Synthesis and Characterization of Bone Ingrowth Associated with Bone Cement Co-Polymerized with a Biodegradable Material
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1 Biomaterials Research (2005) 9(2) : Biomaterials Research C The Korean Society for Biomaterials Synthesis and Characterization of Bone Ingrowth Associated with Bone Cement Co-Polymerized with a Biodegradable Material Cheol Hong Kim, Keun Oh Park, and Jeong Koo Kim* Department of Biomedical Engineering, Inje University, Gimhae , Korea (Received December 28, 2004/Accepted February 21, 2005) To alleviate fixation-related problems that are associated with cemented total hip arthroplasty (THA), the ingrowth of bone into the mantle of porous bone cement was investigated as a means to promote attachment between the host bone and the implanted cement. We co-polymerized poly methyl methacrylate (PMMA) and poly(l-lactic acid) (PLLA) by introducing an unsaturated alkene (vinyl) group into the PLLA, and the powdered vinyl PLLA (v-plla) was co-polymerized with liquid methyl methacrylate (MMA) to form biodegradable bone cement. Biodegradation of the bone cement was simulated by prolonged immersion in phosphate-buffered saline (ph 7.4). Degradation of cement specimens that contained v-plla was slower than cement that contained only unmodified PLLA. This result indicated that the initial fixation period of the v-plla-containing bone cement was sufficiently long to allow for the ingrowth of bone into the cement mantle, which was confirmed by scanning electron microscopic examination of v-plla-containing bone cement that was implanted into the femurs of rabbits. We conclude that the biomechanical properties of v-pllacontaining bone cement make this material suitable for clinical applications such as THA. Key words: Biodegradable bone cement, Polymethylmethacrylate, Vinyl poly-l-lactic acid, Total hip arthroplasty T otal hip arthroplasty (THA) has become one of the most common types of arthroplasty since Sir John Charnley pioneered the fixation of prostheses in the late 1950s using acrylic bone cement. 1) Despite its widespread application, there are many unresolved complications that are associated with THA, including loosening of the fixation between the cement and the prosthesis or host bone, which occurs in about 10 and 11% of cases, respectively. 2,3) To resolve the problems that are associated with THA, several methods have been suggested, including strengthening the bone cement, precoating the prosthesis with bone cement, and promoting the ingrowth of bone into the bone cement. It has been shown that loosening at the cement prosthesis interface can be reduced by precoating the surface of the prosthesis with a layer of bone cement. 4-8) However, loosening at the cement bone interface is not overcome as easily, because detachment in this case arises from the intrinsic properties of the bone cement as well as extrinsic factors such as the cementing technique and condition of the endosteal host bone. The inherent toxicity of the cement monomer and the inevitable formation of pores in the cement also contribute to the loosening of the cement bone interface. 9) Liu et al. 10) proposed a possible solution to the lack of ingrowth of bone into the cement mantle. Specifically, they proposed that the prosthesis be fixed in place initially by using bone cement; subsequently, the prosthesis could be fixed in place biologically by the ingrowth of bone into pores within the cement mantle that would be formed by the resorption of biodegradable particles. This method resembles the use of naturally porous implants to fix prosthetics in place during cementless THA. However, there are still problems with using naturally porous bone cement, including the fact that resorbable particles within the cement mantle ultimately weaken the cement. To solve this problem, in the present study we tested the hypothesis that the introduction of a reactive site (vinyl group) into the biodegradable portion of poly(l-lactic acid) (PLLA) would provide a bone cement with mechanical properties that are superior to cement that contains unmodified PLLA or poly methyl methacrylate (PMMA) alone. We surmised that the v-plla would bond chemically to PMMA within the cement, and that the copolymerization of the PLLA and PMMA would allow for a firm initial fixation of the prosthesis within the medullary cavity; the subsequent development of pores within the cement would then allow for the ingrowth of bone into the cement to affect a firm fixation of the prosthesis. *Corresponding author: jkkim@bse.inje.ac.kr 71
2 72 Cheol Hong Kim, Keun Oh Park, and Jeong Koo Kim MATERIALS AND METHODS Synthesis of Poly(L-lactic acid) and Vinyl PLLA PLLA was prepared by bulk polymerization of L-lactic acid (Purac PF90, Purac Biochem, Gorinchem, Holland) at 200 C for 8 h. No catalyst was used. The target molecular weight of PLLA was ~2,000 g/mol. An unsaturated form of PLLA containing a double bond (alkene group), namely vinyl PLLA (v-plla), was synthesized as follows. A 10% PLLA solution was prepared by dissolving PLLA in chloroform. Thereafter, purified methacryloyl chloride (Fluka, Switzerland) was added drop-wise into the 10% PLLA solution at 0 C under N 2 atmosphere. The chloroform in the solution was eliminated by means of a rotary evaporator (Büchi R-114, Büchi, Switzerland), and the final product was obtained in the form of a powder. The structure of the v-plla was examined using 1 H- and 13 C-nuclear magnetic resonance (NMR). Preparation of Bone Cement A CMW 1 Original bone cement kit (Depuy, England) was used, which is comprised of two components: 40 g of powdered PMMA and 20 g of liquid methylmethacrylate (MMA). For this study, four types of specimens were prepared (Table 1). Control specimens were prepared with unmodified bone cement (i.e., no PLLA). Type I specimens were prepared by mixing powdered v-plla (30% wt) and PMMA (70% wt). Type II specimens were prepared by mixing v-plla (10% wt), unmodified PLLA (20% wt), and PMMA (70% wt). Type III specimens were prepared from unmodified PLLA (30% wt) and PMMA (70% wt). After the PMMA-containing powder mixture had been prepared, this mixture was blended with liquid MMA at a powder to liquid ratio of 2:1. When combined, the powder and liquid portions of the cement mixture formed a viscous product that was poured into a mold to fabricate the specimens. The specimens were cured for 24 h at room temperature. Seven specimens of each type were fabricated. D638M-93 of the American Society for Testing and Materials (ASTM) for a test of their tensile properties. The tensile test was carried out on a MTS Bionix system on specimens that had been immersed in phosphate-buffered saline (ph 7.4, PBS) for 1, 5, or 9 weeks (see below). A constant crosshead speed of 0.05 mm/s was applied to each specimen. In Vitro Simulation of Biodegradation To simulate the biodegradation of bone cement that normally occurs in vivo, each type of specimen was immersed in phosphate buffered saline (PBS; ph 7.4) at 37 C in a shaking incubator (Model SI300R, Jeiotech, South Korea) at 110 rpm for up to 9 weeks. Changes in the ph of the PBS solution were measured with a Corning-430 ph meter throughout the immersion period. The mass of each specimen was measured before and 9 weeks after immersion using an Ohaus AR2140 microbalance. All specimens were washed with distilled water and dried in a vacuum oven for 48 h before their mass was determined. Specimen Morphology After they had been cleaned and dried (see above), sections of each type of specimen were made using a water-cooled diamond saw (Minitom-Struers, Copenhagen, Denmark). The sections were coated with gold in an ion sputter coater (JEOL model JFC-1100). A scanning electron microscope (SEM; JEOL model JSM-35CF) was used to examine the sections at an intensity of 15 kv. Animal Study Three six-month-old New Zealand white rabbits were used. A type I specimen of fabricated bone cement was placed into the femur of each rabbit as shown in Figure 1. The rabbits were sacrificed 4, 6, and 8 weeks after implantation of the specimens. After the rabbits were sacrificed, the femur was dissected free, fixed in formalin, stained with hematoxylin and eosin, embedded in resin, sectioned, and observed using a SEM. Mechanical Properties of Prefabricated Specimens The specimens were prepared according to standard Table 1. Composition of biodegradable bone cement specimens used in this study Powder (wt%) Vinyl PLLA Unmodified PLLA PMMA Control N/A N/A 100 Type I 30 N/A 70 Type II Type III N/A PMMA, polymethylmethacrylate; PLLA, poly-l-lactic acid. Figure 1. Implantation of a type I bone cement specimen into the femur of a rabbit. Biomaterials Research 2005
3 Synthesis and Characterization of Bone Ingrowth Associated with Bone Cement Co-Polymerized with a Biodegradable Material 73 Figure 2. 1 H (left) and 13 C (right) nuclear magnetic resonance (NMR) spectra of vinyl- poly-l-lactic acid (PLLA). RESULTS The average molecular weight of the PLLA was ~2000 g/ mol, which was confirmed by gel permeation chromatography (data not shown). The structure of the v-plla was identified using 1 H- and 13 C-NMR spectroscopy (Figure 2). The NMR spectra confirmed that a vinyl group had been introduced successfully into the PLLA to create v-plla. The results of the tensile test are summarized in Table 2. The tensile strength of the control specimens was ~36 MPa, and this value was not changed by simulated biodegradation (9-week immersion in PBS; p < 0.05). The average tensile strength of the type I specimens was ~19 and 16 MPa after 5 and 9 weeks of immersion in PBS, respectively. For the type II specimens, the tensile strength was ~15 and 14 MPa after 5 and 9 weeks of immersion in PBS, respectively. The tensile strength of the type III specimens was similar to that of the type II specimens. The average elastic modulus of each type of specimen was similar (Table 3), but decreased for each type Table 2. Summary of tensile strength test results Tensile Strength (MPa) Control ± ± ± 2.94 Type I ± ± ± 2.35 Type II ± ± ± 2.95 Type III ± ± ± 1.73 Liu et al. 10) ± 1.00** N/A N/A in phosphate-buffered saline (PBS) to simulate biodegradation (see Methods). **Data are for bone cement specimens that were impregnated with 30% wt bone particles. of specimen following long-term immersion in PBS. As expected, the mass loss of each experimental specimen increased following immersion in PBS (Table 4). The ph of the PBS solution in which the specimens were immersed was ~7.35 initially; this value was unchanged after 9 weeks of immersion of the control specimens (Table 5). By contrast, the ph of the PBS solutions in which the different types of experimental specimen were immersed decreased over time as the degradation of PLLA increased the acidity of Table 3. Summary of elastic modulus values Elastic Modulus (GPa) Control 1.62 ± ± ± 0.08 Type I 2.06 ± ± ± 0.13 Type II 1.96 ± ± ± 0.10 Type III 2.04 ± ± ± 0.05 in PBS to simulate biodegradation (see Methods). Table 4. Decrease in Mass loss of the specimens during the in vitro degradation simulation Mass loss (%) Control N/A N/A N/A Type I 0.07 ± ± ± 0.28 Type II 0.24 ± ± ± 0.40 Type III 0.27 ± ± ± 0.21 in PBS to simulate biodegradation (see Methods). Vol. 9, No. 2
4 74 Cheol Hong Kim, Keun Oh Park, and Jeong Koo Kim Table 5. Changes in the ph of the solutions in which specimens were immersed during the in vitro degradation simulation ph Control N/A N/A N/A Type I 7.36 ± ± ± 0.11 Type II 7.37 ± ± ± 0.04 Type III 7.28 ± ± ± 0.10 in PBS to simulate biodegradation (see Methods). the solutions. For the type I specimens, the ph of the PBS solution was ~7.36 after week 1, ~7.22 after week 5, and ~6.71 after week 9. A similar decrease in ph was noted for the experimental II and III specimens. Relatively few pores were observed in the control specimens. By contrast, surface porosity of the experimental I and II specimens was ~24% after 9 weeks of immersion in PBS, while surface porosity of the type III specimens was 39% after the same period. For the experimental I and III specimens, there was some evidence of PLLA particle absorption after week 5, and many pores were observed after week 9 (Figure 3). However, the pores in the type I specimens (Figure 3B) were larger and deeper than those in the type III specimens (Figure 3D). This may have been due to the inclusion of v- PLLA in the type I specimens. In the rabbits in which a type I specimen had been implanted, there was no apparent bonding between the host bone and the cement specimens 4 weeks after implantation, Figure 4. SEM micrograph of the right femur of a rabbit 8 weeks after implantation of a specimen of bone cement that contained v-plla (type I specimen). The arrow indicates the interface between the host bone and the implanted cement. Note the absence of attachment between the bone and cement. Figure 5. SEM micrograph of the right femur of a rabbit 8 weeks after implantation of a specimen of bone cement that contained v-plla (type I specimen). The arrow indicates the interface between the host bone and the implanted cement. Note the ingrowth of bone into pores within the cement. i.e., the host bone was not attached to the bone cement (Figure 4). However, at 8 weeks after implantation, ingrowth of bone into pores within the bone cement was observed, which increased the strength of the bond between the host bone and the cement (Figure 5). DISCUSSION Figure 3. SEM micrographs of cross-sections of type I and III specimens after 5 (A and C) and 9 (B and D) weeks of immersion in phosphate-buffered saline to simulate biodegradation. Pores that formed following the hydrolysis of PLLA can be seen in the specimens. In the present study, we prepared v-plla and co-polymerized v-plla with PMMA and MMA monomers to produce biodegradable bone cement. Specimens that were fabricated from unmodified bone cement (control specimens) were unaffected by simulated biodegradation (immersion in PBS for up to 9 weeks). Similarly, the tensile strength of the specimens that contained v-plla but no unmodified PLLA (type I specimens) was not changed substantially by long-term immersion in PBS, whereas the tensile strength of the specimens that contained both v-plla and unmodified PLLA (type II specimens) decreased more rapidly than that of the type I specimens. This may have been due to the greater Biomaterials Research 2005
5 Synthesis and Characterization of Bone Ingrowth Associated with Bone Cement Co-Polymerized with a Biodegradable Material 75 amount of copolymerization of v-plla and PMMA in the specimen that did not contain any unmodified PLLA. Nevertheless, the tensile strength of the type III specimens was 14.3% lower after 5 weeks of immersion in PBS, which indicates that the co-polymerized PLLA was degraded, albeit at a slower rate than the non-polymerized PLLA. The difference in the rates of degradation of the type I and II specimens can be explained as follows. First, the PLLA particles dissolved, and this facilitated penetration of the cement mantle by the PBS solution. Second, the PBS solution that penetrated the cement might have accelerated the hydrolysis of the remaining PLLA, thereby weakening the specimen further. However, because co-polymerized v-plla would take longer than unmodified PLLA to be hydrolyzed, the specimens that contained v-plla retained their tensile strength relatively longer than the specimens that contained only unmodified PLLA. Compared with Liu et al. s study, 10) the tensile strength and elastic modulus of the different types of experimental specimen in the present study were similar during the initial period of immersion in PBS, irrespective of whether the specimens contained v-plla. Clearly, the addition of PLLA to the bone cement increased the elastic modulus of the specimens relative to the control specimens, which did not contain any PLLA. An increase in the modulus of elasticity has also been described following the addition of hydroxyapatites to cement, and this phenomenon was predicted qualitatively by Hlavacek s continuum theory of spherical and elliptical inclusion in isotropic elastic materials. 10) In the present study, SEM revealed that pores were visible in the type specimens after 5 weeks of immersion in PBS, but pores had not formed in the type I specimens after 5 weeks of immersion. This observation further supports our conclusion that the copolymerization of PLLA and PMMA delays the degradation of PLLA. In an animal study, the formation of pores appeared to facilitate the attachment of host bone to cement specimens after a period of several weeks. In the rabbits in which type I specimens were implanted in the femur, we found that the cement was not attached to the host bone after 4 weeks of implantation. However, after 8 weeks of implantation, there appeared to be ingrowth of bone into the cement, and the cement and host bone appeared to be closely conjugated. CONCLUSION The crucial factors for preventing the loosening of prosthetics hips are the initial mechanical stability of the prosthesis and bone cement, and the subsequent degradation of the bone cement after an appropriate period to allow for ingrowth of bone into the cement. The results of the present study indicate that copolymerization of bone cement with a biodegradable material, namely v-plla, produced a bone cement that was mechanically stable for approximately 5 weeks, after which it degraded slowly. The degradation of the cement after 5 weeks facilitated the ingrowth of bone into the cement, which occurred via pores within the cement mantle. Therefore, we conclude that co-polymerized bone cement exhibits features that make this material a suitable hybrid fixation material: it is initially mechanically stable, which enables prosthetics to remain fixed in place, and it subsequently facilitates the biological fixation of the prosthetic by the ingrowth of bone. We believe that these biomechanical properties of v-plla containing bone cement make this material suitable for use in clinical applications such as THA. ACKNOWLEDGMENT This work was supported by a grant from Inje University, REFERENCES 1. W. H. Harris, Revision surgery for failed, non-septic total hip arthroplasty, femoral side, Clin. Orthop. Rel. Res., 170, 8-20 (1982). 2. W. H. Harris, R. E. White, S. Mitchell, and F. Barber, A new technique of removal of broken femoral stems in total hip replacement, J. Bone Joint Surg., 63A, (1981). 3. A. Knoell, H. Maxwell, and C. Bechtol, Graphite fiber-reinforced bone cement, Ann. Biomed. Eng., 3, (1973). 4. J. K. Kim and J. B. Park, Fatigue properties and stem subsidence in wire coil reinforced PMMA bone cement: a preliminary in vitro study, Biomed. Mater. Eng., 6, (1996). 5. J. K. Kim and J. B. Park, Reinforcement of bone cement around the femoral prosthesis tip by pre-coated wire coil: a human cadaver bone study, Biomed. Mater. Eng., 6, (1996). 6. J. R. Frigstad and J. B. Park, Reinforcement of PMMA bone cement with a continuous wire coil - a 3D finite element study, Biomed. Mater. Eng., 6, (1996). 7. D. W. Burke, E. I. Gates, and W. H. Harris, Centrifugation as a method of improving tensile and fatigue properties of acrylic bone cement, J. Bone Joint Surg., 66A, (1984). 8. H. C. Amstutz, K. L. Markolf, G. M. McNiece, and T. A. Gruen, Loosening of total hip components; cause and prevention, in: The Hip, Hip Society (Ed.), C. V. Mosby Co., St. Louis, 1976, pp T. S. Gruen, G. M. McNiece, and H. C. Amstutz, Mode of failure of cemented stem-type femoral component: A radiological analysis of loosening, Clin. 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6 76 Cheol Hong Kim, Keun Oh Park, and Jeong Koo Kim 12. J. B. Park, A. F. Von Recum, and G. E. Gratzick, Pre-coated orthopedic implants with bone cement, Biomater. Med. Dev. Artif. Org., 7, (1979). 13. K. R. Dai, Y. K. Liu, J. B. Park, and Z. K. Zhang, Bone particle impregnated bone cement: An in vivo weight-bearing study, J. Biomed. Mater. Res., 25, (1991). 14. J. B. Park, W. W. Choi, Y. K. Liu, and T. W. Haugen, Bone particle impregnated polymethylmethacrylate: An in vivo study, Proc. International Congress on tissue Integration in Oral and Maxillo-Facial Reconstruction, Brussels (Belgium), May 22-24, 1985, pp Biomaterials Research 2005
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