Abstract
Sub-µm CaCO3 (calcite; CC) particles were converted to calcium monohydrogenphosphate dihydrate (DCPD) and hydroxyapatite (HAp) via soaking treatments in K2HPO4 solutions with varied pH (3–12) and concentrations (0.1–1.5 M) at 37°C for up to 10 days. DCPD was derived from the solutions with pH ≤ 6; while hollow HAp was yielded when pH ≥ 7 in assemblies of petal-like crystallites. Results of magic angle spinning (MAS) and cross-polarization magic angle spinning (CP-MAS) NMR studies have shown that the HAp lattice has only PO4 2− but no HPO4 2− at B (phosphate) sites. Trace amounts of CO3 2− have occupied both A (OH) and B (PO4) sites, and H2O is adsorbed on surface crystallites. The primary crystallite size of HAp derived from Scherrer equation increases quickly in a 12 h period and becomes gradually stable afterward. Samples of particles soaked within 3 h in a temperature range of 20–80°C were analyzed by X-ray diffraction. It is shown that the rate constant of 1 M solution is about an order of magnitude greater than that of 0.1 M solution and the apparent activation energy is 33 kJ/mol. In this work, the conversion of CC to HAp can be quantitatively controlled to solve the problem of slow degradation of HAp.
Graphical abstract
1 Introduction
Calcium carbonate (CC) is considered to be a potential bone repair material, because it can be converted to hydroxyapatite (HAp) when soaked in phosphate solutions [1,2,3,4,5,6]. The conversion process is controlled by temperature, concentration and pH value of phosphate solution. Several authors were successful in their efforts to convert CC to HAp. For example, Xia et al. [1] hydrothermally treated mixtures of CC and (NH4)2HPO4 to prepare hollow HAp spheres. Ruffini et al. [2] applied hydrothermal procedure to convert wood-derived CC (calcite) to HAp. Minh et al. [3] soaked CC particles in H3PO4 solutions of varied concentrations at 80°C and found that the conversion reaction was slow and incomplete even after 168 h. Engin and Girgin [4] used H3PO4–H2O–ethanol solution system for the conversion of CC at 80°C and attained calcium phosphate (Ca-P) products with a high carbonate content of 8.5%. Verwilghen et al. [5] soaked CC in (NH4)2HPO4 solution of pH 8.05 at 60°C and observed CO2 evolution as well as HAp formation. Portela da Silva et al. [6] derived HAp from stoichiometric mixtures of CC particles and NH4H2PO4 solution of pH > 7 at 25°C. They found the precipitation of calcium monohydrogenphosphate dihydrate (CaHPO4·2H2O; DCPD) in the course of the reaction, despite that Pourbaix [7] suggesting that HAp was most stable among several Ca-P phases in the range 6 < pH < 13. It is known that pH decides the chemical state of phosphate ions. They can be H2PO4 −, HPO4 2−, or PO4 3− [8]. Natural CaCO3 of a porous framework from coral can also be a source of apatite. For example, Sethmann et al. [9] prepared macroporous apatite ceramics via a hydrothermal treatment of aragonite coral skeletons.
Fujita et al. investigated the factors influencing the conversion of lithium calcium borate glass to HAp in dilute K2HPO4 solutions [10]. According to the Pourbaix diagrams [8], the ratio of [H2PO4 −]/[HPO4 2−] and [HPO4 2−]/[PO4 3−] is 1 at pH 7.19 and 12.03, respectively. When HAp is precipitated in an aqueous solution (6 < pH < 12) containing an alkali hydrogen phosphate (R2HPO4; R = Na or K) and a calcium salt, the pH value of the solution decreases due to the consumption of OH− ions,
Here stoichiometric HAp precipitation is assumed for simplicity though Ca-deficient phases will be commonly formed. The pH value of phosphate solution naturally determines the precipitated Ca-P phases [7]. Moreover, carbonate ions in CC take different forms, either HCO3 − or CO3 2−, depending on the pH of the system. Therefore, the regulation of pH value plays a key role.
Further studies tried to apply the abovementioned conversion reactions to repair bones. Fujita et al. [10] reported that CC induced an apatite layer on CC particle surface in vitro. Neo et al. [11] observed a direct contact between CC implants and surrounding bone tissues. Interestingly, however, neither apatite layer nor continuity between CC and bone was observed in vivo experiment [11]. That is, superficially, CC would not be converted to apatite in vivo, in contrast to the in vitro cases. According to the classic bioactivity theories, such an apatite layer is formed on the surface of bioactive materials [12,13,14,15,16] when they are in contact with human plasma or artificial aqueous solutions, mimicking the plasma and is called simulated body fluid (SBF) [14,16]. The bonding between CC and living bone without an intervening apatite layer was interpreted as a rapid biodegradation or bioresorption of CC under body conditions [11]. Kotani et al. reported a similar in vivo apatite-free bone-bonding behavior of β-tricalcium phosphate (β-TCP) [17], whereas Fu et al. confirmed no in vitro apatite layer on β-TCP in SBF [18]. An important aspect of HAp or HCA is that bioresorption is slower than TCP. Therefore, CC bone repairs blocks, and 3-D printed porous bodies or granules should be improved with regard to their usefulness when the in vivo biodegradation rate is adjusted by partial or full conversion to HAp or HCA before implantation.
Although a lot of knowledge has been gained regarding the conversion of CC to HAp, it is necessary to quantitatively control the conversion of CC into HAp. For bone repairs, partial conversion to HAp or conversion to DCPD may be beneficial. In order to meet such demands, this study was conducted as a systematic study to learn how factors such as pH and phosphate concentration affect the conversion of CC to DCPD or HAp.
2 Materials and methods
Figure 1 shows an SEM image of the as-received CC particles supplied by Shiraishi Kogyo Kaisha (Osaka, Japan). It can be seen that the particles are smaller than 1 µm, with most of them being around 0.4 µm. They were soaked in K2HPO4 solutions of four different concentrations (0.1, 0.15, 1, and 1.5 M (M = mol/L)). The pH values of the solutions were adjusted to 3.0, 5.0, 6.0, 7.0, 10.0, and 12.0 with 0.1 M HCl and KOH. All chemicals used in this study were of reagent grade and supplied by Kaitong Chemical Reagent Corporation, Tianjin, China. CC particles (0.5 g; 5 mmol) were dispersed into phosphate solutions (20 mL) held in 50 mL polystyrene bottles with tight caps. The liquid to solid ratio was set to 0.5 g/20 mL throughout this study. Bottles were kept still in an electric oven at 37°C for up to 10 days. After the soaking procedure, the CC particles were gently rinsed with distilled water for at least three times. They were then placed in glass Petri dishes with a loose cover and dried in an electric oven at 60°C for 12 h. Each experiment was repeated three times.
As-received CC (calcite) particles.
Dry powders were sputter coated with Au to observe their morphology in SEM (JSM-7800F; JEOL, Tokyo, Japan) operated at a 5 kV acceleration voltage. Crystal phases were identified with a X-ray diffraction (XRD) machine (Cu Kα; λ = 0.1542 nm, D8 ADVANCE; Bruker, Berlin, Germany), where the XRD profiles were taken at 8°–70° in θ–2θ mode with a scanning step of 0.02° (2θ) and a holding time of 0.2 s. X-ray area intensities of some diffraction peaks were obtained using a software equipped in the XRD machine. Local structures of 1H, 31P, and 13C nuclei in some conversion products were examined by MAS-NMR spectroscopy (Agilent DD2 500 MHz NMR spectrometer; Agilent Technologies, Santa Clara, CA, USA), with the spinning frequency of ZrO2 sample rotors being set to be 15 kHz for all measurements at 11.74 T. The resonance frequencies of 1H, 31P, and 13C were 499.8, 202.3, and 125.6 MHz, respectively. The direct-polarization MAS spectra of 1H, 31P, and 13C and also the 1H → 31P and 1H → 13C CP MAS spectra were recorded. For the 1H MAS experiments, the π/2 pulse length was 2.3 µs with a 5 s recycle delay. For 31P, the π/4 pulse length was 1.4 µs with a 120 s recycle delay. The contact time for 1H → 31P CP-MAS experiments was either 1 or 10 ms. The signals of 1H → 31P CP-MAS were acquired from 40 to 4,220 pulses, and 10,000–19,600 pulses were used in 1H → 13C CP-MAS. The chemical shift δ was obtained by external secondary references, i.e., NH4H2PO4 for 31P and adamantane for 1H and 13C; whereas NMR profiles were displayed with δ, which is standardized with standard reference materials of 80% H3PO4 and Si(CH3)4. The as-acquired NMR signals involved the signal originated from the rotor, and the NMR spectra presented in this article were based on the net signals after reducing the rotor signals. The NMR spectroscopy was used in this study to primarily examine the presence of HPO4 and CO3 in HAp lattice. The study was not intended to discuss peak assignments in detail.
3 Results
3.1 Effects of solution pH
Figure 2 shows the XRD profiles of CC particles soaked in 1 M K2HPO4 of different pH values (pH 3–12) for 3 days at 37°C. It can be seen in Figure 2 that soaking in solutions of pH ≤ 6 yielded only DCPD or brushite. But only HAp precipitated when the pH of the solutions was ≥ 7. According to ICDD 09-0432 and 09-0077, a set of sharp diffractions at 11.7°, 21.0°, 23.5°, and 29.35° and all other smaller peaks were assigned to DCPD for samples soaked in solutions of pH ≤ 6, and all diffractions in the top three profiles were assigned to HAp. Moreover, the XRD peaks of DCPD are sharper and stronger than those of HAp. This indicates that HAp was precipitated with lower crystallinity. Its primary crystallites may have smaller sizes. Such a pH-dependent precipitation of DCPD and HAp is consistent with the stability diagram for calcium phosphates proposed by Pourbaix [7]. In addition, Figure 2 demonstrates that the conversion reaction was complete within 3 days, even in solution of pH 7.
The XRD profiles of the conversion products after CC being soaked in 1 M K2HPO4 with varied pH 3–12 for 3 days at 37°C.
SEM images in Figure 3 show that particle morphology depends on the pH of phosphate solutions. The images in the upper raw are for acidic solutions (pH 3–6), showing agglomerations of rectangular needle-shaped crystallites with widths of ∼5 µm and lengths of ∼50 µm. They were DCPD according to the XRD profiles in Figure 2. The DCPD crystallites look as if they have grown radially outward. Many smaller pieces were also present in a similar shape. At pH 6, the radial growth was almost lost, and randomly oriented block-like pieces were assembled. Larger crystallites were accompanied by small chunks on their surface, as shown in insert image. When the pH ≥ 7, HAp appeared and the morphology drastically changed to agglomeration of petal-like crystallites (Figure 3d–f). In addition, some HAp agglomerates were hollow, in agreement with Figure 5(c and d) presented later. The size of agglomerates and petal-like components were reduced with increasing solution pH values. Agglomerates formed at pH 7 were about 5 µm in diameter. They consist of petals of about 0.6 µm in size. As the pH increases from 10 to 12, agglomerates’ diameter decreases from 1.5 µm (pH 10) to ∼1 µm (pH 12), while the petal size decreases from ∼0.25 µm (pH 10) to < 0.1 µm (pH 12).
SEM images of the conversion products after CC being soaked in 1 M K2HPO4 with varied pH 3–12 for 3 days at 37°C. (a) pH = 3, (b) pH = 5, (c) pH = 6, (d) pH = 7, (e) pH = 10, and (f) pH = 12. The inset image for (c) pH 6 represents the morphology of the chunks on a larger crystal. Note the difference in magnification for the upper (bar: 10 µm) and bottom raw (bar: 1 µm) images.
The XRD profiles of CC powders after being soaked in 0.1–1.5 M K2HPO4 solution (pH 10) at 37°C for 3 days.
An interesting observation is that the solution of pH 7 generated some bubbles, with many being found on the container wall. This implies a CO2 generation process. In addition, the solution pH changed a little. For a solution of initial pH 7, it reached pH 8–9 in the final stage. Solutions of initial pH 10 and 12 showed a slight decrease in pH to ∼10 and 11–12, respectively.
3.2 Effects of phosphate concentration
Figure 4 demonstrates XRD profiles of CC particles after being soaked in 1.5, 1.0, 0.15, and 0.1 M K2HPO4 at 37°C for 3 days. The initial pH of these four solutions was adjusted to 10. All XRD peaks in Figure 4 were assignable to HAp (1.5 and 1 M) and CC with a trace of HAp (0.15 and 0.1 M), and no other phases were detected. Most peaks were indexed according to ICDD 86-0174 (calcite) and ICDD 09-0432 (HAp). Sharp diffractions of CC mean that it was well crystallized, while noisy and rather broad diffractions of HAp indicate their lower crystallinity or smaller primary crystallites. This is similar to the results already found in Figure 2. With increasing phosphate concentration, the diffraction intensities of CC decreased slightly, whereas those of HAp increased a little. The absence of CC peaks for powders soaked in 1.5 and 1.0 M solutions indicates a full conversion of CC to HAp within 3 days.
SEM images of hollow HAp crystallites formed on CC particles when soaked for 3 days in K2HPO4 solution of varied concentrations (a) 0.1 M, (b) 0.15 M, (c) 1 M, and (d) 1.5 M, pH 10, 37°C. The inserts are close-up images. W/V ratio = 0.5 g/20 mL. Bar: 1 µm (inset: 0.1 µm).
SEM images in Figure 5 demonstrate surface morphologies of particles after being soaked at 37°C for 3 days in four different K2HPO4 solutions of initial pH 10 ((a) 0.1 M, (b) 0.15 M, (c) 1 M, and (d) 1.5 M). All particle surfaces were fully covered by fine floret or petal-like crystallites, which were identified as HAp by XRD analysis (see Figure 4). Morphologies shown in Figure 5 are very similar to that of HAp spontaneously deposited on the surfaces of bioactive materials [13,14,15,16,17]. In addition, a few hollow agglomerations of crystallites can be seen in Figure 5c and d. The agglomerate size seems to be influenced by phosphate concentration. Most agglomerates have a size of around 1 µm, which is larger than the CC particles. But the largest agglomerates of about 2 µm were seen in experiment with 1 M solution (Figure 5c). The size of the petal-like crystallites is too small to be accurately measured.
3.3 Effects of soaking time
3.3.1 Growth of HAp
Figure 6 shows the XRD profiles of samples soaked in 1 M K2HPO4 (pH 10) for a time range from 1 h to 240 h (10 days). It can be seen from Figure 6 that the XRD peak intensity of CC decreased. Yet, a tiny (104) peak was detected at ∼29° indicating that a trace of CC still remained after being soaked for 1 day. An appearance of (002) and (211) diffraction peaks at 26° and 32°, respectively, implies that CC to HAp conversion took place within 1 h. Within 2 days, the CC was almost fully converted to HAp, leaving only a trace of the (104) peak. Within 3 days, the CC peaks disappeared completely and only HAp peaks were seen. SEM images in Figure 7 demonstrate the surface morphologies of samples soaked for (a) 1 h, (b) 2 h, and (c) 7 h. The flower-like crystals were deposited after CC being soaked for 1 h, while soaking for 2 h was sufficient for particle surfaces to be fully covered with crystallites. No apparent difference exists for morphologies of the three samples (Figure 7(a–c)).
The XRD profiles showing effects of soaking period t (h) on CC to HAp conversion in a 1 M K2HPO4 solution of an initial pH 10 at 37°C. •: HAp; ◇: CC (calcite).
Surface microstructure of CC particles after being soaked in 1 M K2HPO4 of pH 10 for varied soaking period at 37°C. (a) 1 h, (b) 2 h, and (c) 7 h. Bar: 5 µm.
3.3.2 HAp growth rate
A XRD technique known as an internal standard method is commonly taken for deriving the volume fraction of a component phase in a mixture [19]. In this study, (104) diffraction peak of residual CC was utilized to represent the volume fraction of HAp. This peak was sharp and distinct and showed no overlapping with any other diffraction peaks of HAp. The seemingly strongest and broad peak at 31°, indexed at 211, is actually an envelope of three lines of (211), (112), and (300) planes. Kallaste and Nemliher [20] deconvoluted (separated) into those component lines. Yet, the present 211 diffraction would not deserve such deconvolution due to its intensity and sharpness.
The integrated area intensity of the (104) diffraction peak of CC was derived from diffraction profiles using an application installed on the XRD machine and then the intensity ratio I(t)/I 0 was calculated. Here I(t) and I 0 are intensities for soaking t (h) and 0 h, respectively. In Figure 8, I(t)/I 0 was plotted as a function of t (h) for two soaking conditions: (a) 1 M K2HPO4 at 37°C, with varying pH of 7, 10, and 12; (b) different K2HPO4 concentrations (0.1–1.5 M) at 37°C and an initial pH 10. Again, the solid to liquid ratio was kept at 0.5 g/20 mL. From Figure 8(a), it can be seen that the conversion proceeded in three stages. In stage I (t < 3 h), CC was converted so rapidly that more than half the amount of CC, even ∼80% for pH 10 and pH 12, was consumed for the conversion reaction. In stage I tr (3 h < t < 12 h), a transition state, I(t)/I 0 decreased more slowly compared to that in stage I. In stage II (12 h < t), the conversion is almost completed within 24 h (1d). I(t)/I 0 decreased in all stages in the order of pH 10, pH 7, and pH 12. This is somehow surprising because the thermodynamic stability of HAp should decrease almost proportionally to pH [7]. Very similar changes were observed in Figure 8(b); in 1 and 1.5 M solutions. One-half amount of CC was exhausted within the initial stage (t < 3 h), and the reaction was completed within 24 h (1 day). Thus, the reaction process can also be divided into stages I, I tr, and II as in Figure 8(a). For 0.1 and 0.15 M solutions, the decrease in I(t)/I 0 was very slow for t > 3 h, and it showed a very little change after 12 h, which may be due to insufficient supply of phosphate ions. Indeed, with a solid to liquid ratio of 0.5 g/20 mL, both 0.1 and 0.15 M solutions contained less amount of HPO4 2− than what was necessary for a full conversion.
The XRD intensity ratio I(t)/I 0 as a function of t (h), showing the effects of (a) pH and (b) K2HPO4 concentration. Soaking temperature = 37°C.
3.4 31P, 1H, and 13C in DCPD and HAp
3.4.1 Assignments
The present HAp converted from CC might involve HPO4 2− and CO3 2− ions in the lattice because HAp from wet chemical routes is prone to be Ca deficient. It is known that bone minerals involve carbonated hydroxyapatite (HCA) [21]. The XRD technique may not have the ability to detect their presence in a low level. Therefore, MAS and CP-MAS NMR spectroscopy were applied to clarify the chemical environments around 1H, 31P, and 13C nuclei in three representative samples S1, S2, and S3. Table 1 lists their soaking conditions as well as the NMR procedures. The chemical shift is presented in δ (ppm) as convention: a deshielded nucleus exhibits a decrease in δ or a downfield (low field) shift, while an increase in δ indicates that a shielded nucleus is characterized by an upfield (high field) shift. Figure 9(a–c) illustrate 31P MAS and CP-MAS spectra and 1H MAS NMR spectra of the designated samples. Figure 9(d) indicates a 13C CP-MAS spectrum of HAp: S3. Peak assignment is based on the results previously selected referencing on Ca-Ps [22,23,24,25,26,27,28,29,30,31,32,33,34,35], such as anhydrous dicalcium phosphate (DCPA or monetite) [24,26,31], DCPD [24,31,32], TCP [31,32], amorphous Ca-P [30], octacalcium phosphate (OCP) [22,28,32], and HAp [22,23,24,25,27,30,33,34,35]. The peak assignments of bones or other living systems were ruled out from the reference because those minerals were not well defined in structure and chemical composition. Table 2 summarizes the chemical shifts δ(1H) and δ(31P) observed in the present study as well as those from the abovementioned references.
The NMR samples, pH of soaking solution (1 M K2HPO4), soaking time (d), and signal-acquiring modes; soaking temperature: 37°C
| Phase: sample | pH | Period (days) | Nuclei, NMR mode |
|---|---|---|---|
| HAp:S1 | 7 | 1 | 1H, MAS; 31P: MAS & 1H → 31P CP-MAS |
| DCPD:S2 | 6 | 1 | 1H, MAS; 31P: MAS & 1H → 31P CP-MAS |
| HAp:S3 | 10 | 2 | 13C: 1H → 13C CP-MAS |
![Figure 9
MAS and CP-MAS NMR spectra for HAp: S1 and DCPD: S2. (a) and (b) 31P MAS and CP-MAS NMR spectra; (c): 1H MAS NMR spectra. See text and Table 1 for sample derivation. Assignments were given to major peaks. (d) 13C CP-MAS spectrum of HAp: S3 from CC in 1 M K2HPO4, pH 10, for 2 days. Arrows a–d indicate peak positions found for 13C-enriched apatite [23,32].](/document/doi/10.1515/ntrev-2020-0070/asset/graphic/j_ntrev-2020-0070_fig_009.jpg)
MAS and CP-MAS NMR spectra for HAp: S1 and DCPD: S2. (a) and (b) 31P MAS and CP-MAS NMR spectra; (c): 1H MAS NMR spectra. See text and Table 1 for sample derivation. Assignments were given to major peaks. (d) 13C CP-MAS spectrum of HAp: S3 from CC in 1 M K2HPO4, pH 10, for 2 days. Arrows a–d indicate peak positions found for 13C-enriched apatite [23,32].
NMR chemical shifts δ(1H) and δ(31P) for samples of the present study [*]1); HAp: S1 and DCPD: S2. Several data were taken from selected references [22,25,29–32,34]. (§)
| Locations | δ (1H) (ppm) | δ (31P) (ppm) | Comments & Ref. |
|---|---|---|---|
| Apatite lattice | OH− | PO4 3− | |
| 0.03 (S1) m,sa | 3.07 (S1) vs,s | [*]b | |
| 0.2 vs,s | —c | [22] | |
| 0.1 vs,s | — | [29] | |
| — | 2.9 | F-apatite [25] | |
| 0 s,s | 3.0 s,s | 2-D [32] | |
| 1.1 (0.8 + 1.3) vw | — | [29] | |
| DCPD lattice | HO-PO3 | HPO4 | |
| 10.56 (S2) vs,s | 1.40 (S2) vs,s | [*] | |
| 10.2 vw | 1.7 | [32] | |
| 10.2 Vs,s | 1.6 | [34] | |
| 10.4 vs,s | — | [31] | |
| 12.1 as a shoulder | 3.05 | 2-Dd [30] | |
| DCPD lattice H2O | H2O | ||
| (structural) | 5.56 (S2) vs,b | — | [*] |
| 4.1 + 6.5e m,b | — | [34] | |
| Surface | H2O adsorbed | HxPO4 | |
| (physi-/chemisorbed) f | — | 0.8 sh | HPO4 F-apatiteg [25] |
| — | 5.4 sh | PO4 3− F-apatite [25] | |
| 5.68 (S1) vs | — | [*] HAp | |
| 5.5 s,s | — | HAp [22] | |
| 5.5 m,b (4.5 + 6.6) | — | DCPD [31] | |
| 5.8 | — | HCA: 2-D [30] | |
| 5.4 | — | HAp + TCP; 2-D [32] | |
| 5.1 | — | [29] | |
| Unassigned | – | 1.03 (S1) w,s | [*] |
| – | -0.34, 3.10, 3.49, 4.02 (S2) | [*] | |
| 0.0 vw (S2) | — | [*] | |
| 0.91∼0.93 w,s (S1, S2) | — | [*] [29] | |
| 1.34 m,s (S1, S2) | — | [*] [29] | |
| 2.11 vw,sh (S1) | — | [*] [29] | |
| 16.0 vw,s (S2) | — | [*] | |
| Other phase | |||
| DCPA (monetite) | 162 vw | — | HPO4 [22] |
| 13.2, 15.8 vs,s | HPO4 [31] | ||
- a
vs, s, m, and w are abbreviations for very strong, strong, medium, and weak, respectively. The symbols s, b, and sh following “,” represent strong, broad, and shoulder. And the symbols (m,s), (vs,s), or (w,s) denote a medium and sharp peak, a very strong and sharp peak, and a weak and sharp peak; sh stands for a shoulder of a dominant peak. Notation was added to the selected peaks.
- b
*: Present study. S1 (HAp): 1 M K2HPO4, pH 7, 1 d; S2 (DCPD): 1 M K2HPO4: pH 6, 1 d.
- c
Symbol – (dash) means no data available or given.
- d
2-D indicate the peak was given on a slice spectrum of the 2-D projection.
- e
Symbol + means that peaks appeared as a doublet or were deconvolutable to component peaks.
- f
Physically or chemically adsorbed on surfaces of crystals.
- g
F-apatite: fluorapatite (Ca5(PO4)3F).
3.4.2 31P spectra
Strong 31P peaks of HAp: S1 and DCPD: S2 in Figure 9(a and b) are located at 3.07 and 1.40 ppm. They are doubtlessly attributed to the lattices PO4 3− of HAp and HPO4 2− of DCPD. Both MAS and CP-MAS 31P spectra of HAp (Figure 9(a)) are accompanied by a sharp but weak signal at 1.0 ppm. None of the references clearly noticed this peak [22– 25,27,30,33 – 35]. Jarlbring et al. [25] proposed a peak of 31P at 0.8 ppm, which originated from a protonated orthophosphate (H x PO4) ion on a surface site of fluorapatite (Ca5(PO4)3F). If this 1.0 ppm peak of 31P would be assigned to a surface HPO4 group of HAp, a sharp but weak peak should also appear around 10 ppm due to OH of HPO4 in a 1H spectrum of HAp. Jarlbring et al. [25] did not present the 1H spectra of their samples. This study could not detect such a 10 ppm peak of 1H in that range as shown later in Section 3.4.3. Thus, the 1.0 ppm peak was denoted unassigned in Table 1. Figure 9(b) of DCPD: S2 shows additional minor 31P signals at −0.3 and ∼3.5 ppm. The possibility of assigning the −0.3 ppm peak to the lattice HPO4 of DCPA was ruled out. According to Yun et al., this peak should be accompanied by a much stronger 31P peak at −1.5 ppm. The weak humps around 3.5 ppm consisted of triplet-like peaks at 3.1, 3.4, and 4.0, as indicated in the enlarged plots (see the insert in Figure 9(b)). Table 2 lists the unassigned weak peaks.
3.4.3 1H spectra
1H MAS NMR spectra in Figure 9(c) shows two strong 1H peaks for each phase: at 0.03 and 5.68 ppm for HAp: S1 and at 5.56 and 10.56 for DCPD: S2. According to the literature, the 0.0 ppm peak of S1 is distinctly located in the OH group at an A-site of the HAp lattice, sometimes designated as a structural OH [22]. A large, strong, and broad peak at 5.6 ppm is attributed to H2O molecules adsorbed on HAp crystals because Jarlbring et al. [25] could not find any correlation between the lattice PO4 and proton of 5.6 δ(1H) from their 1H–31P CP-MAS HETCOR (heteronuclear correlation) experiment along the 1H dimension 1H–{31P}. The same assignment was found in the preceding studies [21,28,29]. Note that the peak intensity of this adsorbed H2O is larger than that of the lattice OH at 0.0 ppm, in accordance with Sfihi and Rey [23] and Jarlbring et al. [25]. The latter group [25] detected both peaks with a comparable intensity, despite heat treating their sample at 105°C for 24 h. This implies that H2O molecules are quite tightly bound to crystallite surfaces. In this study, samples were dried at 60°C for 12 h. Such a moderate drying condition is favored for a relatively large amount of H2O remaining on HAp surfaces. Later in Section 4.2.2 a possible role of such intercrystallite H2O is discussed.
Because a larger chemical shift δ(1H) is associated with a higher acidity of proton, a prominent 1H peak at 10.56 ppm of DCPD:S2 in Figure 9(c) should be assigned to the proton of the lattice HPO4 group, rather than to H2O molecules adsorbed on the surface or involved in the structure of DCPD. This peak assignment is consistent with the reported peaks of 10.4 ppm [22,31] and 10.2 ppm [32,34]. Yesinowski and Eckart [22] designated their 10.4 ppm peak as the signal of an acidic proton. Hence, a broad 1H peak centered at 5.58 ppm of DCPD:S2 is attributable to the structural water. Pourpoint et al. [34] observed a doublet 1H peak at 4.8 and 6.6 ppm using a high-spinning rate (33 kHz). According to their first-principle calculation, the 5 ppm 1H peak should be an envelope of four peaks, corresponding to four different lattice sites in DCPD. In contrast, Yesinowski and Eckart assigned a 6.4 ppm 1H peak to structural H2O of DCPD [22].
Both HAp and DCPD showed a few minor signals in the range of 0.9–2.1 ppm of δ(1H) in Figure 9(c), while Jäger et al. [24] reported very distinct and narrow line signals in the same δ(1H) range for their nano-sized apatite. Osman et al. interpreted those groups as originated from OH groups with different alignments along the c axis of HAp [29]. Table 2 followed their assignment. Figure 9(c) has another minor δ(1H) peak at 16.0 ppm. Yesinowski and Eckert assigned the signal to HPO4 of DCPA [22]. Although the chemical shift of 16 ppm corresponds to a highly acidic proton, probably this assignment would not be adequate. Yu et al. gave a pair of sharp 1H peaks for DCPA at 13.2 and 15.8 ppm. Therefore, 1H: 16 ppm peak observed in the present study was presented unassigned in Table 2.
3.4.4 13C NMR spectra
Figure 9(d) demonstrates a 1H → 13C CP-MAS NMR spectrum of the sample HAp:S3. Despite the relatively low signal to noise ratio, Figure 9(d) clearly exhibits a peak, extending from 150 to 172 ppm. A hump around 173 ppm may be a noise. Babonneau et al. have already reported the presence of a 13C peak for 13C-enriched HCA, and the peak showed four local maxima [26]. This suggested that the presence of at least four different carbonate sites. Sfihi and Rey reported 13C peaks of CO3 2− at 168.5 and 170 ppm for their fluorapatite but found no peak at 166 ppm [23]. Moreover, they stated in their paper that “the CO3 groups at 168.5 ppm will not be located in the bulk but near the surface.” If they meant the presence of the 168.5 ppm CO3 2− so near the surface that they would “talk” (exchange the nuclear magnetic moments) with component species on the surface like adsorbed H2O, correlation should be detected between the carbonate ions and surface water molecules. Unfortunately, however, Babonneau et al. did not find such a correlation between CO3 2− and H2O via 1H–13C CP-MAS NMR HETCOR experiments [26]. But the carbonate ions detected here are surely in the lattice sites. Leroy et al. employed a high-end NMR technology, dynamic nuclear polarization, and carried out a full analysis of the carbonate ion sites, regardless of whether the CO3 2− ions occupy the OH (A) sites or PO4 (B) sites of the apatite lattice [35]. They considered the substitution pairs of A and B sites, and lattice structure, before finalizing the assignments. In brief, the whole peak involved five component contributions, showing A/B substitution (OH− + PO4 3− → 2CO3 2−) gave δ(13C) of 166.5 and 168.0 ppm, while B/B one (Ca2 + + 2PO4 3− → Ca2+ vacancy + 2CO3 2−) resulted in the peaks at 168.3, 170.1, and 171.0 ppm. In this study, the 13C signals were located within the range of those 13C signal assignments [26,35]. Thus, it is reasonable to conclude that CO3 2− ions were involved in the A and B lattice sites of the HAp sample. The conversion from CC and the precipitation pH conditions might favor a carbonate ion involvement.
4 Discussion
4.1 Conversion reaction analysis
4.1.1 The rate analysis of conversion reactions in the earliest period
SEM images in Figures 3 and 5 indicate that soaked particles should have a core (CC)–shell (HAp) structure. Sharp decrease in I(t)/I 0 as can be observed in Figure 8 for the (104) diffraction of CC, which implies that most of conversion reaction finishes within 3 h (in stage I). Such a fast reaction must be accompanied by a fast transportation of reactants to the reaction front. Based on these observations, a reaction model is proposed as presented in Figure 10, with following assumptions:
Spherical CC particles in contact with K2HPO4 solution, as shown in Figure 10(a).
Active site density remains constant on the reaction front.
Component species can freely migrate to the reaction front.
(a) A reaction model of a CC core with a HAp layer, allowing migration of species such as HPO4 2− ions to the reaction front. A square part is enlarged in (c) and (d). (b) An enlarged schematic model of the reaction front at stage I. The surface was in contact with phosphate solution. Hydroxy, calcium, and phosphate ions are presented as OH, Ca(ii), and P(v). (c) and (d): Structures near the reaction front in stages I tr and II (see text).
Figure 10(b) illustrates the formation process of the HAp shell layer. For a simple illustration, hexagonal pieces are aligned flat, as drawn here, with their (002) plane on CC surface. But in reality, CC is polycrystalline and should expose a variety of lattice planes to solution, even if epitaxy would be applicable between calcite and HAp. A random assembly of crystallites is also supported by the observation [36] that wet chemically derived HAp crystallites exhibit a few lattice images randomly stacked when observed under a transmission electron microscope.
A primitive analysis of the reaction rate is only valid in stage I (t < 3 h) because as shown in Figure 8, the conversion precedes in some different modes in later stages, I tr and II. Minh et al. employed arbitrarily two different diffusion models, depending on the reaction temperature in their systems of CC conversion to HAp [3]. Our model assumes a diffusion as described in (c) above. The assumption (b) is the key for the present analysis. It means that the rate of decrease in volume V of a CC particle during conversion is proportional to the surface area S. This leads to equation (2) with k′ as the rate constant
Substituting the particle radius r to V and S and applying V ∝ I(t)/I 0, equation (2) can be modified to equation (3):
Here C is the constant of integral and k is the apparent rate constant related to the XRD intensity ratio in CC → HAp conversion. Note again this equation (2) is only valid at the beginning stage of the conversion. From linear correlations between (I(t)/I 0)1/3 and the soaking period t in Figure 11(a) (0.1 M, pH 10) and (b) (1 M, pH 10), the apparent conversion rate constant k is derived for each temperature and listed in the inserted tables. Figure 11(c) demonstrates an Arrhenius-type correlation between k (1/h) and 1/T (1/K),
Here f is the frequency factor and Δε is the apparent activation energy. Thus, the derived Δε for both 0.1 M and 1 M K2HPO4 solutions is practically identical and close to Δε (4.3 kcal/mol = 35.7 kJ/mol) for H2PO4 − ion diffusion in NaH2PO4 aqueous solution (∞ dilution), as given by Krauss and Sinks [37]. This observation, therefore, implies that the diffusion of phosphate ions controls the conversion reaction. In other words, Ca2+ and OH− would be sufficiently available at the reaction sites to wait for phosphate ions. The frequency factor of 1 M solution (the upper line in Figure 11(c)) is an order of magnitude greater than that for 0.1 M solution. This can be simply interpreted as the effect of the phosphate ion concentration.
Plots of (I(t)/I 0)1/3 vs soaking period t (h) for CC → HAp conversion reaction at 293–353 K (20°C–80°C) in (a) 0.1 M K2HPO4 and (b) 1 M K2HPO4. The inserted tables list the apparent rate constant k derived from equation (2). (c) The broken lines represent Arrhenius-type correlations (Equation (3)), and the derived values of the apparent activation energy are in the parentheses.
4.1.2 Primary crystallite size and ripening
Application of Scherrer formula, equation (5), to broadened XRD lines derives an approximate size (τ) of a primary crystal in a polycrystalline phase [19].
Here K is the Scheler constant (K = 0.9), λ is the X-ray wavelength (Cu Kα; 0.1540 nm), full width at half maximum (FWHM) is the line width, and θ is the diffraction angle. The XRD profiles of HAp in Figures 2, 4, and 6 are accompanied by the sharp (104) line of calcite (CC), and this peak is used to calibrate XRD machine broadening before the derivation of τ for samples. Figure 12 plots the so-calculated HAp crystallite size τ as a function of soaking period t (h). τ increases quickly to ∼30 nm within 12 h. This reaction range corresponds to stages I and I tr in Figure 8. Unfortunately, It was impossible to derive τ for sample after being soaked for t < 7 h because the (002) diffraction is too weak. Then τ increases slowly and reaches ∼40 nm at 240 h (10 days; stage II). The size is in accord with that of HAp nanoparticles derived wet chemically [36]. Results in Figure 12 imply that seven or eight pieces of primary crystallites are assembled to form a petal-like HAp crystallite layer with a size of approximately 250 nm, as shown in Figure 5.
![Figure 12
Crystallite size τ (nm) of HAp precipitated in 1 M K2HPO4 solutions of pH 7 (○) and pH 10 (□) derived from Scherrer equation, i.e., Equation (8) [19]. Conversion stages I and II are indicated as in Figure 8(a). The broken line is a guide for eyes.](/document/doi/10.1515/ntrev-2020-0070/asset/graphic/j_ntrev-2020-0070_fig_012.jpg)
Crystallite size τ (nm) of HAp precipitated in 1 M K2HPO4 solutions of pH 7 (○) and pH 10 (□) derived from Scherrer equation, i.e., Equation (8) [19]. Conversion stages I and II are indicated as in Figure 8(a). The broken line is a guide for eyes.
4.1.3 Growth of a petal-like crystal
The changes in the size of primary crystal in Figure 12 indicate that the mechanism of HAp formation is different in stages I and II. A drastic growth of primary crystals in stage I (t < 3 h) is achieved only under sufficient supply of Ca2+, HPO4 2−, and OH− ions to the reaction front, as described in Figure 10(b). In the course of conversion, the primary crystallites are formed in random orientations with respect to the CC surfaces. They grow into contact and fuse with each other, leaving some space among primary crystallite assemblies. The presence of H2O in these spaces is supported by the large 1H NMR band assigned to surface H2O (5.6 ppm in δ(1H): Figure 9(c)). The fused crystallites are assembled repeatedly, which grow into a floret-like agglomerations in stages I tr and II. Along such crystallizing events, the CC particles would continue to be dissolved. Their volumes will decrease or keep shrinking. Therefore, Ca2+ ions are always supplied sufficiently at the reaction front, and phosphate ions should migrate into primary crystallites via water channels. Both ions take OH− from solution and form agglomerated secondary crystals. This is a plausible growth model. It considers the apparent activation energy (Δε; Figure 11(c)) of CC → HAp conversion, which is in a good agreement with that of H2PO4 diffusion [37].
4.2 Microstructure of HAp agglomerates
4.2.1 Formation of hollow HAp particles
Calcite is sparingly soluble in water, with a solubility product K sp being 3.36 × 10−9 (mol/L)2 [38]. The solubility of 58 µM/L (∼0.58 mg/100 g-H2O) is high enough to supply component ions to the aqueous medium in contact, according to equation (6a).
Extremely low-solubility product of HAp (∼5 × 10−118) [39] and the stability of HAp [7] are thermodynamically favorable for HAp precipitation when its components are available. At the very beginning (stage I), the liberated Ca2+ ions found many phosphate ions on particle surfaces (Figure 10(b)), and hence they instantly form a HAp layer. In later stages I tr and II, the phosphate ions migrate through the layer, driven by the concentration gradient that is established around particles, to the reaction front. Another possible way of deposition of a Ca-P phase is a direct reaction due to the withdrawal of Ca2+ ions from solid CC by HPO4 2− ions, arriving at the surface (equation (6b)).
This case implies that the rate of free Ca2+ ion supply is too small to meet the frequency of HPO4 2− and OH− ions to arrive at particular reaction sites. That is, the apparent activation energy should be associated with CC dissociation but not with phosphate ion diffusion. This is similar to the direct conversion of OCP to HAp reported by Tseng et al. [40]. If equation (6b) were valid, the precipitation should always take place on CC surface, as depicted in Figure 10(c), until the CC is exhausted. This would lead to solid particles [41,42].
In contrast, equation (6a) implicitly represents that calcium ions should be liberated into aqueous region, adjacent to CC surface, as presented in Figure 10(d). They wait for phosphate ions to reach the inner surface of the HAp shell or the reaction front. That is, the conversion reaction allows the HAp layer to be separated from the surface in later stages. This is a plausible interpretation for formation of hollow HAp particles detected in Figures 3 and 7. The OH ions will be supplied via water dissociation equilibrium when they are consumed at the reaction front. Such a scheme is compatible with the apparent activation energy of the net conversion reaction and apparent activation energy of H2PO4 ion diffusion in aqueous solution [37,43,44,45]. In both cases in Figure 10(c and d), HAp grows inwardly as in the case of HAp nano-rod array grown on sodium calcium silicate glass substrate which were soaked in 0.01 M Na2HPO4 solution [46,47,48,49].
4.2.2 Net conversion reaction
Equation (7) is a probable net reaction for CC → HAp conversion when a high pH (>10) stabilizes CO3 2− (pK 2 (H2CO3) = 10.33 [8,38]):
In a lower pH region, where an insufficient amount of OH− is available, OH− will be supplied via H2O → H+ + OH−. Then equation (7′) is derived.
The yielded H+ would be scavenged by carbonate ions to form HCO3 −, (pK 1 (H2CO3) = 6.33) [8,38]. Then equation (8) replaces equation (7) to represent the net reaction that may occur when pH < 10:
Equation (8) explains why the pH of K2HPO4 solutions increased after the completion of the reaction with initial pH of solutions being adjusted to 7 or 10. With the solubility 6.15 × 10−4 mol of CO2 (100 kPa) in 1 mol water and volume fraction of CO2 in air (408 ppm) [38], the solubility limit of CO2 in 20 mL solution is as low as ∼2.8 nano mol, and the expected CO2 evolution from 0.5 g CC was 5 m mol. In consequence, H+ in equation (7′) should drive the CO2–H2O equilibria to favor the formation of CO2. This explains the bubbling observed in the course of reaction in solution of pH 7. Equation (9) then represents the CC → HAp conversion accompanying CO2 evolution:
5 Conclusion
Based on the results obtained in this study, following conclusions can be drawn:
Soaking CC for 72 h in 1 M K2HPO4 solution, only DCPD is yielded with pH ≤ 6 while only HAp was obtained with pH ≥ 7. DCPD shows a morphology consisting of assemblies of long rectangular crystallites extending outward. The morphology of HAp consists of hollow shells with petal-like crystallites forming porous shell walls. Such a porous shell structure is more conducive to tissue growth.
By analyzing CC to HAp conversion rate at a beginning stage, an apparent activation energy of about 34 kJ/mol has been obtained, which is in accordance with the diffusion of H2PO4 − in aqueous solutions.
Primary crystal size of HAp, derived due to Scherrer equation, shows a rapid growth within the first 7 h and a slow ripening afterward.
Results of MAS and CP-MAS NMR spectra can be summarized as below: (a) prominent peaks of 31P indicate HPO4 2− and PO4 3− in the lattice sites of DCPD, and PO4 3− in the lattice sites of HAp. (b) 1H peaks of HAp implies that H2O and OH are adsorbed on its crystallite surfaces. (c) HAp shows a tiny 13C peak, indicating the presence of CO3 2− in both A (OH) and B (PO4) sites of the HAp lattice.
Acknowledgments
This work was supported by the Chinese 02 Special Fund (Grand No. 2017ZX02408003), the Innovative Research Team Program of Henan University of Science and Technology (Grant No. 2015XTD006), and the Natural Science Fund Cultivation Project of Henan Province (Grant No. 162300410087).
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Conflict of interest: The authors declare no conflict of interest regarding the publication of this paper.
References
[1] Xia X, Chen J, Shen J, Huang D, Duan P, Zou G. Synthesis of hollow structural hydroxyapatite with different morphologies using calcium carbonate as hard template. Adv Powder Technol. 2018;29(7):1562–70.10.1016/j.apt.2018.03.021Search in Google Scholar
[2] Ruffini A, Sprio S, Tampieri A. Study of the hydrothermal transformation of wood-derived calcium carbonate into 3D hierarchically organized hydroxyapatite. Chem Eng J. 2013;217:150–8.10.1016/j.cej.2012.11.107Search in Google Scholar
[3] Minh DP, Rio S, Sharrock P, Sebei H, Lyczko N, Tran ND, et al. Hydroxyapatite starting from calcium carbonate and orthophosphoric acid: synthesis, characterization, and applications. J Mat Sci. 2014;49(12):4261–9.10.1007/s10853-014-8121-7Search in Google Scholar
[4] Engin A, Girgin I. Synthesis of hydroxyapatite by using calcium carbonate and phosphoric acid in various water–ethanol solvent systems. Cent Eur J Chem. 2009;7(4):745–51.10.2478/s11532-009-0063-6Search in Google Scholar
[5] Verwilghen C, Chkir M, Rio S, Nzihou A, Sharrock P, Depelsenaire G. Convenient conversion of calcium carbonate to hydroxyapatite at ambient pressure. Mat Sci Eng C. 2008;29(3):771–3.10.1016/j.msec.2008.07.007Search in Google Scholar
[6] Portela da Silva NM, Espitalier F, Nzihou A. Precipitation process of calcium phosphate from calcium carbonate suspension. KONA Powder Part J. 2016;33:219–27.10.14356/kona.2016002Search in Google Scholar
[7] Pourbaix M. Atlas of Electrochemical Equilibria in Aqueous Solutions. Oxford: Pergamon Press; 1966. Chap. IV, §18.2, p. 504–515. Pourbaix M (1966), Atlas of electrochemical equilibria in aqueous solutions, 1st edn., Chap. IV, §18.2. Pergamon Press, Oxford, England.Search in Google Scholar
[8] Chow LC. Next generation calcium phosphate-based biomaterials. Dental Mater J. 2009;28(1):1–10.10.4012/dmj.28.1Search in Google Scholar PubMed PubMed Central
[9] Sethmann I, Luft C, Kleebe H-J. Development of phosphatized calcium carbonate biominerals as bioactive bone graft substitute materials, Part I: incorporation of magnesium and strontium ions. J Funct Biomater. 2018;9:69.10.3390/jfb9040069Search in Google Scholar PubMed PubMed Central
[10] Fujita Y, Yamamuro T, Nakamura T, Kotani S, Ohtsuki C, Kokubo T. The bonding behavior of calcite to bone. J Biomed Mater Res. 1991;25(8):991–1003.10.1002/jbm.820250806Search in Google Scholar PubMed
[11] Neo M, Kotani S, Fujita Y, Nakamura T, Yamamuro T, Bando Y, et al. Differences in ceramic-bone interface between surface-active ceramics and resorbable ceramics: a study by scanning and transmission electron microscopy. J Biomed Mater Res. 1992;26(2):255–67.10.1002/jbm.820260210Search in Google Scholar PubMed
[12] Ban I, Stergar J, Maver U. NiCu magnetic nanoparticles: review of synthesis methods, surface functionalization approaches, and biomedical applications. Nanotechnol Rev. 2018;7(2):187–207.10.1515/ntrev-2017-0193Search in Google Scholar
[13] Zang ST, Chang SJ, Shahzad MB, Sun X, Jiang X, Yang H. Ceramics-based drug delivery system: a review and outlook. Rev Adv Mater Sci. 2019;58(1):82–97.10.1515/rams-2019-0010Search in Google Scholar
[14] Guo SH, Fu DW, Utupova A, Sun D, Zhou M, Jin Z, et al. Applications of polymer-based nanoparticles in vaccine field. Nanotechnol Rev. 2019;8(1):143–55.10.1515/ntrev-2019-0014Search in Google Scholar
[15] Kokubo T, Yamaguchi S. Simulated body fluid and the novel bioactive materials derived from it. J Biomed Mater Res Part A. 2019;107(5):968–77.10.1002/jbm.a.36620Search in Google Scholar PubMed
[16] Manohar CS, Kumar BS, Sadhu SPP, Srimadh SK, Muthukumar VS, Venketesh S,et al. Novel Lead-free biocompatible piezoelectric hydroxyapatite (HA) – BCZT (Ba0.85Ca0.15Zr0.1Ti0.9O3) nanocrystal composites for bone regeneration. Nanotechnol Rev. 2019;8(1):61–78.10.1515/ntrev-2019-0006Search in Google Scholar
[17] Ohtsuki C, Kokubo T, Neo M, Kotani S, Yamamuro T, Nakamura T, et al. Bone-bonding mechanism of sintered β-3CaO.P2O5. Phosphorus Res Bull. 1991;1:191–6.Search in Google Scholar
[18] Fu H, Rahaman MN, Day DE. Effect of process variables on the microstructure of hollow hydroxyapatite microspheres prepared by a glass conversion method. J Am Ceram Soc. 2010;93(10):3116–23.10.1111/j.1551-2916.2010.03833.xSearch in Google Scholar PubMed PubMed Central
[19] Cullity BD. Elements of X-ray diffraction, 2nd edn. MA: Addison-Wesley, Reading; 1978; chap. 3–7 and 14–11.Search in Google Scholar
[20] Kallaste T, Memliher J. Apatite varieties in extant and fossil vertebrate mineralized tissues. J Appl Crsyt. 2005;38(4):587–94.10.1107/S0021889805011404Search in Google Scholar
[21] Schröder R, Pohlit H, Schüler T, Panthöfer M, Unger RE, Frey H, et al. Transformation of vaterite nanoparticles to hydroxycarbonate apatite in a hydrogel scaffold: relevance to bone formation. J Mater Chem B. 2015;3(35):7079–89.10.1039/C5TB01032BSearch in Google Scholar
[22] Yesinowski JP, Eckert H. Hydrogen environments in calcium phosphates: 1H MAS NMR at high spinning speeds. J Am Chem Soc. 1987;109:6274–82.10.1021/ja00255a009Search in Google Scholar
[23] Sfihi H, Rey C. 1-D and 2-D double heteronuclear magnetic resonance study of the local structure of type b carbonate fluoroapatite, magnetic resonance in colloid and interface science. Nato ASI Ser II. 2002;76:409–22.Search in Google Scholar
[24] Jäger C, Welze T, Meyer-Zaika W, Epple M. A solid-state NMR investigation of the structure of nanocrystalline hydroxyapatite. Magn Reson Chem. 2006;44:573–80.10.1002/mrc.1774Search in Google Scholar PubMed
[25] Jarlbring M, Sandström DE, Antzutkin ON, Forsling W. Characterization of active phosphorus surface sites at synthetic carbonate-free fluorapatite using MAS NMR single-pulse 1H, 31P, and 31P CP. Langmuir. 2006;22(10):4787–92.10.1021/la052837jSearch in Google Scholar PubMed
[26] Babonneau F, Bonhomme C, Hayakawa S, Osaka A. Solid state NMR characterization of nano-crystalline hydroxy-carbonate apatite using 1H-31P-13C triple resonance experiments. Mater Res Soc Symp Proc. 2007;984:6.10.1557/PROC-984-0984-MM06-05Search in Google Scholar
[27] Barheine S, Hayakawa S, Jäger C, Shirosaki Y, Osaka A. Effects of disordered structure of boron-containing calcium phosphates on their in vitro biodegradability. J Am Ceram Soc. 2011;94(8):2656–62.10.1111/j.1551-2916.2011.04400.xSearch in Google Scholar
[28] Davies E, Duer MJ, Ashbrook SE, Griffin JM. Applications of NMR crystallography to problems in biomineralization: refinement of the crystal structure and 31P solid-state NMR spectral assignment of octacalcium phosphate. J Am Chem Soc. 2012;134(30):12508–15.10.1021/ja3017544Search in Google Scholar PubMed
[29] Osman MB, Diallo-Garcia S, Herledan V, Brouri D, Yoshioka T, Kubo J, et al. Discrimination of surface and bulk structure of crystalline hydroxyapatite nanoparticles by NMR. J Phys Chem C. 2015;119:23008–20.10.1021/acs.jpcc.5b08732Search in Google Scholar
[30] Mathew R, Turdean-Ionescu C, Yu Y, Stevensson B, Izquierdo-Barba I, García A, et al. Proton environments in biomimetic calcium phosphates formed from mesoporous bioactive CaO−SiO2−P2O5 Glasses in vitro: insights from solid-state NMR. J Phys Chem C. 2017;121(24):13223–38.10.1021/acs.jpcc.7b03469Search in Google Scholar PubMed PubMed Central
[31] Yu Y, Guo H, Pujari-Palmer M, Stevensson B, Grins J, Engqvist H, et al. Advanced solid-state 1H/31P NMR characterization of pyrophosphate-doped calcium phosphate cements for biomedical applications: the structural role of pyrophosphate. Ceram Int. 2019;45:20642–55.10.1016/j.ceramint.2019.07.047Search in Google Scholar
[32] Konishi T, Yamashita K, Nagata K, Lim PN, Thian ES, Aizawa M. Solid-state nuclear magnetic resonance study of setting mechanism of β-tricalcium phosphate-inositol phosphate composite cements. J Phys Mater. 2019;2:034007.10.1088/2515-7639/ab17e5Search in Google Scholar
[33] Tseng Y-H, Mou Y, Chen P-H, Tsai TWT, Hsieh C-I, Mou C-Y, et al. Solid-state P-31 NMR study of the formation of hydroxyapatite in the presence of glutaric acid. Magn Reson Chem. 2008;46(4):330–4.10.1002/mrc.2096Search in Google Scholar PubMed
[34] Pourpoint F, Gervais C, Bonhomme-Coury L, Azaîs T, Coelho C, Mauri F, et al. Calcium phosphates and hydroxyapatite: solid-state NMR experiments and first-principles calculations. Appl Mag Reson. 2007;32(4):435–57.10.1007/s00723-007-0040-1Search in Google Scholar
[35] Leroy C, Aussenac F, Bonhomme-Coury L, Osaka A, Hayakawa S, Babonneau F, et al. Hydroxyapatites: key structural questions and answers from dynamic nuclear polarization. Anal Chem. 2017;89(19):10201–7.10.1021/acs.analchem.7b01332Search in Google Scholar PubMed
[36] Hayakawa S, Kanaya T, Tsuru K, Shirosaki Y, Osaka A, Fujii E, et al. Heterogeneous structure and in vitro degradation behavior of wet-chemically derived nanocrystalline silicon-containing hydroxyapatite particles. Acta Biomater. 2013;9(1):4856–67.10.1016/j.actbio.2012.08.024Search in Google Scholar PubMed
[37] Krauss CJ, Spinkes JWT. Temperature coefficients for self-diffusion in solution. 1954;32(2):71–78.10.1139/v54-012Search in Google Scholar
[38] Rumble JR, editor. CRC handbook of chemistry and physics, 100th edn. NM, USA: CRC Press; 2019.Search in Google Scholar
[39] Tsuru K, Kubo M, Hayakawa S, Ohtsuki C, Osaka A. Kinetics of apatite deposition of silica gel dependent on the inorganic ion composition of simulated body fluids. J Ceram Soc Jpn. 2001;109(1269):412–8.10.2109/jcersj.109.1269_412Search in Google Scholar
[40] Tseng Y-H, Mou C-Y, Chan JCC. Solid-state NMR study of the transformation of octacalcium phosphate to hydroxyapatite: a mechanistic model for central dark line formation. J Am Chem Soc. 2006;128(21):6909–18.10.1021/ja060336uSearch in Google Scholar PubMed
[41] Zhang Y, Chai Z, Volinsky AA, Tian B, Sun H, Liu P, et al. Processing maps for the Cu-Cr-Zr-Y alloy hot deformation behavior. Mater Sci Eng A. 2016;662(4):320–9.10.1016/j.msea.2016.03.033Search in Google Scholar
[42] Lin NM, Xie RZ, Zou JJ, Li D, Yuan S, Wang Z, et al. Surface damage mitigation of titanium and its alloys via thermal oxidation: a brief review. Rev Adv Mater Sci. 2019;58(1):132–46.10.1515/rams-2019-0012Search in Google Scholar
[43] Long F, Guo X, Song K, Jia S, Yakubov V, Li S, et al. Enhanced arc erosion resistance of TiB2/Cu composites reinforced with the carbon nanotube network structure. Mater Des. 2019;183:108136.10.1016/j.matdes.2019.108136Search in Google Scholar
[44] Nakonieczny DS, Basiaga M, Sambok A, Antonowicz M, Paszenda Z, Ziębowicz AM, et al. Ageing of zirconia dedicated to dental prostheses for bruxers part 1: influence of accelerating ageing for surface topography and mechanical properties. Rev Adv Mater Sci. 2019;58(1):189–94.10.1515/rams-2019-0026Search in Google Scholar
[45] Hu C, Sun JX, Long C, Wu L, Zhou C, Zhang X. Synthesis of nano zirconium oxide and its application in dentistry. Nanotechnol Rev. 2019;8(1):396–404.10.1515/ntrev-2019-0035Search in Google Scholar
[46] Hayakawa S, Li YX, Tsuru K, Osaka A, Fujii E, Kawabata K. Preparation of nanometer-scale rod array of hydroxyapatite crystal. Acta Biomater. 2009;5(6):2152–60.10.1016/j.actbio.2009.02.018Search in Google Scholar PubMed
[47] Feng J, Song K, Liang S, Guo X, Jianga Y. Electrical wear of TiB2 particle-reinforced Cu and Cu-Cr composites prepared by vacuum arc melting. Vacuum. 2020;175:109295.10.1016/j.vacuum.2020.109295Search in Google Scholar
[48] Muthukumar T, Sreekumar G, Sastry TP, Chamundeeswari M. Collagen as a potential biomaterial in biomedical applications. Rev Adv Mater Sci. 2018;53(1):29–39.10.1515/rams-2018-0002Search in Google Scholar
[49] Zhang Y, Volinsky AA, Tran H, Chai Z, Liu P, Tian BH, et al. Aging behavior and precipitates analysis of the Cu-Cr-Zr-Ce alloy. Mater Sci and Eng A. 2016;650(1):248–53.10.1016/j.msea.2015.10.046Search in Google Scholar
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