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Surface Modification of Nano-Hydroxyapatite Using Bisphosphonate Moieties: Effect on Morphology and Crystalline Nature at Higher Temperature.


A large number of clinical methods are used for the replacement or repair of tissues in the human body that have been damaged through disease or injury. Therapies available currently like autografts, allografts or xenografts are based on replacement of the damaged tissue using donor graft tissues that pose numerous problems mainly related to shortage of donors or donor sites, volume of donor tissues, donor site pain and morbidity, rejection of grafts by human immune system and transmission of diseases [1]. To avoid the risks in grafting, tissue engineering provides effective alternative based on its fundamental principal of regenerating damaged tissues instead of replacing them. The scientific research in this field is therefore focused on developing biological substitutes like scaffolds which serves as a framework to support the cell migration into the defect from the surrounding tissues and provides a suitable substrate for cell attachment, cell proliferation, differentiated function and cell migration [1,2].

They can also be used to achieve drug delivery with high loading and efficiency [3]. They can be fabricated using natural polymers such as alginate, proteins, collagens, gelatin, fibrins, and albumin or biodegradable synthetic polymers such as polyvinyl alcohol, Poly (glycolic acid), Poly (lactic acid) then copolymers poly (p-dioxane), poly(caprolactone) polyurethanes and polyorthoesters. But for the synthesis of scaffold, biocompatibility, biodegradability and mechanical strength are important parameters to be considered. Addition of an osteoconductive component i.e. biomaterial is one of the important methods for the fabrication of biodegradable scaffolds with higher mechanical strength and improved biocompatibility.

Hydroxyapatite, bioglass, apatite, calcium phosphate etc. are some of the biomaterials that are widely used for the synthesis of scaffolds. Out of these materials, hydroxyapatite (HA) provides excellent mechanical properties and osteoconductivity to the scaffold. It is one of the most biocompatible, bioactive ceramics because of its significant chemical and physical resemblance to the mineral constituents of human bones and teeth [4]. HA is widely used as powders or in particulate forms in various bone repairs and as coatings for metallic prostheses to improve their biological properties [5, 6]. Thermodynamically, it is the most stable calcium phosphate ceramic compound nearest to the pH, temperature and composition of the physiological fluid [7]. It has an exact stoichiometric Ca/P ratio of 1.67 and is chemically very similar to the mineralized human bone. Due to the chemical similarity between HA and mineralized bone of human tissue, synthetic HA exhibits strong affinity to host hard tissues [8]. Due to its wide application in human body a due attention is required to synthesize well characterized hydroxyapatite with comparative standards of bone. Many methods have been reported to synthesize nano-hydroxyapatite like hydrothermal [9], mechanochemical [10] and sol-gel [5] etc. Among which sol gel technique is simple, cheap and suitable technique for bulk preparation, which make it promising for commercialization [5]. However, HA is difficult to shape in the specific form required for bone repair and implantation because of its intrinsic hardness, fragility, and lack of flexibility, which limits its use as a load-bearing implant material. Also its reactivity with human bone is low and the rate at which bone appose and integrate with HA is relatively slow i.e. the biocompatibility of the hydroxyapatite surface with bone is slow [11].

Since the surface of Hydroxyapatite consists mainly of two functional groups a"Ca-OH and a"P=OH acting as the active sites [12]. Modification on the surface of these biomaterials is an effective technique to enhance the biocompatibility rate which significantly improves and accelerate invasion of bone tissues in scaffolds [13]. Therefore the surface of hydroxyl apatite is modified with various organic substances consisting of bisphosphonate group due to its interaction between calcium or phosphate ions on the apatitic surface and the anionic groups of the organic molecule [14]. Bisphosphonate are used in treatment of a variety of bone diseases which are associated with high bone resorption, such as metastatic bone disease, paget's disease, and osteoporosis as the two phosphonate groups in its structure (P-C- P) helps in binding of calcium on hydroxyapatite [14, 15]. Several studies on the modification of hydroxyapatite by different compounds of bisphosphonate groups such alendronate [16], zoledronate [17], risedronate [18] and clodronate [19] have been reported [20]. Among these etidronate (disodium (1-hydro xyethylidene) bisphosphonic acid) is now the most widely used drugs for the treatment of osteoporosis [21]. Modified nano-hydroxyapatite may possess some special properties due to its large specific surface area and has applications in composites with organic polymers as nanocomposites prepared using these nanoparticles results in better mechanical properties but due to plate like shape and higher densification it is difficult to disperse which can be overcome by sintering/calcination at higher temperatures resulting in needle shape [14, 22, 23]

The aim of this research was to enhance the biocompatibility of the hydroxyapatite by its surface modification with bisphosphonate compound i.e. etidronic acid using precipitation technique. The modified HA was calcined at different temperatures i.e. 60, 400, 600 and 800[degrees]C to obtain modified hydroxyapatite with different crystallite sizes and morphologies. The effect of sintering on chemical, structural and morphological properties of the modified HA was studied.

Materials and Method


Calcium nitrate tetra hydrate (CaN[O.sub.3] x 4[H.sub.2]O) (AR) and Potassium dihydrogenphosphate (K[H.sub.2]P[O.sub.4]) (AR) were procured from Merck India Ltd. Liquid Ammonia 25% concentration and Etidronic acid were purchased from Rankem India and Sigma-Aldrich, respectively.

Synthesis of Nanohdroxyapatite (HA)

Hydroxyapatite was synthesized according to a well established sol gel method using Calcium nitrate and potassium dihydrogenphosphate used as calcium and phosphorus precursors, respectively. Solution of Calcium nitrate was added drop wise to a solution of potassium dihydrogenphosphate under stirring. The molar ratio of the Calcium nitrate and potassium dihydrogenphosphate was 1.67 and the pH was maintained at 10 using liquid ammonia. Gel obtained after precipitation was aged for 24 hrs and then centrifuged 3-4 times at 3000 RCF with double distilled water which was then dried overnight at 60[degrees]C in a vacuum oven.

Surface Modification and Sintering of Hydroxyapatite

The surface of the above prepared hydroxyapatite was modified using a biphosphonate compound i.e. etidronic acid. An etidronate solution of 0.1M concentration in double distilled water was used for modification as reported in literature [4]. 0.5 gm of prepared hydroxyapatite and 100ml of 0.1M etidronate solution was mixed using mechanical stirring for 48hrs at 25 [+ or -] 2[degrees]C temperature and pH was maintained using ammonia solution. Mixture so obtained was ultra centrifuged 3-4 times at 6000 RCF in double distilled water for 10 minutes to remove the unreacted etidronic acid and ammonia. The obtained composite material was dried in vacuum oven at 60[degrees]C for 24 hrs. Finally the surface modified hydroxyapatite was sintered at different temperatures 400, 600 and 800[degrees]C in electrical furnace in air with heating rate of 10[degrees]C/min to obtain different particle size. Based on sintering temperature, samples were designated as SF60, SF400, SF600 and SF800. Scheme for Surface modification and Sintering of Synthesized hydroxyapatite is shown in Figure 1.

Characterization of Unmodified, Modified and Sintered Hydroxyapatite

Fourier Transform Infrared Spectroscopy (FTIR)

The chemical structures of unmodified, modified and modified sintered hydroxyapatite were characterized by Fourier transform infrared spectroscopy (FT-IR) in Perkin Elmer RZX spectrometer using KBr technology. FTIR spectra were recorded in a spectral range of 4000-450 [cm.sup."1] with a resolution of 2 [cm.sup."1] with two scans for each sample.

X-ray diffraction

Phase analysis was performed by X-ray diffractometer (XRD) using a Philips X'Pert Pro X-ray diffractometer system. The radiation was Cu Ka ([??] = 0.15406 nm) with 40 kV voltage and 40 mA intensity. The mean crystallite size (D) of the particles was calculated from the XRD line broadening measurement using the Scherrer equation, equation(l) [24]:

D = 0.89 [lambda] / [beta] cos[theta] (1)

Where [lambda] is the wavelength (Cu-K[alpha]), [beta] is the full width at the half maximum of the HA (211) line and [theta] is the diffraction angle.

The fraction of crystalline phase ([X.sub.c]) of the HA powders was evaluated by equation, (2) [25]:

Xc = 1-[v.sub.112/300] / [I.sub.300] (2)

Where I300 is the intensity of (3 0 0) diffraction peak and [v.sub.112/300] is the intensity of the hollow between (1 1 2) and (3 0 0) diffraction peaks.

Transmission Electron Microscopy (TEM) and Scanning Electron Microscopy (SEM)

The morphology of unmodified, modified and sintered modified hydroxyapatite was examined using transmission electron microscope (TEM) and Scanning Electron Microscope (SEM). TEM was also used to determine crystallite size.

Model Hitachi-2100 was used for TEM and Images were taken at 80 kV accelerating voltage. A drop of a dilute sample in suspension was deposited on the carbon-coated grids and allowed to dry at room temperature. Particle size distribution of unmodified, modified and modified sintered hydroxyapatite in TEM images was undertaken using a UTHSCSA Image Tool image analyzer program (IT version 3). The images were loaded into the software and particle size measured using a two point measuring analysis. The scale of the software was calibrated using the scale bars on each TEM image (given below each TEM image). Approximately, 300 measurements were taken to obtain the distribution.

SEM model JSM JEOL-6100 was used. Powder of unmodified, modified and modified sintered hydroxyapatite was gold coated in order to make the surface conductive.

Dynamic light scattering (DLS)

DLS particle size measurements of unmodified, modified and sintered modified hydroxyapatite were carried out using a Horiba SZ-100 Nano Particle Size analyzer to obtain mean intensity particle sizes. Before the DLS measurements were carried out, nanoparticles were ultrastabily suspended in ethanol solution by sonicating for 2 h in order to disperse the particles within the solution. Two milliliters of the sonicated solution was then transferred into a disposable cuvette and placed inside the sample holder. Three replication were done for each sample.

Contact Angle Measurement

Contact angles of unmodified, modified and sintered modified hydroxyapatite were measured on DSA 10 Mk 2 (Kruess) equipped with a video-imaging system. Sessile deionized-water drops were placed on the surface in the ambient environment, with a drop volume of 5[micro]L. Images were recorded after every 3 minutes and 5 images every second were taken with a video system. Contact angle values were calculated using the drop shape analysis system (DSA 1) and selected at 10 s

Wavelength Dispersive X-ray Fluorescence (WDXRF)

The elementary composition and Ca/P ratio of unmodified, modified and sintered modified hydroxyapatite was determined with Wavelength Dispersive X-ray Fluorescence-S8 Tiger from Bruker (WD-XRF), Germany.

Results and Discussion

FTIR Analysis

FTIR spectra of Unmodified, surface modified sintered hydroxyapatite at various temperatures, i.e. 60, 400, 600 and 800 0C, designated as HA, SF60, SF400, SF600 and SF800, respectively are shown in Figure 2. The spectrum of unmodified HA consists characteristic peaks of [(P[O.sub.4]).sup.3-] group near wave number 1023-1047[cm.sup.-1], 961 [cm.sup.-1], 560-599 [cm.sup.-1] and 474[cm.sup.-1] . The two weak peaks near wave number 1419 [cm.sup."1] and 1455 [cm.sup."1] also confirms the presence of traces of carbonate in pure HA during the synthesis of via sol gel, calcium monophosphate and calcium dehydrates are formed which disappear during sintering. The peak near wave number 875[cm.sup.-1] belongs to [(HPO4).sup.2"] groups due to protonation of phosphate groups present in pure HA[26].

A new absorption band at 810-820 [cm.sup.-1] corresponding to i (PC- P) group is seen in all the spectra of modified HA. A peak attributing to i (P- O) group at 920-996 [cm.sup."1] is observed in modified HA samples while absorption band of i (P-O) group confirming the surface modification is seen at 1150-1160 [cm.sup."1]. The formation of these bisphosphonate groups in the modified samples confirms the reaction of etidronic acid with hydroxyapatite. The weak bands near 3000 and 3200 [cm.sup."1] are attributed to the C- H and the O- H stretching vibration mode of etidronates [20]. The formation of these band in the modified samples further indicates grafting of etidronic groups i.e. etidronates on the HA surface. The FTIR spectra further illustrates the effect of sintering of HA at higher temperatures. The new bands appeared in the modified HA at 810-820, 920996 and 1150-1160 [cm.sup."1] increased in intensity with increase in temperature from 60 to 800[degrees]C. However, the intensity of band near wave number 875 [cm.sup."1] belonging to [(HPO4).sup.2"] group, remained conserved at higher sintering temperatures [23]. It indicates that the organic moieties have not interacted by [(HPO4).sub.2"] groups, particularly the P-OH active sites, but etidronates are superficially attached with hydroxyapatite via covalent bonding[27].

XRD Analysis

The X-ray diffraction profiles of unmodified and modified Hydroxyapatite (HA) sintered at different temperatures i.e. 400, 600 and 800[degrees]C are shown in Figure 3. The XRD spectra of modified Hydroxyapatite sintered at different temperatures shows that all the samples are in structural resemblance with that of pure HA material. There is no significant phase change in HA after modification with etidronic acid. From Fig.2 it is revealed that as the sintering temperature increased from 60 to 800[degrees]C, several of the HA peaks become more distinct and narrower signifying an increase in the crystallite size and crystallinity confirming the important role of sintering. Table 1 shows value of crystallite size (CS) and crystallinity index (CI) calculated for different samples. The crystallite size and crystalline index increased tremendously for SF400, SF600 and SF800 samples. For pure HA crystallinity index is about 39% and crystallite size is about 10nm, while for the modified HA sample SF800, crystallinity index is about 90% and crystallite size about 91nm as depicted in Table 1 and also confirmed by the TEM results.

Morphological Analysis

TEM images of unmodified and modified Hydroxyapatite sintered at various temperatures are shown in figure 4(i). From TEM images it is clear that all samples possess crystalline rod like morphology. Pure HA depicts individual particles with irregular rod like shapes with broad size distribution as seen in Figure 4 (i(a)). When the HA particles are modified with etidronic acid, the particle morphology steadily changes from rod like to plate like and further to needle like as the sintering temperature increases as also confirmed by SEM. From SEM micrographs given in Figure 5 analyzed that the modification results in the agglomeration which is the most important morphological characteristic for its use as a bioactive element in tissue engineering. The structure of human bone and teeth represents similar morphology and hence such a characteristic provide a better biocompatibility. The modification of nano HA with etidronic acid further provide enhanced mechanical strength due to its high specific surface area, superior & defect free chemical structure and improved resemblance with the human bone due to its modification at micro level [14, 22]. The morphology of modified HA samples shows that the crystallite size of the nanoparticles increased from 10 to 100nm with increasing sintering temperature from 60 to 800[degrees]C. This is because etidronic acid increased the surface reactivity of the individual HA nanoparticles thus promoting the formation of layer particles which is also the reason for agglomeration. The change in morphology with sintering temperature may also be attributed to the relative specific surface energies of modified HA. Particle size obtained by image analysis software shown in Fig. 4(ii) and crystallite size estimated from XRD results are in the same order of magnitude suggesting that the particle size increased with increase in sintering temperature.

SEM images of unmodified and modified HA sintered at various temperatures i.e. 400, 600 and 800 [degrees]C are shown in Figure 5. As evidenced in Figure 5(a) simple HA possess very small particles with cylindrical shape, which changes to plate shape (Figure 5(b)) due to agglomeration thus showing that the modification promotes change in shape which increases the surface area making it more effective in bone tissue engineering [20]. With increase in sintering temperature the plate type shape changes to needle type shape increasing its compatibility with the bone tissue. Best results were obtained for sample SF-400 as it shows fine needles of HA resembling the structure of bone. These results are in coherence with results of TEM.

Dynamic Light Scattering (DLS) Analysis

Particle size of unmodified and modified Hydroxyapatite sintered at various temperatures obtained by dynamic light scattering measurement is shown in Fig. 6(ii). The particle size increased from 10 to 100nm with increase in sintering temperature from 60 to 800UC showing the same trend as evidenced from XRD and TEM results.

Contact Angle Analysis

The contact angle characterizes the wettability of the surface of a solid by a liquid i.e. the interaction between a solid and a liquid surface at the interface [28]. It is a highly desirable parameter for loading of drug to the ceramics and delivering to the desired target. The contact angles of unmodified and modified Hydroxyapatite (HA) sintered at different temperatures i.e. 400, 600 and 800[degrees]C are shown in Figure 6(i). No significant differences were demonstrated in contact angles and were below 40U revealing the hydrophilic behavior thus allowing the loading of drug to the ceramics and delivery of drug by aqueous solution incubation [28].

WD-XRF Analysis

The chemical composition, Ca/P ratio and percent carbon of unmodified and modified HA sintered at different temperature determined using WD-XRF (Wavelength Dispersive X-ray Fluorescence) are given in Table 1. From the data in the Table 1 it is clear that etidronic acid did not significantly affect the stoichiometry of hydroxyapatite and the Ca/P molar ratio for modified HA is close to the stoichiometry value of 1.67 [+ or -] 0.02[29]. The incorporation of etidronic acid in HA structure is also confirmed by the total carbon analysis, showing almost constant amount of the total carbon ~0.90% in the powder while the total amount of carbon in unmodified HA is less than 0.30.


The overall purpose of the study was to modify HA nanoparticles for better incorporation in scaffolds. Modification of nano-hydroxyapatite was successfully done by grafting of etidronic acid on the surface of HA as observed in XRD and FTIR results. The chemical compositions and structural study showed undisturbed stoichiometry and phase stability of surface modified HA which is a good indication. Further, morphology and particle size studied using SEM and TEM technique confirmed improvement in agglomeration tendency, crystallite size and shape of HA nanoparticles. The study revealed that SF400 sample modified at 400[degrees]C showed needle and plate like shapes with high agglomeration tendency and can be best used in tissue engineering.

Introduction of bisphosphonate groups in HA nanoparticles resulted in its enhanced surface area along with high reactivity. The surface modifying agent used in this study can act as an interface providing a strong bond between HA and polymer matrices that can possibly improve bioactivity of scaffolds in bone tissue engineering.


We gratefully acknowledge University Grant Commission and for providing financial assistance through Rajiv Gandhi National Fellowship Program to one of the author and Council of Scientific and Industrial Research (CSIR), India and Technical Education Quality Improvement Program-II, India for giving financial support for carrying out this research work.


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Lokesh Kumar, Anupama Kaushik *

Dr. SSB University Institute of Chemical Engineering and Technology, (Formerly known as Department of Chemical Engineering and Technology), Panjab University, Chandigarh 160014, India

Received 18 February 2017; Accepted 11 April 2017; Published online 31 December 2017

* Coresponding author: Dr. Anupama Kaushik; E-mail: anupamasharma@pu. ac. in

Caption: Figure 1: Scheme showing Surface modification and sintering of Synthesized Hydroxyapatite (HA)

Caption: Figure 2: FTIR Spectra of unmodified and Modified Hydroxyapatite Sintered at various Temperatures (a) HA (b) SF60 (c) SF400 (d) SF600 (e) SF800

Caption: Figure 3: XRD profiles of unmodified and Modified Hydroxyapatite Sintered at various Temperatures (a) HA (b) SF60 (c) SF400 (d) SF600 (e) SF800

Caption: Figure 4(i): TEM Images of unmodified and Modified Hydroxyapatite Sintered at various Temperatures (a) HA (b) SF60 (c) SF400 (d) SF600 (e) SF80

Caption: Figure 4(ii)): Crystallite size (diameter) analysis of the given TEM images of unmodified and Modified Hydroxyapatite Sintered at various Temperatures (a) HA (b) SF60 (c) SF400 (d) SF600 (e) SF800 using UTHSCSA image tool software

Caption: Figure 5: SEM Micrographs of unmodified and Modified Hydroxyapatite Sintered at various Temperatures (a) HA (b) SF60 (c) SF400 (d) SF600 (e) SF800

Caption: Figure 6 (1): Contact Angle images of unmodified and Modified Hydroxyapatite Sintered at various Temperatures (a) HA (b) SF60 (c) SF400 (d) SF600 (e) SF800

Caption: Figure 6 (ii): DLS of unmodified and Modified Hydroxyapatite Sintered at various Temperatures
Table 1: Crystallite size, Crystallinity, Ca/P ratio and Total %
carbon of unmodified and Modified Hydroxyapatite Sintered at various

Sample ID    Sintering    Cryst-     Crystal-   Ca/P    Total%C
            Temperature   allite     linity     ratio
            ([degree]C)   size (nm)  (%)

HA              60         -10        39       1.65     0.20
SF60            60         -12        40       1.66     0.90
SF400           400        -45        59       1.67     0.89
SF600           600        -70        SO       1.71     0.86
SF800           800        -91        90       1.72     0.85
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Title Annotation:Original Article
Author:Kumar, Lokesh; Kaushik, Anupama
Publication:Trends in Biomaterials and Artificial Organs
Date:Apr 1, 2017
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