Halide-Dependent Dissolution of Dicalcium Phosphate Dihydrate and

Article pubs.acs.org/crystal

Halide-Dependent Dissolution of Dicalcium Phosphate Dihydrate and Its Modulation by an Organic Ligand Lihong Qin,† Lijun Wang,*,† Christine V. Putnis,‡,§ and Andrew Putnis‡,∥ †

College of Resources and Environment, Huazhong Agricultural University, Wuhan 430070, China Institut für Mineralogie, University of Münster, 48149 Münster, Germany § Department of Chemistry, Curtin University, Perth, Western Australia 6845, Australia ∥ The Institute for Geoscience Research (TIGeR), Curtin University, Perth, Western Australia 6845, Australia ‡

S Supporting Information *

ABSTRACT: In situ atomic force microscopy (AFM) combined with X-ray photoelectron spectroscopy (XPS) and ζ potential were used to investigate how citrate (50 μM) modified the nanoscale dissolution of brushite (dicalcium phosphate dihydrate, CaHPO4·2H2O) by NaX (X = Cl, Br, or I) at a constant pH of 7.0. Results showed that on the brushite (010) surface, halide ions with large sizes (such as I−) enhanced adsorption of Na+ that cannot be desorbed by water flow, inhibiting the retreat rates of [1̅00]Cc steps. The introduction of 50 μM citrate resulted in desorption of Na+ ions and caused the disappearance of specific salt effects on the dissolution of the brushite (010) face. With further increasing salt concentrations up to 100 mM, pit deepening was initiated, and it could possibly be attributed to hydrated Na+ ions at the negatively charged surface that orient the interfacial water so as to increase the entropy of the interfacial system, and hence the dissolution rate. Following the addition of 50 μM citrate to 100 mM salt solutions, deep pits immediately disappeared, suggesting that citrate covers the brushite (010) surface to form a protective film to decrease the number of active sites of dissolution reactions on the brushite surface. The findings improve fundamental understanding of biomineral interfacial dissolution, with clinical implications of bone demineralization and resorption as well as prevention of osteoporosis.

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INTRODUCTION In addition to amorphous calcium phosphate (ACP), HPO42−enriched phases were detected as the bone precursor phases in vivo,1,2 and brushite (CaHPO4·2H2O), one of the precursors of hydroxyapatite (HAP) mineralization in vitro,3−5 has been used for fabrication of biomaterials for hard tissue repair such as bone.6,7 Brushite exhibits a high resorption rate through osteoclastic action and/or demineralization.8,9 Therefore, direct observations of brushite dissolution in physiological solutions are central to understand the resorption mechanisms and bone development. The sensitivity of dissolution at the Ca−P−saline water interface has attracted significant interest due to sodium chloride (NaCl) accounting for more than 90% of the ionic strength of human body fluid and exacerbation of bone resorption induced by high salt intake.10,11 At pH > 6.0, the Ca−P surfaces are negatively charged12,13 and counterions adsorb to the interface from the solutions, causing surface-charge screening and leading to the formation of the so-called electrical double layer.14−16 Also, the presence of counterions at the charged interface is found to have an effect on the hydrogen-bond strength of water or a direct strong interaction with the surface.17 This is related to the location of ions at the interface that is critical during mineral dissolution. The dissolution kinetics of the mineral−water © XXXX American Chemical Society

interface is determined by the hydration of the constituent ions of the crystal and hence to the rearrangement of water molecules around these ions as well as the interaction between the solvent molecules.18−20 Adsorbed cations at a negatively charged interface are identified as inner-sphere (IS) and outer-sphere (OS) complexes or both.21−26 Recent AFM results provide a direct and atomic-level image of cations adsorbed preferentially at certain locations of the solid−water interface or at some distance from the surface, depending on their hydration.15,27,28 Compared to cations, halide anions are generally known to have more significant effects on the interface.29−35 Flores et al.36 showed less exclusion of the more weakly hydrated halide anions from the negatively charged hydrophobic or hydrophilic solid surface. Azam et al.37 observed that the larger halide anions exhibit a cooperativity with cations to promote deprotonation among the more acidic silanol groups at negatively charged interfaces. Therefore, it is of great interest to investigate how halide-induced counterions (Na+) influence the dissolution at negatively charged brushite interfaces. Received: April 5, 2017 Revised: May 15, 2017 Published: May 30, 2017 A

DOI: 10.1021/acs.cgd.7b00488 Cryst. Growth Des. XXXX, XXX, XXX−XXX

Crystal Growth & Design

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Figure 1. Time sequence of AFM deflection images showing the dissolution of triangular etch pits along the [1̅00]Cc, [101̅]Cc, and [101]Cc step directions on the brushite (010) face after exposure to (A) 7 mM sodium halides or (B) 50 mM sodium halides. Images A and B, 6 × 6 μm2. edge morphology and measured velocities. Prior to injection of reaction solutions, water (pH 7.0) was passed over the plate-like brushite (010) cleavage surface,42 which was used to establish the crystallographic orientation.42 Then, NaX solutions (X = Cl, Br, or I) (1−100 mM, pH 7.0) in the absence and presence of 50 μM citrate were passed through the fluid cell for 1−2 h, and all experiments were conducted under a constant flow rate (1 mL/min) to ensure surfacecontrolled reaction rather than diffusion control.41 Different locations of three different crystals per solution condition were imaged to ensure reproducibility of the results. X-ray Photoelectron Spectroscopy. X-ray photoelectron spectroscopy (XPS) is a surface sensitive technique that gives quantitative chemical analysis of surfaces (to a depth of about 10 nm).43 The brushite crystal samples after exposure to the reaction solutions for 1 day were rinsed with water (pH 7.0) and dried under vacuum for at least 8 h. Sealed tubes for all samples44 were used to minimize surface contamination prior to the XPS determinations. The samples were then placed on an aluminum (Al) platform for XPS measurements (VG multilab 2000 equipment, ThermoVG scientific, East Grinstead, West Sussex, U.K.) using the Al Kα X-ray line of 1486.6 eV excitation energy at 300 W. To correct for sample charging, we used highresolution spectra as a reference by setting the C 1s hydrocarbon peak to 284.6 eV. The background was linearly subtracted. The quantitative analyses of Na 1s, Cl 2p, Br 3d, I 3d, and P 2p spectra were performed by considering the atomic sensitivity factors (ASFs) and the transmission function of the electron analyzer,45,46 yielding ASF values of 10.59, 2.74, 2.73, 42.42, and 1.35, respectively. For comparisons among different samples of brushite crystals, the normalized ion concentration, c/c0 (%), where c is the average adsorbed ion and c0 is the concentration of P in molecule CaHPO4· 2H2O of the brushite (010) face treated with 7−100 mM NaX in the absence and presence of 50 μM citrate at pH 7.0. XPS experiments were repeated three times to ensure the reproducibility of results. ζ Potential Measurements. The ζ potential was measured with a Zetasizer Nano ZS90 instrument (Malvern, Worcestershire, U.K.). Samples were prepared by adding 0.15 μg of brushite seed crystals to 3 mL of a saturated solution (0.45 mM) with respect to brushite.47 Samples containing NaX (0−100 mM, pH 7.0) in the absence and presence of 50 μM citrate were stirred for 1 h prior to the measurement to allow sufficient time for adsorption of ions on brushite crystal surfaces.48 Each solution was transferred to a DTS 1070 cell (1.0 mL) with a palladium electrode. All ζ measurements were performed at room temperature.

In addition to background electrolytes, citrate comprises 1−2 wt % of bone and is identified to be essential for imparting the stability, strength, and resistance to fracture of bone.38−40 However, whether citrate intervenes in specific salt effects on bone dissolution remains unclear. To explore the halideinduced counterions (Na+ ions) effects on the dissolution of brushite and its modulation by citrate, we systematically observed real-time nanoscale dissolution occurring at the negatively charged brushite surface after exposure to aqueous solutions containing NaX (X = Cl, Br, or I) (1−100 mM, pH 7.0) in the absence and presence of 50 μM citrate. The results reveal that either halide-dependent interfacial counterions of dehydrated Na+ ions are retained at the interface or hydrated Na+ ions are easily removed from the surface. The two counterions have different roles in brushite dissolution, and their roles can be weakened by citrate. The findings observed here may improve fundamental understanding of interfacial demineralization and resorption of bone and biomimetic bone materials in physiological fluids, with clinical implications for the prevention of osteoporosis.

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EXPERIMENTAL SECTION

Brushite Crystal Synthesis. Brushite single crystals were synthesized by a gel method.41 The harvested crystals were rinsed with deionized water and ethanol and characterized by X-ray diffraction (Bruker D8, Billerica, MA, USA) to identify them as a single crystal phase. In Situ AFM of Brushite Dissolution. Synthetic brushite crystals were used for in situ AFM surface dissolution experiments. Reaction solutions were prepared from high-purity solids ((Sigma-Aldrich, St. Louis, MO, USA)) dissolved in ultrahigh-purity water (18 MΩ·cm, pH 5.8) from a two-step purification treatment including doubly distilled (YaR, SZ-93, Shanghai, China) and deionized (Milli-Q, Billerica, MA, USA) treatments. The pH values of all reaction solutions were adjusted to 7.0 by the addition of 0.01 M NaOH. All experiments were performed under ambient conditions (22 ± 1 °C and partial pressure CO2 ∼ 10−3.5 atm.). In situ dissolution experiments were performed in contact mode using an Agilent 5500 AFM (Phoenix, AZ, USA). The AFM images were collected using Si3N4 tips (Nanosensor pointprobe plus contact with a force constant of 0.2 N/m) with scan rates of 3−5 Hz and an average scan time of 75 s. Minimizing tip−surface force interactions during the flow-through of solutions reduced artifact effects on step B



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Figure 2. Time sequence of AFM deflection images showing the dissolution of triangular etch pits on the brushite (010) face after exposure to (A, B) water, (C, D) 100 mM sodium halides, and (E) water (pH 7.0). (F) Deepening velocities of triangular etch pits in water or 100 mM sodium halide solutions in the absence and presence of 50 μM citrate at pH 7.0. Note deep pits occurred until the concentration of sodium halides reached 100 mM. Images A−E, 5.5 × 5.5 μm2.

Figure 3. Evolution of the [1̅00]Cc step retreat velocities on the brushite (010) surface in the order of exposure to (A) 1.0 mM NaX, 7.0 mM NaX, H2O, 7.0 mM NaX in the presence of 50 μM citrate, and H2O and (B) 50 mM NaX, 100 mM NaX, H2O, 100 mM NaX in the presence of 50 μM citrate, and H2O. The horizontal line and two dashed lines in A and B indicate the retreat rate range in water (black) or 50 μM citrate (red) at pH 7.0.

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RESULTS AND DISCUSSION Specific Ion Effects on the Brushite (010) Surface Dissolution in the Absence and Presence of Citrate. a. Deepening Velocity of Etch Pits. Typical shallow (one unit cell, about 0.76 nm41) etch pits with step edges normal to the [1̅00]Cc, [101̅]Cc, and [101]Cc directions on the brushite (010) surface were immediately formed upon dissolution in lowconcentration salt solutions (≤50 mM, NaX, X = Cl, Br, or I) (Figure 1A,B) or in water (Figure 2A,B) at pH 7.0. When the NaX concentration was increased to 100 mM at a constant pH of 7.0, deep etch pits formed (Figure 2C) and developed (Figure 2D). The deepening rate in the presence of NaCl, NaBr, or NaI solutions (100 mM, pH 7.0) was 3.4 ± 0.5 (n = 3), 3.5 ± 0.6 (n = 3), or 4.3 ± 0.3 nm/min (n = 3), respectively (Figure 2F). Upon injection of water (pH 7.0) to replace NaX, the pit deepening velocity recovered to 0.4 ± 0.3 nm/min (n = 3) (Figure 2F), with the formation of shallow pits with flat bases (Figure 2E). However, on further addition of a solution of 100 mM NaX together with 50 μM citrate (pH 7.0), the deepening velocity remained at 0.3 ± 0.2 nm/min (n = 3) (Figure 2F and Supporting Information Figure S1). It is

noteworthy that the shape of the dissolution pits did not change and atomic steps were maintained at about 7.7 Å deep that exactly matches the (010) interlayer distance of brushite41 in NaX solutions in the absence and presence of 50 μM citrate (Figures 1, 2, and S2), suggesting that NaX and/or citrate does not change the surface crystal structure of the brushite (010) face. b. Step Retreat Velocity of Etch Pits. The [1̅00]Cc step retreat rates in water (pH 7.0) and in 50 μM citrate (pH 7.0) were measured as 4.7 ± 0.4 (n = 10, the number of crystals which were imaged) and 4.0 ± 0.2 (n = 3) nm/s, respectively (Figure 3). The presence of 1.0 or 7.0 mM NaCl (pH 7.0) increased the step retreat rates to 5.2 ± 0.2 (n = 3) and 5.9 ± 0.2 nm/s (n = 3), respectively (Figure 3A). However, in the presence of 7.0 mM solutions of NaBr or NaI, the step retreat rates decreased to 3.9 ± 0.2 (n = 3) and 3.4 ± 0.1 nm/s (n = 3). For 1.0 mM solutions, the retreat rates remained at 4.8 ± 0.2 (n = 3) and 4.1 ± 0.2 nm/s (n = 3) (Figure 3A). Following a thorough flow of pure water for about 25 min (pH 7.0), step retreat rates in water that replaced NaBr or NaI (7.0 mM, pH 7.0) remained almost unchanged, whereas the step retreat rates in water to replace NaCl rapidly recovered to 4.5 ± 0.2 nm/s (n C



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Figure 4. Step retreat rates of etch pits along the [101̅]Cc and [101]Cc directions in NaX solutions in the absence and presence of 50 μM citrate at pH 7.0. The horizontal line and two dashed lines in A−D indicate the retreat rate range in water (black) or 50 μM citrate (red) at pH 7.0.

Figure 5. Representative XPS spectra of (A) Na+ and (B) Br− adsorbed on brushite after exposure to NaX in the absence and presence of 50 μM citrate at pH 7.0. According to XPS measurements, ion concentrations adsorbed on the brushite (010) face treated with (C) 7 mM and (D) 100 mM NaX in the absence and presence of 50 μM citrate at pH 7.0.

with the 50 μM citrate (pH 7.0), the step retreat velocities along the [1̅00]Cc direction recovered to 4.9 ± 0.2 (n = 3), 4.8 ± 0.2 (n = 3), or 4.6 ± 0.1 nm/s (n = 3), respectively (Figure 3A). With further increasing NaCl, NaBr, or NaI concentrations (50−100 mM, pH 7.0), the step retreat maintained velocities of

= 3) (Figure 3A). Surprisingly, when 50 μM citrate (pH 7.0) was introduced into NaCl, NaBr, or NaI solutions (7.0 mM, pH 7.0), the step retreat rates increased in each case to 5.7 ± 0.2 (n = 3), 5.5 ± 0.2 (n = 3), and 5.5 ± 0.2 nm/s (n = 3), respectively (Figure 3A). Repeatedly, following addition of water (pH 7.0) to replace the 7.0 mM NaCl, NaBr, or NaI solutions together D



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6.3 ± 0.2 (n = 3), 3.2 ± 0.2 (n = 3), and 4.1 ± 0.3 nm/s (n = 3), respectively (Figure 3B). Upon input of water (pH 7.0) to replace NaCl solutions (100 mM, pH 7.0), the step retreat rate along the [10̅ 0]Cc direction decreased to 4.1 ± 0.2 nm/s (n = 3) (Figure 3B), whereas using water to replace NaBr or NaI solutions (100 mM, pH 7.0), the step retreat rates were rapidly lowered to 2.4 ± 0.2 (n = 3) and 2.0 ± 0.2 nm/s (n = 3), respectively (Figure 3B). Moreover, using solutions of 50 μM citrate with 100 mM NaCl or NaBr (pH 7.0) to replace water, the step retreat velocities appeared to be 7.9 ± 0.2 (n = 3), 8 ± 0.2 nm/s (n = 3), respectively; whereas using solutions of 50 μM citrate with 100 mM NaI (pH 7.0) to replace water, the step spreading rate changed only slightly to 2.8 ± 0.2 nm/s (n = 3) (Figure 3B). Furthermore, the step spreading rates recovered to 4.4 ± 0.2 nm/s (n = 3) by replacing NaCl or NaBr using water (pH 7.0), whereas the step spreading rate was still maintained at 2.7 ± 0.3 nm/s (n = 3) by replacing NaI with water (pH 7.0) (Figure 3B). For both the [101̅]Cc and [101]Cc steps, the retreat rates were not obviously changed in the presence of all salts in the absence and presence of 50 μM citrate, compared to that in water or in 50 μM citrate solutions (Figure 4). Ion Adsorption in the Absence and Presence of Citrate. Using XPS (Figures 5A,B, S3, and S4), we measured adsorbed ion concentrations on the brushite (010) face treated with 7.0 mM NaCl, NaBr, or NaI (pH 7.0). The adsorbed Na+ concentration was 0, 5.5 ± 0.6%, or 6.9 ± 0.8%, respectively, whereas Cl−, Br−, or I− concentration was 0, 2.8 ± 1%, or 3.8 ± 1%, respectively (Figure 5C). Following addition of 50 μM citrate (pH 7.0) into 7.0 mM NaCl, NaBr, or NaI solutions (pH 7.0), no adsorbed cations and anions on the brushite surface were detected (Figure 5C). When the concentration of NaCl, NaBr, or NaI was increased to 100 mM (pH 7.0), the adsorbed Na+ level increased to 3.0 ± 1.5%, 12.8 ± 0.8%, or 15.1 ± 1.0%, respectively, and the Cl − , Br − , and I − concentrations increased to 0.6 ± 0.6%, 7.0 ± 1%, and 8.4 ± 1.0%, respectively (Figure 5D). With the addition of 50 μM citrate (pH 7.0) to 100 mM NaCl or NaBr (pH 7.0), the adsorbed Na+ concentration was decreased to about 2.2%, and Cl− and Br− anions were absent (Figure 5D). For 100 mM NaI solutions (pH 7.0) in the presence of 50 μM citrate, the concentrations of adsorbed Na+ and I− decreased to 6.6 ± 0.5% and 2.0 ± 1% (Figure 5D). Specific Ion Effects on ζ Potential in the Absence and Presence of Citrate. The ζ potential in a saturated brushite solution (pH 7.0) in the absence (as the control) and presence of 50 μM citrate (pH 7.0) was −22 ± 0.5 mV (Figure 6A) and −26.5 ± 0.5 mV (Figure 6B), respectively. After addition of NaX to the control solution, ζ increased with increasing of the concentration of NaCl, NaBr, or NaI (pH 7.0) from 0.5 to 20 mM, reaching a maximum of −29 ± 0.7, −32 ± 0.7, or −34 ± 0.7 mV, respectively (Figure 6A). When the concentrations of NaCl, NaBr, or NaI solutions were increased to 100 mM (pH 7.0), ζ decreased to −22 ± 1.0 mV (Figure 6A). After 50 μM citrate was introduced into NaX at 7 or 20 mM (pH 7.0), ζ tended to be constant at −29 ± 0.6 or −35 ± 1.0 mV, respectively (Figure 6B), whereas on addition of 50 μM citrate (pH 7.0) to 100 mM NaX (pH 7.0), no obvious changes in ζ were observed (Figure 6B) compared to the control. Figure 7A schematically shows an exponential decay in counterion (Na+) concentrations with increasing distance from the charged mineral surface beyond the diffuse double layer (>LD16,48), reaching the concentration equal to that in the bulk

Figure 6. ζ potential at brushite interfaces with exposure to (A) 0−100 mM sodium halide solutions (pH 7.0) and (B) 7, 20, or 100 mM sodium halide solutions in the presence of 50 μM citrate (pH 7.0).

solutions. With the brushite surfaces exposed to NaX (pH 7.0), the Na+ concentrations were greatest near the negatively charged surfaces,12,13 and they reside within regions defined as an inner Helmholtz plane ii (or Stern layer)16,48 (Figure 7A) and an outer Helmholtz plane iii, which is shifted to further distances from the crystal surface due to the hydrated shell surrounding the adsorbed Na+ ions (Figure 7A). A common assumption is that surface potential, ψ0, is approximately equal to ζ potential that is measured at the plane of shear iv48 (Figure 7A). Citrate Weakening Halide-Dependent Counterion (Na+) Effect on Step Spreading Velocities. The step spreading velocity of etch pits on the brushite (010) surface increased with the increase of NaCl concentrations (1−7 mM, pH 7.0), whereas it was inhibited with increasing NaBr or NaI concentrations (1−7 mM, pH 7.0). This suppression cannot be recovered after water injection over the brushite surface (Figure 3A). In the presence of NaCl, the increase of dissolution rates has been traditionally attributed to the increase of crystal solubility through the strong long-range electric fields emanating from the ions of the background electrolyte to screen the charges of the hydrated ions building the crystal, thereby shifting the chemical equilibrium.19 However, the dissolution inhibition correlates with the change of brushite surface properties after the introduction of NaBr or NaI. XPS results in Figure 5C demonstrate the presence of obvious concentration differences between Na+ and halide anions ([Na+]/[X−, Br−, or I−] ≈ 2). Another important phenomenon in Figure 5C is a strongly halide-dependent Na+ concentration adsorbed on the brushite surface, which increases in the order NaCl < NaBr < NaI. This is a typical order of the Hofmeister series where halide anions are known to have different properties at the interface.49 Thus, the inhibited step spreading E



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Figure 7. (A) Schematic illustration of a general trend of electrostatic potential decay as a function of distance from a negatively charged brushite crystal surface. The distribution of counterions (Na+) is governed by the Boltzmann equation that predicts a higher concentration of counterions within the diffuse double layer that decays to the concentration of the bulk solution (>LD, the length over which the electric field extends into the bulk solution from the surface).16,48 The double layer (both Stern and diffuse layers) consists of distinct regions including (i−iv) surface potential, Helmholtz potential (inner), Helmholtz potential (outer), and ζ potential at the shear plane.16,48 (B) Schematic of the halide-induced Na+ distribution and its modulation by citrate at the negatively charged brushite−solution interface. During an electrostatic screening process, the deprotonation of -OH groups of the brushite surface is highlighted by red circles.

rates presumably occur because of the contribution of I−- or Br−-enhanced Na+ adsorption on the brushite (010) surface. The adsorption cannot be removed by water flow. As the larger halide anions (I− or Br−) move across the interface, they can progressively shift their charges toward the area that remains hydrated due to the larger polarity, thereby allowing them to reduce the free energy cost.50,51 In addition, the larger I− or Br− anions exhibit a lower electronic charge density and weaker hydration and can therefore be less easily excluded from the negatively charged interface.36 The layer of larger halide anions at the brushite interface will favor the interactions between the negatively charged solid surface and Na+ cations37 (Figure 7B). Beyond specific ion effects on brushite dissolution, the addition of citrate to solutions containing NaCl, NaBr, or NaI (7.0 mM, pH 7.0) results in the absence of significant changes in step retreat rates (Figure 3A). This combined with observations of no adsorbed ions retained at brushite surfaces in the presence of 50 μM citrate and NaX (7.0 mM, pH 7.0) (Figure 5C) suggests that citrate governs the ion distribution at

the brushite interface by “expelling” or “ejecting” halidedependent adsorbed Na+ ions. After further increasing NaX concentrations to 100 mM, a stronger inhibition in step retreat rates appeared upon injecting water for the NaI treatment (Figure 3B), which led to the inability of citrate to remove all adsorbed Na+ on the brushite surface (Figure 5D), consistent with a stronger I−-enhanced Na+ adsorption (Figure 5D). In addition, the local pH changes resulting from the adsorption of citrate (50 μM, pH 7.0) at the brushite−solution interface do not influence the result because the changes in the dissolution features appear to be statistically insignificant when a brushite (010) face is exposed to water in a pH range (6.0−8.0).52 Citrate Weakening Halide-Dependent Counterion (Na+) Effect on Deepening Velocity of Etch Pits. With increasing the NaX concentrations to 100 mM (pH 7.0), the dissolution on the brushite (010) surface mainly proceeded by deepening of etch pits (Figure 2C,D). It should be noted that the ζ potential at the interface increased with the NaX concentrations ranging from 0.5 to 20 mM, approaching a F



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occurred after 3 min of the addition of 100 mM MgCl2 (pH 7.0) (Figure 8A,A′), whereas the addition of 50 μM citrate to

maximum at 20 mM (Figure 6A), in good agreement with an enhanced deprotonation of −OH groups of the brushite surface as electrostatic screening28,53−55 increases (Figure 7B). The maximum of negative ζ potential follows the order NaCl < NaBr < NaI (Figure 6A). This may be attributed to larger halide anions present at the interface to induce a stronger deprotonation by a synergistic effect between Na+ and halide anions (Figure 7B). When the NaX concentrations increased to 100 mM, the surface charge greatly decreased and the halidedependent effect disappeared (Figure 6A), leading to a large amount of counterions (Na+) that could accumulate at the shear plane iv (Figure 7B). Meanwhile, the immediate disappearance of deepening pits upon injecting water to replace 100 mM NaX (Figure 2E,F) suggests that these interfacial hydrated Na+ ions are easily removed by water flow, compared to dehydrated Na+ ions bound tightly to the surface that inhibit the step retreat rate (Figures 3, 5, and 7B). This may suggest that hydrated Na+ ions attracted to the negatively charged brushite surface perturb the interfacial solvent from its initial structure56 and reorient the interfacial water so as to increase the entropy of the interfacial system,56 and hence the dissolution rate. As a result, enhanced deepening velocity is observed only at a higher salt level. It is presumably attributed to interfacial water with a high active structural orientation resulting from hydrated Na+ near the negatively charged brushite surface. Also, the interfacial water is prone to be disrupted by the addition of a higher concentration of Na+ (≥100 mM) revealed by in situ vibrational sum frequency generation spectroscopy,17,57,58 validating a hypothesis that mineral dissolution in salt water is enhanced due to the changes of the interfacial solvent structure.59,60 The response of the molecular arrangement of the interfacial solvent to the presence of Na+ cations is pH-dependent with the highest sensitivity at neutral pH,56 relevant to biological environments. Therefore, we just performed all in situ observations at constant pH of 7.0. Furthermore, a higher deepening velocity induced by NaI (100 mM, pH 7.0) is presumably attributed to a higher activity of interfacial water due to a greater Na+ concentration at the interface, which is required to balance the more negatively charged surface (Figure 7B). Interestingly, no deep pits were observed after the addition of 50 μM citrate (pH 7.0) to 100 mM NaX (pH 7.0) (Figure S1). This cannot be attributed to the substantial decrease of hydrated Na+ ions observed on the negatively charged surface with increasing NaX concentrations up to 100 mM in the presence of 50 μM citrate (Figures 6A,B and 7B). The most likely explanation is that citrate weakens the adsorption of the interfacial water layer through preferential adsorption directly onto the crystal surface to form a protective film that decreases the number of active sites available for dissolution reactions on the brushite surface. Zobel et al. have shown that polar and nonpolar solvents universally restructure around mineral particles, and hence the surface reactivity of solvated particles will be modified from a solvation shell of the particles itself.61 Moreover, recent DFT simulation results indicate that it is impossible to form the citrate−calcium phosphate complex at pH 7.0.52 To confirm this hypothesis that enhanced brushite dissolution with the formation of deep pits is caused by orienting water molecules by interfacial hydrated Na+ (≥100 mM), we introduced a strongly hydrated cation, Mg2+, that more strongly orients water at the interface.17,62,63 Expectedly, rough surfaces with a high density of deep pits immediately

Figure 8. Pairs of AFM deflection images of the brushite (010) surfaces after 3 min of injecting (A, A′) 100 mM MgCl2, (B, B′) 100 mM MgCl2 in the presence of 50 μM citrate, and (C, C′) 100 mM MgCl2 in the presence of 50 μM aspartate (Asp) at pH 7.0. Images A− C and A′−C′, 5.5 × 5.5 μm2.

100 mM MgCl2 (pH 7.0) resulted in the disappearance of deep pits with a low density of shallow etch pits (Figure 8B,B′). This phenomenon should occur after addition of similar organic molecules with additional positive charge, for example, aspartate having the -NH3+ group at neutral pH. It was observed that 50 μM aspartate (pH 7.0) exhibited a greater ability to hinder the attack of interfacial water with high activity generated by the presence of Mg2+ (Figure 8C,C′). This may be due to the less negatively charged aspartate at pH 7.0 that is favorable for a negatively charged interface.64,65

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CONCLUSIONS Halide ions with large sizes (such as I−) enhance adsorption of Na+ on the brushite (010) surface and cannot be desorbed by water flow, inhibiting the retreat rates of [1̅00]Cc steps during dissolution. The introduction of 50 μM citrate results in desorption of Na+ ions and causes the disappearance of specific salt effects on dissolution of the brushite (010) face. With further increasing salt concentrations up to 100 mM, etch pit deepening is initiated, and it is presumably attributed to G



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hydrated Na+ ions at the negatively charged surface, able to orient the interfacial water so as to increase the entropy of the interfacial system, and hence the total dissolution rate. Following the addition of 50 μM citrate to 100 mM salt solutions, deep pits immediately disappear, suggesting that citrate inhibits dissolution by covering the brushite (010) surface to form a protective film that effectively decreases the number of active sites for dissolution reactions on the brushite surface. The findings improve fundamental understanding of mineral dissolution in the presence of salt solutions, as well as possible interfacial bone demineralization and resorption, the latter providing potential clinical implications for the prevention of osteoporosis.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.cgd.7b00488. Brushite dissolution in the presence of 100 mM (Figure S1) or 1 mM NaX (Figure S2) with 50 μM citrate at pH = 7.0; XPS of Na 1s, Cl 2p, Br 3d, and I 3d adsorbed on brushite (Figures S3 and S4) (PDF)

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AUTHOR INFORMATION

Corresponding Author

* E-mail: [email protected]. Phone/Fax: +86-27-87288382. ORCID

Lijun Wang: 0000-0001-7125-9480 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by the National Natural Science Foundation of China (Grants 41471245 and 41071208) and the Fundamental Research Funds for the Central Universities (Grant 2662015PY206). C.V.P. and A.P. acknowledge funding through the EU Seventh Framework Marie S. Curie ITNs: Minsc; CO2 React; and Flowtrans.

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Halide-Dependent Dissolution of Dicalcium Phosphate Dihydrate and

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