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Delivery Systems for the BMPs   |    
Biodegradable Poly-d,l-Lactic Acid-Polyethylene Glycol Block Copolymers as a BMP Delivery System for Inducing Bone
Naoto Saito, MD, PhD; Takao Okada, MS; Hiroshi Horiuchi, MD; Narumichi Murakami, MD; Jun Takahashi, MD; Masashi Nawata, MD; Hiroshi Ota, MD; Shimpei Miyamoto, MD, PhD; Kazutoshi Nozaki, PhD; Kunio Takaoka, MD, PhD
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Investigation performed at the Department of Orthopaedic Surgery, Shinshu University School of Medicine, Matsumoto, Japan
Naoto Saito, MD, PhD
Hiroshi Horiuchi, MD
Narumichi Murakami, MD
Jun Takahashi, MD
Masashi Nawata, MD
Hiroshi Ota, MD
Kunio Takaoka, MD, PhD
Department of Orthopaedic Surgery, Shinshu University School of Medicine, Asahi 3-1-1, Matsumoto, 390-8621, Japan. E-mail address for N. Saito: saitoko@hsp.md.shinshu-u.ac.jp

Takao Okada, MS
Research Institute, Taki Chemical Co., Ltd., 64-1 Nishiwaki, Befucho, Kakogawa, Hyogo 675-0125, Japan

Shimpei Miyamoto, MD, PhD
Department of Orthopaedic Surgery, Osaka University Medical School, 2-2 Yamadaoka, Suita, Osaka 565-0871, Japan

Kazutoshi Nozaki, PhD
Applied Pharmacology Laboratories, Institute for Drug Discovery Research, Yamanouch Pharmaceutical Co., Ltd., 21 Miyukigaoka, Tsukuba, Ibaraki 305-8585, Japan

In support of their research or preparation of this manuscript, one or more of the authors received grants or outside funding from a Grant-in-Aid for Scientific Research from the Ministry of Education, Science, Sports and Culture, Japan, a Grant from Japan Rheumatism Foundation, and a Grant from Hip Joint Foundation of Japan. None of the authors received payments or other benefits or a commitment or agreement to provide such benefits from a commercial entity. No commercial entity paid or directed, or agreed to pay or direct, any benefits to any research fund, foundation, educational institution, or other charitable or nonprofit organization with which the authors are affiliated or associated.

The Journal of Bone & Joint Surgery.  2001; 83:S92-S98 
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Abstract

Background: Bone morphogenetic proteins (BMPs) are biologically active molecules capable of eliciting new bone formation. In combination with biomaterials, these proteins can be used in a clinical setting as bone-graft substitutes to promote bone repair. Collagen from animal sources has previously been the preferred carrier material in animal experiments. More recently, synthetic biodegradable polymers have been tested as a delivery vehicle for osteoinductive agents. In earlier studies performed in our laboratory, it was found that the polylactic acid homopolymers (PLA650) and poly-d,l-lactic acid-polyethylene glycol block copolymers (PLA650-PEG200) are viscous liquids that can be used as BMP delivery systems.

Methods: To obtain new PLA-PEG polymers that exhibit greater plasticity, the molecular sizes of PLA and PEG segments in the copolymer chains were increased. Plastic PLA-PEG polymers with various molecular sizes and PLA/PEG ratios were synthesized, mixed with recombinant human (rh) BMP-2, and implanted into the dorsal muscles of mice for 3 weeks to evaluate their capacity to elicit new bone formation. To compare the plastic PLA-PEG polymer with the liquid PLA650-PEG200 polymer, these two polymers were combined with rhBMP-2, implanted, and harvested after 3 weeks. Bone mineral content (BMC), bone area, and bone mineral density (BMD) of the ectopic new bone were measured by means of single energy X-ray absorptiometry (SXA).

Results: All of the PLA6,500-PEG3,000 implants with 10 or 20 g of rhBMP-2 showed new bone formation. In contrast, little or no bone formation was seen in other plastic PLA-PEG implants with rhBMP-2. Control implants that lacked rhBMP-2 did not show new bone formation. Radiographic and histologic examinations showed that the PLA6,500-PEG3,000 implants with rhBMP-2 harvested 3 weeks after implantation had normal bone characteristics with hematopoietic marrow and osseous trabeculae. SXA analysis showed that the values for bone mineral content (BMC), bone area, and bone mineral density (BMD) of new bone resulting from the use of plastic PLA6,500-PEG3,000 polymers with rhBMP-2 were significantly higher than those obtained with the liquid PLA650-PEG200 polymers (p < 0.001 for each of the three values).

Conclusions: These results indicate that the PLA6,500-PEG3000 block copolymer with plastic properties works effectively as a BMP delivery system. These data suggest that the total molecular size and ratio of PLA size to PEG size is an essential factor in determining the efficacy of a BMP delivery system. After implantation, it is possible that the PLA6,500-PEG3,000 pellets might have absorbed tissue fluids and become swollen, resulting in bone formation that exceeded the size of the original implants. This expansion characteristic is a potentially beneficial property, given the intended practical application of the polymer in the repair of bone defects.

Clinical Relevance:

New synthetic biodegradable delivery systems will play an important role in the clinical applications of rhBMPs in which local formation of bone via an osteoinductive graft material is needed. Further pre-clinical and clinical work is necessary to establish the safety of these implants before they are adopted for widespread clinical use.

Figures in this Article
    Bone morphogenetic proteins (BMPs) elicit new bone formation in vivo and have great potential application in orthopaedics to promote hard-tissue repair and reconstruction6,8,18,19,24,27. Some BMP molecules can be successfully synthesized by means of DNA recombination methods28,29. The protein products of human type (recombinant human [rh] BMPs) possess the bone-inducing activity. A large amount of rhBMPs can now be prepared for clinical use as bone-graft substitutes. However, some issues need to be addressed before rhBMPs can be fully applied in clinical practice. One major challenge is to define the optimal delivery system for BMPs10,24. The need for a suitable delivery system can be seen from experimental data that show that implantation of a small amount of pure BMP alone cannot induce new bone formation25,26. However, when the BMP is combined with a suitable delivery system and implanted into muscles, new bone is consistently formed. Until now, collagen from animal sources has been used as a delivery system for BMPs and frequently utilized in animal experiments and in clinical trials1,4,9,11,20,23,26. However, some potential risks in the use of xenogeneic animal collagen—disease transfer and unexpected immunogenic or inflammatory reactions from the host tissues2,5,7—need to be considered.The need to solve these problems led to the development of synthetic polymers that would be suitable as a BMP delivery system3,12,14-17,22,30. However, a limited number of polymer carriers have been developed to date10,24. In general, the carrier materials for BMP must have several specific physical and biological properties10,13. The materials should not be inflammatory or cytotoxic, because an intense inflammatory reaction impedes bone formation by BMP. They should be insoluble under physiological conditions in order to retain the BMP molecules but absorbable by host tissue a few weeks after implantation so that they can be replaced by the newly forming bone.
    As candidate materials with these desired properties, synthetic polylactic acid homopolymers (PLA) were tested in our early studies16(Fig. 1-A). The physical properties, degradation rate, and biological reactions of these polymers change depending on their molecular size. PLA polymers in a range of molecular sizes were synthesized, mixed with BMP, and implanted in mice to test the bone-forming activity of the PLA/BMP composites. New bone formation was seen when a PLA polymer with a molecular size of 650 was combined with BMP and implanted into the mice. Histological analysis of the bone induced by the PLA650/BMP composite showed that the original PLA implant had been completely absorbed and replaced by new bone and marrow. These results suggested that PLA with a molecular size of 650 could be used as a carrier material for BMP. However, it was still unsatisfactory because the induced bone mass was significantly smaller than the original size of the implant. This was thought to be due to the rapid degradation of PLA-650 because of its small molecular size and high acidity, which might have had a harmful effect on the host tissue.
    To make the PLA-650 polymer a more effective carrier, poly-d,l-lactic acid-polyethylene glycol block copolymers (PLA-PEG) were synthesized17(Fig. 1-B). The underlying concept in this approach was that a hydrophilic polyethylene glycol polymer (PEG) with a molecular size of 200 was linked to the PLA650 polymer (PLA650-PEG200 block copolymer) to retard the degradation rate by increasing the molecular size and reduce the acidity by modification of the carboxyl radical. This modification was successful in slowing down the degradation, and the low pH value of PLA-650 improved to reach a neutral value. This modified polymer resulted in improved bone formation by BMP, and the bone mass induced with a constant dose of BMP reached the original size of the implant. This PLA-PEG block copolymer is a viscous liquid at room temperature, and therefore it is difficult to mold into a three-dimensional shape. Because of this difficulty, we developed another new type of PLA-PEG block copolymer that exhibits greater plasticity?21. This was achieved by increasing the molecular sizes of both PLA and PEG segments in the copolymer chains. This type of polymer degrades more slowly than the liquid PLA-PEG polymers.
    This paper describes the results of screening tests of the new PLA-PEG polymers with greater plasticity and comparative tests of these new polymers and the original liquid PLA-PEG polymer in terms of BMP delivery and resultant bone-forming capacity.
     
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    +Fig. 1-A:Fig. 1: A: Structural formula of poly-d,l-lactic acid homopolymer (PLA). m: number of units. B: Structural formula of poly-d,l-lactic acid-polyethylene glycol block copolymer (PLA-PEG). m, n, and o: number of units.
     
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    +Fig. 1-B:Fig. 1: A: Structural formula of poly-d,l-lactic acid homopolymer (PLA). m: number of units. B: Structural formula of poly-d,l-lactic acid-polyethylene glycol block copolymer (PLA-PEG). m, n, and o: number of units.
     
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    +Fig. 2:Classification of six types of poly-d,l-lactic acid-polyethylene glycol block copolymer (PLA-PEG) with plastic properties into four groups according to the calculated molecular weight of the PLA segment and PEG segment. The PLA6,500-PEG3,000 belonged to all four groups.
     
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    +Fig. 3-A:Fig. 3: A and B: A soft radiograph and light micrograph of the new bone formed 3 weeks after implantation in the poly-d,l-lactic acid-polyethylene glycol block copolymer (PLA6,500-PEG3,000) implant with 10 g of recombinant human bone morphogenetic protein (rhBMP-2). (Reprinted, with permission, from: Saito N, Okada T, Toba S, Miyamoto S, and Takaoka K: New synthetic absorbable polymers as BMP-carriers: plastic properties of poly-d,l-lactic acid-polyethylene glycol block copolymers. J Biomed Mater Res 47:104-110, 1999, and: Saito N and Takaoka K: Study of clinical applications of bone morphogenetic proteins. Orthop Surg Traumatol 42:953-958, 1999.) A: A trabecular pattern was observed in the radiopaque area. B: New bone formation with hematopoietic marrow (M) and osseous trabeculae (T) was observed. Hematoxylin and eosin stain.
     
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    +Fig. 3-B:Fig. 3: A and B: A soft radiograph and light micrograph of the new bone formed 3 weeks after implantation in the poly-d,l-lactic acid-polyethylene glycol block copolymer (PLA6,500-PEG3,000) implant with 10 g of recombinant human bone morphogenetic protein (rhBMP-2). (Reprinted, with permission, from: Saito N, Okada T, Toba S, Miyamoto S, and Takaoka K: New synthetic absorbable polymers as BMP-carriers: plastic properties of poly-d,l-lactic acid-polyethylene glycol block copolymers. J Biomed Mater Res 47:104-110, 1999, and: Saito N and Takaoka K: Study of clinical applications of bone morphogenetic proteins. Orthop Surg Traumatol 42:953-958, 1999.) A: A trabecular pattern was observed in the radiopaque area. B: New bone formation with hematopoietic marrow (M) and osseous trabeculae (T) was observed. Hematoxylin and eosin stain.
     
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    +Fig. 4-A:Fig. 4: A and B: The swelling characteristic of the poly-d,l-lactic acid-polyethylene glycol block copolymer (PLA6,500-PEG3,000) is thought to be beneficial when considering the practical application of polymer/bone morphogenetic protein (BMP) composites to repair bone defects. A: Expansion would ensure close contact of the polymer/BMP composite with host bone. B: Impregnating this expandable composite into porous-surfaced solid biomaterials might result in exudation from the surface; therefore, the surface of the implant is covered with new bone.
     
    Anchor for JumpAnchor for Jump
    +Fig. 4-B:Fig. 4: A and B: The swelling characteristic of the poly-d,l-lactic acid-polyethylene glycol block copolymer (PLA6,500-PEG3,000) is thought to be beneficial when considering the practical application of polymer/bone morphogenetic protein (BMP) composites to repair bone defects. A: Expansion would ensure close contact of the polymer/BMP composite with host bone. B: Impregnating this expandable composite into porous-surfaced solid biomaterials might result in exudation from the surface; therefore, the surface of the implant is covered with new bone.
     
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    +Fig. 5:An example of bone induction on the surface of a block of porous hydroxyapatite (HA) combined with bone morphogenetic protein-2 and the plastic and swelling carrier polymer. The composite was implanted into the dorsal muscles of a mouse for 3 weeks. A considerable volume of bone covers the porous HA block.
     
    Anchor for JumpAnchor for Jump  TABLE 1 Characteristics of poly-d,l-lactic acid-polyethylene glycol block copolymers (PLA-PEG)
    PolymerSwelling RatioDegradation Rate (%)
    PLA6,500-PEG3,0001.521
    PLA11,500-PEG3,0000.570
    PLA17,500-PEG3,0000.395
    PLA6,500-PEG1,0000.298
    PLA15,000-PEG8,0001.787
    PLA8,500-PEG1,0000.194
    (Reprinted, with permission, from: Saito N, Okada T, Toba S, Miyamoto S, and Takaoka K: New synthetic absorbable polymers as BMP-carriers: plastic properties of poly-d,l-lactic acid-polyethylene glycol block copolymers. J Biomed Mater Res 47:104-110, 1999.)
     
    Anchor for JumpAnchor for Jump  TABLE 2 Incidence of new bone formation by of poly-d,l-lactic acid-polyethylene glycol block copolymers (PLA-PEG)/recombinant human bone morphogenetic protein-2 (rhBMP-2) composites 3 weeks after implantation
    Amount of rhBMP-2
    Polymer0 g10 g20 g
    PLA6,500-PEG3,0000/66/66/6
    PLA11,500-PEG3,0000/62/63/6
    PLA17,500-PEG3,0000/60/60/6
    PLA6,500-PEG1,0000/60/60/6
    PLA15,000-PEG8,0000/62/62/6
    PLA8,500-PEG1,0000/60/60/6
    (Reprinted, with permission, from: Saito N, Okada T, Toba S, Miyamoto S, and Takaoka K: New synthetic absorbable polymers as BMP-carriers: plastic properties of poly-d,l-lactic acid-polyethylene glycol block copolymers. J Biomed Mater Res 47:104-110, 1999.)
     
    Anchor for JumpAnchor for Jump  TABLE 3 BMC, bone area, and BMD of ectopic new bone induced by polymers with 10 g of rhBMP-2 3 weeks after implantation
    PLA6,500-PEG3,000PLA650-PEG200
    SXA-BMC (mg)19.3 ± 6.3*?6.2 ± 1.3
    Bone area (x10—2 mm2)88.9 ± 10.7*56.1 ± 5.7
    SXA-BMD (mg/cm2)21.3 ± 4.4*11.1 2.0
    Values are mean ± SD. SXA, single energy X-ray absorptiometry; BMC, bone mineral content; BMD, bone mineral density, and rhBMP = recombinant human bone morphogenetic protein. *Significantly different from poly-d,l-lactic acid-polyethylene glycol block copolymers (PLA650-PEG200), p < 0.001.

    Experiment 1

    In order to identify the optimal molecular size of PLA and PEG blocks of plastic polymer, six PLA-PEG block copolymers were synthesized: PLA6,500-PEG3,000, PLA11,500-PEG3,000, PLA17,500-PEG3,000, PLA6,500-PEG1,000, PLA15,000-PEG 8,000, and PLA8,500-PEG1,000 (Table 1). These polymers were further divided into four groups (Fig. 2). In group A, the molecular size of the PEG segment in the copolymer chains was fixed at 3,000 and the molecular size of PLA in the copolymer chains was varied in steps from 6,500 to 17,500. In group B, the molecular size of PLA was fixed at 6,500 and the PEG sizes were changed from 1,000 to 3,000. In group C, the PLA/PEG ratio of molecular size was set at approximately two. In group D, the total molecular size of PLA-PEG was set at 9,500 and ratio of PLA to PEG was changed in steps from 2.2 to 8.5. These plastic block copolymers are hydrophilic and thus swell when placed in water. The swelling property of the polymers was calculated by dividing the weight of the polymer block after swelling in phosphate-buffered saline (PBS) for 24 hours at 37°C by the original weight of the polymer block. To examine the degradation rate, the polymer samples were immersed in PBS and kept in a water bath at 37°C for 20 days. The degradation rate was represented by the weight (percent) of the remaining material (Table 1). These polymers appeared waxy and plastic, with varying degrees of hardness at room temperature.
    Fifty milligrams of each of the polymers was placed in a test tube, and 500 l of acetone was added to dissolve the polymer. After this step, 0 (control), 10, or 20 g of rhBMP-2 dissolved with a buffer (5 mM glutamic acid, 2.5% glycine, 0.5% sucrose, and 0.01% Tween 80) at a concentration of 1 g/l was mixed with the polymer solutions. The mixture was evaporated in a centrifuge/evaporator (by centrifugation in a vacuum) to restore the plasticity of the polymer. The BMP/polymer composite implants thus prepared were implanted into the back muscles of male ddy mice (5 weeks old) to examine their bone-inducing activity (one implant per animal, six mice for the respective dose/carrier material group). Three weeks after implantation, the implants were harvested and examined for new bone formation by radiological and histological methods.

    Experiment 2

    To compare the efficacy of the plastic PLA-PEG polymer that was regarded as the most suitable BMP delivery system in experiment 1 with that of the liquid PLA650-PEG200 polymer, an additional animal experiment was designed. Twenty-five milligrams of the most suitable plastic PLA-PEG polymer was mixed with 10 g of rhBMP-2. For comparison, the same amounts of liquid PLA650-PEG200 polymer with 10 g of rhBMP-2 were also prepared. All implants were inserted into the dorsal muscle pouches of male 5-week-old ddy mice (one implant per animal, five mice for the respective dose/carrier material group). The implants were harvested after 3 weeks and examined for ectopic new bone formation by means of single energy X-ray absorptiometry (SXA) using the analysis program for small animals (DCS-600; Aloka Co., Ltd., Tokyo, Japan). Bone mineral content (BMC) and bone area of the ossicles were measured, and their bone mineral density (BMD) was calculated as BMC/bone area. For analysis of differences between the groups, the unpaired Student’s t test was used. P < 0.05 was considered statistically significant.

    Experiment 1

    At harvest 3 weeks after implantation, none of the PLA-PEG group that lacked BMP (control) showed new bone formation. All of the PLA6,500-PEG3,000 implants with 10 or 20 g of rhBMP-2 showed bone formation with hematopoietic marrow and osseous trabeculae (Figs. 3-A and 3-B). In the PLA11,500-PEG3,000 and PLA15,000-PEG8,000 samples, two or three of six implants with 10 or 20 g of rhBMP-2 showed bone formation. No bone formation was seen in the PLA17,500-PEG3,000, PLA6,500-PEG1,000, and PLA8,500-PEG1,000 samples with any dose of rhBMP-2 (Table 2). From these experimental results, we conclude that a plastic PLA-PEG polymer composed of PLA 6,500 and PEG 3,000 works well as a synthetic carrier of rhBMP-2 and could be a candidate for clinical use for this purpose. There was no evidence of inflammatory or foreign-body reaction from the host tissues adjacent to the new bone in the PLA6,500-PEG3,000 polymer.

    Experiment 2

    The PLA6,500-PEG3,000 polymer identified as the most suitable delivery system for rhBMP-2 in the six plastic polymers from the results of experiment 1 was compared with the liquid PLA650-PEG200 polymer. SXA was used to analyze and compare ectopic bone formation in this experiment. Three weeks after implantation, all the polymers with 10 g of rhBMP-2 showed bone formation. The values for BMC, bone area, and BMD of the ossicles are given in Table 3. The BMC and bone area of ectopic new bone were significantly higher for the PLA6,500-PEG3,000 group than for the PLA650-PEG200 group (p < 0.001, for both values). The BMD of new bone for the PLA6,500-PEG3,000 group was also significantly higher than that for the PLA650-PEG200 group (p < 0.001). This experiment demonstrated that the plastic PLA6,500-PEG3,000 polymer with rhBMP-2 induced a larger amount of new bone with a higher BMD than did the liquid PLA650-PEG200 polymer.
    In experiment 1, various PLA-PEG polymers were synthesized and classified into four groups (A, B, C, and D) according to total molecular size and PLA/PEG ratios. The results demonstrated the efficacy of a PLA-PEG block copolymer with a PLA molecular weight (polymer chain segment molecular weight) of 6,500 and a PEG molecular weight of 3,000 as a rhBMP-2 delivery system. These data suggest that both the total molecular size and the ratio of PLA size to PEG size are essential factors to be considered in creating an effective BMP delivery system. These factors influence both the degradation rate and the swelling ratio, and the PLA6,500-PEG3,000 copolymer showed a high swelling ratio and a rapid degradation (Table 1). This would account for the satisfactory performance of the PLA6,500-PEG3,000 polymer variant.
    In experiment 2, values for BMC, bone area, and BMD of new bone resulting from the use of PLA6,500-PEG3,000 polymer with rhBMP-2 were significantly higher than the values recorded for the PLA650-PEG200 polymer. The reason for the smaller amount of bone induced by PLA650-PEG200 implants might be that this liquid polymer diffuses into the surrounding tissues and thus loses its capacity to provide a scaffold for new bone when implanted in muscle. However, when this polymer is applied to a dead space in bone or to a fracture surface, it could adhere to the site and work well as a BMP delivery system. Because of its viscous liquid nature, the PLA650-PEG200 polymer might be suitable for clinical applications as an injectable semi-liquid composite implant bone repair by means of minimally invasive surgery. Alternatively, the plastic properties of the PLA6,500-PEG3,000 polymer make it convenient for molding the implant to a desired configuration in an intraoperative situation.
    The PLA6,500-PEG3,000 polymer offers an additional advantage as a BMP delivery system for clinical use. The inherent hydrophilic nature of the polymer and resultant swelling property when placed in contact with water for a few hours is a novel and valuable feature of this material. This expansion characteristic of the PLA6,500-PEG3,000 might be advantageous in cases of implantation into bone defects. Because of polymer swelling after implantation, contact between the implant and the bone will become tight and any dead space will be filled more easily after surgery (Fig. 4-A). Another advantage of a polymer with this property would be in combination with biomaterials that have a porous surface. When the pores of the solid implant are filled with the polymer/BMP composite and implanted, the composite will exude from the pores and form a layer of bone covering the surface of the biomaterials. This layer of bone may encase the implant and enhance biological fixation or osseointegration of the biomaterials to the host bone (Fig. 4-B). Figure 5 shows an example of bone induction on the surface of a block of porous hydroxyapatite combined with BMP-2 and this carrier polymer.
    In this study, large new osseous ossicles were induced by the PLA6,500-PEG3,000 block copolymers with rhBMP-2 3 weeks after implantation. However, remnants of the PLA-PEG polymer were observed in the cores of the ossicles, probably due to slow degradation in vivo. To solve this problem, we conducted a subsequent study involving the design of a novel co-polymer with the goal of improving biodegradability and thereby optimizing the delivery system for BMPs. Our approach was founded on the principle of randomly combining para-dioxanone with the PLA segment to control the degradation rate without changing the total molecular weight and PEG molar ratio of the PLA-PEG polymer that showed the most prominent bone-inducing efficacy. The random insertion of para-dioxanone in the PLA segment appeared to promote degradation of the polymer. Thus, a poly-d,l-lactic acid-para-dioxanone-polyethylene glycol block copolymer (PLA-DX-PEG) with a total molecular weight of approximately 9,500 was synthesized. This novel synthetic biodegradable polymer was found to be an effective and suitable carrier polymer for BMP (detailed data will be published elsewhere).
    rhBMPs can now be used for clinical testing 4,9,24. We believe that these new synthetic biodegradable delivery systems will play an important role in the clinical applications of rhBMPs. To substantiate the efficacy of the synthetic polymer/BMP composite for promoting bone healing in clinical situations, further tests on large animals or primates will be essential before human trials of these bone-inducing implants can be conducted.
    AspenbergP,Turek T. BMP-2 for intramuscular bone induction: effect in squirrel monkeys is dependent on implantation site. Acta Orthop Scand,67: 3-6. 1996;673  1996  [PubMed]
     
    BachFH, Fishman JA, Daniels N, Proimos J, Anderson B, Carpenter CB, Forrow L, Robson SC,Fineberg HV. Uncertainty in xenotransplantation: individual benefit versus collective risk. Nat Med,4: 141-144. 1998;4141  1998  [PubMed]
     
    BostromM, Lane JM, Tomin E, Browne M, Berberian W, Turek T, Smith J, Wozney J,Schildhauer T. Use of bone morphogenetic protein-2 in the rabbit ulnar nonunion model. Clin Orthop,327: 272-282. 1996;327272  1996  [PubMed]
     
    BoynePJ, Marx RE, Nevins M, Triplett G, Lazaro E, Lilly LC, Alder M,Nummikoski P. A feasibility study evaluating rhBMP2/absorbable collagen sponge for maxillary sinus floor augmentation. Int J Periodontics Restorative Dent,17: 11-25. 1997;1711  1997  [PubMed]
     
    Butler D: . Last chance to stop and think on risks of xenotransplants. Nature ,391: 320-324. 1998;391320  1998  [PubMed]
     
    CelesteAJ, Iannazzi JA, Taylor RC, Hewick RM, Rosen V, Wang EA,Wozney JM. Identification of transforming growth factor beta family members present in bone inductive protein purified from bovine bone. Proc Natl Acad Sci U S A,87: 9843-9847. 1990;879843  1990  [PubMed]
     
    DeLustroF, Dasch J, Keefe J,Ellingsworth L. Immune responses to allogeneic and xenogeneic implants of collagen and collagen derivatives. Clin Orthop,260: 263-279. 1990;260263  1990  [PubMed]
     
    EinhornTA. Enhancement of fracture-healing. J Bone Joint Surg [Am] ,77: 940-956. 1995;77940  1995  [PubMed]
     
    GeesinkRG, Hoefnagels NH,Bulstra SK. Osteogenic activity of OP-1 bone morphogenetic protein (BMP-7) in a human fibular defect. J Bone Joint Surg [Br],81: 710-718. 1999;81710  1999  [PubMed]
     
    HoffingerJO,Leong K. Poly(alpha-hydroxy acids): carriers for bone morphogenetic proteins. Biomaterials,17: 187-194. 1996;17187  1996  [PubMed]
     
    ItohH, Ebara S, Kamimura M, Tateiwa Y, Kinoshita T, Yuzawa Y,Takaoka K. Experimental spinal fusion with use of recombinant human bone morphogenetic protein. Spine,24: 1402-1405. 1999;241402  1999  [PubMed]
     
    KenleyR, Marden L, Turek T, Jin L, Ron E,Hoffinger JO. Osseous regeneration in the rat calvarium using novel delivery systems for recombinant human bone morphogenetic protein-2 (rhBMP-2). J Biomed Mater Res,28: 1139-1147. 1994;281139  1994  [PubMed]
     
    LangerR. Drug delivery and targeting. Nature,392(6679 Suppl): 5-10. 1998;392(6679 Suppl)5  1998 
     
    LeeSC, Shea M, Battle MA, Kozitza K, Ron E, Turek T, Schaub RG,Hayes WC. Healing of large segmental defects in rat femurs is aided by rhBMP-2 in PLGA matrix. J Biomed Mater Res ,28: 1149-1156. 1994;281149  1994  [PubMed]
     
    MayerM, Hollinger J, Ron E,Wozney J. Maxillary alveolar cleft repair in dogs using recombinant human bone morphogenetic protein-2 and a polymer carrier. Plast Reconstr Surg,98: 247-259. 1996;98247  1996  [PubMed]
     
    MiyamotoS, Takaoka K, Okada T, Yoshikawa H, Hashimoto J, Suzuki S,,Ono K. Evaluation of polylactic acid homopolymers as carriers for bone morphogenetic protein. Clin Orthop,278: 274-285. 1992;278274  1992  [PubMed]
     
    MiyamotoS, Takaoka K, Okada T, Yoshikawa H, Hashimoto J, Suzuki S,Ono K. Polylactic acid-polyethylene glycol block copolymer: a new biodegradable synthetic carrier for bone morphogenetic protein. Clin Orthop,294: 333-343. 1993;294333  1993  [PubMed]
     
    ReddiAH. Symbiosis of biotechnology and biomaterials: applications in tissue engineering of bone and cartilage. J Cell Biochem,56: 192-195. 1994;56192  1994  [PubMed]
     
    ReddiAH. BMPs: actions in flesh and bone. Nat Med,3: 837-839. 1997;3837  1997  [PubMed]
     
    RodeoSA, Suzuki K, Deng XH, Wozney J,Warren RF. Use of recombinant bone morphogenetic protein-2 to enhance tendon healing in a bone tunnel. Am J Sports Med,27: 476-488. 1999;27476  1999  [PubMed]
     
    SaitoN, Okada T, Toba S, Miyamoto S,Takaoka K. New synthetic absorbable polymers as BMP carriers: plastic properties of poly-D,L-lactic acid-polyethylene glycol block copolymers. J Biomed Mater Res ,47: 104-110. 1999;47104  1999  [PubMed]
     
    SandhuHS, Kanim LE, Kabo JM, Toth JM, Zeegen EN, Liu D, Seeger LL,Dawson EG. Evaluation of rhBMP-2 with an OPLA carrier in a canine posterolateral (transverse process) spinal fusion model. Spine,20: 2669-2682. 1995;202669  1995  [PubMed]
     
    SchimandleJH, Boden SD,Hutton WC. Experimental spinal fusion with recombinant human bone morphogenetic protein-2. Spine,20: 1326-1337. 1995;201326  1995  [PubMed]
     
    SchmittJM, Hwang K, Winn SR,Hoffinger JO. Bone morphogenetic proteins: an update on basic biology and clinical relevance. J Orthop Res,17: 269-278. 1999;17269  1999  [PubMed]
     
    TakaokaK, Nakahara H, Yoshikawa H, Masuhara K, Tsuda T,Ono K. Ectopic bone induction on and in porous hydroxyapatite combined with collagen and bone morphogenetic protein. Clin Orthop ,234: 250-254. 1988;234250  1988  [PubMed]
     
    TakaokaK, Koezuka M,Nakahara H. Telopeptide-depleted bovine skin collagen as a carrier for bone morphogenetic protein. J Orthop Res,9: 902-907. 1991;9902  1991  [PubMed]
     
    UristMR. Bone formation by autoinduction. Science,150: 893-899. 1965;150893  1965  [PubMed]
     
    WangEA, Rosen V, D’Alessandro JS, Bauduy M, Cordes P, Harada T, Israel DI, Hewick RM, Kerns KM, LaPan P, Luxenberg DP, McQuaid D, Moutsatsos IK, Nove J,Wozney JM. Recombinant human bone morphogenetic protein induces bone formation. Proc Natl Acad Sci U S A ,87: 2220-2224. 1990;872220  1990  [PubMed]
     
    WozneyJM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM,Wang EA. Novel regulators of bone formation: molecular clones and activities. Science,242: 1528-1534. 1988;2421528  1988  [PubMed]
     
    ZegzulaHD, Buck DC, Brekke J, Wozney JM,Hoffinger JO. Bone formation with use of rhBPMP-2 (recombinant human bone morphogenetic protein-2). J Bone Joint Surg [Am],79: 1778-1790. 1997;791778  1997  [PubMed]
     

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    Anchor for JumpAnchor for Jump
    +Fig. 1-A:Fig. 1: A: Structural formula of poly-d,l-lactic acid homopolymer (PLA). m: number of units. B: Structural formula of poly-d,l-lactic acid-polyethylene glycol block copolymer (PLA-PEG). m, n, and o: number of units.
    Anchor for JumpAnchor for Jump
    +Fig. 1-B:Fig. 1: A: Structural formula of poly-d,l-lactic acid homopolymer (PLA). m: number of units. B: Structural formula of poly-d,l-lactic acid-polyethylene glycol block copolymer (PLA-PEG). m, n, and o: number of units.
    Anchor for JumpAnchor for Jump
    +Fig. 2:Classification of six types of poly-d,l-lactic acid-polyethylene glycol block copolymer (PLA-PEG) with plastic properties into four groups according to the calculated molecular weight of the PLA segment and PEG segment. The PLA6,500-PEG3,000 belonged to all four groups.
    Anchor for JumpAnchor for Jump
    +Fig. 3-A:Fig. 3: A and B: A soft radiograph and light micrograph of the new bone formed 3 weeks after implantation in the poly-d,l-lactic acid-polyethylene glycol block copolymer (PLA6,500-PEG3,000) implant with 10 g of recombinant human bone morphogenetic protein (rhBMP-2). (Reprinted, with permission, from: Saito N, Okada T, Toba S, Miyamoto S, and Takaoka K: New synthetic absorbable polymers as BMP-carriers: plastic properties of poly-d,l-lactic acid-polyethylene glycol block copolymers. J Biomed Mater Res 47:104-110, 1999, and: Saito N and Takaoka K: Study of clinical applications of bone morphogenetic proteins. Orthop Surg Traumatol 42:953-958, 1999.) A: A trabecular pattern was observed in the radiopaque area. B: New bone formation with hematopoietic marrow (M) and osseous trabeculae (T) was observed. Hematoxylin and eosin stain.
    Anchor for JumpAnchor for Jump
    +Fig. 3-B:Fig. 3: A and B: A soft radiograph and light micrograph of the new bone formed 3 weeks after implantation in the poly-d,l-lactic acid-polyethylene glycol block copolymer (PLA6,500-PEG3,000) implant with 10 g of recombinant human bone morphogenetic protein (rhBMP-2). (Reprinted, with permission, from: Saito N, Okada T, Toba S, Miyamoto S, and Takaoka K: New synthetic absorbable polymers as BMP-carriers: plastic properties of poly-d,l-lactic acid-polyethylene glycol block copolymers. J Biomed Mater Res 47:104-110, 1999, and: Saito N and Takaoka K: Study of clinical applications of bone morphogenetic proteins. Orthop Surg Traumatol 42:953-958, 1999.) A: A trabecular pattern was observed in the radiopaque area. B: New bone formation with hematopoietic marrow (M) and osseous trabeculae (T) was observed. Hematoxylin and eosin stain.
    Anchor for JumpAnchor for Jump
    +Fig. 4-A:Fig. 4: A and B: The swelling characteristic of the poly-d,l-lactic acid-polyethylene glycol block copolymer (PLA6,500-PEG3,000) is thought to be beneficial when considering the practical application of polymer/bone morphogenetic protein (BMP) composites to repair bone defects. A: Expansion would ensure close contact of the polymer/BMP composite with host bone. B: Impregnating this expandable composite into porous-surfaced solid biomaterials might result in exudation from the surface; therefore, the surface of the implant is covered with new bone.
    Anchor for JumpAnchor for Jump
    +Fig. 4-B:Fig. 4: A and B: The swelling characteristic of the poly-d,l-lactic acid-polyethylene glycol block copolymer (PLA6,500-PEG3,000) is thought to be beneficial when considering the practical application of polymer/bone morphogenetic protein (BMP) composites to repair bone defects. A: Expansion would ensure close contact of the polymer/BMP composite with host bone. B: Impregnating this expandable composite into porous-surfaced solid biomaterials might result in exudation from the surface; therefore, the surface of the implant is covered with new bone.
    Anchor for JumpAnchor for Jump
    +Fig. 5:An example of bone induction on the surface of a block of porous hydroxyapatite (HA) combined with bone morphogenetic protein-2 and the plastic and swelling carrier polymer. The composite was implanted into the dorsal muscles of a mouse for 3 weeks. A considerable volume of bone covers the porous HA block.
    Anchor for JumpAnchor for Jump  TABLE 1 Characteristics of poly-d,l-lactic acid-polyethylene glycol block copolymers (PLA-PEG)
    PolymerSwelling RatioDegradation Rate (%)
    PLA6,500-PEG3,0001.521
    PLA11,500-PEG3,0000.570
    PLA17,500-PEG3,0000.395
    PLA6,500-PEG1,0000.298
    PLA15,000-PEG8,0001.787
    PLA8,500-PEG1,0000.194
    (Reprinted, with permission, from: Saito N, Okada T, Toba S, Miyamoto S, and Takaoka K: New synthetic absorbable polymers as BMP-carriers: plastic properties of poly-d,l-lactic acid-polyethylene glycol block copolymers. J Biomed Mater Res 47:104-110, 1999.)
    Anchor for JumpAnchor for Jump  TABLE 2 Incidence of new bone formation by of poly-d,l-lactic acid-polyethylene glycol block copolymers (PLA-PEG)/recombinant human bone morphogenetic protein-2 (rhBMP-2) composites 3 weeks after implantation
    Amount of rhBMP-2
    Polymer0 g10 g20 g
    PLA6,500-PEG3,0000/66/66/6
    PLA11,500-PEG3,0000/62/63/6
    PLA17,500-PEG3,0000/60/60/6
    PLA6,500-PEG1,0000/60/60/6
    PLA15,000-PEG8,0000/62/62/6
    PLA8,500-PEG1,0000/60/60/6
    (Reprinted, with permission, from: Saito N, Okada T, Toba S, Miyamoto S, and Takaoka K: New synthetic absorbable polymers as BMP-carriers: plastic properties of poly-d,l-lactic acid-polyethylene glycol block copolymers. J Biomed Mater Res 47:104-110, 1999.)
    Anchor for JumpAnchor for Jump  TABLE 3 BMC, bone area, and BMD of ectopic new bone induced by polymers with 10 g of rhBMP-2 3 weeks after implantation
    PLA6,500-PEG3,000PLA650-PEG200
    SXA-BMC (mg)19.3 ± 6.3*?6.2 ± 1.3
    Bone area (x10—2 mm2)88.9 ± 10.7*56.1 ± 5.7
    SXA-BMD (mg/cm2)21.3 ± 4.4*11.1 2.0
    Values are mean ± SD. SXA, single energy X-ray absorptiometry; BMC, bone mineral content; BMD, bone mineral density, and rhBMP = recombinant human bone morphogenetic protein. *Significantly different from poly-d,l-lactic acid-polyethylene glycol block copolymers (PLA650-PEG200), p < 0.001.
    AspenbergP,Turek T. BMP-2 for intramuscular bone induction: effect in squirrel monkeys is dependent on implantation site. Acta Orthop Scand,67: 3-6. 1996;673  1996  [PubMed]
     
    BachFH, Fishman JA, Daniels N, Proimos J, Anderson B, Carpenter CB, Forrow L, Robson SC,Fineberg HV. Uncertainty in xenotransplantation: individual benefit versus collective risk. Nat Med,4: 141-144. 1998;4141  1998  [PubMed]
     
    BostromM, Lane JM, Tomin E, Browne M, Berberian W, Turek T, Smith J, Wozney J,Schildhauer T. Use of bone morphogenetic protein-2 in the rabbit ulnar nonunion model. Clin Orthop,327: 272-282. 1996;327272  1996  [PubMed]
     
    BoynePJ, Marx RE, Nevins M, Triplett G, Lazaro E, Lilly LC, Alder M,Nummikoski P. A feasibility study evaluating rhBMP2/absorbable collagen sponge for maxillary sinus floor augmentation. Int J Periodontics Restorative Dent,17: 11-25. 1997;1711  1997  [PubMed]
     
    Butler D: . Last chance to stop and think on risks of xenotransplants. Nature ,391: 320-324. 1998;391320  1998  [PubMed]
     
    CelesteAJ, Iannazzi JA, Taylor RC, Hewick RM, Rosen V, Wang EA,Wozney JM. Identification of transforming growth factor beta family members present in bone inductive protein purified from bovine bone. Proc Natl Acad Sci U S A,87: 9843-9847. 1990;879843  1990  [PubMed]
     
    DeLustroF, Dasch J, Keefe J,Ellingsworth L. Immune responses to allogeneic and xenogeneic implants of collagen and collagen derivatives. Clin Orthop,260: 263-279. 1990;260263  1990  [PubMed]
     
    EinhornTA. Enhancement of fracture-healing. J Bone Joint Surg [Am] ,77: 940-956. 1995;77940  1995  [PubMed]
     
    GeesinkRG, Hoefnagels NH,Bulstra SK. Osteogenic activity of OP-1 bone morphogenetic protein (BMP-7) in a human fibular defect. J Bone Joint Surg [Br],81: 710-718. 1999;81710  1999  [PubMed]
     
    HoffingerJO,Leong K. Poly(alpha-hydroxy acids): carriers for bone morphogenetic proteins. Biomaterials,17: 187-194. 1996;17187  1996  [PubMed]
     
    ItohH, Ebara S, Kamimura M, Tateiwa Y, Kinoshita T, Yuzawa Y,Takaoka K. Experimental spinal fusion with use of recombinant human bone morphogenetic protein. Spine,24: 1402-1405. 1999;241402  1999  [PubMed]
     
    KenleyR, Marden L, Turek T, Jin L, Ron E,Hoffinger JO. Osseous regeneration in the rat calvarium using novel delivery systems for recombinant human bone morphogenetic protein-2 (rhBMP-2). J Biomed Mater Res,28: 1139-1147. 1994;281139  1994  [PubMed]
     
    LangerR. Drug delivery and targeting. Nature,392(6679 Suppl): 5-10. 1998;392(6679 Suppl)5  1998 
     
    LeeSC, Shea M, Battle MA, Kozitza K, Ron E, Turek T, Schaub RG,Hayes WC. Healing of large segmental defects in rat femurs is aided by rhBMP-2 in PLGA matrix. J Biomed Mater Res ,28: 1149-1156. 1994;281149  1994  [PubMed]
     
    MayerM, Hollinger J, Ron E,Wozney J. Maxillary alveolar cleft repair in dogs using recombinant human bone morphogenetic protein-2 and a polymer carrier. Plast Reconstr Surg,98: 247-259. 1996;98247  1996  [PubMed]
     
    MiyamotoS, Takaoka K, Okada T, Yoshikawa H, Hashimoto J, Suzuki S,,Ono K. Evaluation of polylactic acid homopolymers as carriers for bone morphogenetic protein. Clin Orthop,278: 274-285. 1992;278274  1992  [PubMed]
     
    MiyamotoS, Takaoka K, Okada T, Yoshikawa H, Hashimoto J, Suzuki S,Ono K. Polylactic acid-polyethylene glycol block copolymer: a new biodegradable synthetic carrier for bone morphogenetic protein. Clin Orthop,294: 333-343. 1993;294333  1993  [PubMed]
     
    ReddiAH. Symbiosis of biotechnology and biomaterials: applications in tissue engineering of bone and cartilage. J Cell Biochem,56: 192-195. 1994;56192  1994  [PubMed]
     
    ReddiAH. BMPs: actions in flesh and bone. Nat Med,3: 837-839. 1997;3837  1997  [PubMed]
     
    RodeoSA, Suzuki K, Deng XH, Wozney J,Warren RF. Use of recombinant bone morphogenetic protein-2 to enhance tendon healing in a bone tunnel. Am J Sports Med,27: 476-488. 1999;27476  1999  [PubMed]
     
    SaitoN, Okada T, Toba S, Miyamoto S,Takaoka K. New synthetic absorbable polymers as BMP carriers: plastic properties of poly-D,L-lactic acid-polyethylene glycol block copolymers. J Biomed Mater Res ,47: 104-110. 1999;47104  1999  [PubMed]
     
    SandhuHS, Kanim LE, Kabo JM, Toth JM, Zeegen EN, Liu D, Seeger LL,Dawson EG. Evaluation of rhBMP-2 with an OPLA carrier in a canine posterolateral (transverse process) spinal fusion model. Spine,20: 2669-2682. 1995;202669  1995  [PubMed]
     
    SchimandleJH, Boden SD,Hutton WC. Experimental spinal fusion with recombinant human bone morphogenetic protein-2. Spine,20: 1326-1337. 1995;201326  1995  [PubMed]
     
    SchmittJM, Hwang K, Winn SR,Hoffinger JO. Bone morphogenetic proteins: an update on basic biology and clinical relevance. J Orthop Res,17: 269-278. 1999;17269  1999  [PubMed]
     
    TakaokaK, Nakahara H, Yoshikawa H, Masuhara K, Tsuda T,Ono K. Ectopic bone induction on and in porous hydroxyapatite combined with collagen and bone morphogenetic protein. Clin Orthop ,234: 250-254. 1988;234250  1988  [PubMed]
     
    TakaokaK, Koezuka M,Nakahara H. Telopeptide-depleted bovine skin collagen as a carrier for bone morphogenetic protein. J Orthop Res,9: 902-907. 1991;9902  1991  [PubMed]
     
    UristMR. Bone formation by autoinduction. Science,150: 893-899. 1965;150893  1965  [PubMed]
     
    WangEA, Rosen V, D’Alessandro JS, Bauduy M, Cordes P, Harada T, Israel DI, Hewick RM, Kerns KM, LaPan P, Luxenberg DP, McQuaid D, Moutsatsos IK, Nove J,Wozney JM. Recombinant human bone morphogenetic protein induces bone formation. Proc Natl Acad Sci U S A ,87: 2220-2224. 1990;872220  1990  [PubMed]
     
    WozneyJM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM,Wang EA. Novel regulators of bone formation: molecular clones and activities. Science,242: 1528-1534. 1988;2421528  1988  [PubMed]
     
    ZegzulaHD, Buck DC, Brekke J, Wozney JM,Hoffinger JO. Bone formation with use of rhBPMP-2 (recombinant human bone morphogenetic protein-2). J Bone Joint Surg [Am],79: 1778-1790. 1997;791778  1997  [PubMed]
     
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    Benjamin W. Kenny
    Posted on February 22, 2009
    Novel Bone Methodologies: The Biomimetic Implant
    Redcliffe Hospital

    To the Editor:

    Today’s social demographic is changing, with the proportion of people older than 65 years in Australia projected to increase from 12% to 21% by 2031 (1). As a result, it is predicted that the number of fractures suffered annually by Australians will also increase (2). It has been established that 15% of fractures result in non-union and require surgical intervention. The treatment of fracture non-unions is therefore clearly set to become an increasingly important issue from both a public health and an individual perspective. For this reason, there has recently been increasing focus on bone implants and the development of improved methodologies.

    Recent articles have discussed/examined the possibility of using a biodegradable implant in a load bearing application (3,4). However the principles behind the development of these implants need to be addressed because without in-depth focus and analysis on potential vascularisation of these implants, regardless of their possible osteoinductive properties, these novel/biomimetic scaffolds are bound to fail. As such, the ideal implant has remained an elusive entity.

    Wintermantel and Mayer (5) developed criteria to describe the ideal implant, which include biocompatibility, bioactivity, native bone growth and angiogenesis., Biocompatibility is the chemical, biological and physical suitability of an implant to the host tissue, and is enhanced when it resembles the tissue it is replacing (6,7). Bioactivity occurs when healthy progenitor cells can ultimately replace lost or damaged tissue, thus allowing cell and vessel in-growth (8,9,10). Native bone growth is required in order for an implant to be considered as a suitable alternative to current grafting techniques and angiogenesis is necessary for bone metabolism, nutrient delivery and therefore bone regeneration.

    Biomimetic scaffolding holds promise for the future as an ideal implant material. It has been suggested that composite materials offer greater potential of surface biocompatibility than the homogenous monolithic materials (11). However, to date, no graft alternative has been found to combine all of the aforementioned aspects.

    There are currently many composite materials at the forefront of bone implant options for load bearing applications. Many of which fulfill components of the criteria set out by Wintermantel and Mayer (5). Some are true homogenous nano-scaffolds that resembles Hodge Petruska’s model of bone (12) while others are composites made at certain percentage ratios with calcium phosphate crystals.

    For load bearing applicability and eventual use as an arthroplasty device, vessel in-growth is essential. For an implant to be replaced by native tissue and consequently fail due to avascular necrosis is pointless. As stated above, if an implant prevents vascularisation or angiogenesis from taking place, bone regeneration will consequently fail.

    The authors did not receive any outside funding or grants in support of their research for or preparation of this work. Neither they nor a member of their immediate families received payments or other benefits or a commitment or agreement to provide such benefits from a commercial entity. No commercial entity paid or directed, or agreed to pay or direct, any benefits to any research fund, foundation, division, center, clinical practice, or other charitable or nonprofit organization with which the authors, or a member of their immediate families, are affiliated or associated.

    References

    1. Williamson OD. Measuring the success of joint replacement surgery. Med J Aust. 1999;179;229-30.

    2. Sanders KM, Nicholson GC, Ugoni AM, Pasco JA, Seeman E, Kotowicz MA. Health burden of hip and other fractures in Australia beyond 2000. Projections based on the Geelong Osteoporosis Study. Med J Aust. 1999;170;467-70.

    3. Cool SM, Kenny B, Wu A, Nurcombe V, Trau M, Cassady AI, Grøndahl L. Poly(3-hydroxybutyrate-co-3-hydroxyvalerate) composite biomaterials for bone tissue regeneration: in vitro performance assessed by osteoblast proliferation, osteoclast adhesion and resorption, and macrophage proinflammatory response. J Biomed Mater Res A. 2007;82;599-610.

    4. Bostman OM. Absorbable implants for the fixation of fractures. J Bone Joint Surg Am. 1991;73:148-153.

    5. Wintermantel E, Mayer J. Anisotropic biomaterials strategies and developments for bone implantation. In: Wise DL, editor. Encyclopedic Handbook of Biomaterials and Bioengineering. New York: CRC; 1995. p 3-42.

    6. Wintermantel E, Ha SW. Biokompatible Werkstoffe und Bauweisen: Implantate fur Medizen und Umwelt. Berlin: Springer; 1998. p 1-36.

    7. Hellman KB, Picciolo GL, Fox CF. Prospects for application of biotechnology-derived biomaterials. J Cell Biochem. 1994;56;210-24.

    8. Shea LD, Wang D, Franceschi RT, Mooney DJ. Engineered bone development from a pre-osteoblast cell line on three-dimensional scaffolds. Tissue Eng. 2000;6;605-17.

    9. Ishaug-Riley SL, Crane-Kruger GM, Yaszemski MJ, Mikos AG. Three-dimensional culture of rat calvarial osteoblasts in porous biodegradable polymers. Biomaterials. 1998;19:1405-12.

    10. Lutton C, Read J, Trau M. Nanostructured biomaterials: a novel approach to artificial bone implants. Aust J Chem. 2001;54:621-23.

    11. Peter SJ, Kim P, Yasko AW, Yaszemski MJ, Mikos AG. Crosslinking characteristics of an injectable poly(propylene fumarate)/beta-tricalcium phosphate paste and mechanical properties of the crosslinked composite for use as a biodegradable bone cement. J Biomed Mater Res. 1999;44:314-21.

    12. Rho JY, Kuhn-Spearin L, Zioupos P. Mechanical properties and the hierarchical structure of bone. Med Eng Phys. 1998;20:92-102.

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