Ovid: PREIDLER: Invest Radiol, Volume 31(11).November 1996.716-723

© Lippincott-Raven Publishers

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Volume 31(11), November 1996, pp 716-723

Coralline Hydroxyapatite Bone Graft Substitutes: Evaluation of Bone Density with Dual Energy XRay Absorptiometry [Original Investigation]

PREIDLER, KLAUS W. MD*; LEMPERLE, STEFAN M. MD†; HOLMES, RALPH E. MD†; CALHOUN, CHRISTOPHER J. MB†; SHORS, EDWIN C. PHD‡; BROSSMANN, JOACHIM MD*; SARTORIS, DAVID J. MD* From the *Department of Radiology, Veterans Affairs Medical Center and University of California San Diego; the †Department of Plastic Surgery, University of California San Diego; and ‡ Interpore International Inc., Irwine, California. Supported in part by Schrödinger Stipendium J01080-Med. Reprint requests: Klaus W. Preidler, Dept. of Radiology, Auenbruggerplatz 9, 8036 Graz, Austria. Received June 11, 1996, and accepted for publication, after revision, July 15, 1996.

Abstract RATIONALE AND OBJECTIVES: The authors evaluate whether dual-energy x-ray absorptiometry (DXA) is a reliable method to determine the density of natural coralline hydroxyapatite (HA) blocks used as bone graft substitutes. METHODS: To evaluate the basic density of HA blocks from the same coral heads with and without titanium meshes, densitometry of 12 HA-500 blocks (genus Goniopora) and 12 HA-200 blocks (genus Porites) was performed. In addition, density measurements of 30 HA blocks (HA500, n = 15; HA-200, n = 15) from different coral heads were obtained to assess if the originating coral head influences the basic density of blocks within one coral genera. To assess standard deviation serial measurements on eight coralline HA blocks, four with titanium meshes and four without were performed. In the ex vivo study, densitometry of 12 HA blocks (HA-500, n = 4; HA-200, n = 8) used as bone graft substitutes in the mandibles and craniums of adult mongrel dogs was performed. Densities were measured after bone ingrowth for 2 and 4 months, respectively. All measurements were obtained with a Lunar DPX with scan mode “slow 750” in the spine program with the regions-of-interests selected manually. Bone ingrowth was assessed by computerassisted histomorphometry, which was considered the gold standard. Statistical analysis was performed to correlate the densities of plain HA blocks with and without meshes to the specific weights of the blocks. RESULTS : Significant positive correlation was found between the density of each HA block (both coral species) with and without meshes and the calculated specific weights. Densitometry values showed no significant differences depending on the originating coral heads. Standard deviation ranged between ±3.8% and ±4.1% (HA-500) and between ±3.0% and ±3.8% (HA200). Hydroxyapatite-500 blocks showed marked increased densities between 15% and 34% after 4 months in three specimens in which bone ingrowth between 16.9% and 21.1% was revealed by histomorphometry; no increase of density was observed in one specimen, which presented only minimal bone ingrowth and signs of infection. Despite bone invasion between 12% and 25.8%, no increased densities were observed for HA-200 implants. http://gateway.uk.ovid.com.proxy.lib.umich.edu/gw2/ovidweb.cgi

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CONCLUSIONS: Dual-energy x-ray absorptiometry is an accurate and reproducible modality to assess the densities of plain coralline HA blocks and to monitor bone ingrowth into coralline HA500 but not into HA-200 block implants.

POROUS HYDROXYAPATITE (HA) IN THE FORM OF large blocks is of considerable interest as a possible bone graft substitute. As a symmetrically oriented structure with a pore size and interconnecting fenestrations of larger than 100 µm, bone cells and vessels can invade this structure and fill it uniformly without any signs of graft rejection.1-4 Two species of corals with different pore sizes and interconnecting fenestrations have been established for use as bone substitutes when converted to HA forms: coral from the genus Porites (HA-200), which has an architectural similarity to cortical bone, and from the genus Goniopora (HA-500), which is similar structurally to cancellous bone 4-8 (Fig. 1). The course of bone ingrowth and the biomechanical properties of these different types of coralline HA have been described in numerous studies using mainly histomorphometric evaluation. 2,3,5,9 Accurate noninvasive assessment of bone ingrowth in coralline HA implants is important for follow-up in clinical practice. However, there are few studies in the literature in which the radiographic characteristics of bone ingrowth have been described. These features include slight loss of distinctness of implant architecture with increasing bone density.6,7,10 In all of these studies, conventional radiographs were used for assessment of bone ingrowth. Dual-energy x-ray absorptiometry (DXA) is a well-established, noninvasive technique for analysis of bone mineral content and density.11 In this study, we attempted to evaluate whether DXA is a reliable method to determine the basic density of coralline HA derived from the two major coral genera and to assess the density of coralline implants according to the degree of bone ingrowth.

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Figure 1. Two species of coralline hydroxyapatite bone substitutes. (A) Hydroxyapatite [HA]-500 (genus Geniopora) has architectural similarity to cancellous bone and was used as a mandibular bone graft substitute. (B) HA-200 (genus Porites) with architectural similarity to cortical bone was used as cranial bone graft substitutes.

Materials and Methods To evaluate the basic density of corals, we performed densitometry on 12 blocks of HA-500 (Pro Osteon 500, Interpore Int., Irvine, CA) originating from the same coral head and 12 blocks of HA-200 (Interpore 200, Interpore Int., Irvine, CA) originating again from the same coral head. The volumes of the blocks varied from 8.237 cm 3 to 8.707 cm 3 for HA-500 and from 1.899 cm 3 to 2.368 cm 3 for HA-200. The weights of the blocks ranged from 7.3 to 8.4 g for the HA-500 blocks and from 2.52 to 3.36 g for the HA-200 blocks. Specific weights (g/cm 3) were calculated by dividing the weight of the block by the block volume. To eliminate inaccurate densitometry measurements caused by air within the coral pores, all coral blocks were sucked with water under vacuum and motion. Subsequently, the blocks were placed into a container filled with water (kept at a constant depth of 10 cm). For densitometry measurements, we used a Lunar DPX unit (Lunar Corporation, Madison, WI) with the scan mode “slow 750” in the spine program. To minimize the scan time, four blocks were measured together in one scan. The regions of interests (ROI) were selected manually and included the entire HA block. Measurement results were given in g/cm 2 (areal density). After dividing these results through the third dimension (height) of the blocks, the results allowed expression of the density of the entire coral block in g/cm 3 (true density) (Fig. 2).

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Figure 2. Schematic drawing of a coralline hydroxyapatite block. Dual-energy x-ray absorptiometry areal density values in g/cm 2 are referring to the x-y plane. To get the true density for the entire block (g/cm 3) this value must be divided by the third dimension (z). Densitometry was repeated on all 24 coralline HA blocks after wrapping them with a fine titanium mesh (Milas Titanium, 24-inch, 0.010 wire; Codman & Shurtieff Inc., Randolph, MA), because this technique was used in our surgical samples. The ex vivo samples in our study were wrapped with titanium mesh only to maintain experimental consistency with control defects treated with particulated cancellous bone autografts where the mesh provided containment. In addition, densitometry was performed on another 15 blocks of HA-500 and 15 blocks of HA-200, each originating from three different coral heads, to determine whether blocks from the same species but different coral heads show marked differences in density. The dimensions of the blocks ranged from 8.611 cm 3 to 8.928 cm 3 and weights ranged from 6.72 g to 8.24 g for the HA-500 blocks; values ranged from 1.761 cm 3 to 2.01 cm 3 and 1.72 g to 2.26 g, respectively, for the HA-200 blocks. The specific weight was calculated for each coral block. Density measurements were performed as described previously with the coral blocks suctioned with water. With the goal to evaluate the measurement deviation of the densitometry unit for coral blocks with and without meshes, eight HA 500 blocks (four wrapped with a titanium mesh, four without mesh) were measured 12 times consecutively using the same scan parameters and constant positioning. Statistical analysis was performed using Pearson's correlation to evaluate the relation between the specific weight and the calculated density values (g/cm 3) for the entire coral blocks with and without titanium meshes.

Experimental Animal Study Hydroxyapatite-500. Four healthy adult mongrel dogs (weight 23-24 kg), which were part of an experimental animal study (approved by the Animal Care and Use Committee) conducted by the http://gateway.uk.ovid.com.proxy.lib.umich.edu/gw2/ovidweb.cgi

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experimental animal study (approved by the Animal Care and Use Committee) conducted by the Department of Plastic Surgery, underwent mandibular resection after having edentulation. Under general anesthesia, the body of the right mandible was exposed by circumferential subperiosteal dissection. After creating a 30-mm segmental defect, the mandible was stabilized rigidly by internal fixation using a titanium plate and screws (THORP Reconstruction Set, Synthes Maxillofacial, Paoll, PA). Subsequently, the defects were filled with a steam-sterilized coralline HA-500 block (30 mm × 20 mm × 12 mm) that was wrapped with a titanium mesh to maintain consistency with other experimental treatments and to prevent soft-tissue prolapse (Figs. 3A and 3B) . After 2 months (n = 1) and after 4 months (n = 3) the dogs were killed by intravenous injection of a euthanasia solution; the implants were harvested en bloc and fixed in 10% formalin solution. The specimens were devoided of all soft tissues and divided in two hemi-mandibles at the symphysis (Fig. 3C).

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Figures 3A-3C. Mandibular specimen (hydroxyapatite [HA]-500 block). (A) Surgical model: A 30-mm segmental defect in the mandible was closed with a 30-mm × 12-mm × 20-mm HA-500 block (arrow) surrounded by a titanium mesh (open arrowheads) to prevent softtissue prolapse. Internal fixation was provided by a titanium plate (short arrows) and screws. (B) A segmental defect is filled with a HA-500 block (arrow). Titanium plate and screws (arrowheads) provide stability of the bone graft substitute. The coral block is wrapped with a titanium mesh (short arrows). Note elevation of the mesh to render the HA block visible. (C) Mandibular specimen as available for our densitometry measurements. Hydroxyapatite-200. Four adult mongrel dogs (weighing 24-25 kg) underwent bilateral craniectomy. The parietal bones were exposed bilaterally after skin incision and elevation of the muscle layers. Fullthickness window defects measuring 20 mm × 15 mm were created bilaterally in the temporal fossae lateral to the sagittal crest. The defects were filled with coralline HA-200 blocks that were covered with a titanium mesh on both intracranial and extracranial surfaces (Fig. 4A) . One dog was killed after 2 months and the other three were killed after 4 months with intravenous injection of euthanasia solution. After en block harvest of the coralline implants, the experimental areas were fixed in 10% formalin solution (Fig. 4B) .

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Figures 4A and 4B. Cranial specimen (hydroxyapatite [HA]-200 block). (A) Surgical model: Bilateral cortical defects in the cranium were fitted with 20-mm × 15-mm × 5-mm HA-200 blocks (long arrows) surrounded by a titanium mesh (short arrow) to prevent softtissue prolapse. (B) Cranial specimen as available for our densitometry measurements. Densitometry of four mandibular specimens (one at 2 months, three at 4 months) and eight cranial specimens (two at 2 months, six at 4 months) was performed with the titanium mesh left in place. The mandibular specimens were positioned identically to the plain coralline samples, and the cranium http://gateway.uk.ovid.com.proxy.lib.umich.edu/gw2/ovidweb.cgi

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mandibular specimens were positioned identically to the plain coralline samples, and the cranium specimens were positioned with the convex side facing upward. All density measurements were performed with the specimens placed in a container filled with a constant amount of 70% methyl alcohol. We used a Lunar DPX unit (Lunar Corporation, Madison, WI) using scan mode “slow 750” in the spine program. The ROIs were selected manually to include only the coralline implant and to exclude the stabilizing titanium plates and screws.

Histomorphometric Analysis After removal of adjacent soft tissue, all specimens (HA-200 and HA-500) were dehydrated in alcohol, vacuum infiltrated, and embedded in methylmethacrylate Technovit 7200 VLC for histologic processing. Three 2-mm thick sections along the longitudinal axis of each specimen were obtained for scanning electron microscopy back-scattered electron imaging and computer-assisted histomorphometry. Histomorphometric analysis was performed according to protocols found in the literature, whose results are considered the gold standard. 12

Results True densities of the 12 HA-500 blocks ranged from 0.849 g/cm 3 and 0.989 g/cm 3; for the HA-200 blocks, densities ranged from 1.327 g/cm 3 and 1.597 g/cm 3. Areal density values for the HA-500 blocks ranged from 1.643 g/cm 2 and 1.896 g/cm 2 for specimens without meshes and from 1.660 g/cm 2 and 2.067 g/cm 2 in specimens with meshes; for the HA-200 blocks, the corresponding values were 0.825 g/cm 2 to 1.157 g/cm 2 without meshes and 0.937 g/cm 2 to 1.178 g/cm 2 with meshes. The DXA density values in g/cm 2 and g/cm 3 for the entire blocks as well as the specific weight for each separate block with and without meshes are given in Tables 1 and 2.

TABLE 1. Densitometric Measurements and Specific Weights of Plain Coralline Hydroxyapatite 500 and Hydroxyapatite 200 Blocks Without Titanium Meshes

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TABLE 2. Densitometric Measurements and Specific Weights of Plain Coraline Hydroxyapatite 500 and Hydroxyapatite 200 Blocks Surrounded with a Titanium Mesh The specific weights of 15 HA-500 blocks from three different coral heads (five blocks from each location) were as follows: coral head A, 0.802 to 0.954 g/cm 3; coral head B, 0.840 to 0.920 g/cm 3; coral head C, 0.763 to 0.833 g/cm 3. The DXA density values for blocks from the same three coral heads were as follows: coral head A, 0.783 to 0.940 g/cm 3; coral head B, 0.856 to 0.855 g/cm 3; coral head C, 0.748 to 0.860 g/cm 3. The calculations of specific weight for 15 HA-200 blocks from three different coral heads revealed the following values: coral head 1, 0.984 to 1.036 g/cm 3; coral head 2, 1.054 to 1.108 g/cm 3; coral head 3, 0.950 to 1.132 g/cm 3. Dual-energy x-ray absorptiometry density measurements for blocks from the same coral heads were as follows: coral head 1, 0.859 to 0.996 g/cm 3; coral head 2, 0.878 to 1.101 g/cm 3; coral head 3, 0.820 to 1.019 g/cm 3. The DXA density values in g/cm 3 and g/cm 3 for the entire blocks and specific weights for each separate block are given in Tables 3 (HA-500) and 4 (HA-200).

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TABLE 3. Densitometric Measurements and Specific Weights of Plain Coralline Hydroxyapatite 500 Blocks Originating from Three Different Coral Heads Results of our precision measurements showed density values for the four HA-500 blocks without meshes of 0.839 g/cm 3 ± 0.0346 (4.1%), 0.942 g/cm 3 ± 0.0364 (3.8%), 0.847 g/cm 3 ± 0.035 (4.1%), 0.884 g/cm 3 ± 0.036 (4.1%). Density values for the four HA-500 blocks wrapped with titanium meshes were as follows: 0.921 g/cm 3 ± 0.0326 (3.5%), 0.879 g/cm 3 ± 0.0334 (3.8%), 0.932 g/cm 3 ± 0.0277 (3.0%), 0.883 g/cm 3 ± 0.0313 (3.5%). Statistical analysis revealed a highly significant positive correlation between the specific weight and the density measurements for all 27 HA-500 blocks without the meshes (r = 0.8436; P < 0.0001), and for all 27 HA-200 blocks without meshes (r = 0.9276; P < 0.0001). Significant positive correlation also was observed between the densities of the coral blocks with meshes and the specific weights of the plain HA-500 blocks (r = 0.7437; P = 0.006) and the HA-200 blocks (r = 0.503; P = 0.0230).

Animal Study Densitometry of three mandibular specimens (4 months after implantation) (specimens 1-3) revealed calculated density values (height of the block, 20 mm) from 0.852 g/cm 3 to 1.249 g/cm 3. One mandibular specimen (2 months after implantation) had a density of 1.117 g/cm 3 (specimen 4). In six cranial http://gateway.uk.ovid.com.proxy.lib.umich.edu/gw2/ovidweb.cgi

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specimen (2 months after implantation) had a density of 1.117 g/cm 3 (specimen 4). In six cranial specimens (5-10), (4 months after implantation) densitometry values calculated for the entire block (height of the blocks, 5 mm) ranged from 1.322 g/cm 3 to 1.724 g/cm 3. For two cranial specimens (11 and 12), 2 months after implantation, density values were 1.570 g/cm 3 and 1.672 g/cm 3. All density values in g/cm 3 for each individual block are given in Table 4.

TABLE 4. Densitometric Measurements and Specific Weights of Plain Coralline Hydroxyapatite 200 Blocks Originating from Three Different Coral Heads Histomorphometric results revealed the following percentages of bone ingrowth: into the mandibular specimens, between 6.6% and 21.1%; and into the cranial specimens, between 12.0% and 26.6%. The histomorphometric data for all individual coral specimens are given in Table 5.

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TABLE 5. Densitometric Measurements of Four Mandibular and Eight Cranial Specimens After Bone Ingrowth for 2 and 4 Months

Discussion The skeletons of both species of corals, Porites and Goniopora, consist mainly of calcium carbonate and are converted into hydroxyapatite using a hydrothermal chemical conversion. 13-16 Our densitometry results reflect the amount of hydroxyapatite per block and as well as the pore size and the size of the interconnecting fenestrations within the block. The HA-200 blocks with a pore size of 230 µm and interconnecting windows of 190 µm in diameter had higher basic density values calculated for the entire block than the HA-500 blocks, which have a pore size of 600 µm and interconnecting fenestration size of 260 µm. Among HA blocks originating from the same coral head, we found only minimal differences in densities. This is not surprising considering their symmetrically oriented structure. Coralline HA blocks of the same coral genera, even when originating from different coral heads, also revealed only minimal differences in their basic densities. The highly significant correlation between our densitometry results from the plain blocks of both coral species and the calculated true densities shows that the true density is nearly identical to the densitometry result of the same HA block. Therefore, it seems unnecessary to obtain densitometry of a coralline HA block before implantation surgery to obtain a baseline value for monitoring the bone ingrowth, because the true densities can be calculated instead. Following this procedure it is important to keep in mind that the true density is given in g/cm 3, but the results of the follow-up densitometries are given in g/cm 3. Although titanium mesh is not used clinically to wrap around HA blocks, it is used to maintain particulated cancellous bone autografts. Its use in our animal model allowed us to evaluate the influence http://gateway.uk.ovid.com.proxy.lib.umich.edu/gw2/ovidweb.cgi

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particulated cancellous bone autografts. Its use in our animal model allowed us to evaluate the influence of titanium mesh in our densitometry results. A relatively wide range of densities between the blocks with and those without mesh wraps was observed. For the HA-500 blocks there was an increase of 1% to 11%; for the HA-200 blocks, there was an increase of 0% to 25%. The reason for this wide range may lie in some diversion of the x-ray beam at the surface of the titanium mesh, which may change the densitometry results, or in the definition of the ROIs, which were performed manually. However, the mesh did not alter the precision of our measurements, as shown by the densities of eight coral blocks (four with and four without meshes), which were measured in constant position 12 times. The measurement deviation for the blocks with and without meshes revealed only minimal differences. Therefore, we conclude that densitometry measurements for both blocks with and without meshes are accurate and reproducible. Coralline hydroxyapatite implants show good compatibility with human tissue and adequate mechanical strength, and therefore represent a unique bone substitute. 4,7,8,10 However, in clinical practice, noninvasive assessment of bone ingrowth into the coralline microstructure will be essential to monitor the therapeutic course. Earlier studies using conventional radiography and radiographic densitometry had indicated higher implant density after bone ingrowth combined with increased strength and stiffness compared with autografts.7,8 The clinical portion of our study has one major limitation, because we did not determine the density values of the specific coral blocks wrapped with a mesh before surgery. Therefore, we had no baseline values for each specific block. Instead of this, we measured the density of 12 HA-500 blocks and 12 HA-200 blocks surrounded by titanium meshes, all of them of approximately the same weight and size, as with the blocks used in the clinical part of the study. We found an average density of 1.850 g/cm 2 (0.897 g/cm 3) for the HA-500 blocks and of 1.072 g/cm 2 (1.617 g/cm 3) for the HA-200 blocks, which we then used as baseline values for the clinical part of our study. However, our results show that noninvasive densitometry with DXA of coralline implants might be useful to monitor bone ingrowth. We found increases in bone density of between 24% and 39% in three of our four mandibular specimens (HA-500) (specimens 1, 3, and 4) (Fig. 5A) . The increasing bone densities in relation to the average values for HA implants from this coral species after 2 and 4 months were far greater than the standard deviation of our measurements would potentially explain and seems therefore to be caused by progressive bone invasion into the coralline microstructure, with concomitant preservation of the implant architecture.5 In one mandibular specimen (specimen 2), very low density was measured 4 months after implantation. In this case, histomorphometry showed only minimal bone ingrowth with signs of infection and resorption of parts of the coralline microstructure (Fig. 5B) .

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Figures 5A-5C. Histologic sections of hydroxyapatite (HA)-500 blocks 4 months after implantation (A, B), and of a HA-200 block after bone ingrowth of 4 months (C). (A) Ingrowth of new bone formation (arrows) in an HA-500 block (specimen 3) from the periosteum of the mandibular alveolar ridge (large arrow). Note the absence of bone formation in the lower part of the implant. (B) Infection (arrow) due to an http://gateway.uk.ovid.com.proxy.lib.umich.edu/gw2/ovidweb.cgi

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intraoral fistula in an HA-500 block (specimen 2) with alteration of the coralline microstructure. (C) New bone formation (arrows) within HA-200 block (specimen 7). Different results were found with respect to the HA-200 blocks. In all eight blocks, bone ingrowth of between 12% and 26.8% was demonstrated histomorphometrically (Fig. 5C). However, the densitometry results showed values only minimally higher or even lower compared with the average value. Because all density values for these blocks ranged within the standard deviation established by our study, we believe that these minimal differences in density are due to the methodology used. It appears that bone ingrowth of 25% or less cannot be detected by DXA in the HA-200 blocks. The reason for this may be the result of the high intrinsic density of this coral genera, which certainly renders it more difficult to detect a small increase in density as produced by limited bone ingrowth into such a small structure and to x-ray beam hardening. However, further studies, in which baseline values for each block specifically have been obtained, must be performed to verify our results. In conclusion, we can state that DXA represents an accurate modality to evaluate the density of coralline HA blocks and has a relatively high degree of reproducibility when the ROI and the object's position of the bone graft substitutes are kept constant. In addition, although established on the basis of a small number of specimens, our preliminary data suggest that DXA is an accurate technique to monitor ingrowth of bone into HA-500 blocks but seems to be unreliable in the detection of bone ingrowth into the HA-200 blocks.

Acknowledgments The authors thank David van Sickle, RT, for his help and special interest in this study, and Paul Clopton, MS, Director of VAMC Statistical Research Laboratory, for statistical assistance.

References 1. Holmes R, Mooney V, Buchholz R, Tencer A. A coralline hydroxyapatite bone graft substitute. Clin Orthop 1984;188:252-262. Ovid Full Text Bibliographic Links Library Holdings [Context Link] 2. Eggli PS, Müller W, Schenk RK. Porous hydroxyapatite and tricalcium phosphate cylinders with two different pore size ranges implanted in the cancellous bone of rabbits. Clin Orthop 1988;232:127-138. Ovid Full Text Bibliographic Links

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3. Holmes RE. Bone regeneration within a coralline hydroxyapatite implant. Plast Reconstr Surg 1979;63:626-633. Bibliographic Links

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4. Light M, Kanat IO. The possible use of coralline hydroxyapatite as a bone implant. J Foot Surg 1991;30:472-476. Bibliographic Links

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5. Holmes RE, Bucholz RW, Mooney V. Porous hydroxyapatite as a bone graft substitute in diaphyseal defects: A histomorphometric study. J Orthop Res 1987;5:114-121. [Context Link] 6. Sartoris DJ, Gershuni DH, Akeson WH, Holmes RE, Resnick D. Coralline hydroxyapatite bone graft substitutes: Preliminary report of radiographic evaluation. Radiology 1986;159:133-137. Bibliographic Links Library Holdings [Context Link]

7. Sartoris DJ, Holmes RE, Tencer A, Mooney V, Resnick D. Coralline hydroxyapatite bone graft substitutes in a canine metaphyseal defect model: Radiographic-biomechanical correlation. Skeletal Radiol 1986;15:635-641. Bibliographic Links

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8. Martin RB, Chapman MW, Holmes RE, et al. Effects of bone ingrowth on the strength and noninvasive assessment of a coralline hydroxyapatite material. Biomaterials 1969;10:481-488. [Context Link] http://gateway.uk.ovid.com.proxy.lib.umich.edu/gw2/ovidweb.cgi

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9. Kühne JH, Bartl R, Frisch B, Hammer C, Janson V, Zimmer M. Bone formation in coralline hydroxyapatite: Effects of pore size studies in rabbits. Acta Orthop Scand 1994;65:246-252. Bibliographic Links Library Holdings [Context Link]

10. Sartoris DJ, Holmes RE, Bucholz RW, Resnick D. Coralline hydroxyapetite bone graft substitutes in a canine diaphyseal defect model: Radiographic features of failed and successful union. Skeletal Radiol 1988;15:642-647. Bibliographic Links

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11. Sartoris D, Resnick D. Current and innovative methods for noninvasive bone densitometry. Radiol Clin North Am 1990;28:257-278. Bibliographic Links Library Holdings [Context Link] 12. Holmes RE, Hagler HK, Coletta CA. Thick-section histometry of porous hydroxyapatite implants using backscattered electron imaging. J Biomed Mater Res 1967;21:731-739. [Context Link] 13. Weber JN, White EW, Libiedzik J. New porous materials by replication of echinoderm skeletal microstructures. Nature 1971;233:337-339. [Context Link] 14. White RA, Weber JN, White EW. Replamniform: A new process for preparing porous ceramic, metal, and polymer prosthetic materials. Science 1972;176:922-924. [Context Link] 15. White RA, White EW, Nelson RJ. Uniform microporous biomaterials prepared by the replamineform technique. Devices Artif Organs 1979;7:127-132. [Context Link] 16. White RA, Shors E, White EW. Uniform microporous biomaterials prepared from marine skeletal precursors. Proceedings of the International Coral Reef Symposium 1961;2:95-98. [Context Link]

KEY WORDS: Coralline hydroxyapatite; bone graft substitutes; dual-energy x-ray absorptiometry

Accession Number: 00004424-199611000-00006 Copyright (c) 2000-2006 Ovid Technologies, Inc. Version: rel10.3.1, SourceID 1.12052.1.95

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From the *Department of Radiology, Veterans Affairs Medical Center and University ... San Diego; and ‡ Interpore International Inc., Irwine, California. ..... Weber JN, White EW, Libiedzik J. New porous materials by replication of echinoderm ...

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re-thinking its educational approach to prepare youth for the 21st century workplace. Working in partnership with business and community leaders such as Tim Hebert, Chief Client Officer of Carousel Industries and. Leadership Rhode Island, the Academy