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Processing and Properties of Strong and Non-rigid Calcium Phosphate Cement

100 Bureau Drive Stop 8546, Paffenbarger Research Center, American Dental Association Health Foundation at the National Institute of Standards and Technology, Gaithersburg, MD 20899-8546, USA;

*corresponding author, hockin.xu{at}nist.gov

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS & METHODS RESULTS DISCUSSION DISCLAIMER REFERENCES

 
A calcium phosphate cement (CPC) sets to form hydroxyapatite and has been used in dental and craniofacial applications. However, when CPC was used in periodontal repair, tooth mobility resulted in the fracture and exfoliation of the brittle implants. The aim of this study was to develop CPC-chitosan lactate composites with higher strength and increased strain before failure. It was hypothesized that the incorporation of chitosan lactate would render CPC non-rigid with improved properties. Two-way ANOVA showed significant effects of chitosan lactate and powder:liquid ratio (p < 0.001) on flexural strength, strain-at-peak-load, work-of-fracture, and elastic modulus. At powder:liquid = 2, the strength (mean ± SD; n = 6) at 20% chitosan lactate was 15.7 ± 1.3 MPa, higher than 4.9 ± 1.4 MPa of CPC without chitosan lactate. At powder:liquid = 1, the strain-at-peak-load was 0.2% for CPC without chitosan lactate; it increased to 15.8% for CPC containing 15% chitosan lactate. The work-of-fracture was increased by more than ten times. The novel strong and non-rigid CPC may provide compliance for tooth mobility without fracturing the implant, and may also extend the use of CPC into the repair of larger defects in stress-bearing locations.

KEY WORDS: calcium phosphate cement • hydroxyapatite • chitosan • non-rigid • periodontal defects • strength • work-of-fracture

	INTRODUCTION

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The need for biomaterials has increased as the world's population ages (Laurencin et al., 1999), and hydroxyapatite has found wide use due to its chemical and crystallographic similarity to the carbonated apatite in human bones and teeth (Hench, 1998; Suchanek and Yoshimura, 1998). Several calcium phosphate cements self-harden to form hydroxyapatite (Brown and Chow, 1986; Ginebra et al., 1997; Constantz et al., 1998). One such cement (Brown and Chow, 1986), referred to as CPC, is comprised of a mixture of particles of tetracalcium phosphate [TTCP: Ca₄(PO₄)₂O] and dicalcium phosphate anhydrous (DCPA: CaHPO₄) (Chow et al., 1993). The CPC powder can be mixed with water to form a paste that can be sculpted during surgery, and this paste converts in situ to hydroxyapatite. Due to its osteoconductivity and bone replacement capability, CPC is highly promising for use in numerous dental and craniofacial procedures, including the reconstruction of frontal sinus, augmentation of craniofacial skeletal defects, endodontics, and the repair of periodontal bone defects and tooth defects (Sugawara et al., 1990; Costantino et al., 1992; Chow et al., 1993; Shindo et al., 1993; Friedman et al., 1998).

When CPC was used in periodontal bone repair, tooth mobility resulted in early fracture and eventual exfoliation of the rigid and brittle implants (Brown et al., 1998). CPC, like other brittle ceramics, fractures catastrophically at a relatively small strain. It is desirable to have CPC in a non-rigid form that can sustain large strains without fracture. Such a non-rigid CPC implant would provide the needed compliance for tooth motion without fracturing the implant. Chitosan and its derivatives are good candidates for forming non-rigid elastomeric matrices. These natural biopolymers are biocompatible, biodegradable (Machida et al., 1986), osteoconductive (Muzzarelli et al., 1993), and have been used in the surgical reduction of periodontal pockets (Muzzarelli, 1989). Chitosan has also been used as a matrix material for hydroxyapatite particle-filled composites (Maruyama and Ito, 1996; Ito et al., 1999; Yamaguchi et al., 2001).

The aims of this study were: (1) to develop non-rigid CPC-chitosan composites with increased strain-before-failure as well as higher strength and fracture resistance; and (2) to investigate the effects of chitosan content and powder-to-liquid ratio on composite properties. It was hypothesized that the CPC strength and fracture resistance would depend on chitosan content and powder-to-liquid ratio, and that the incorporation of chitosan would render the CPC non-rigid with larger deformation strains.

	MATERIALS & METHODS

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Specimen Fabrication
The tetracalcium phosphate (TTCP) powder was synthesized from a solid-state reaction between equimolar amounts of CaHPO₄ (dicalcium phosphate anhydrous, or DCPA) and CaCO₃ (Baker Analyzed Reagents, J.T. Baker Chemical, Phillipsburg, NJ, USA), which were mixed and heated at 1500°C for 6 hrs in a furnace (Model 51333, Lindberg, Watertown, WI, USA). The heated mixture was quenched to room temperature, ground in a ball mill (Retsch PM4, Brinkman, NY, USA), and sieved so that we could obtain TTCP particles with sizes ranging from approximately 1 µm to 80 µm, with a median particle size of 17 µm. The DCPA powder was ground for 24 hrs and sieved, yielding particles with sizes ranging from approximately 0.4 µm to 3 µm, with a median particle size of 1 µm. Then, the TTCP and DCPA powders were mixed in a micromill (Bel-Alert Products, Pequannock, NJ, USA) in equimolar amounts to form the CPC powder (Chow et al., 1993).

In a pilot study, chitosan lactate (Lot #RNS-570, technical grade, VANSON, Redmond, WA, USA) was mixed with distilled water at a single mass fraction of 15% to form the CPC liquid (Takagi et al., 1999). This liquid was then mixed with the CPC powder to make specimens. In the present study, the chitosan lactate fraction was expanded to the widest range possible, with homogeneous mixtures at chitosan lactate/(chitosan lactate + water) mass fractions of 0% (distilled water without chitosan lactate), 2%, 5%, 10%, 15%, and 20%, respectively. Higher chitosan lactate fractions were not used because the CPC paste became too dry during mixing at 25% chitosan lactate. Each of these 6 liquids was then mixed with the CPC powder to form a paste. A powder:liquid mass ratio of 2 was selected because this ratio was used successfully in the pilot study (Takagi et al., 1999) and in another study on fiber reinforcement (Xu and Quinn, 2002). The paste was placed into stainless steel molds of 3 mm x 4 mm x 25 mm to make flexural specimens. The paste in each mold was sandwiched between two glass slides, and set in a humidor with 100% relative humidity at 37°C for 4 hrs. The hardened specimens were demolded and immersed in a simulated physiological solution (1.15 mmol/L Ca, 1.2 mmol/L P, 133 mmol/L NaCl, 50 mmol/L HEPES, buffered to a pH of 7.4) stored in an oven at 37°C for 20 hrs prior to being tested. Six specimens were made with each of the 6 liquids, for a total of 36 specimens.

The specimens above showed substantially higher strength due to chitosan lactate, but the increase in strain was limited. Therefore, the CPC powder-to-liquid ratio was lowered to 1 to increase the chitosan lactate content relative to the CPC powder, to increase the deformability of the specimens. Thirty-six specimens were made, with 6 specimens at each of the 6 liquids at chitosan lactate/(chitosan lactate + water) of 0%, 2%, 5%, 10%, 15%, and 20%, with CPC powder:liquid ratio = 1.

Substantially higher strains were obtained for specimens at powder:liquid = 1, and the specimens with 15% chitosan lactate had the highest strain. Therefore, further testing was done with a 2x4 design with two chitosan lactate contents (0% and 15%) and four levels of powder:liquid ratio (3, 2, 1.5, and 1) for systematic investigation of the effect of CPC powder:liquid ratio. These ratios covered the widest range possible, because at a higher ratio of 4, the paste was too dry with 15% chitosan lactate; a lower ratio of 0.5 produced a paste that was too liquid. Six repeats yielded a total of 48 specimens.

Testing
We used a standard three-point flexural test with a span of 20 mm to fracture the specimens at a crosshead speed of 1 mm per min on a computer-controlled Universal Testing Machine (model 5500R, Instron Corp., Canton, MA, USA) (Xu et al., 1999a). The test was conducted in air at a relative humidity of about 50%. Flexural strength, strain-at-peak-load, elastic modulus, and work-of-fracture were measured. Work-of-fracture is a measure of the energy required to fracture the specimen, obtained from the area under the load-displacement curve divided by the specimen's cross-section area (Xu and Quinn, 2002). In cases where the CPC-chitosan lactate specimens deformed extensively without fracture, the test was stopped at a maximum displacement of approximately 3.5 mm, and a cut-off displacement of 3 mm was used for calculation of the work-of-fracture. Hence, in these cases, the work-of-fracture is the energy required to deform the specimen to the cut-off displacement.

Selected specimen surfaces were examined with a scanning electron microscope (SEM, model JSM-5300, JEOL, Peabody, MA, USA). Hydroxyapatite formation was examined with x-ray diffraction (XRD). We used the 002 peak intensity of hydroxyapatite to measure the percentage of CPC conversion to hydroxyapatite. The specimens were milled into powder by mortar and pestle, and the XRD patterns were recorded with a powder x-ray diffractometer (Rigaku, Danvers, MA, USA) with graphite-monochromatized copper K radiation ( = 0.154 nm) generated at 40 kV and 40 mA. All data were collected in a continuous scan mode (1° 2 min-1, step time 0.6 sec, step size 0.01°) and stored in a computer. We performed two-way ANOVA to detect significant ( = 0.05) effects of the variables. Tukey's multiple comparison procedures were used for comparison of the measured values at a family confidence coefficient of 0.95.

	RESULTS

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Results of CPC-chitosan lactate at power:liquid = 2 are plotted in Fig. 1 for (A) flexural strength, (B) strain-at-peak-load, (C) work-of-fracture, and (D) elastic modulus, vs. chitosan lactate fraction. Each datum is the mean of 6 measurements (n = 6), with the error bar showing one standard deviation (SD). Two-way ANOVA was performed on the 6x2 design with 6 levels of chitosan lactate percentage (0%, 2%, 5%, 10%, 15%, and 20%) and 2 levels of powder:liquid ratio (2 and 1). Both chitosan lactate content and powder:liquid ratio had significant effects (p < 0.001) on composite strength, strain, work-of-fracture, and elastic modulus, with significant interactions (p < 0.001) between chitosan lactate content and powder:liquid ratio. The strengths (mean ± SD; n = 6) of specimens with 15% and 20% chitosan lactate were 12.4 ± 2.0 MPa and 15.7 ± 1.3 MPa, respectively, about 3 times higher than 4.9 ± 1.4 MPa for 0% chitosan lactate. Compared with CPC without chitosan lactate, the work-of-fracture was increased by about ten times. The changes in elastic modulus were relatively small, with the elastic modulus at 20% chitosan lactate significantly higher than those at 10%, 5%, and 2% (Tukey's multiple comparison test; family confidence coefficient = 0.95).

View larger version (26K): [in this window] [in a new window]   Figure 1. Data for powder:liquid mass ratio = 2, showing standard deviations. (A) Flexural strength, (B) strain-at-peak-load, (C) work-of-fracture, and (D) elastic modulus, plotted vs. chitosan lactate mass fraction.

View larger version (23K): [in this window] [in a new window]   Figure 2. Data for powder: liquid ratio = 1. (A) Load-displacement curves for specimens with 0%, 5%, and 15% chitosan lactate. (B-E) Strength, strain-at-peak-load, work-of-fracture, and elastic modulus. Note that in (C) the strain was increased dramatically, from a mean strain of 0.2% for CPC control without chitosan lactate to a mean strain of 15.8% for specimens with 15% chitosan lactate.

View larger version (28K): [in this window] [in a new window]   Figure 3. Results from the 2x4 design with 2 levels of chitosan lactate and 4 levels of powder:liquid ratio. In (A), a brittle-to-ductile transition occurred at 15% chitosan lactate, and the strain-at-peak-load was increased over 70 times. In (B), at each powder:liquid ratio, the strengths with 15% chitosan lactate were always higher than those without chitosan lactate (p < 0.05).

View larger version (94K): [in this window] [in a new window]   Figure 4. The CPC-chitosan lactate specimens were loaded to 3.5 mm displacement, unloaded, and the tensile surfaces examined with SEM. (A) Most of the surfaces were smooth and crack-free. Seldom were microcracks observed after extensive deformation. (B) A microcrack is shown in a specimen with 15% chitosan lactate (arrow indicates the crack tip). (C) The microcracks in CPC-chitosan lactate specimens were surface-localized (arrows), even after extensive deformation.

	DISCUSSION

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Nearly two-orders-of-magnitude increases in the strain-at-peak-load as well as enhanced strength and work-of-fracture were achieved in the novel CPC-chitosan lactate composites. CPC without chitosan lactate had a strain-at-peak-load of 0.2%, typical for brittle materials. For comparison, dental enamel has a strain of about 1% before failure, and that for dentin is nearly 3% (Anusavice, 1996). This is consistent with dentin being more ductile than enamel (Xu et al., 1998). The more brittle materials have a higher tendency to crack under contact indentation (Ferracane, 1989; Xu et al., 1999a) or wear (Xu et al., 1999b). Large strains before failure are beneficial; for example, the American Dental Association Specification No. 5 requires a minimum strain before failure of 10% to 18% for dental casting alloys (Anusavice, 1996). The CPC-chitosan lactate specimens in the present study reached strains of 12% to 15% (Figs. 2A, 2C). The specimens did not fracture at these strains; rather, the test was stopped because the specimens were highly bent and approaching the bottom of the test fixture. These CPC-chitosan lactate composites were hence ductile and relatively non-rigid compared with the CPC control without chitosan lactate, which was substantially more rigid and brittle.

Both the chitosan lactate content and CPC powder:liquid ratio were key microstructural parameters that determined the composite properties. Different properties of the composite showed different trends of dependence on chitosan lactate content. At a powder:liquid ratio of 2, the strength, strain-at-peak-load, and work-of-fracture increased profoundly with chitosan lactate content, but the elastic modulus was relatively constant. At a powder:liquid ratio of 1, the strength, strain-at-peak-load, and work-of-fracture increased, but the elastic modulus decreased, with chitosan lactate incorporation. Different properties of the composite also showed different levels of dependence on the CPC powder:liquid ratio. The results of the 2x4 design (Fig. 3) revealed that the strain-at-peak-load and work-of-fracture increased, while the strength and elastic modulus decreased with decreasing powder:liquid ratio and at 15% chitosan lactate. These microstructural relationships should provide guidance to the future design of CPC tailored for specific applications, and may also have applicability to the improvements of strength and strain to failure for other biomedical materials.

The highly osteoconductive, resorbable, and non-rigid CPC-chitosan lactate cements are promising for numerous applications. Previous studies used particulate hydroxyapatite in the correction of deficient alveolar ridges to enhance denture support and stability (Rothstein et al., 1984), repair of periodontal defects (Ogilvie et al., 1987), and restoration of tooth extraction sockets to maintain alveolar ridge height (Scheer and Boyne, 1987). However, the hydroxyapatite particles tended to migrate from the implantation site, and the settling of the particles resulted in loss of contour (Larsen and McDonald, 1984). Bulk hydroxyapatite, due to its brittleness, is difficult to shape into the required forms. Therefore, the self-setting CPC is advantageous for retaining implant shape without the need for machining. The CPC control fractured at a displacement of approximately 0.05 mm. This is consistent with a previous study showing that tooth mobility resulted in early fracture and displacement and eventual exfoliation of CPC (Brown et al., 1998). Tooth crown mobility varies from 0.2 mm to 1 mm in Degree 1 periodontal disease, to 1 mm or more in Degree 2 periodontal disease (Lindhe, 1984). In the present study, the CPC-chitosan lactate composites withstood a bending displacement of 3.5 mm without fracture. This was coupled with a four- to six-fold increase in strength, and an increase in work-of-fracture by 10-600 times, over that of the corresponding CPC without chitosan lactate. Therefore, these strong, tough, and relatively non-rigid CPCs may be useful in periodontal repair to provide compliance for tooth mobility without fracturing the implant. The substantial enhancements in strength and fracture resistance should improve the use of this self-setting hydroxyapatite cement in other dental and craniofacial procedures, and may also extend its use to the repair of larger defects in stress-bearing locations. The tailoring of processing parameters and the method of substantially increasing the implant strength and strain, demonstrated in the present study, may be applicable to the improvement of other dental and craniofacial materials.

	DISCLAIMER

TOP ABSTRACT INTRODUCTION MATERIALS & METHODS RESULTS DISCUSSION DISCLAIMER REFERENCES

 
Certain commercial materials and equipment are identified in this paper to specify experimental procedures. In no instance does such identification imply recommendation by NIST or the ADA Health Foundation or that the material identified is necessarily the best available for the purpose.

	ACKNOWLEDGMENTS

 
We thank Dr. F.C. Eichmiller for discussions and A.A. Giuseppetti for help with the Instron. This study was supported by USPHS grants R29 DE12476 and DE11789, by NIST, and by the ADAHF.

Received July 16, 2001; Last revision January 10, 2002; Accepted January 14, 2002

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