Discrimination of Surface and Bulk Structure of Crystalline

Article pubs.acs.org/JPCC

Discrimination of Surface and Bulk Structure of Crystalline Hydroxyapatite Nanoparticles by NMR Manel Ben Osman,†,‡ Sarah Diallo-Garcia,†,‡ Virginie Herledan,†,‡ Dalil Brouri,†,‡ Tetsuya Yoshioka,§ Jun Kubo,§ Yannick Millot,*,†,‡ and Guylène Costentin*,†,‡ †

Sorbonne Université, UPMC Univ Paris 06, UMR 7197, Laboratoire Réactivité de Surface, F-75005 Paris, France CNRS, UMR 7197, Laboratoire Réactivité de Surface, F-75005 Paris, France § Central Research Center, Sangi Co., Ltd., Fudoinno 2745-1, Kasukabe-shi, Saitama 344-0001, Japan ‡

S Supporting Information *

ABSTRACT: Solid state 1H and 31P NMR spectroscopy was used to characterize wellcrystallized hydroxyapatite samples of different stoichiometry prepared by a precipitation route. The aim of the paper was to investigate the bulk structural features of samples with different stoichiometry and to discriminate signals related to the surface from those related to the bulk. Thanks to the implementation of (i) in situ thermal pretreatment at 623 K, (ii) filling of the NMR rotor in a controlled atmosphere, (iii) relative proton enrichment of the surface performed under controlled isotopic H-D exchanges, and (iv) specific NMR sequences including inversion recovery measurements, two-dimensional HETCOR and DQSQ spectra, new resolved NMR signals originating from the surface and from the bulk were identified alongside already reported signals associated with adsorbed water, structural phosphates, and OH groups. In particular, considering the influence of the stoichiometry, it was possible to identify a specific signature associated with defective hydrogenophosphate groups present in the bulk. Despite the well-ordered surface terminations of the nanoparticles, specific surface signals associated with nonprotonated and protonated surface terminating phosphate groups could be identified. In addition, from the three resolved 1H signals associated with columnar OH channels, two from the bulk and one from the surface, a structural model describing the relative organization of hydroxyl groups running along the c axis inside the columnar OH channel in the well-crystallized particles is proposed: the two types of bulk hydroxyls are associated with the presence of both up and down orientations of their related protons in a same tunnel. Corresponding 1H signatures of the surface-terminating hydroxyls or structured water molecules emerging from the OH channels were also identified. Moreover, in addition to the broad 5.1 ppm line associated with water adsorbed on calcium cations and hydrogenophosphate groups, the 1.1 ppm line is ascribed to structured external water molecules stacking in continuity to the OH channels.

1. INTRODUCTION

hydroxyapatites) are easily obtained, depending on the preparation conditions.1 The latter are associated with Ca10−x(HPO4)x(PO4)6−x(OH)2−xnH2O formula, accounting for the formation of bulk hydrogenophosphate groups HPO42− and of OH− vacancies to counterbalance the calcium deficiency.10 Such under-stoichiometric compositions Ca/P ∼ 1.5 together with the high carbonation level [up to 8 wt (%)] are classically associated with hydroxyapatites studied in biological fields.33 The calcium to phosphorus ratio was also reported as one of the most relevant key parameter influencing the catalytic properties of this system: decreasing the bulk Ca/P ratio from stoichiometric to under-stoichiometric compounds changes the reactivity of the system from basic to acidic.11,34 Such control of the surface reactivity by the bulk composition is still controversial, mainly based on the assumption that the

Calcium hydroxyapatites (HAp) are compounds of great interest in various application fields. Being the main mineral component of bone tissue and teeth, they are important biomaterials1 with biomedical applications in reconstructive surgery,2 drug carriers,3 or bone regeneration.4−8 More recently, in the context of energetic mutation, the increasing demands of biomass valorization pave the way toward the development of new catalytic reactions,9 for which hydroxyapatites are considered as very promising heterogeneous catalysts. Indeed, they are quite stable systems with tunable surface properties thanks to a large versatility of composition,10,11 opening the route toward bifunctional12−14 and acid− base11,12,15−32 catalytic applications. In fact, beyond the reference calcium phosphate that is associated with Ca10(PO4)6(OH)2 formulation, with a Ca/P ratio of 1.67 corresponding to a full occupancy of calcium cations in the tridimensional framework,10 calcium deficient materials (Ca/P < 1.67, referred to as under stoichiometric © XXXX American Chemical Society

Received: July 23, 2015 Revised: September 15, 2015

A

DOI: 10.1021/acs.jpcc.5b08732 J. Phys. Chem. C XXXX, XXX, XXX−XXX

Article

The Journal of Physical Chemistry C

to the filling of the NMR rotors under controlled environments, (ii) comparing the spectra obtained after controlled isotopic H-D exchanges to improve the resolution and highlight the surface contributions, and (iii) recording various NMR sequences including inversion recovery sequence and 2D HECTOR to improve the resolution and asses the spatial proximity of the various species. This approach allows us to evidence new NMR signals related to both the surface and the bulk. The structural environment of the associated hydroxyl, water, phosphate, and hydrogenophosphates contributions is discussed, which leads to clearly assign the various species present in the bulk or at the surface and to propose a structural model for the organization inside the columnar OH channels and for the corresponding surface termination.

surface composition is in line with the bulk one: when going from stoichiometric to under-stoichiometric composition [i.e., from Ca10(PO4)6(OH)2 to Ca10−x(HPO4)x(PO4)6−x(OH)2−x,H2O], there would be a decrease of the amount of basic sites, possibly OH− and/or PO43−, to the benefit of the formation of new acidic sites such as HPO42−. If this evolution of the surface acid base balance was clearly observed based on the chemical nature of the products formed,32 there is no direct identification of the nature of the surface species involved yet. To enhance the understanding of how hydroxyapatite works as a catalyst, there is a need for characterizations at a molecular level in order to identify the nature and properties of the surface species really acting as active sites. Indeed, there is still a lack of spectroscopic techniques allowing to discriminate bulk from surface signals. Recently, using controlled H-D isotopic exchanges, we succeeded in assigning the distinct contributions of νO−H vibrations originating from the bulk (OH channels and HPO42− defects) and from the surface (OH emerging from the columnar channels and protonation of phosphate groups resulting from the surface relaxation process).35 However, the fingerprint of the surface OH emerging from the columns is not well-resolved from that of bulk OH and some surface PO-H contributions overlap with that from the bulk. If solid state NMR is one of the main techniques used to characterize the hydroxyapatite systems,32,33,36−46 most of the studies have been devoted to the investigation of biomaterials or biomimetic materials. In these systems, the core of the hydroxyapatite particles is associated with ordered crystalline hydroxyapatites, whereas their surface is described as a disordered layer involving nonapatitic structure enriched in HPO42− species.33,44,46 Thus, besides the NMR signals ascribed to structural PO43−33,40,45 and OH−,33,40,41,44,47,48 entities building up the three-dimensional crystalline framework of hydroxyapatite structure, other NMR signals that are ascribed to HPO42−40,49,50 or OH−45 groups present in the disordered surface layer were reported. A broad and intense signal, characteristic of physisorbed water molecules, is also assigned to this disordered hydrated layer,51,52 even if some authors also proposed that part of the related water molecules may be occluded in the bulk structure37,49,53 (as expected for the low Ca/P systems). In addition, although a thin proton line at 1.1 ppm is often observed, its assignment has been quite rapidly skipped.41,50 Moreover, up to now, no signal has been assigned yet to bulk HPO42− species that are expected to be present as defects in the bulk, especially in the case of understoichiometric HAp’s, as recently shown by infrared spectroscopy.35 Similarly, even though the crystalline surface of HAp catalysts was shown to involve terminal reactive acidic HPO42− and basic OH− groups,54 there is a lack of NMR investigations dealing with their associated fingerprints. The aim of this work is to discriminate the 1H and 31P NMR fingerprints of all the species likely to be present in the bulk or at the surface of crystalline hydroxyapatite particles. Model hydroxyapatite samples involving not only crystalline bulk structure but also well-organized surface terminations55 are studied. Weakly carbonated stoichiometric and under-stoichiometric samples have been synthesized by precipitation route followed by implementation of a subsequent thermal treatment at 623 K. Moreover, to discriminate the surface from the bulk features, complementary sets of NMR data have been accumulated (i) using specific procedures to prepare the samples before recording the spectra with implementation of a controlled pretreatment to desorb most of the water in addition

2. EXPERIMENTAL SECTION 2.1. HAp Preparation. A stoichiometric calcium hydroxyapatite sample [Ca10(PO4)6(OH)2] was prepared according to the procedure previously described:34 the coprecipitation of Ca(NO3)2 and (NH4)H2PO4 solutions adjusted beforehand at pH = 10 was performed at 353 K under N2 flow to limit the carbonation of the material. The pH was kept at pH = 10 during the precipitation and maturation time by periodic addition of NH3. The washed precipitate was then dried overnight at 373 K and thermally treated under Ar flow (150 mL min−1) up to 623 K (5 K min−1) and maintained at this temperature for 90 min. An under stoichiometric sample was prepared following the same procedure but without any addition of NH3 during the precipitation and maturation steps. From elemental analysis performed by ICP-AES by the “Service Central d’Analyse” of the CNRS (Solaize, France), the Ca and P contents were determined leading to Ca/P ratio of 1.67 and 1.52, respectively, for the two samples. The C content was found to be about 0.5 wt %. It was also checked from XRD diffractogramms [Siemens diffractometer equipped with a copper anode generator (λ = 1.5418 Å)] that the samples were very well-crystallized and exhibited the hexagonal hydroxyapatite structure [ICDD pattern 01-074-9780(A)] (not shown). HRTEM characterizations were performed using a JEOL 2011 microscope. It was observed that the particles are elongated rods that are well-crystallized even until their surface terminations, as shown in Figure 1. 2.2. NMR. 2.2.1. Pretreatment of the Samples Prior to NMR Measurements. Two series of samples were studied: the as-synthesized samples were pretreated up to 623 K for 90 min under vacuum (HAp); the second set of samples corresponds to the stoichiometric HAp sample, which OH content was modified by H-D exchanges. In this latter case, the HAp sample was also first pretreated up to 623 K (5 K/min) for 90 min under vacuum and then was modified by isotopic labeling using H-D exchanges. For this purpose, the same procedure already used to discriminate between infrared signals associated with the surface and bulk protons was achieved.35,54 Once the pretreatment at 623 K was implemented, the temperature was cooled down to 573 K; then D2O (1333 Pa) was adsorbed for 10 min before the sample was outgassed at this temperature for 10 min. This cycle was repeated twice leading to a deuterated hydroxyapatite sample (DAp). A soft rehydration step procedure was then performed: the DAp sample was cooled down to 373 K and H2O under 266 Pa was introduced for 10 min on the fully deuterated sample before the sample was outgassed at this temperature for 10 min. This cycle was repeated twice. From previous infrared data, this rehydration B


Article


202.47 MHz, respectively. A Bruker 4 mm CP MAS probe was used to perform all the experiments at a spinning speed of 12.5 kHz and 10 kHz. The 1H and 31P chemical shifts were referenced to external standards of tetra-methylsilane (TMS) and 85% H3PO4 aqueous solution, respectively. 1H MAS NMR spectra are performed with a 90° pulse duration of 3 μs, a recycle delay of 15 s, and a scan number of 32. The MAS equipment for rotation was carefully cleaned with ethanol then dried to avoid spurious proton signals. From two successive experiments performed in the same recording conditions and using the same empty or filled rotor, the probe and rotor signals were subtracted from the total FID. For the 1H MAS inversion recovery measurements, we used the pulse sequence: “180° − τr − 90° − acquisition” with different recovery times, τr (from 50 ms to 4 s). Spectra were decomposed with DMFIT program to determine the chemical shift values;56 then the SIMFIT program from TOPSPIN of Bruker was used to determine the T1 values (standard deviations from 10−3 to 10−2). 31P MAS NMR spectra are performed with a 90° pulse duration of 3.2 μs, a recycle delay of 300 s, and a scan number of 64. The 1H−31P HETCOR NMR spectra with CP polarization transfer were acquired with 3.4 μs for proton 90° pulse duration, a contact time and a recycle delay of 3 ms and 10 s, respectively. We used 100 t1 increments of 80 μs for F1 dimension acquisition and 208 scans. The 1H DQ-SQ spectrum was recorded with the PC7 sequence for excitation and conversion block, and we used a RF filed strength during the dipolar recoupling sequence of 70 kHz and 150 t1 increments of 100 μs for F1 dimension acquisition.

Figure 1. HRTEM micrograph of a particle obtained on the stoichiometric HAp sample. The measured inter-reticular distance of 8.1 Å reported in the inset corresponds to the (100) planes structure of hexagonal hydroxyapatite.

step mostly impacts the surface. However, an additional evacuation step at 473 K for 20 min was required to desorb most of the residual physisorbed and weakly chemisorbed H2O. This latter thermal step finally resulted in a limited bulk reprotonation.54 Thus, the obtained material that will be hereafter referred to as HDAp sample finally exhibits (i) a lower H concentration than the starting HAp sample, (ii) it is mostly deuterated in the bulk even if a few bulk hydroxyls are still on their protonated OH form, and (iii) it is fully reprotonated on the surface. 2.2.2. Filling of the NMR Rotor. For the two sets of HAp and HDAp samples, two different procedures were used to fill the 4 mm (external diameter) zirconia NMR rotor and close them with Kel-F caps. In the first one, 200 mg of the powdered sample were first heated inside a quartz reactor that was equipped with valves and connected to a vacuum ramp. One of the two abovedescribed procedures was implemented then the valves of the reactor were closed to isolate the sample from air before transferring it into a glovebag (Ar atmosphere) where the NMR rotor was filled and closed. The corresponding NMR spectra will be hereafter referred to H(D)Apt‑f (thermal treatment achieved before filling the rotor). In the second one, prior to the implementation of the pretreatment procedures, the as-prepared HAp sample was first introduced in the 4 mm NMR rotor; the open rotor was then placed in a larger reactor connected to the vacuum ramp where the two types of pretreatment procedure could be in situ implemented. Finally, the rotor was rapidly closed. The corresponding NMR spectra will be hereafter referred to as H(D)Apf‑t (filling of the rotor, then implementation of thermal treatment). It was checked that the close rotors are perfectly air- and moisture-tight. 2.2.3. NMR Sequences. All the one-dimensional (1D) and two-dimensional (2D) MAS NMR (HECTOR and POST C7 DQ-SQ) spectra were recorded at room temperature using a Bruker Advance spectrometer operating in a static field of 11.7 T. The resonance frequency of 1H and 31P were 500.16 and

3. RESULTS AND DISCUSSION 3.1. 1H NMR on HApt‑f and HDApt‑f Samples. 3.1.1. 1H MAS NMR. 3.1.1.a. HApt‑f Samples. The 1H MAS NMR spectra of the stoichiometric (spectrum a) and understoichiometric (spectrum b) HApt‑f samples are displayed in Figure 2. The spectra of the two samples show the typical main resonance peaks classically observed for hydroxyapatites, with (i) an intense and very narrow line centered at −0.01 ppm corresponding to column OH− proton resonance,33,40,41,44,47,48 (ii) a water peak at about 5.1 ppm that is usually assigned to physisorbed water51,52 and/or to structural water trapped inside the channels along the c axis,37,49,53,57 and (iii) a weak and narrow contribution around 1.1 ppm, which assignment is still a matter of debate.41,50 It is controversially ascribed to H-bonded structural OH (in the presence of structural water), mobile water, or even to organic impurities.33,37,38,40,41,50,53 However, the relative intensities of the various components are significantly modified compared to the spectra usually reported in literature. In particular, in relation with the implementation of the thermal pretreatment, the relative intensities of the water contribution at 5.1 ppm, as well as the signal at 1.1 ppm are decreased compared to that of the main OH signal. Indeed, the studied materials being most of the time under-stoichiometric biomimetic carbonated hydroxyapatites,33 no in situ thermal pretreatment was applied before NMR spectra were recorded. Moreover, the broad contribution around 3−17 ppm usually ascribed to the lone surface HPO42− groups40,49,50 appears here quite low in intensity and is partly hidden by the water contribution. Note, however, that it is better seen in the case of the under-stoichiometric sample (spectrum b) compared to the stoichiometric sample (spectrum a), as shown in the inset of Figure 2. It is questionable if it could also be related to the higher expected concentration of C


Article


Figure 3. 1H MAS Inversion recovery NMR spectra of stoichiometric (a) HApt‑f and (b) HDApt‑f at different 1H recovery times, τr (from 50 ms to 4 s; not all spectra are show, for purposes of clarity). Inset: zoom on the OH 1H MAS NMR signal of (c) HApt‑f and (d) HDApt‑f (solid lines) and decomposition of OH peak with three contributions (sum in dash lines).

Figure 2. 1H MAS NMR spectra of (a) stoichiometric HApt‑f, (b) under stoichiometric HAp, (c) stoichiometric HDApt‑f, and (d) stoichiometric HApf‑t [the intensities of the (b) and (c) spectra have been multiplied by 1.5]. Inset: zoom of stoichiometric HApt‑f (solid line) and under stoichiometric HAp (dash line).

HPO42− present in the bulk of an under-stoichiometric sample. On the other hand, the signal centered at −0.01 ppm is more intense in the case of the stoichiometric HApt‑f sample (spectrum a), which is consistent with the higher expected OH content in stoichiometric hydroxyapatites versus un der-sto ich io met ric o nes [ Ca 1 0 (PO 4 ) 6 (OH) 2 vs Ca10−x(PO4)6−x(HPO4)x(OH)2−x].10 Thus, on the one hand, the dependence of the two spectra a and b reported in Figure 2 on stoichiometry that is a bulk property, and on the other hand, the effect of thermal pretreatment (spectra presented here compared to literature) that is expected to mainly impact the surface raise the question of the bulk and/or surface origins of the several proton signals. 3.1.1.b. HDApt‑f Sample. To deepen this point, complementary data were obtained from H-D exchanged samples since isotopic labeling impacts differently the bulk and surface of the materials. As expected, due to the loss of the signal of the deuterated species that have been mainly exchanged in the bulk, the global intensity of the 1H MAS spectrum of the DHApt‑f sample (spectrum c in Figure 2) is largely decreased compared to that of the corresponding HApt‑f sample (spectrum a). Indeed, the intensity of the peak at −0.01 ppm has been greatly decreased. On the other hand, there is an enhancement of the broad contribution (3−17 ppm) that results in the apparent broadening of the signal at 5.1 ppm. This is consistent with the relative enrichment in surface HPO42− species compared to bulk OH expected from the isotopic labeling procedure applied. Moreover, when zooming on this −0.01 ppm line, the shape of the hydroxyl contribution was also modified upon isotopic labeling procedure, becoming more symmetrical for HDApt‑f than for the HApt‑f sample (see spectrum d vs spectrum c in the inset of Figure 3). This modification of the line shape is clearly indicative that there are various NMR components within this hydroxyl peak and that they are not similarly impacted upon

the isotopic labeling procedure. Considering that this treatment was shown to enhance the relative contribution of surface protons versus that of bulk species,35 it can thus be inferred that the 1H peak centered at −0.01 ppm includes bulk and surface components. 3.1.2. 1H MAS Inversion Recovery. To discriminate more clearly the various contributions in the hydroxyl peak, inversion recovery 1H MAS measurements were performed for the HApt‑f and HDApt‑f samples. Figure 3a shows the spectra obtained for the HApt‑f sample at different recovery times τr. Only two different OH contributions can be pointed out for this HApt‑f sample (Figure 3a). The most intense one appears at 0.10 ppm (T1 = 2.372 s). The less intense one is at −0.13 ppm (T1 = 1.630 s). Isobe et al. also concluded from inversion recovery 1H MAS measurements that there were two OH contributions.45 However, in their case, the involvement of two different OH components that were still superposed was deduced from two relatively different spin−lattice and apparent spin−spin (T2*) relaxation times. They proposed that these contributions might be associated with OH of the columns localized in the well-ordered region of the bulk and in the disordered near-surface layer. However, in the present study, contrary to what is suspected for under stoichiometric biomimetic materials,33,44,46 HRTEM characterizations (Figure 1) do not show any disordered amorphous phase at the near surface of the particles. Consistently, the behavior of the related surfaces in catalytic reaction was shown to be directly in line with the structure of the hydroxyapatite phase (involvement of surface OH emerging from the channels as active sites).34 Such improvement of the surface crystallinity associated with the implementation of thermal treatment prior to recording NMR spectra is responsible for the better resolution obtained here. Figure 3b shows the spectra obtained for different recovery times for the HDApt‑f sample. In this case, due to lower OH D


Article

The Journal of Physical Chemistry C concentration in the HDApt‑f sample than in the HApt‑f sample, the resolution of the peak was even more improved, revealing the presence of three different contributions at 0.10, −0.01, and −0.13 ppm with T1 values of 2.328, 2.365, and 1.517 s, respectively. Taking into account the respective positions of these three contributions, a decomposition of the peak was achieved for HApt‑f and HDApt‑f samples (Figure 3, panels c and d). It appears that the central contribution at −0.01 ppm is the less intense one for the two samples. However, this contribution is comparatively greatly increased in the case of the HDApt‑f sample. This points toward an assignment to surface hydroxyl groups emerging from the OH columns that will be hereafter referred to as OHS. The two other contributions at 0.10 and −0.13 ppm are rather assigned to two different bulk hydroxyl groups. Such differentiation has never been reported yet by NMR. They will be hereafter referred to as OHB‑1 and OHB‑2 bulk hydroxyls. Note that considering, their quite similar relative concentration, and the low carbon content in these series of materials, the local modification of some hydroxyl groups due to neighboring A or B type carbonation10,54,58−60 cannot be responsible for their differentiation. Complementary data on their local surrounding will be provided in Sections 3.1.4 and their detailed structural assignments will be discussed in Section 3.3.2.a. Also, note that despite the clear improvement of the resolution of the peak centered at −0.01 ppm observed for the HDApt‑f sample, only one water contribution could be observed in the present case, (Figure 3b), whereas Isobe et al. discriminated two water contributions in a broad signal around 5 ppm.45 This is consistent with the different nature of the hydroxyapatite samples considered. Indeed on the one hand, structural water molecules might be occluded in the bulk of under stoichiometric hydroxyapatites,1 and on the other hand, the implementation of the thermal pretreatment also resulted in the desorption of the physisorbed water, and only the most strongly chemisorbed water on the surface, interacting with surface PO-H and or calcium cations, are detected in the present conditions. 3.1.3. Influence of the Procedure of Filling of the Rotor: 1H NMR on HApf‑t and HDApf‑t Samples. 3.1.3.a. HApf‑t Sample. From Figure 2 spectrum d, and the zoom presented on Figure 4a, bottom spectrum, the implementation of the pretreatment procedure on the powder that had previously been put inside the NMR rotor (HApf‑t sample) was more efficient to remove water since the peak at 5.1 ppm has almost been completely removed. Such water desorption also resulted in the disappearance of the peak at 1.1 ppm to the benefit of low intensity lines at 1.8 and 1.4 ppm (see Figure 4, the modification from spectrum e (HApt‑f) to spectrum c (HApf‑t) in the inset). In addition, another new low intensity contribution at 3.1 ppm was also revealed. These contributions at 3.1, 1.8, and 1.4 ppm can be observed regardless of the Ca/P ratios of hydroxyapatites (data not shown). 3.1.3.b. HDApf‑t Sample. To get deeper insight on the bulk or surface attributions of these proton species, the same experiment was performed for the HDApf‑t sample (Figure 4b, bottom spectrum). On the partially deuterated sample only the two lines at 1.3 and 0.8 ppm could still be observed, and these contributions have even been comparatively intensified compared to the 1.8 and 1.4 ppm contributions observed for the HApf‑t sample (inset Figure 4, spectrum d). On the opposite, the one at 3.1 ppm was not detected any more. This

Figure 4. 1H MAS NMR spectra of stoichiometric (a) HApf‑t and (b) HDApf‑t (bottom spectra) and after transient opening of the rotor and exposure of the samples to ambient atmosphere (top spectra) for 2h (HApf‑t) and for 5 min, 20 min, and 1 h (HDApf‑t). Inset: zoom of 1H MAS NMR spectra of stoichiometric (c) HApf‑t, (d) HDApf‑t, and (e) HApt‑f.

infers a surface and bulk origin for these two series of proton signals, respectively. Taking into account that due to the isotopic labeling procedure, the HDAp sample remains more hydrated than that of the HAp one,35 the hydration level of the samples decreases along the series as follows: HApt‑f > HDApf‑t > HApf‑t. The associated decrease of the homonuclear dipole−dipole interaction results in the splitting of the 1.1 ppm line into the two 1.3 and 0.8 ppm contributions and finally in the shift of these two contributions to 1.8 and 1.4 ppm. Consistently, recording a new series of spectra after transitory opening of the rotor and exposing HDApf‑t samples (Figure 4b, top spectra) to ambient atmosphere led to the clear reappearance of water signal at 5.1 ppm and to the increase of the intensity and progressive shift of the lines at 0.8 and 1.3 ppm. Similarly, in the case of exposure of the HApf‑t sample to ambient atmosphere, the intensity of the detected bands increases and their position is slightly shifted (Figure 4a, top spectrum). Note that on the contrary, the fact that the signal at 3.1 ppm could not be recovered on the HDApt‑f sample after exposure of this sample to ambient atmosphere confirms its bulk origin. It should be also underlined that the behavior of the 1.1 ppm line observed on hydroxyapatite samples described above is clearly in line with previous data reported by Jarlbring et al.40 dealing with fluoroapatite samples. They reported that the intensity of a line at 0.9 ppm (corresponding to that usually observed at 1.1 ppm for hydroxyapatite) was decreased and splitted into two lines at 1.3 and 0.9 ppm after decreasing the amount of physisorbed water. Due to the small amount of hydroxyl groups present in the sample, they assigned the related species to bulk hydroxyls close to calcium building up the tunnels40 (F species substituted for OH). Such assignment is not consistent with the detection of the same species in E


Article

The Journal of Physical Chemistry C hydroxyapatite samples. The surface localization of the related species should rather be considered. These species will be hereafter referred to as HS‑1 and HS‑2. 3.1.4. Double Quantum-Single Quantum Spectra. In order to clarify the nature and the local environment of the various hydroxyl contributions detected in the peak centered at −0.01 ppm and of the protons involved in the two 0.8 and 1.3 ppm lines, 2D DQ-SQ spectra were recorded. To benefit from on the one hand the decrease of the homonuclear dipole−dipole interaction on the resolution of these lines and on the other hand the intensity increase of the 0.8 and 1.3 ppm lines upon transient opening of the rotor, the HDApf‑t sample that was exposed to ambient atmosphere for 1 h (Figure 5) was studied.

Figure 6. 31P MAS NMR spectra of (a) stoichiometric HApf‑t, (b) under stoichiometric HApf‑t, and (c) HDApf‑t. Inset: zoom of 31P MAS NMR spectra of stoichiometric (d) HAp f‑t and (e) under stoichiometric HApf‑t.

samples are narrower, which is consistent with the higher crystallinity of the particles. However, the line width of the peak corresponding to the under-stoichiometric sample (Figure 6, spectrum b) is comparatively broader. Moreover, a broadening of the lower part of the line at low and high chemical shifts can be clearly observed from the inset in Figure 6, spectrum e). They might be linked to the contributions at approximately −7 ppm and a shoulder at 0.8 ppm usually reported for bone36 or calcium deficient hydroxyapatite minerals.61 These broad signals were usually assigned to the lone protonated surface phosphates groups arising from the disordered near surface hydrated layer.33,46,62,63 Indeed, these hydroxyapatite particles are described as an ordered hydroxyapatite core surrounded by a disordered nonapatitic hydrated surface layer.33,44,46 The corresponding phase associated either with an OCP-like structure64 or with amorphous calcium phosphate46,62 is always reported to be enriched in HPO42− groups.44 The absence of such disordered surface layer (Figure 1) explains the lower intensity of the related contributions. Thus, the origin of the residual broad contributions has to be discussed thanks to HETCOR spectra reported below. The more unusual part is the shoulder observed at 6.3 ppm that is more resolved in the case of the stoichiometric sample. Its lower detection than for the under-stoichiometric one might be related to (i) the broadening of the 2.9 ppm band, (ii) its hindering by the involvement of an additional contribution around 5 ppm (see below), and/or (iii) the lower concentration of the related species. Recently, a similar signal around 6.5 ppm was reported on hydroxyapatite samples with high Ca/P ratios.32 It was ascribed to a distribution of phosphorus species in relation with the structural modifications possibly induced by the incorporation of carbonates. However, in the present case, the samples are not deeply carbonated. Moreover, biological and biomimetic apatites that classically contain up to 8 wt % of carbonates10,42,43 do not exhibit such a shoulder. Note that this signal was not enhanced neither by cross-polarization sequence nor by proton decoupling (not

Figure 5. 1H POST C7 DQ-SQ spectrum of HDApf‑t sample exposed to ambient atmosphere for 1 h.

As far as hydroxyl signal (centered at −0.01 ppm) is concerned, only two associated correlation lines could be detected on the DQ-SQ spectra (Figure 5), although we have shown that it includes two bulk contributions OHB and one surface contribution OHs. This is probably due to the narrowness of this signal. The two correlation signals associated with the two most intense lines (OHB) are clearly centered on each side of the diagonal. It means that the proton of one group is close to proton of the other type (short distance between OHB1−OHB2) so that they can be involved into homonuclear dipole interactions, whereas the protons of the same type are too far from each other (long distances OHB1−OHB1 or OHB2−OHB2). There are also only two correlation signals related to the surface protons HS‑1 and HS‑2 associated with the 0.8 and 1.3 ppm lines. They are located on the diagonal: protons of each type are only correlated with protons of the same nature, which is indicative of the spatial proximity of the surface protons of the same type (HS‑1 close to HS‑1 and HS‑2 close to HS‑2), whereas the HS‑1 and HS‑2 are more distant from each other. A more detailed structural assignment for the OHB‑1, OHB‑2, HS‑1, and HS‑2 species will be proposed in Section 3.3.2.b. 3.2. 31P NMR on the HApt‑f and HApf‑t Samples. 3.2.1. 31P MAS NMR. The 31P MAS NMR spectra of the understoichiometric and stoichiometric HApt‑f samples are shown in Figure 6. The main resonance peak at 2.9 ppm is typical of bulk phosphate groups PO43− of hydroxyapatites.33,40,45 Note that, compared to biomimetic materials,33,40,45 the line width of both F


Article

The Journal of Physical Chemistry C shown). This rather points out toward the involvement of surface deprotonated phosphate groups, PO43−. The existence of such surface-terminated PO43− groups is confirmed by their involvement in the interaction with CO2 to form surface carbonates that are not stable after a thermal treatment similar to that achieved in the present work.54 A geometrical deformation of the related surface tetrahedra (surface relaxation) might explain the chemical shift observed. This assignment is also supported by the fact that nonprotonated phosphate groups are expected to be less shielded than protonated ones.65 Besides, Jarlbring at al. also reported a shoulder signal at high chemical shift, around 5.4 ppm, which they attributed to surface nonprotonated phosphate groups on the basis of the dependence of this contribution on thermal treatment and on the pH of solution let in contact with the sample.40 Such surface PO43− assignment might also explain the relative higher contribution of this species in the stoichiometric compound (and also in over stoichiometric compounds, results not shown, and in ref 32) compared to the under-stoichiometric one: one may reasonably expect a higher concentration of terminal nonprotonated phosphate groups at the surface of a stoichiometric compound. Indeed, beyond the increase of the PO43−/HPO42− relative concentration in the bulk with increasing the Ca/P ratio [Ca10−x(HPO4)x(PO4)6−x) (OH)2−x],10 the same trend is expected to occur at the surface. Indeed, the well-established experimental relationship between the bulk Ca/P ratio and the control of surface acid−base properties (the higher the Ca/P ratio, the higher the basicity and the lower the acidity)11,34 is in line with the expected surface relaxation process resulting in protonation of phosphate groups to ensure the surface charge balance, especially in the case of a calcium deficiency.66 3.2.2. 31P−1H HETCOR NMR. 2D 1H−31P heteronuclear correlation spectra (HETCOR) were recorded in order to better assess the assignments and to describe the proximity of phosphorus and protons (Figure 7). Figure 7 (A and B) show the 2D spectra of the under-stoichiometric and stoichiometric HApt‑f samples, respectively. As expected, for both samples, the 2D spectra show the main signal resonating at −0.01 ppm along the H axis (OH from the channels) that cross polarizes with the main P signal at 2.9 ppm along the P axis (structural bulk phosphates groups) (area I). Consistently with the larger distribution of various phosphorus contributions described above, the dispersion of this correlation signal along the 31P axis is wider in the case of the understoichiometric sample (Figure 7A). In the case of the stoichiometric compound (Figure 7B), the good resolution of the contribution at 6.3 ppm clearly allows for the observation that this signal is also coupled to hydroxyl (area I′). The resolution along the H axis is however not sufficient to discriminate between the different types of OH described in the previous sections to confirm its surface origin. The main difference between the two samples is the intensity of the second correlation signal (area II), that is centered around 5 ppm along the 1H axis. The related protons do not cross polarize with the main band at 2.9 ppm along the 31P axis, but, rather with contributions that are centered on either side on this main line. In fact, these 31P contributions spread from 7 ppm for both samples to approximately −13 ppm for the under stoichiometric sample. For this under stoichiometric sample, the involved 1H contribution also spreads to high chemical shift (∼17 ppm). Up to now, this whole correlation area was ascribed to water and/or hydrogenophosphates from the

Figure 7. 2D 31P−1H HECTOR spectra of (A) under stoichiometric HApt‑f, (B) stoichiometric HApt‑f, and (C) stoichiometric HApf‑t.

disordered surface layer of biological or biomimetic hydroxyapatites.33,46 In the present case, considering both the crystallinity of the surface and the lower amount of water resulting from pretreatment performed at 623 K for HApt‑f samples, the intensity and dispersion of this correlation is greatly decreased compared to previous reported data,33 G


Article

The Journal of Physical Chemistry C Table 1. 1H and 31P NMR Signals Detected on Well Crystalline Hydroxyapatites Samples and Their Corresponding Assignments

especially for the stoichiometric sample. Thus, considering the surface crystallinity of the two samples of different stoichiometries, the question of the surface or bulk origin of this correlation area can be raised. Indeed, Silvester et al. although considering samples of various stoichiometries did not discuss the possible influence of the related variations of bulk water and hydrogenophosphates content and only concluded to the involvement of surface hydrogenophosphate groups responsible for the Brønsted acidic properties, even if no dehydration of the sample was previously achieved.32 To get a better insight on the water or hydrogenophosphate assignment of this signal, the same HETCOR experiment was performed on the stoichiometric HApf‑t sample (Figure 7C). Due to the enhanced dehydration already described in Section 3.1.3.a, the 2D spectra are more resolved. The correlation between phosphorus at 6.3 ppm and hydroxyl groups appears even more clearly (area I′). Besides, due to the almost full desorption of water (peak at 5.1 ppm), the residual second correlation area (area II on Figure 7B) is now split into two contributions (areas II and II′ on Figure 7C). The first one, annotated as area II, involves the proton line at 3.1 ppm that was revealed upon full dehydration process and was shown from isotopic labeling experiment to be related to the bulk. It is therefore assigned to bulk hydrogenophosphates. Close examination along the 31P axis reveals a quite large dispersion. On the one hand, one can identify a main contribution around 4.8 ppm that might correspond to the broadening of the bottom of the main phosphorus peak observed for the under stoichiometric sample (consistently under stoichiometric samples are expected to exhibit a higher relative amount of bulk HPO42− compared to stoichiometric compounds). On the other hand, a more diffuse contribution associated with broader P contribution might account for different local environments possibly due to the perturbation of the symmetry of these hydrogenophosphate groups induced by the presence of few bulk carbonates,10,54,58−60 as shown by infrared.35,54 The second contribution, annotated as area II′, is associated with protons with higher chemical shifts. It is quite diffuse, ranging from 8 to 13 ppm. On the basis of the fact that infrared studies showed that, regardless of the stoichiometry, the surface of crystalline hydroxyapatite surface is always terminated by protonated phosphate groups, and that the related PO-H vibrators were shown to be stable up to high temperature,35,54 it is proposed that this correlation signal is associated with surface protonation of terminal phosphate groups. The quite diffuse contribution is in line with the numerous surface νPO-H contributions observed by infrared. This might be explained by different local surface structure and different protonation levels, HxPO4, as proposed by Jarlbring et al.40 3.3. Structural Model for Bulk and Surface Termination of Crystalline Hydroxyapatite Nanoparticles. On the basis of the complementary set of data obtained, and thanks to an improved resolution, new 1H and 31P NMR signals have been detected for crystalline hydroxyapatite samples. Their bulk or surface origins could be assessed, as summarized in Table 1. New NMR features concerning the local surroundings of both the phosphate and columnar OH groups allow us to refine the structural model for bulk and surface of crystalline hydroxyapatite nanoparticles. 3.3.1. Phosphate Groups. Figure 8 reports the various 31P contributions detected in this study. To sum up, beside the line related to bulk PO43− groups of the tridimensional HAp framework, for the first time, we could also identify the NMR

NMR chemical shift (ppm) bulk

1

H − 0.10b −0.13b 3.1 (+2−7)

P 2.9 − − 4.8

(+2−6)

5.1

surface

− 8−13 −0.01

6.3 3−7 −

1.3b

− −

0.8b

−

1.1

−

5.1

assignment

comments

31

PO4 OHB‑up OHB‑down HPO4 distorded HPO4 occluded H2O PO4 HxPO4 OHs‑up or OHs-down OHs‑down structured H2O−up structured H2O−down structured stacking H2O physi/ chemisorbed H2 O

main linea main linec defects to ideal HAp structurec a,c

not resolved from the physi/chemisorbed waterc low intensity not resolved

d

split into 1.3 and 0.8 ppm contributions at low water contentd d

a

The line width depends on the crystallinity and on the carbonate content. bArbitrary assignment of ≪up≫ and ≪down≫ conformations to high and low chemical shifts, respectively. cRelative intensities found to be dependent on the stoichiometry. dRelative intensity found to be controlled by the hydration level (dependent on the efficiency of the in situ thermal treatment, H-D exchanged procedure, and/or on the contact with ambient atmosphere).

signatures of bulk defective HPO42− species. The presence of few bulk carbonates could be responsible for the symmetry perturbation of these hydrogenophosphates groups leading to different local environments which explain the two related contributions observed. Associated 1 H and 31 P NMR contributions are reported in Table 1. NMR spectra are thus clearly dependent on the stoichiometry of the hydroxyapatite samples. NMR is also sensitive enough to provide information on the surface of these crystalline particles. Consistently with experimental data obtained by infrared spectroscopy,35,67,68 it is confirmed from solid state NMR that the surface of the wellcrystallized particles are terminated by protonated phosphates groups (Table 1). If the 31P fingerprints of these terminated protonated phosphate groups is quite qualitatively similar to that usually described in literature for enriched HPO42− disordered surface layer, the intensity of this contribution is greatly decreased compared to what is observed in biological or biomimetic HAp systems. In addition, beside the bulk and surface discrimination of the protonated phosphate groups, it was also possible to detect a 31P surface contribution at 6.3 ppm associated with surface terminated nonprotonated phosphate groups. Thus, NMR provides data that could not be simply obtained from infrared spectroscopy: up to now, the presence of surface-terminated PO43− groups was only indirectly probed by infrared spectroscopy and deduced from their interaction with CO2 to form specific surface carbonates species.54 H


Article


Figure 8. Typical multicomponent 31P NMR spectrum of well-crystallized hydroxyapatite sample. The different contributions are schematically reported. For the sake of clarity, unlike the positions of the different contributions, the relative intensities are not represented within a realistic manner.

Figure 9. Typical multicomponent 1H NMR spectrum of well crystallized hydroxyapatite sample. The different contributions are schematically reported. For the sake of clarity, unlike the positions of the different contributions, the relative intensities are not represented within a realistic manner.

3.3.2. OH Channels. Besides the 1H contribution of the protonated phosphates mentioned above, and those expected for water and structural OH, the 1H NMR spectra were shown to include several additional contributions. They are all schematically summarized in Figure 9. These new contributions were shown to be related to either the bulk or the surface and needed to be more precisely assigned. 3.3.2.a. Bulk Organization Inside the OH Channels. In the hydroxyapatite structure, the hydroxyl groups are localized in channels along the c axis. We propose that the two different types of bulk hydroxyl groups OHB‑1 and OHB‑2 might correspond to the so-called “up” and “down” orientations of the proton of the hydroxyl groups in the OH columns69,70

(Table 1). In the monoclinic hydroxyapatite phase, the OH dipoles are all oriented in the same way inside a given tunnel but in opposite way in two neighboring tunnels.70,71 However, the hexagonal hydroxyapatite phase being more stable than the monoclinic one,72 the samples of this study exhibit the hexagonal symmetry [ICDD pattern 01−074−9780(A)]. As far as the hexagonal structure is concerned, there are two proposed models for the orientations of the OH dipole in the channels: either the consecutive OH dipoles from a given tunnel may be all oriented in the same way (only OHB‑up or OHB‑down in the same channel) with a random orientation in neighboring tunnels or they may be oriented differently in a I


Article


corresponding terminated surface OHs‑up(down) groups explains the close proximity of the chemical shift associated with OH belonging to these bulk or surface OH resulting in a narrow band. As far as the two other HS‑1 and HS‑2 surface signals at 0.8 and 1.3 ppm are concerned, they can definitively not be ascribed to these terminal hydroxyl groups: (i) from DQ-SQ spectra, there is no spatial proximity with OH present in the bulk and (ii) two adjacent columns are too far from each other to be consistent with the homonuclear dipole−dipole interaction observed within species of the same type. On the opposite, the two associated correlation lines (Figure 5) observed rather points toward the involvement of either surface Ca(OH)2-like species associated with the two different calcium sites present in hydroxyapatites10 or peculiar surface water molecules of two different types. At this stage, the assignment to Ca(OH)2 must be rejected for a set of reasons: (i) no related νOH infrared band has been detected, (ii) 1H NMR chemical shift for Ca(OH)2 is expected at 1.57 ppm,73 (iii) among the two types of surface terminations, either Ca rich one or phosphate rich one,55 previous XPS and CO adsorption data showed that the studied samples do not exhibit calcium rich surface terminations and are rather terminated by protonated phosphates.54 (iv) How to explain the increased intensity of the related lines upon contact with ambient atmosphere? (v) A broad signal would be expected for such hydroxylation of surface calcium cations. On the opposite, the lines are very narrow which is quite unusual for surface species. It is the sign of the involvement of well-structured surface species. On the basis of the DQ-SQ data and on the evolution of the related lines within exposure to ambient atmosphere, we conclude to the involvement of peculiar surface water molecules. Unlike the previous authors also proposing water assignment for the 1.1 ppm line,33,50 these new experimental results enable us to discuss the bulk or surface location of the 0.8 and 1.3 ppm lines, to make precise their nature, and to explain their differentiation with the water involved in the broad line at 5.1 ppm. The narrowness of these two contributions accounts for a surface structuration of these water molecules. As depicted in Figure 10, it can be proposed that surface water molecules may be formed at the surface termination of some OH tunnels via a surface relaxation process of some terminal OHS‑up(down) groups, leading thus to structured surface water molecules aligned with OH inside the channels. The two lines at 0.8 and 1.3 ppm associated with low water content could be relative to the H2OS‑up or H2OS‑down termination of different columns. Indeed the local configuration of the related two types of water molecules would be governed by their formation from terminal OHS‑up or OHS‑down hydroxyls. The multilayer stacking of such “external columnar” water in continuity with the organization of the “internal OH” channels with increasing hydration level progressively favors the homonuclear dipole−dipole interaction between these water columns finally resulting in a loss of resolution explaining the detection of a single line at 1.1 ppm (stacking of external water molecules along the c axis). Such model could also account for the peculiar tendency of hydroxyapatite particles to be perfectly coaligned along the c axis, as described in literature, even in absence of any organic compounds.46 Such structured surface water which stacks up in alignment with bulk OH present inside the channels is clearly different from that associated with the broad 5.1 ppm line. The latter corresponds to physisorbed water and weakly chemisorbed water on the surface calcium and phosphates (mostly

same channel (both OHB‑up and OHB‑down are present, with a random distribution). However, up to now, no experimental spectroscopic proof of the involvement of two types of OH in the bulk of hydroxyapatite structure had been reported yet. A unique νO−H vibration at 3572 cm−1 can be observed by infrared. The narrowness of this band is consistent with the distance of 0.344 nm between two adjacent O belonging to hydroxyls groups (no H-bonding interaction).71 Hence, the present study shows for the first time an experimental spectroscopic feature based on 1 H NMR that accounts for the presence of two types of bulk OH at 0.10 and −0.13 ppm. Moreover, from the DQ-SQ experiment, the two OHB‑1 and OHB‑2 species correspond to the so-called “OHB‑up” and “OHB‑down” that are simultaneously present in the same tunnel. Indeed, as schematically represented in Figure 10, such structural model leads to two

Figure 10. Schematic representation of the possible configurations of different columnar OH channels in hexagonal hydroxyapatite crystalline particles in the bulk (gray area) and at the surface and organization of structured surface water molecules aligned with OH inside the channels. The various columns along the c axis being distant from 9.4 nm, there is no H-bonding lateral interaction from one column to the other in the bulk or between the first layers of water molecules adsorbed at the surface terminations of the columns.

different distances between two protons of adjacent hydroxyl groups, (between protons of dipole oriented differently (OHB‑up close to OHB‑down) and between two protons oriented in the same way (OHB‑up close to OHB‑up or OHB‑down close to OHB‑down), which is consistent with the two corresponding correlation lines observed on Figure 5. 3.3.2.b. Surface Terminations of the OH Channels. Thanks to H-D exchanges experiments and to the adsorption of probe molecules, it was possible to identify the infrared fingerprint of terminal OH emerging from the OH tunnels at the surface.35,54 Corresponding 1H NMR fingerprint at −0.01 ppm could be obtained in the present work combining the data obtained from the isotopic labeling and 1H NMR inversion recuperation experiments. From the very similar positions of the infrared or 1 H NMR fingerprints of bulk and surface OH, it can be concluded that the local structure of the related OH at the surface is not deeply modified by surface relaxation processes. Thus, by analogy with the “up” or “down” orientations for bulk OH, one might reasonably expect two corresponding orientations for surface OHS (OHs‑up and OHs‑down) (Figure 10). Unfortunately, the low concentration of these surface OHS‑up and OHS‑down groups and the lack of resolution of the two spectroscopic techniques prevent their discrimination. The ordered organization of the channels in the bulk and of the J


Article


terminated by structured water molecules (0.8 and 1.3 ppm). This leads to the stacking of structured water molecules (1.1 ppm) along the c axis in continuation with the internal OH channels. NMR being the only technique able to probe the presence of PO4, HxPO4, OH, and water at the surface of hydroxyapatite samples, it could be very useful to describe the respective role of these various surface entities in various fields of application of the hydroxyapatite system. In particular, it may help discussing their involvement in the catalytic processes, the surface reactivity being directly dependent on the surface composition. Moreover, the surface model described for the termination of crystalline hydroxyapatite particles might also be useful to help rationalize the formation of the interface between hydroxyapatite core and disordered surface layer of biomimetic hydroxyapatite samples.

on their protonated form). The intensities of 1.1 ppm (or corresponding 0.8 and 1.3 ppm for very low water content) and 5.1 ppm water contributions are all greatly impacted by the hydration/dehydration level of the samples.

4. CONCLUSION Combining the 1H and 31P NMR characterizations performed on well-crystallized stoichiometric and under-stoichiometric hydroxyapatite samples that have been in situ thermally heated just before or after filling of the NMR rotor and the implementation of the H-D exchanges, well-resolved NMR spectra could be obtained. In addition to the 1H and 31P signals already observed in literature, which assignments were revisited, some new signals were detected. Considering that the isotopic labeling procedure applied impacts differently the signals associated with bulk or surface species, the surface and bulk location of the 1H NMR signals could be discussed. From complementary data obtained from the 2D NMR characterizations (DQSQ and HETCOR sequences), the relative proximity of the various species was assessed which allowed us to assign the OH−, H2O, PO43−, or HPO42− nature of the different NMR signals and to describe their respective localization in the bulk and at the relaxed surface of these well-crystallized materials. First of all, the main structural contributions associated with bulk OH and phosphate groups exhibit narrow lines, which is in line with the high crystallinity of the studied samples and probably with their low-carbonation levels. Moreover, a dependence on the stoichiometry Ca 1 0 − x (PO 4 ) 6 − x (HPO4)x(OH)2−x of the relative intensities of the various MAS NMR contributions could be observed: the higher the Ca/P ratio, the more intense is the 1H line centered at −0.01 ppm associated with OH columnar. Similarly, the high dehydration level conditions revealed a more intense shoulder at 1H 2−7 ppm in the case of the under stoichiometric sample that is ascribed to bulk HPO42− species. Indeed, for the first time the NMR signature of the HPO4 species present as defective sites in the bulk could be revealed. Moreover, spectroscopic features dealing with the hydroxyl groups from the columns were also revisited, with the discrimination of two different types of OH columnar channels in the bulk, at 0.10 and −0.13 ppm, corresponding to up and down orientations of their related protons. From the different spatial proximity of these related protons inside the columns, it is concluded that these two OHB‑up and OHB‑down hydroxyl orientations are statistically distributed inside a same tunnel. This thorough description of the bulk structure of crystalline hydroxyapatite samples could be important to rationalize the polarization and conductivity properties of hydroxyapatite ceramic electrets.69−72 As far as signals related to the surface are concerned, besides the signals ascribed to terminated protonated phosphate groups, it could also be possible to detect a phosphorus signal at 6.3 ppm associated with nonprotonated phosphates. Originally, for the first time the NMR signature of surface hydroxyl groups emerging from the channels was also identified at −0.01 ppm. The surface of the hydroxyapatite particles has however a great affinity for hydration, which could be monitored by a peculiar attention devoted to the filling of the NMR rotor combined with thermal pretreatment of the samples: besides the well-known broad 5.1 ppm signal associated with water adsorbed on surface calcium cations and hydrogenophosphate groups, the OH columns can also be

■

ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpcc.5b08732. Complete ref 46 (PDF)

■

AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. *E-mail: [email protected]. Tel: +33 1 44 27 36 32. Fax: +33 1 44 27 60 33. Notes

The authors declare no competing financial interest.

■

REFERENCES

(1) Rey, C.; Combes, C.; Drouet, C.; Grossin, D. Bioactive Ceramics: Physical Chemistry; Elsevier: Amsterdam, 2011; Vol. 1, pp 187−221. (2) Lee, D. W.; Kim, J. Y.; Lew, D. H. Use of Rapidly Hardening Hydroxyapatite Cement for Facial Contouring Surgery. Journal of Craniofacial Surgery 2010, 21, 1084−1088. (3) Hong, M. H.; Oh, D. S.; Lee, Y. K. Drug Release from Porous Hydroxyapatite Spheres as a Synthetic Bone-Graft Material. Bone 2011, 48 (Supplement2), S186. (4) Heughebaert, M.; LeGeros, R. Z.; Gineste, M.; Guilhem, A.; Bonel, G. Physicochemical Characterization of Deposits Associated with Ha Ceramics Implanted in Nonosseous Sites. J. Biomed. Mater. Res. 1988, 22, 257−268. (5) Glowacki, J.; Rey, C.; Cox, K.; Lian, J. Effects of Bone Matrix Components on Osteoclast Differentiation. Connect. Tissue Res. 1989, 20, 121−129. (6) Cho, J. H.; Garino, J. P.; Choo, S. K.; Han, K. Y.; Kim, J. H.; Oh, H. K. Seven-Year Results of a Tapered, Titanium, HydroxyapatiteCoated Cementless Femoral Stem in Primary Total Hip Arthroplasty. Clin. Orthop. Surg. 2010, 2, 214−220. (7) Choudhury, P.; Agrawal, D. C. Sol−Gel Derived Hydroxyapatite Coatings on Titanium Substrates. Surf. Coat. Technol. 2011, 206, 360− 365. (8) Wang, M. Developing Bioactive Composite Materials for Tissue Replacement. Biomaterials 2003, 24, 2133−2151. (9) Sheldon, R. A. Green and Sustainable Manufacture of Chemicals from Biomass: State of the Art. Green Chem. 2014, 16, 950−963. (10) Elliot, J. C. Structure and Chemistry of the Apatites and Other Calcium Orthophosphates; Elsevier: Amsterdam, 1994; Vol. 18, 1−404. (11) Tsuchida, T.; Kubo, J.; Yoshioka, T.; Sakuma, S.; Takeguchi, T.; Ueda, W. Reaction of Ethanol over Hydroxyapatite Affected by Ca/P Ratio of Catalyst. J. Catal. 2008, 259, 183−189. (12) Sugiyama, S.; Iguchi, Y.; Minami, T.; Hayashi, H.; Moffat, J. B. Partial Oxidation of Methane to Methyl Chloride with TetrachloroK


Article

The Journal of Physical Chemistry C methane on Strontium Hydroxyapatites Ion-Exchanged with Lead. Catal. Lett. 1997, 46, 279−285. (13) Sugiyama, S.; Nitta, E.; Hayashi, H.; Moffat, J. B. Alkene Selectivity Enhancement in the Oxidation of Propane on CalciumBased Catalysts. Catal. Lett. 1999, 59, 67−72. (14) Sugiyama, S.; Osaka, T.; Hirata, Y.; Sotowa, K. I. Enhancement of the Activity for Oxidative Dehydrogenation of Propane on Calcium Hydroxyapatite Substituted with Vanadate. Appl. Catal., A 2006, 312, 52−58. (15) Joris, S. J.; Amberg, C. H. The Nature of Deficiency in Nonstoichimetric Hydroxyapatites. I Catalytic Activities of Calcium and Strontim Hydroxyapatites. J. Phys. Chem. 1971, 75, 3167−3171. (16) Monma, H. Catalytic Behavior of Calcium Phosphates for Decompositions of 2-Propanol and Ethanol. J. Catal. 1982, 75, 200− 203. (17) Sebti, S.; Tahir, R.; Nazih, R.; Boulaajaj, S. Comparison of Different Lewis Acid Supported on Hydroxyapatite as New Catalysts of Friedel−Crafts Alkylation. Appl. Catal., A 2001, 218, 25−30. (18) Sebti, S.; Smahi, A.; Solhy, A. Natural Phosphate Doped with Potassium Fluoride and Modified with Sodium Nitrate: Efficient Catalysts for the Knoevenagel Condensation. Tetrahedron Lett. 2002, 43, 1813−1815. (19) Sebti, S.; Solhy, A.; Tahir, R.; Smahi, A. Modified Hydroxyapatite with Sodium Nitrate: An Efficient New Solid Catalyst for the Claisen-Schmidt Condensation. Appl. Catal., A 2002, 235, 273−281. (20) Smahi, A.; Solhy, A.; El Badaoui, H.; Amoukal, A.; Tikad, A.; Maizi, M.; Sebti, S. Potassium Fluoride Doped Fluorapatite and Hydroxyapatite as New Catalysts in Organic Synthesis. Appl. Catal., A 2003, 250, 151−159. (21) Zahouily, M.; Abrouki, Y.; Bahlaouan, B.; Rayadh, A.; Sebti, S. Hydroxyapatite: New Efficient Catalyst for the Michael Addition. Catal. Commun. 2003, 4, 521−524. (22) Tahir, R.; Banert, K.; Solhy, A.; Sebti, S. Zinc Bromide Supported on Hydroxyapatite as a New and Efficient Solid Catalyst for Michael Addition of Indoles to Electron-Deficient Olefins. J. Mol. Catal. A: Chem. 2006, 246, 39−42. (23) Kumar, P. A.; Reddy, M. P.; Ju, L. K.; Phil, H. H. Novel Silver Loaded Hydroxyapatite Catalyst for the Selective Catalytic Reduction of NOx by Propene. Catal. Lett. 2008, 126, 78−83. (24) Tsuchida, T.; Yoshioka, T.; Sakuma, S.; Takeguchi, T.; Ueda, W. Synthesis of Biogasoline from Ethanol over Hydroxyapatite Catalyst. Ind. Eng. Chem. Res. 2008, 47, 1443−1452. (25) Chen, W.; Huang, Z. L.; Liu, Y.; He, Q. J. Preparation and Characterization of a Novel Solid Base Catalyst Hydroxyapatite Loaded with Strontium. Catal. Commun. 2008, 9, 516−521. (26) Opre, Z.; Mallat, T.; Baiker, A. Epoxidation of Styrene with Cobalt-Hydroxyapatite and Oxygen in Dimethylformamide: A Green Technology? J. Catal. 2007, 245, 482−486. (27) Sugiyama, S.; Osaka, T.; Hirata, Y.; Sotowa, K. I. Enhancement of the Activity for Oxidative Dehydrogenation of Propane on Calcium Hydroxyapatite Substituted with Vanadate. Appl. Catal., A 2006, 312, 52−58. (28) Opre, Z.; Grunwaldt, J. D.; Mallat, T.; Baiker, A. Selective Oxidation of Alcohols with Oxygen on Ru-Co-Hydroxyapatite: A Mechanistic Study. J. Mol. Catal. A: Chem. 2005, 242, 224−232. (29) Sugiyama, S.; Minami, T.; Moriga, T.; Hayashi, H.; Koto, K.; Tanaka, M.; Moffat, J. B. Surface and Bulk Properties, Catalytic Activities and Selectivities in Methane Oxidation on near-Stoichiometric Calcium Hydroxyapatites. J. Mater. Chem. 1996, 6, 459−464. (30) Ogo, S.; Onda, A.; Yanagisawa, K. Selective Synthesis of 1Butanol from Ethanol over Strontium Phosphate Hydroxyapatite Catalysts. Appl. Catal., A 2011, 402, 188−195. (31) Liu, J.; Ye, X.; Wang, H.; Zhu, M.; Wang, B.; Yan, H. The Influence of pH and Temperature on the Morphology of Hydroxyapatite Synthesized by Hydrothermal Method. Ceram. Int. 2003, 29, 629−633. (32) Silvester, L.; Lamonier, J. F.; Vannier, R. N.; Lamonier, C.; Capron, M.; Mamede, A. S.; Pourpoint, F.; Gervasini, A.; Dumeignil,

F. Structural, Textural and Acid-Base Properties of CarbonatesContaining Hydroxyapatites. J. Mater. Chem. A 2014, 2, 11073−11090. (33) Jäger, C.; Welzel, T.; Meyer-Zaika, W.; Epple, M. A Solid-State NMR Investigation of the Structure of Nanocrystalline Hydroxyapatite. Magn. Reson. Chem. 2006, 44, 573−580. (34) Diallo-Garcia, S.; Laurencin, D.; Krafft, J. M.; Casale, S.; Smith, M. E.; Lauron-Pernot, H.; Costentin, G. Influence of Magnesium Substitution on the Basic Properties of Hydroxyapatites. J. Phys. Chem. C 2011, 115, 24317−24327. (35) Diallo-Garcia, S.; Ben Osman, M.; Krafft, J. M.; Boujday, S.; Costentin, G. Discrimination of Infra Red Fingerprints of Bulk and Surface POH and OH of Hydroxypatites. Catal. Today 2014, 226, 81− 88. (36) Wu, Y.; Glimcher, M. J.; Rey, C.; Ackerman, J. L. A Unique Protonated Phosphate Group in Bone Mineral Not Present in Synthetic Calcium Phosphates: Identification by Phosphorus-31 Solid State NMR Spectroscopy. J. Mol. Biol. 1994, 244, 423−435. (37) Yesinowski, J. P.; Eckert, H. Hydrogen Environments in Calcium Phosphates: NMR at High Spinning Speed. J. Am. Chem. Soc. 1987, 109, 6274−6282. (38) Hinedi, Z. R.; Goldberg, S.; Chang, A. C.; Yesinowski, J. P. A 31P and 1H MAS NMR Study of Phosphate Sorption onto Calcium Carbonate. J. Colloid Interface Sci. 1992, 152, 141−160. (39) Miquel, J. L.; Facchini, L.; Legrand, A. P.; Rey, C.; Lemaitre, J. Solid State NMR to Study Calcium Phosphate Ceramics. Colloids Surf. 1990, 45, 427−433. (40) Jarlbring, M.; Sandström, D. E.; Antzutkin, O. N.; Forsling, W. Characterization of Active Phosphorus Surface Sites at Synthetic Carbonate-Free Fluoroapatite Using Single Pulse 1H, 31P and 31P CP MAS NMR. Langmuir 2006, 22, 4787−4792. (41) Kolmas, J.; Kolodziejski, W. Concentration of Hydroxyl Groups in Dental Apatites: A Solid-State 1H MAS NMR Study Using Inverse 31P→ 1H Cross-Polarization. Chem. Commun. 2007, 4390−4392. (42) Pourpoint, F.; Gervais, C.; Bonhomme-Coury, L.; Azais, T.; Coelho, C.; Mauri, F.; Alonso, B.; Babonneau, F.; Bonhomme, C. Calcium Phosphates and Hydroxyapatite: Solid State NMR Experiments and First Principles Calculations. Appl. Magn. Reson. 2007, 32, 435−457. (43) Laurencin, D.; Wong, A.; Dupree, R.; Smith, M. E. Natural Abundance 43Ca Solid-State NMR Characterisation of Hydroxyapatite: Identification of the Two Calcium Sites. Magn. Reson. Chem. 2008, 46, 347−350. (44) Pajchel, L.; Kolodziejski, W. Solid-State Mas NMR, TEM, and TGA Studies of Structural Hydroxyl Groups and Water in Nanocrystalline Apatites Prepared by Dry Milling. J. Nanopart. Res. 2013, 15 (1868), 1−15. (45) Isobe, T.; Nakamura, S.; Nemoto, R.; Senna, M.; Sfihi, H. SolidState Double Nuclear Magnetic Resonance Study of the Local Structure of Calcium Phosphate Nanoparticles Synthesized by a WetMechanochemical Reaction. J. Phys. Chem. B 2002, 106, 5169−5176. (46) Wang, Y.; et al. Water-Mediated Structuring of Bone Apatite. Nat. Mater. 2013, 12, 1144−1153. (47) Mason, H. E.; Kozlowski, A.; Phillips, B. L. Solid-State NMR Study of the Role of H and Na in AB-Type Carbonate Hydroxylapatite. Chem. Mater. 2008, 20, 294−302. (48) Turki, T.; Aissa, A.; Goze Bac, C.; Rachdi, F.; Debbabi, M. Study of Mixed Ca−Zn Hydroxyapatite Surface Modified by Lactic Acid. Appl. Surf. Sci. 2012, 258, 6759−6764. (49) Tseng, Y. H.; Mou, C. Y.; Chan, J. C. C. 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, 6909−6918. (50) Kaflak-Hachulska, A.; Samoson, A.; Kolodziejski, W. 1H MAS and 1H → 31P CP/MAS NMR Study of Human Bone Mineral. Calcif. Tissue Int. 2003, 73, 476−186. (51) Cho, G.; Wu, Y.; Ackerman, J. L. Detection of Hydroxyl Ions in Bone Mineral by Solid-State NMR Spectroscopy. Science 2003, 300, 1123−1127. L


Article

The Journal of Physical Chemistry C (52) Sandstrom, D. E.; Jarlbring, M.; Antzutkin, O. N.; Forsling, W. A Spectroscopic Study of Calcium Surface Sites and Adsorbed Iron Species at Aqueous Fluorapatite by Means of 1H and 31P MAS NMR. Langmuir 2006, 22, 11060−11064. (53) Nassif, N.; Martineau, F.; Syzgantseva, O.; Gobeaux, F.; Willinger, M.; Coradin, T.; Cassaignon, S.; Azaïs, T.; Giraud-Guille, M. M. In Vivo Inspired Conditions to Synthesize Biomimetic Hydroxyapatite. Chem. Mater. 2010, 22, 3653−3663. (54) Diallo-Garcia, S.; Ben Osman, M.; Krafft, J. M.; Casale, S.; Thomas, C.; Kubo, J.; Costentin, G. Identification of Surface Basic Sites and Acid-Base Pairs of Hydroxyapatite. J. Phys. Chem. C 2014, 118, 12744−12757. (55) Ospina, C. A.; Terra, J.; Ramirez, A. J.; Farina, M.; Ellis, D. E.; Rossi, A. M. Experimental Evidence and Structural Modeling of Nonstoichiometric (0 1 0) Surfaces Coexisting in Hydroxyapatite Nano-Crystals. Colloids Surf., B 2012, 89, 15−22. (56) Massiot, D.; Fayon, F.; Capron, M.; King, I.; Le Calvé, S.; Alonso, B.; Durand, J.-O.; Bujoli, B.; Gan, Z.; Hoatson, G. Modelling One- and Two-Dimensional Solid-State NMR Spectra. Magn. Reson. Chem. 2002, 40, 70−76. (57) Gopal, R.; Calvo, C.; Ito, J.; Sabine, W. K. Crystal Structure of Synthetic Mg-Whitlockite, Ca10Mg2H2(PO4)14. Can. J. Chem. 1974, 52, 1155−1164. (58) Cheng, Z. H.; Yasukawa, A.; Kandori, K.; Ishikawa, T. FTIR Study of Adsorption of CO2 on Nonstoichiometric Calcium Hydroxyapatite. Langmuir 1998, 14, 6681−6686. (59) Cheng, Z. H.; Yasukawa, A.; Kandori, K.; Ishikawa, T. FTIR Study on Incorporation of CO2 into Calcium Hydroxyapatite. J. Chem. Soc., Faraday Trans. 1998, 94, 1501−1505. (60) Holcomb, D. W.; Young, R. A. Clinical Investigation Thermal Decomposition of Human Tooth. Calcif. Tissue Int. 1980, 31, 189− 201. (61) Wilson, R. M.; Elliott, J. C.; Dowker, S. E. P.; RodriguezLorenzo, L. M. Rietveld Refinements and Spectroscopic Studies of the Structure of Ca-Deficient Apatite. Biomaterials 2005, 26, 1317−1327. (62) Bertinetti, L.; Tampieri, A.; Landi, E.; Ducati, C.; Midgley, P. A.; Coluccia, S.; Martra, G. Surface Structure, Hydration, and Cationic Sites of Nanohydroxyapatite: UHR-TEM, IR, and Microgravimetric Studies. J. Phys. Chem. C 2007, 111, 4027−4035. (63) Cazalbou, S.; Combes, C.; Eichert, D.; Rey, C. Adaptative Physico-Chemistry of Bio-Related Calcium Phosphates. J. Mater. Chem. 2004, 14, 2148−2153. (64) Davies, E.; Duer, M. J.; Ashbrook, S. E.; Griffin, J. M. 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, 12508−12515. (65) Johnson, B. B.; Ivanov, A. V.; Antzutkin, O. N.; Forsling, W. 31P Nuclear Magnetic Resonance Study of the Adsorption of Phosphate and Phenyl Phosphates on γ-Al2O3. Langmuir 2002, 18, 1104−1111. (66) Wilson, R. M.; Elliott, J. C.; Dowker, S. E. P. Formate Incorporation in the Structure of Ca-Deficient Apatite: Rietveld Structure Refinement. J. Solid State Chem. 2003, 174, 132−140. (67) Ishikawa, T.; Teramachi, A.; Tanaka, H.; Yasukawa, A.; Kandori, K. Fourier Transform Infrared Spectroscopy Study of Deuteration of Calcium Hydroxyapatite Particles. Langmuir 2000, 16, 10221−10226. (68) Tanaka, H.; Watanabe, T.; Chikazawa, M. FTIR and TPD Studies on the Adsorption of Pyridine, N-Butylamine and Acetic Acid on Calcium Hydroxyapatite. J. Chem. Soc., Faraday Trans. 1997, 93, 4377−4381. (69) Yashima, M.; Yonehara, Y.; Fujimori, H. Experimental Visualisation of Chemical Bonding and Structural Disorder in Hydroxypatite through Charge and Nuclear Density Analysis. J. Phys. Chem. C 2011, 115, 25077−2508710.1021/jp208746y. (70) Hitmi, N.; Lacabanne, C.; Young, R. A. OH- Dipole Reorientability in Hydroxyapatite: Effect of Tunnel Size. J. Phys. Chem. Solids 1986, 47, 533−546.

(71) Nakamura, S.; Takeda, H.; Yamashita, K. Proton Transport Polarization and Depolarization of Hydroxyapatite Ceramics. J. Appl. Phys. 2001, 89, 5386. (72) Tanaka, Y.; Iwasaki, T.; Nakamura, M.; Nagai, A.; Katayama, K.; Yamashita, K. Polarization and Microstructural Effects of Ceramics Hydroxyapatite Electrets. J. Appl. Phys. 2010, 107, 014107−014110. (73) Nebel, H.; Neumann, M.; Mayer, C.; Epple, M. On the Structure of Amorphous Calcium Carbonate - a Detailed Study by Solid-State NMR Spectroscopy. Inorg. Chem. 2008, 47, 7874−7879.

M


Discrimination of Surface and Bulk Structure of Crystalline

Recommend Documents