elastic modulus of about 3 GPa and ultimate compressive and shear strengths of 35 to 40 MPa. The v o l u m e porosity of the final structure was about 75% to 80%, and the average pore size, determined by measuring the width of 1,000 pores in a given plane using the line intercept method, was 427 + 303 p m (Fig. 1) [16]. A hemispherical cup was designed for the canine acetabulum with an outer diameter of 28 mm. A 3-mm-thick porous t a n t a l u m metal backing was created for the direct compression molding of a 5- to 6-mm-thick lining of GUR 1020 ultra-high-molecular-weight polyethylene (without calcium stearate). The processing parameters were such that the polyethylene intruded into the porous tantalum to a depth of about 1 ram, leaving the outer 2 m m of the backing available for tissue ingrowth (Fig. 1). The inner diameter of the cup was 16 mm, and one peripheral edge was chamfered to a c c o m m o d a t e the inferior n o t c h of the canine acetabulum. The acetabular implants were used in conjunction with w r o u g h t cobalt-chrome alloy femoral heads and n o n c e m e n t e d titanium alloy femoral implants that formed the basis of a separate study.

Surgical Protocol Eleven m a t u r e mongrel dogs weighing b e t w e e n 30 and 40 kg u n d e r w e n t staged bilateral noncem e n t e d total hip arthroplasties with a 4 - w e e k interval b e t w e e n operations. Using a modified Hardinge

Tissue Response to Porous Tantalum •

approach to the hip, the head and neck of the f e m u r were exposed, the l i g a m e n t u m teres was divided, and the hip was dislocated. All periacetabular soft tissue, including that in the fovea, was r e m o v e d by sharp dissection and curettage. The acetabulum was r e a m e d sequentially u n d e r copious irrigation with 25- and 2 7 - m m basket reamers. Reaming was continued until some bleeding of the subchondral bone was evident. Care was taken to r e m o v e all cartilage w i t h o u t excessively thinning the acetabular walls. As a result, it was not possible to ream medially to the true acetabular floor in most cases. The final reaming established a 1-mm press-fit b e t w e e n the implant and bone. After irrigation with n o r m a l saline, the cup was impacted into position in 40 ° to 45 ° of abduction and 15 ° to 20 ° of anteversion. A gross assessment of implant stability was made by exerting m a n u a l pressure on the cup rim at circumferential locations. In cases in which the cup required repositioning for improved hip stability, it was either levered out of the acetabulum using a small periosteal elevator or disimpacted using a slaphammer and an i n s t r u m e n t clamped onto the inferior rim. Postoperatively the dogs were administered analgesic and prophylactic antibiotic therapy. They were exercised out of their pens once a day and allowed to weight bear as tolerated. This practice resulted in normal or n e a r - n o r m a l activity levels within 2 to 3 weeks of each surgery. Although force plate analysis was not available to quantify loading, there were no instances of an obvious limp, and there was notable spreading of the hindlimb toes o n ambulation, a positive sign of load bearing. There were 5 dislocations, all within the first 3 weeks of surgery, in 4 cases after the second surgery and once after the initial surgery. An open reduction was p e r f o r m e d in all cases, 2 of which (6 and 8 days postoperatively) required repositioning of the cup. All 5 cases resolved w i t h o u t further complication. The primary factor causing dislocation was the inadequate neck length and offset of the femoral stem. Each e x p e r i m e n t was t e r m i n a t e d 26 weeks from the midpoint of the 2 surgery dates for each dog, establishing implantation periods of 24 and 28 weeks for both sides. The few days of implantation difference for the 2 cases in which the cup was repositioned during open reduction were not factored into the data analysis.

Histologic Analysis After en bloc resection of the acetabular cups and s u r r o u n d i n g bone, the specimens w e r e radiographed in anteroposterior and lateral views. They

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were subsequently stripped of soft tissue, fixed in 10% formalin, dehydrated in increasing concentrations of ethanol, defatted in ether/acetone, and e m b e d d e d in p o l y m e t h y l m e t h a c r y l a t e . The acetabula were sectioned in a coronal plane using a low-speed diamond saw (Isomet I000, Buehler, Lake Bluff, IL) to yield two 2-mm-thick sections t h r o u g h the apical region of the implant. The sections were radiographed on high-resolution film with a Faxitron apparatus (Hewlett Packard, Palo Alto, CA), progressively polished to 600 grit, and ultrasonically cleaned in ethanol. They were sputter coated with gold-palladium ( H u m m e r IV, Anatech Ltd, Alexandria, VA) in preparation for backscattered scanning electron microscopy (JEOL 840A, Peabody, MA). Computerized image analysis based on gray level discrimination was used to generate quantitative information on the percentage of the available porosity that was filled with n e w bone. For each region of interest, 3 area fractions were defined: metal, bone, and n o n b o n e . The v o l u m e fraction or extent of bone ingrowth was calculated by dividing the bone area by the sum of the bone and n o n b o n e areas. This value has b e e n referred to in prior studies as normalizing bone ingrowth for the a m o u n t of available pore space [ 17]. By analyzing 5 contiguous regions of interest across the b o n e - i m p l a n t interface (A, B, C, D, E), the extent of bone ingrowth was determined across the entire circumference of each cup section (Fig. 2). In regions A and E w h e r e the implant backing was outside the bone envelope, the porous tantalum was not included in the available porosity for bone ingrowth. To obtain accurate representation of the area fraction available for bone ingrowth, the inner 1 m m of the porous tantalum was excluded from the calculations because the pores in this region were filled with compression-molded polyethylene (Fig. 1). Differences in bone ingrowth b e t w e e n the left and right sides (4-week implantation difference) and in cases with and w i t h o u t dislocations were assessed for statistical significance using the paired Student's t test and the Wilcoxon rank sum test. Bone density m e a s u r e m e n t s were made of cancellous bone adjacent to the porous interfaces from 18 different cup specimens. This value was calculated by dividing the area fraction of bone by the total area of the region of interest. This value provided an indication of the i n h e r e n t cancellous bone density within the canine acetabulum. One section from each cup was m o u n t e d to a plexiglass slide, progressively t h i n n e d with petrographic grinding techniques, stained with paragon, coverslipped, and e x a m i n e d with transmitted light

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Fig. 2. Radiograph of a coronal section illustrating division of the bone-implant interface into 5 contiguous regions. This section was typical in that it displays uniform bone contact in the peripheral regions (A, B, D, E) and an apical gap caused by conservative reaming of the foveal region (C).

m i c r o s c o p y to obtain qualitative impressions of the tissue response to the p o r o u s tantalum. This response included identification of calcified a n d fibrous tissue, the p r o x i m i t y of n e w b o n e to the t a n t a l u m struts, a n d vascularity and cellularity of n e w bone.

Results Radiography At the time of explantation, all of the cups a p p e a r e d firmly attached to the acetabula. Radiographs on high-resolution film revealed stable b o n e implant interfaces w i t h o u t radiolucencies. Radiograp h y of the sections f r o m 22 cups m o r e clearly revealed the characteristics of the b o n e - i m p l a n t interfaces. In general, close b o n e apposition to the p o r o u s t a n t a l u m was consistent t o w a r d the periphery of the interfaces, w h e r e the acetabular b o n e generally a p p e a r e d m o r e dense (Fig. 2). In 16 of 22 cups in region C, there was a gap b e t w e e n the i m p l a n t a n d b o n e up to 3 m m because the fovea h a d b e e n left incompletely r e a m e d (Fig. 2). In 13 implants, the sections indicated n e w b o n e t o r m a t i o n filling s o m e of the foveal gap. All sections of all implants s h o w e d m a n y regions of a p p a r e n t b o n e contact with p o r o u s tantalum. There w e r e no cases of a c o n t i n u o u s radiolucency that w o u l d indicate fibrous encapsulation.

Microscopy Backscattered scanning electron microscopy confirmed the presence of b o n e i n g r o w t h in all i m p l a n t sections. The extent of i n g r o w t h varied considerably along the circumference of the interfaces, tending to be l o w e r in the m o r e cancellous regions B a n d D (Fig. 3) a n d higher n e a r the peripheral regions A

and E, w h e r e b o n e contact was m o r e u n i f o r m a n d host b o n e was m o r e dense (Fig. 4). As w o u l d be expected, in the d o m e regions w h e r e there was the least p r o x i m i t y to host bone, the extent of i n g r o w t h was often m i n i m a l or absent. The d e p t h of i n g r o w t h varied f r o m a b o u t 0.2 m m in the m o r e central interface regions to the m a x i m a l limit of 2 m m , the level at w h i c h the c o m p r e s s i o n - m o l d e d polyethylene infiltrated the pores. Regions ot gap filling w e r e evidenced by the presence of n e w b o n e b e t w e e n the i m p l a n t and the r e a m e d edge of the a c e t a b u l u m , a feature that was often a p p a r e n t on microscopic e x a m i n a t i o n . Some of these regions w e r e characterized by b o n e ing r o w t h that was continuous with the n e w b o n e within the gaps. In 4 implants, there was evidence that the porous t a n t a l u m material h a d b e e n def o r m e d slightly because it was i m p a c t e d against the h a r d b o n e n e a r the acetabular rim. There was no evidence of material f r a g m e n t a t i o n or separation f r o m the bulk porous structure. The extent of b o n e i n g r o w t h in the 5 contiguous regions of the b o n e - i m p l a n t interface f r o m all histologic sections ranged b e t w e e n 0 % and 60.2% and averaged 16.8% _+ 5.7%. Excluding the central d o m e region C (Fig. 2) representing 2 0 % of the interface in the 16 cases w i t h incomplete i m p l a n t seating, the extent of i n g r o w t h averaged 17.3% _+ 9.2%. E x a m i n i n g only the 2 m o s t peripheral interface regions A and E n e a r the acetabular rim (Fig. 4), the extent of i n g r o w t h for all cups averaged 25.1% _+ 10.1%. The extent of i n g r o w t h on the left and right sides was almost identical (16.9% vs 16.7%), indicating no influence of the 4 - w e e k time interval on the tissue response. In the 5 dislocation cases, the side with the dislocation averaged m o r e b o n e ing r o w t h ( 15.7 %) t h a n the side w i t h o u t ( 14.8 %) but

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Fig. 3. Backscattered scanning electron micrograph of the bone-implant interface in a cancellous bone region corresponding to B or D (Fig. 2). The ingrowth ranges from superficial to deep.

the difference was n o t statistically significant (P > .6). Eighteen different m e a s u r e m e n t s of cancellous bone density were made in areas adjacent to regions B and D of the interface (Fig. 4). The cancellous bone density averaged 17.7% + 5.5%.

Fig. 4. Backscattered scanning electron micrograph of a peripheral region of the interface illustrating a high extent and depth of new bone formation within the porous tantalum. Near the edge of the acetabulum, the bone is more cortical than cancellous in density. Many regions of bone contact with the tantalum struts are apparent.

The histologic analysis by transmitted microscopy confirmed the scanning electron microscopy findings of multiple regions of cancellous-like bone i n g r o w t h in each cup, with variable depth of ingrowth and greater i n g r o w t h at the periphery (Figs. 5 and 6). The bone within the pores and in apparent

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Fig. 7. Histologic sections stained with paragon. (Top) The bone ingrowth is quite sparse overall but denser near the periphery. There is new bone within the foveal gap. (Bottom) Higher magnification of a region of cancellous bone ingrowth. (Original magnification, × 20.)

contact w i t h the t a n t a l u m struts was n o r m a l in structure, cellularity, a n d vascularity, w i t h o u t evidence of cyst f o r m a t i o n or osteoclastic activity. N e w b o n e f o r m a t i o n within the foveal gap was evident in the thin sections as well (Fig. 5). Of i m p o r t a n t note was the c o m m o n feature of the presence of dense fibrous tissue filling m o s t of the pores that w e r e not i n g r o w n with n e w b o n e (Fig. 6). Under polarized light, the fibrous tissue a p p e a r e d r a n d o m l y striated. The overall a p p e a r a n c e was of complete or nearcomplete occlusion of the t a n t a l u m porosity w i t h either fibrous or osseous tissue.

Discussion The p u r p o s e of this study was to evaluate the b o n e tissue response to p o r o u s t a n t a l u m in a loadbearing e n v i r o n m e n t . The hip r e p l a c e m e n t m o d e l is suitable for assessing the potential of a p o r o u s biomaterial for biologic fixation. It is clear f r o m the results of this study that p o r o u s t a n t a l u m supports canine b o n e i n g r o w t h in a reproducible fashion, with all 22 acetabular implants showing signs of

Fig. 6. Histologic sections stained with paragon. (Top) The bone ingrowth is dense and deep near the periphery. Much of the porosity that is void of bone is filled with pink-stained fibrous tissue. (Bottom left) Higher magnification of a region illustrating cellularity and vascularity of newly formed bone. (Original magnification, × 50.) (Bottom right) Higher magnification of a region illustrating bone ingrowth near the top, stained fibrous tissue in the middle, and compression*molded polyethylene at the bottom. (Original magnification, x20.)

stable fixation 6 m o n t h s after surgery. The absolute values of the extent of b o n e i n g r o w t h m a y not h a v e direct clinical relevance, a l t h o u g h t h e y are quite similar to those reported by Pidhorz et al. [8] in a study of autopsy-retrieved, fiber m e t a l - c o a t e d acetabular cups. The data are best c o m p a r e d with similar data f r o m other canine studies on porouscoated acetabular implants. Jasty et al. {13,18] c o m p a r e d the extent of b o n e i n g r o w t h for canine acetabular cups with porous surfaces m a d e of t i t a n i u m fiber m e t a l (21.5% _+ 4.4%) and c o b a l t - c h r o m e beads (13.4% -+ 9.9%). The data f r o m the present study, ranging f r o m 16.8% to 25.1% depending on different regions of the interface, are b o t h comparable a n d within the expected limits given the 17.7% m e a s u r e d i n h e r e n t

Tissue Responseto Porous Tantalum

density of canine acetabular cancellous bone. In terms of the absolute v o l u m e of n e w bone formation within a porous material, for a given percentage of bone ingrowth, m o r e bone would occupy the porous t a n t a l u m t h a n other porous materials. This is because its 75% to 85% porosity is greater than either fiber metal (45% to 50%) or sintered beaded (30% to 35%) coatings. F r o m a theoretical perspective, greater v o l u m e of bone at the interface w o u l d have the effect of increasing the interface mechanical strength. The absence of d o m e contact in the majority of cases was primarily due to incomplete reaming of the fovea to the true floor of the acetabulum. This incomplete reaming resulted from the n e e d to protect the peripheral bone and thin medial wall from excessive reaming because most of the acetabula were smaller than w o u l d have b e e n ideal for a 2 8 - m m diameter implant. The filling of gap regions with n e w bone in the present study occurred to a greater extent t h a n has b e e n reported in prior canine studies with porous-coated acetabular implants [I8]. The most consistent and u n i f o r m b o n e - i m p l a n t contact occurred peripherally, resulting in denser bone ingrowth. In some of the peripheral regions, the bone was dense and ingrowth progressed to the full depth of the porosity. Some of the b o n e densification and additional ingrowth near the rim possibly occurred as a remodeling response to localized stress transfer because of concentrated peripheral contact. Of potential importance was the finding of fibrous tissue t h r o u g h o u t the pores in regions w i t h o u t bone ingrowth, tissue that might represent a mechanical barrier to fluid and particulate material access to the b o n e - i m p l a n t interface. The structural properties of the porous t a n t a l u m material appeared to be suitable u n d e r conditions resembling clinical use. From an engineering standpoint, the compressive and shear strengths of 35 to 40 MPa are comparable with those of other porous metals. Also, finite e l e m e n t studies have s h o w n that peak material stresses experienced during implant loading in the h u m a n acetabulum for low-modulus materials, such as b o n e c e m e n t and porous tantalum, are only in the range of 1 to 2 MPa. Additional strength and structural rigidity could be engineered, if required, by increasing the thickness of t a n t a l u m o n the struts during the chemical vapor deposition process. Deformation of the porous material against hard cortical bone ridges w i t h o u t fragmentation signifies material elasticity and ductility, properties that could help improve initial frictional and geometric fit and facilitate complete implant seating, while reducing the potential for acetabular fracture. The higher friction coefficient of porous tantalum against

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bone compared with conventional porous materials probably contributes to initial implant fixation {19]. The porous t a n t a l u m biomaterial evaluated in this study represents a departure from conventional porous materials in m a n y respects. Although the manufacturing process could theoretically use other metallic biomaterials for deposition onto the carbon skeleton, tantalum is particularly well suited because of its chemical properties, high corrosion resistance, and excellent biocompatibility [20,21]. This suitability has led to its use in a wide variety of clinical settings for m o r e t h a n 40 years, including wire and foil for nerve repair, pacemaker electrodes, radiographic markers, and plates to repair cranial defects {20,22-24]. No adverse response of any type was n o t e d in the histologic analyses, and bone of n o r m a l appearance contacted the tantalum struts. From the perspectives of bone ingrowth and biologic fixation, the data from this study support the further research and d e v e l o p m e n t of porous tantalum for clinical use.

Acknowledgments The authors are grateful for the manufacture and donation of the implants by Implex Corporation, Allendale, New Jersey, and for funding from the Medical Research Council of Canada. Assistance was kindly provided by Dr. Simon Chan and Mr. Justin Bobyn.

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