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Forsterite-hydroxyapatite composite scaffolds with photothermal antibacterial activity for bone repair

Forsterite-hydroxyapatite composite scaffolds with photothermal antibacterial activity for bone... Journal of Advanced Ceramics 2021, 10(5): 1095–1106 ISSN 2226-4108 https://doi.org/10.1007/s40145-021-0494-x CN 10-1154/TQ Research Article Forsterite–hydroxyapatite composite scaffolds with photothermal antibacterial activity for bone repair a,b,† c,† a,b a,* Weiye LIU , Rongtai ZUO , Tanglong ZHU , Min ZHU , c,* b,* Shichang ZHAO , Yufang ZHU School of Materials Science and Engineering, University of Shanghai for Science and Technology, Shanghai 200093, China State Key Laboratory of High Performance Ceramics and Superfine Microstructure, Shanghai Institute of Ceramics, Chinese Academy of Sciences, Shanghai 200050, China Department of Orthopedics, Shanghai Jiao Tong University affiliated Sixth People’s Hospital, Shanghai Jiao Tong University, Shanghai 200233, China Received: December 26, 2020; Revised: March 16, 2021; Accepted: May 5, 2021 © The Author(s) 2021. Abstract: Bone engineering scaffolds with antibacterial activity satisfy the repair of bacterial infected bone defects, which is an expected issue in clinical. In this work, 3D-printed polymer-derived forsterite scaffolds were proposed to be deposited with hydroxyapatite (HA) coating via a hydrothermal treatment, achieving the functions of photothermal-induced antibacterial ability and bioactivity. The results showed that polymer-derived forsterite scaffolds possessed the photothermal antibacterial ability to inhibit Staphylococcus aureus (S. aureus) and Escherichia coli (E. coli) in vitro, owing to the photothermal effect of free carbon embedded in the scaffolds. The morphology of HA coating on forsterite scaffolds could be controlled through changing the hydrothermal temperature and the pH value of the reaction solution during hydrothermal treatment. Furthermore, HA coating did not influence the mechanical strength and photothermal effect of the scaffolds, but facilitated the proliferation and osteogenic differentiation of rat bone mesenchymal stem cells (rBMSCs) on scaffolds. Hence, the HA-deposited forsterite scaffolds would be greatly promising for repairing bacterial infected bone defects. Keywords: forsterite scaffolds; hydroxyapatite (HA) coating; bone repair; photothermal effect; antibacterial activity injuries, osteoporosis, bone tumors, and other diseases 1 Introduction are a serious problem in clinical [1]. Generally, the repair of critical-sized bone defects should be helped Bone defects caused by the postoperative infections, with bone repair materials [2]. Among them, silicate- based bioceramics, such as bioglass, calcium silicate, † Weiye Liu and Rongtai Zuo contributed equally to this work. akermanite, and bredigite, have received increasing * Corresponding authors. attention to treat bone defects due to their high bioactivity E-mail: M. Zhu, mzhu@usst.edu.cn; [3–6]. Forsterite (Mg SiO ) as one type of silicate-based 2 4 S. Zhao, zhaoshichang0404@163.com; bioceramics also has great potential for load-bearing Y. Zhu, zjf2412@163.com www.springer.com/journal/40145 1096 J Adv Ceram 2021, 10(5): 1095–1106 bone repair owing to their biocompatibility, excellent On the other hand, hydrothermal method can induce HA mechanical property, and slow biodegradation behavior nucleation on the active sites of matrix materials, and [7]. Choudhary et al. [8] fabricated cylindrical forsterite further promate to grow and crystallize, which facilitates scaffolds by molding forsterite powder and sintering, HA to bond on the surface of matrix materials [26]. and the compressive strength and Young’s modulus of Hence, hydrothermal method has been developed to forsterite scaffolds were 201 MPa and 4.8 GPa, deposit HA coating on the surface of scaffolds. Yang et respectively. Such mechanical property could match al. [27], as an illustration, deposited an HA coating with the cortical bones. Hence, forsterite can be used with a controllable nanostructure on the surface of a as a potential material for bone repair in load-bearing 3D-printed pure iron scaffold by a hydrothermal areas [9,10]. method. The results demonstrated that the mechanical Recently, the combination of organosilicon polymer- performances of the composite scaffolds were derived ceramics (PDCs) strategy with 3D printing comparable to natural bones. The HA coating was has been demonstrated to fabricate silicate ceramic highly bonded to the substrate materials, and significantly scaffolds [11]. We also developed to fabricate forsterite promoted cell response of rBMSCs. Similarly, Hu et al. scaffolds by 3D printing of silicone resin/MgO precursor [28] used a hydrothermal method to deposit nano HA and sintering in an inert atmosphere [12]. Such forsterite with rod-like morphology on porous biphasic calcium scaffolds exhibited photothermal-induced antibacterial phosphate (BCP) scaffolds, and achieved better activity due to the embedded free carbon in the scaffolds osteogenic differentiation of BMSCs compared with [12,13]. However, the relatively poor bioactivity of pure BCP scaffolds. It indicated that a hydrothermal forsterite would affect its osteogenesis ability [14]. To method to deposit HA coating could be an efficient address this issue, an efficient strategy is developed to strategy to enhance the bioactivity of scaffolds for modify the surface of forsterite scaffolds with bioactive bone repair. materials, which could stimulate cell responses of bone In this study, we proposed to deposit HA coating on mesenchymal stem cells (BMSCs) including cell the surface of 3D-printed polymer-derived forsterite adhesion, proliferation, and osteogenic differentiation, scaffolds by a hydrothermal method to improve the thereby promoting bone repair [15,16]. bioactivity. On one hand, the morphology and size of HA, one main mineral composition of human bones, HA coating could be regulated by changing the pH possesses the outstanding bioactivity and biocompatibility, value and hydrothermal temperature. On the other which has become one of the most popular bioactive hand, HA coating did not destroy the structure and materials to modify the metal implants [17]. Nowadays, influence the photothermal effect of scaffolds owing to some coating techniques, such as electrophoretic the excellent stability of forsterite scaffolds. Hence, the deposition and plasma spraying, have been applied to HA-coated forsterite scaffolds would be promising for produce uniform HA coatings on the implants and repair bone defects with bacterial infection. scaffolds [18,19]. Studies demonstrated that the coating morphology and bonding strength between the coating and matrix material are crucial for cell response and in 2 Experimental vivo bone integration [20]. Recently, hydrothermal method was increasingly 2. 1 Materials developed to fabricate HA coating on the scaffolds for All raw materials were utilized without further purification improving the performance of scaffolds [21,22]. including a commercial silicone resin (SilresMK, Wacker Studies demonstrated that hydrothermal method could Chemie, Germany), isopropyl alcohol, magnesium controllably synthesize HA with different morphologies oxide (MgO, ≥ 99.5%), ethylene diamine tetraacetic including whiskers, microspheres, nanorods, and acid disodium salt (EDTA-2Na, ≥ 99.5%), diammonium nanowires [23,24]. Zhang et al. [25] reported the utili- phosphate ((NH ) HPO , ≥ 99.0%), tetrahydrate calcium zation of calcium nitrate and diammonium hydrogen 4 2 4 nitrate (Ca(NO ) ·4H O, 98.5%), urea (CO(NH ) , phosphate as raw materials to synthesize HA by a 3 2 2 2 2 ≥ 99.0%), and sodium hydroxide (NaOH, ≥ 96.0%), hydrothermal method, and different morphological HA which were all purchased from Sinopharm Chemical could be synthesized by controlling the pH values of the reaction solutions during hydrothermal treatments. Reagent Co., Ltd., China. www.springer.com/journal/40145 J Adv Ceram 2021, 10(5): 1095–1106 1097 2. 2 Fabrication of HA-coated forsterite (M S–HA) wet condition), respectively. The photothermal stabilities scaffolds of scaffolds were analyzed after three cycles with a laser “on and off” state at a power density of 1.0 W/cm . The 3D-printed silicone resin-derived forsterite (Mg SiO , 2 4 M S) scaffolds were fabricated after sintering at 1400 ℃ 2. 5 Cell response of rBMSCs on M S–HA scaffolds in a continuous argon atmosphere on the basis of our In this study, the third-generation rBMSCs were used previous report [12]. HA deposition on forsterite to evaluate cell response on M S–HA scaffolds. Firstly, scaffolds was successfully treated via a hydrothermal 2 the M S and M S–HA scaffolds sterilized by dry 2 2 method. Typically, 11.8 g of Ca(NO ) ·4H O and 18.61 g 3 2 2 heating at 200 ℃ for 2 h were put in 24-well plates, of EDTA-2Na were completely dissolved in 500 mL and 1.0×10 cells were seeded on each scaffold. deionized water, and 3.96 g of (NH ) HPO and 15.15 g 4 2 4 Subsequently, the rBMSCs-seeded scaffolds were of CO(NH ) were subsequently added. After stirring 2 2 placed in an incubator (5% CO , 37 ℃) for 2 h to to dissolve completely, NaOH liquor (1 mol/L) was allow the cell attachment on the scaffolds, and then used to regulate the pH value of the mixed solution added 1 mL culture medium in each well for reaching 6. Next, the above mixed solution (45 mL) continuing the culture. was transferred into a 70 mL Teflon autoclave, and five The proliferation of rBMSCs on scaffolds was M S scaffolds were put in it. A hydrothermal treatment evaluated by a Cell Counting Kit-8 (CCK-8) assay, was conducted at 160 ℃ for 10 h before cooling to which was determined by measuring the absorbance at room temperature, and the HA-deposited M S a wavelength of 450 nm with a microplate reader (M S–HA) scaffolds were ultrasonically treated in (Bio-Rad680, USA). Furthermore, the distribution of deionized water bath for 30 s and rinsed with ethanol. rBMSCs with fluorescence labeling was observed by a The final scaffolds were then oven-dried at 100 ℃. The confocal laser scanning microscope (CLSM, Leica, pH values of the mixed solution (4, 6, 8, and 10) and Germany). Cell nuclei and cytoskeleton of rBMSCs were hydrothermal temperatures (140, 160, 180, and 200 ℃) stained with 10 mg/mL 4′,6-diamidino-2-phenylindole were changed to investigate the phase, morphology, (DAPI, Yeasen, China) and 5 mg/mL rhodamine and structure of HA coating. phalloidin (Yeasen, China) for 5 min, respectively. The alkaline phosphatase (ALP) activity of rBMSCs 2. 3 Characterization on scaffolds was tested by an ALP assay kit. Firstly, The phases of scaffolds were characterized by wide-angle 5 1.0×10 rBMSCs were seeded on each M S or M S–HA 2 2 X-ray diffraction (XRD) measured with a Bruker D8 scaffold, and the culture medium was renewed every ADVANCE X-ray powder diffractometer (Bruker Corp, two days [29]. When cultured for 7 and 14 days, the Billerica, MA, USA). The surface morphology of HA culture medium was removed and the attached cells coating on forsterite scaffolds was observed and were gently rinsed with PBS for three times and with analyzed by a scanning electron microscope (SEM, cold Tris buffer (50 mM) once. Next, the cells were FEI Quanta 450, USA). A static material testing lysed using a 0.2% Triton X-100 (200 μL), and the machine (2.5 kN, Zwick Roell, Germany) was utilized lysates were sonicated to disperse after being centrifuged to measure the compressive strength of scaffolds. The for 15 min (14,000 rpm, 4 ℃). Afterward, 50 μL of overall porosity of scaffolds was measured using supernatant was mixed with 150 μL working solution traditional Archimedes principle according to Ref. [3]. on the basis of the supplier’s protocol for determining. The conversion of p-nitrophenylphosphate into 2. 4 Photothermal effect of scaffolds p-nitrophenol in the presence of ALP was determined The photothermal effect of scaffolds was detected with by the absorbance at 405 nm measured with a microplate reader. The ALP activity was calculated from a standard an infrared thermal imager (FLIRTM A325SC camera, USA) after an 808 nm laser irradiation. The real-time curve after normalizing to the total protein content. Real-time quantitative reverse transcription-polymerase surface temperature changes of each M S or M S–HA 2 2 scaffold were tested after laser irradiation at different chain reaction (qPCR) was utilized to detect the related osteogenic gene expression of rBMSCs on both types power densities (0.5, 0.75, and 1.0 W/cm ) and in different environmental conditions (in air for dry of scaffolds including genes collagen typeⅠ (COL-1), osteocalcin (OCN), runt-related transcription factor 2 condition and in phosphate buffer solution (PBS) for www.springer.com/journal/40145 1098 J Adv Ceram 2021, 10(5): 1095–1106 (RUNX2), and ALP. The expression level of genes was normalized by the glyceraldehyde-3- phosphate dehydrogenase (GAPDH), and the results were ΔΔCt estimated with reference to 2 method according to Ref. [30]. 2. 6 In vitro photothermal antibacterial ability of scaffolds Staphylococcus aureus (S. aureus) and Escherichia coli (E. coli), as the representative Gram-positive and Fig. 1 Optical photographs of (a) M S and (b) M S–HA 2 2 Gram-negative bacteria, were used to investigate in scaffolds; (c) XRD patterns of M S and M S–HA scaffolds. 2 2 vitro antibacterial ability of M S–HA scaffolds. M S 2 2 scaffolds were used as a control. The antibacterial scaffolds well to form M S–HA scaffolds through a efficiency of M S or M S–HA scaffolds with or 2 2 hydrothermal process. without an 808 nm laser irradiation was determined by To optimize the nucleation and growth state of HA a spread plate counting method [31], and the operation coating on M S scaffolds, the effects of pH value of the procedures were followed as Ref. [12]. reaction solution and hydrothermal temperature on HA coating were subsequently investigated in this study. 2. 7 Statistical analysis Here, Ca(NO ) ·4H O and (NH ) HPO were utilized 3 2 2 4 2 4 The results were expressed as the mean±standard as the Ca and P sources for HA coating by a hydrothermal deviation (SD), which were based on the data from treatment, and the ratio of Ca to P was precisely three rational parallel experiments. The one-way adjusted to be 1.67 which is consistent with natural HA. ANOVA and Student–Newman–Keuls post hoc tests Figure 2 shows the XRD patterns of the M S–HA were used to determine the level of significance and P scaffolds that were hydrothermally treated at 140–200 ℃ values < 0.05 were commonly deemed to be significant. when pH values were from 4 to 10. The HA phase almost could not be observed for M S–HA scaffolds while the reaction condition was set to pH = 6 and 3 Results and discussion hydrothermally treated at 140 ℃, but M S–HA scaffolds that were hydrothermally treated at 160, 180, and 200 ℃ The structure, surface macro/micro morphology, and obviously exhibited the diffraction peaks of HA phase, phase change can be directly reflected by simple physical indicating the HA deposition on M S scaffolds. On the and chemical characterization. Figure 1 shows the other hand, the diffraction peak intensities of HA were representative photographs and XRD patterns of M S similar for M S–HA scaffolds hydrothermally treated and M S–HA scaffolds. It can be seen that M S scaffold 2 2 at 160, 180, and 200 ℃, suggesting that the deposited became rougher and the scaffold color changed from HA with parallel crystallinity could be obtained at the black to gray after HA coating (Figs. 1(a) and 1(b)), hydrothermal temperatures of 160–200 ℃. It can also suggesting the deposition of white HA on M S scaffolds be seen that HA could deposit on M S scaffolds at a was successfully achieved via a simple hydrothermal hydrothermal temperature of 160 ℃ when pH value of process. XRD technique was simultaneously utilized to the reaction solution was adjusted from 4 to 10, which further confirm HA coating on the surface of scaffolds was confirmed by the diffraction peaks of HA phase by analyzing the phases of M S scaffolds before and 2 appeared in M S–HA scaffolds. However, the diffraction after hydrothermal treatments. As shown in Fig. 1(c), peak intensity increased with the increase of pH only the diffraction peaks of forsterite phase (JCPDS value of the reaction solution, suggesting that the pH Card 34-0189) were observed for M S scaffolds; environment could regulate the HA crystallinity during however, the diffraction peaks of HA phase (JCPDS the hydrothermal treatments. Card 09-0432) also appeared on M S–HA scaffolds Figure 3 shows SEM images of the surfaces of the except for the diffraction peaks of forsterite phase. It M S and M S–HA scaffolds treated at different 2 2 obviously revealed that HA could deposit on M S hydrothermal temperatures. It can be observed that no www.springer.com/journal/40145 J Adv Ceram 2021, 10(5): 1095–1106 1099 Fig. 2 XRD patterns of M S–HA scaffolds obtained under different hydrothermal conditions: (a) different hydrothermal temperatures at pH = 6 and (b) different pH values of the reaction solution at a hydrothermal temperature of 160 ℃. Fig. 3 SEM images of the surfaces of (a) M S scaffolds; and M S–HA scaffolds hydrothermally treated at different hydrothermal 2 2 temperatures at (b) 140, (c) 160, (d) 180, and (e) 200 ℃ when the pH value of the reaction solution was set to 6. HA was covered on the surface of the scaffolds like, spherical, or rod-like HA particles on the scaffold hydrothermally treated at 140 ℃, although the surface surface, respectively. Here, during the hydrothermal morphology suffered from a little change due to the process in this study, urea was utilized as an effectual dissolution occurrence by hydrothermal treatment. precipitant to adjust the pH value of the hydrothermal However, different morphological particles were reaction, which promoted the various HA formation. obviously observed on the surfaces of the M S–HA Low hydrothermal temperature (140 ℃) was not able scaffolds hydrothermally treated at 160, 180, and to decompose urea, and thereby did not form HA 200 ℃, which could be identified to be HA particles coating. When the hydrothermal temperature raised, based on the XRD analysis above. Interestingly, the the decomposition rate of urea could be accelerated. regular changes of hydrothermal temperature induced Thus, the pH value of the reaction solution slowly different shapes and structures of HA coatings. It can increased, which contributed to the formation of HA be observed that the hydrothermal temperatures at 160, particles on the surfaces of scaffolds. The higher 180, and 200 ℃ induced the formation of the flower- hydrothermal temperature induced rapid decomposition www.springer.com/journal/40145 1100 J Adv Ceram 2021, 10(5): 1095–1106 of urea, resulting in the rapid increase of alkalinity in To investigate the effects of HA coating on the the solution, which accelerated the nucleus formation S physicochemical and biological performances of M and growth of HA, and thereby formed diverse scaffolds, the M S–HA scaffolds hydrothermally treated morphologies of HA particles on the surfaces of with the reaction solution of pH = 6 and at hydrothermal M S–HA scaffolds. temperature of 160 ℃ were used in this study. The Figure 4 shows SEM images of the surfaces of porosity and compressive strength of the M S scaffolds M S–HA scaffolds hydrothermally treated at 160 ℃ before and after HA coating were summarized in Table 1. with the pH values of the reaction solutions from 4 to The compressive strength of M S–HA scaffolds was 10. HA particles could be observed on the surfaces of determined to be 32.4±4.6 MPa at a porosity of M S–HA scaffolds treated with different pH values of 51.5%±4.3%, and there are no significant decreases in the reaction solutions. However, the morphology of the porosity and compressive strength of the M S HA particles changed from spherical to flower-like and scaffolds after HA coating, indicating that HA coating rod-like. Furthermore, irregular HA particles were process via hydrothermal treatment did not destroy the deposited on the scaffolds when the pH value of the structure of scaffolds. reaction solution was at 4 or 10, suggesting that the Zhu et al. [12] demonstrated that polymer-derived weakly acidic or alkaline environment of the original forsterite scaffolds exhibited excellent photothermal reaction solution facilitates to form regular HA particles, performance due to the embedded free carbon. Here, which was similar to other reported study [32]. On the whether the HA coating on the surface of the scaffold other hand, the M S–HA scaffolds were ultrasonically will affect the photothermal performance was further treated in deionized water bath for 30 s and rinsed with confirmed. Figure 5 shows the influence of HA coating ethanol, and SEM observation confirmed that the on the photothermal effect of scaffolds. It can be seen deposited HA particles have not been dropped off from S and M S–HA scaffolds exhibited excellent that both M 2 2 the scaffolds, suggesting that HA particles could stably photothermal effect under dry (in air) or wet (500 μL bond to the surface of the scaffolds. PBS) condition with an 808 nm laser irradiation, and Fig. 4 SEM images of the surfaces of M S–HA scaffolds hydrothermally treated at different pH values of (a) 4, (b) 6, (c) 8, and (d) 10 when the hydrothermal temperature was set to 160 ℃. www.springer.com/journal/40145 J Adv Ceram 2021, 10(5): 1095–1106 1101 Table 1 Porosity and compressive strength of M S to above 50 ℃. Here, the photothermal effect of the and M S–HA scaffolds M S and M S–HA scaffolds were determined by the 2 2 Scaffold Porosity Compressive strength (MPa) free carbon content in the scaffolds. We have detected MS 52.7%±3.8% 33.8±5.1 2 the carbon element of the cross section of the M S and MS–HA 51.5%±4.3% 32.4±4.6 M S–HA scaffolds by energy disperse spectroscopy 2 2 (EDS) analysis, and the carbon contents were estimated there are negligible changes after HA coating on M S to be 10.37% and 10.68%, respectively. It indicated that HA coating did not influence the photothermal scaffolds. After laser irradiation with an 808 nm laser at a power density of 0.75 W/cm for 5 min, the surface effect of M S scaffolds. Hence, the M S–HA scaffolds 2 2 had photothermal antibacterial ability. Furthermore, the temperatures of both M S and M S–HA scaffolds in 2 2 dry condition increased from room temperature to above temperature of M S–HA scaffolds caused by the photothermal effect increased with the increase of laser 100 ℃, and the solution temperatures of both M S and M S–HA scaffolds in wet condition could still increase power density, suggesting that the photothermal Fig. 5 Photothermal heating curves of both M S and M S–HA scaffolds in (a) dry and (b) wet conditions under an 808 nm 2 2 laser irradiation with a power density of 0.75 W/cm . The photothermal heating curves of M S–HA scaffolds in (c) dry and (d) wet conditions under an 808 nm laser irradiation with different laser power densities (0.5, 0.75, and 1.0 W/cm ). The time–temperature curve of the laser “on–off” cycle (0.75 W/cm ) of M S–HA scaffolds in (e) dry and (f) wet conditions under an 808 nm laser irradiation. www.springer.com/journal/40145 1102 J Adv Ceram 2021, 10(5): 1095–1106 temperature of M S–HA scaffolds could be controlled scaffolds after 3-day culture, which indicated that by adjusting the laser power density to meet the rBMSCs were well adhered on both scaffolds, and the photothermal antibacterial temperature (Figs. 5(c) and interconnected porous structure facilitated cell migration 5(d)). On the other hand, an 808 nm laser with a power and further proliferation. density of 0.75 W/cm was utilized to irradiate the Figure 6(b) shows the proliferation of rBMSCs on M S–HA scaffolds for 5 min (turn on), followed by a S and M S–HA scaffolds for 1, 3, and 7 days. both M 2 2 2 cooling process to room temperature (turn off), and With increasing culture time, the number of rBMSCs three “on–off” cycles were performed. As shown in on both M S and M S–HA scaffolds increased 2 2 Figs. 5(e) and 5(f), the increased temperature of M S–HA significantly. However, both M S and M S–HA scaffolds 2 2 2 scaffolds after each “on–off” cycle did not significantly showed similar level of cell proliferation at each decrease, whatever in dry or wet condition, which culture time point, revealing the good biocompatibility indicated that the M S–HA scaffolds had remarkable for both M S and M S–HA scaffolds. Here, the OD 2 2 2 photothermal stability, and showed a great potential for value for the M S–HA scaffold group showed a little long-term photothermal antibacterial function. decrease compared to that for the M S scaffold group, The cell adhesion and in vitro osteogenic activity of but both groups had no significant difference, suggesting M S–HA scaffolds were investigated to confirm if HA that HA coating did not influence the biocompatibility coating could enhance the bioactivity of M S scaffolds. of the scaffolds. ALP activity of rBMSCs on both M S 2 2 The adhesion of rBMSCs on both M S and M S–HA and M S–HA scaffolds was further evaluated to assess 2 2 2 scaffolds were visualized by confocal laser scanning the early differentiation of osteoblasts. As shown in Fig. microscopy (CLSM). As shown in Fig. 6(a), the dense 6(c), the level of ALP activity increased with culture and uniform layers of rBMSCs with a typical time, and both M S and M S–HA scaffolds showed 2 2 cytoskeleton morphology were distributed on both higher level of ALP activity than the blank group. Fig. 6 In vitro cellular response on the M S and M S–HA scaffolds. (a) CLSM images of rBMSCs seeded on the M S and 2 2 2 M S–HA scaffolds for 3 days (scale bar: 50 μm); (b) proliferation of rBMSCs cultured on the M S and M S–HA scaffolds for 1, 2 2 2 * ** 3, and 7 days; (c) ALP activity of rBMSCs cultured on the M S and M S–HA scaffolds for 7 and 14 days ( P < 0.05, P< 0.01). 2 2 www.springer.com/journal/40145 J Adv Ceram 2021, 10(5): 1095–1106 1103 Furthermore, the ALP activity of rBMSCs on M S–HA related genes. More importantly, M S–HA scaffolds 2 2 scaffolds was much higher than that on M S scaffolds. showed much higher expression level of osteogenic It indicated that HA coating on M S scaffolds could related genes than M S scaffolds, which indicated that 2 2 improve the bioactivity of scaffolds and promote the HA coating on M S scaffolds could improve the early osteogenic differentiation of rBMSCs [33]. osteogenic differentiation. Previous studies also To further evaluate the osteogenic differentiation of demonstrated that HA coating as a bioactive surface rBMSCs on the M S and M S–HA scaffolds, the could enhance cell attachment, proliferation, and 2 2 expression of osteogenic related genes of rBMSCs osteogenic differentiation of stem cells in vitro [34]. (COL-1, OCN, ALP, and RUNX2) on both M S and It has demonstrated that M S scaffolds had excellent 2 2 M S–HA scaffolds was tested in this study. GAPDH photothermal-induced antibacterial activity due to the was used as the internal reference for standardization. embedded free carbon with photothermal effect [12]. Primers (BioTNT, Shanghai, China) used for the Here, using S. aureus and E. coli as Gram-positive and amplification reaction are listed in Table 2. Figure 7 Gram-negative bacteria, respectively, the photothermal- shows the expression of osteogenic related genes of induced antibacterial activity of the M S–HA scaffolds rBMSCs on the scaffolds after 7-day culture. The was also evaluated by dilution plate counting method. expression levels of COL-1, OCN, ALP, and RUNX2 As shown in Fig. 8, after 15 min of irradiation with an genes on the M S and M S–HA scaffolds were much 808 nm laser irradiation, the number of viable bacterial 2 2 higher compared to blank group, suggesting that both colonies of the samples containing M S–HA scaffolds scaffolds could promote the expression of osteogenic on the AGAR plates decreased significantly, and the Table 2 Primer sequences used for qPCR Gene Forward primer sequence (5’-3’) Reverse primer sequence (5’-3’) ALP CAAGGATGCTGGGAAGTCCG CTCTGGGCGCATCTCATTGT RUNX2 CCGAGACCAACCGAGTCATTTA AAGAGGCTGTTTGACGCCAT OCN TCAACAATGGACTTGGAGCCC AGCTCGTCACAATTGGGGTT COL-1 GGAGAGTACTGGATCGACCCTAAC CTGACCTGTCTCCATGTTGCA GAPDH GAAGGTGAAGGTCGGAGTC GAAGATGGTGATGGGATTTC Fig. 7 Osteogenesis-related gene expression of (a) COL-1, (b) OCN, (c) ALP, and (d) RUNX2 for rBMSCs cultured on the * ** M S and M S–HA scaffolds for 7 days by qPCR analysis ( P < 0.05, P < 0.01). 2 2 www.springer.com/journal/40145 1104 J Adv Ceram 2021, 10(5): 1095–1106 Fig. 8 In vitro photothermal-induced antibacterial ability of the M S–HA scaffolds. (a) Optical images of S. aureus and E. coli colonies formed on AGAR plates after different treatments; bacterial colony viability of (b) S. aureus and (c) E. coli after different treatments. antibacterial efficiency increased with increasing the rBMSCs due to the enhanced bioactivity. Hence, laser power density. It can be observed that the M S–HA scaffolds show great potential for bone repair antibacterial efficiencies of M S–HA scaffolds against against bacterial infection. S. aureus and E. coli were 57.7% and 51.9% after 0.5 W/cm laser irradiation for 15 min, respectively. 4 Conclusions However, when the laser power density was increased to 1.0 W/cm , the antibacterial efficiencies of M S–HA In summary, forsterite–HA composite scaffolds with scaffolds against S. aureus and E. coli were significantly photothermal-induced antibacterial ability have been enhanced, even up to 96.1% and 95.6%, respectively, successfully fabricated through HA deposition on which showed similar antibacterial efficiencies for the 3D-printed polymer-derived forsterite scaffolds via a M S and M S–HA scaffolds at the same irradiation 2 2 hydrothermal method. The morphology of HA coating conditions [12]. Therefore, M S–HA scaffolds still had could be regulated by controlling the hydrothermal excellent photothermal antibacterial ability, and the temperature and pH value of the reaction solution. The antibacterial efficiency could be regulated by controlling HA-coated forsterite scaffolds not only dramatically the laser power density. boosted the proliferation and promoted osteogenic HA coating did not influence the photothermal effect differentiation of rBMSCs on the M S–HA, but also of the M S scaffolds, and thereby endowed the M S–HA 2 2 2 maintained excellent photothermal-induced antibacterial scaffolds with excellent photothermal-induced antibacterial ability under an 808 nm laser irradiation. Therefore, activity. On the other hand, HA coating on the M S such HA-coated forsterite scaffolds showed great scaffolds promoted the osteogenic differentiation of www.springer.com/journal/40145 J Adv Ceram 2021, 10(5): 1095–1106 1105 therapy and bone regeneration. Chem Eng J 2020, 382: potential for bacterial infected bone repair. [14] Tavangarian F, Emadi R. Improving degradation rate and Acknowledgements apatite formation ability of nanostructure forsterite. 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Regulation of osteoblast Commons Attribution 4.0 International License, which permits differentiation and iron content in MC3T3-E1 cells by use, sharing, adaptation, distribution and reproduction in any static magnetic field with different intensities. Biol Trace medium or format, as long as you give appropriate credit to the Elem Res 2018, 184: 214–225. original author(s) and the source, provide a link to the Creative [31] Wiedmer D, Cui C, Weber F, et al. Antibacterial surface Commons licence, and indicate if changes were made. coating for bone scaffolds based on the dark catalytic effect The images or other third party material in this article are of titanium dioxide. ACS Appl Mater Interfaces 2018, 10: included in the article’s Creative Commons licence, unless 35784–35793. indicated otherwise in a credit line to the material. If material is [32] In Y, Amornkitbamrung U, Hong MH, et al. On the not included in the article’s Creative Commons licence and your crystallization of hydroxyapatite under hydrothermal intended use is not permitted by statutory regulation or exceeds conditions: Role of sebacic acid as an additive. ACS Omega the permitted use, you will need to obtain permission directly 2020, 5: 27204–27210. from the copyright holder. [33] Cui BC, Zhang RR, Sun FB, et al. Mechanical and To view a copy of this licence, visit http://creativecommons. org/licenses/by/4.0/. biocompatible properties of polymer-infiltrated-ceramic- www.springer.com/journal/40145 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Advanced Ceramics Springer Journals

Forsterite-hydroxyapatite composite scaffolds with photothermal antibacterial activity for bone repair

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Springer Journals
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Copyright © The Author(s) 2021
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2226-4108
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2227-8508
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10.1007/s40145-021-0494-x
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Abstract

Journal of Advanced Ceramics 2021, 10(5): 1095–1106 ISSN 2226-4108 https://doi.org/10.1007/s40145-021-0494-x CN 10-1154/TQ Research Article Forsterite–hydroxyapatite composite scaffolds with photothermal antibacterial activity for bone repair a,b,† c,† a,b a,* Weiye LIU , Rongtai ZUO , Tanglong ZHU , Min ZHU , c,* b,* Shichang ZHAO , Yufang ZHU School of Materials Science and Engineering, University of Shanghai for Science and Technology, Shanghai 200093, China State Key Laboratory of High Performance Ceramics and Superfine Microstructure, Shanghai Institute of Ceramics, Chinese Academy of Sciences, Shanghai 200050, China Department of Orthopedics, Shanghai Jiao Tong University affiliated Sixth People’s Hospital, Shanghai Jiao Tong University, Shanghai 200233, China Received: December 26, 2020; Revised: March 16, 2021; Accepted: May 5, 2021 © The Author(s) 2021. Abstract: Bone engineering scaffolds with antibacterial activity satisfy the repair of bacterial infected bone defects, which is an expected issue in clinical. In this work, 3D-printed polymer-derived forsterite scaffolds were proposed to be deposited with hydroxyapatite (HA) coating via a hydrothermal treatment, achieving the functions of photothermal-induced antibacterial ability and bioactivity. The results showed that polymer-derived forsterite scaffolds possessed the photothermal antibacterial ability to inhibit Staphylococcus aureus (S. aureus) and Escherichia coli (E. coli) in vitro, owing to the photothermal effect of free carbon embedded in the scaffolds. The morphology of HA coating on forsterite scaffolds could be controlled through changing the hydrothermal temperature and the pH value of the reaction solution during hydrothermal treatment. Furthermore, HA coating did not influence the mechanical strength and photothermal effect of the scaffolds, but facilitated the proliferation and osteogenic differentiation of rat bone mesenchymal stem cells (rBMSCs) on scaffolds. Hence, the HA-deposited forsterite scaffolds would be greatly promising for repairing bacterial infected bone defects. Keywords: forsterite scaffolds; hydroxyapatite (HA) coating; bone repair; photothermal effect; antibacterial activity injuries, osteoporosis, bone tumors, and other diseases 1 Introduction are a serious problem in clinical [1]. Generally, the repair of critical-sized bone defects should be helped Bone defects caused by the postoperative infections, with bone repair materials [2]. Among them, silicate- based bioceramics, such as bioglass, calcium silicate, † Weiye Liu and Rongtai Zuo contributed equally to this work. akermanite, and bredigite, have received increasing * Corresponding authors. attention to treat bone defects due to their high bioactivity E-mail: M. Zhu, mzhu@usst.edu.cn; [3–6]. Forsterite (Mg SiO ) as one type of silicate-based 2 4 S. Zhao, zhaoshichang0404@163.com; bioceramics also has great potential for load-bearing Y. Zhu, zjf2412@163.com www.springer.com/journal/40145 1096 J Adv Ceram 2021, 10(5): 1095–1106 bone repair owing to their biocompatibility, excellent On the other hand, hydrothermal method can induce HA mechanical property, and slow biodegradation behavior nucleation on the active sites of matrix materials, and [7]. Choudhary et al. [8] fabricated cylindrical forsterite further promate to grow and crystallize, which facilitates scaffolds by molding forsterite powder and sintering, HA to bond on the surface of matrix materials [26]. and the compressive strength and Young’s modulus of Hence, hydrothermal method has been developed to forsterite scaffolds were 201 MPa and 4.8 GPa, deposit HA coating on the surface of scaffolds. Yang et respectively. Such mechanical property could match al. [27], as an illustration, deposited an HA coating with the cortical bones. Hence, forsterite can be used with a controllable nanostructure on the surface of a as a potential material for bone repair in load-bearing 3D-printed pure iron scaffold by a hydrothermal areas [9,10]. method. The results demonstrated that the mechanical Recently, the combination of organosilicon polymer- performances of the composite scaffolds were derived ceramics (PDCs) strategy with 3D printing comparable to natural bones. The HA coating was has been demonstrated to fabricate silicate ceramic highly bonded to the substrate materials, and significantly scaffolds [11]. We also developed to fabricate forsterite promoted cell response of rBMSCs. Similarly, Hu et al. scaffolds by 3D printing of silicone resin/MgO precursor [28] used a hydrothermal method to deposit nano HA and sintering in an inert atmosphere [12]. Such forsterite with rod-like morphology on porous biphasic calcium scaffolds exhibited photothermal-induced antibacterial phosphate (BCP) scaffolds, and achieved better activity due to the embedded free carbon in the scaffolds osteogenic differentiation of BMSCs compared with [12,13]. However, the relatively poor bioactivity of pure BCP scaffolds. It indicated that a hydrothermal forsterite would affect its osteogenesis ability [14]. To method to deposit HA coating could be an efficient address this issue, an efficient strategy is developed to strategy to enhance the bioactivity of scaffolds for modify the surface of forsterite scaffolds with bioactive bone repair. materials, which could stimulate cell responses of bone In this study, we proposed to deposit HA coating on mesenchymal stem cells (BMSCs) including cell the surface of 3D-printed polymer-derived forsterite adhesion, proliferation, and osteogenic differentiation, scaffolds by a hydrothermal method to improve the thereby promoting bone repair [15,16]. bioactivity. On one hand, the morphology and size of HA, one main mineral composition of human bones, HA coating could be regulated by changing the pH possesses the outstanding bioactivity and biocompatibility, value and hydrothermal temperature. On the other which has become one of the most popular bioactive hand, HA coating did not destroy the structure and materials to modify the metal implants [17]. Nowadays, influence the photothermal effect of scaffolds owing to some coating techniques, such as electrophoretic the excellent stability of forsterite scaffolds. Hence, the deposition and plasma spraying, have been applied to HA-coated forsterite scaffolds would be promising for produce uniform HA coatings on the implants and repair bone defects with bacterial infection. scaffolds [18,19]. Studies demonstrated that the coating morphology and bonding strength between the coating and matrix material are crucial for cell response and in 2 Experimental vivo bone integration [20]. Recently, hydrothermal method was increasingly 2. 1 Materials developed to fabricate HA coating on the scaffolds for All raw materials were utilized without further purification improving the performance of scaffolds [21,22]. including a commercial silicone resin (SilresMK, Wacker Studies demonstrated that hydrothermal method could Chemie, Germany), isopropyl alcohol, magnesium controllably synthesize HA with different morphologies oxide (MgO, ≥ 99.5%), ethylene diamine tetraacetic including whiskers, microspheres, nanorods, and acid disodium salt (EDTA-2Na, ≥ 99.5%), diammonium nanowires [23,24]. Zhang et al. [25] reported the utili- phosphate ((NH ) HPO , ≥ 99.0%), tetrahydrate calcium zation of calcium nitrate and diammonium hydrogen 4 2 4 nitrate (Ca(NO ) ·4H O, 98.5%), urea (CO(NH ) , phosphate as raw materials to synthesize HA by a 3 2 2 2 2 ≥ 99.0%), and sodium hydroxide (NaOH, ≥ 96.0%), hydrothermal method, and different morphological HA which were all purchased from Sinopharm Chemical could be synthesized by controlling the pH values of the reaction solutions during hydrothermal treatments. Reagent Co., Ltd., China. www.springer.com/journal/40145 J Adv Ceram 2021, 10(5): 1095–1106 1097 2. 2 Fabrication of HA-coated forsterite (M S–HA) wet condition), respectively. The photothermal stabilities scaffolds of scaffolds were analyzed after three cycles with a laser “on and off” state at a power density of 1.0 W/cm . The 3D-printed silicone resin-derived forsterite (Mg SiO , 2 4 M S) scaffolds were fabricated after sintering at 1400 ℃ 2. 5 Cell response of rBMSCs on M S–HA scaffolds in a continuous argon atmosphere on the basis of our In this study, the third-generation rBMSCs were used previous report [12]. HA deposition on forsterite to evaluate cell response on M S–HA scaffolds. Firstly, scaffolds was successfully treated via a hydrothermal 2 the M S and M S–HA scaffolds sterilized by dry 2 2 method. Typically, 11.8 g of Ca(NO ) ·4H O and 18.61 g 3 2 2 heating at 200 ℃ for 2 h were put in 24-well plates, of EDTA-2Na were completely dissolved in 500 mL and 1.0×10 cells were seeded on each scaffold. deionized water, and 3.96 g of (NH ) HPO and 15.15 g 4 2 4 Subsequently, the rBMSCs-seeded scaffolds were of CO(NH ) were subsequently added. After stirring 2 2 placed in an incubator (5% CO , 37 ℃) for 2 h to to dissolve completely, NaOH liquor (1 mol/L) was allow the cell attachment on the scaffolds, and then used to regulate the pH value of the mixed solution added 1 mL culture medium in each well for reaching 6. Next, the above mixed solution (45 mL) continuing the culture. was transferred into a 70 mL Teflon autoclave, and five The proliferation of rBMSCs on scaffolds was M S scaffolds were put in it. A hydrothermal treatment evaluated by a Cell Counting Kit-8 (CCK-8) assay, was conducted at 160 ℃ for 10 h before cooling to which was determined by measuring the absorbance at room temperature, and the HA-deposited M S a wavelength of 450 nm with a microplate reader (M S–HA) scaffolds were ultrasonically treated in (Bio-Rad680, USA). Furthermore, the distribution of deionized water bath for 30 s and rinsed with ethanol. rBMSCs with fluorescence labeling was observed by a The final scaffolds were then oven-dried at 100 ℃. The confocal laser scanning microscope (CLSM, Leica, pH values of the mixed solution (4, 6, 8, and 10) and Germany). Cell nuclei and cytoskeleton of rBMSCs were hydrothermal temperatures (140, 160, 180, and 200 ℃) stained with 10 mg/mL 4′,6-diamidino-2-phenylindole were changed to investigate the phase, morphology, (DAPI, Yeasen, China) and 5 mg/mL rhodamine and structure of HA coating. phalloidin (Yeasen, China) for 5 min, respectively. The alkaline phosphatase (ALP) activity of rBMSCs 2. 3 Characterization on scaffolds was tested by an ALP assay kit. Firstly, The phases of scaffolds were characterized by wide-angle 5 1.0×10 rBMSCs were seeded on each M S or M S–HA 2 2 X-ray diffraction (XRD) measured with a Bruker D8 scaffold, and the culture medium was renewed every ADVANCE X-ray powder diffractometer (Bruker Corp, two days [29]. When cultured for 7 and 14 days, the Billerica, MA, USA). The surface morphology of HA culture medium was removed and the attached cells coating on forsterite scaffolds was observed and were gently rinsed with PBS for three times and with analyzed by a scanning electron microscope (SEM, cold Tris buffer (50 mM) once. Next, the cells were FEI Quanta 450, USA). A static material testing lysed using a 0.2% Triton X-100 (200 μL), and the machine (2.5 kN, Zwick Roell, Germany) was utilized lysates were sonicated to disperse after being centrifuged to measure the compressive strength of scaffolds. The for 15 min (14,000 rpm, 4 ℃). Afterward, 50 μL of overall porosity of scaffolds was measured using supernatant was mixed with 150 μL working solution traditional Archimedes principle according to Ref. [3]. on the basis of the supplier’s protocol for determining. The conversion of p-nitrophenylphosphate into 2. 4 Photothermal effect of scaffolds p-nitrophenol in the presence of ALP was determined The photothermal effect of scaffolds was detected with by the absorbance at 405 nm measured with a microplate reader. The ALP activity was calculated from a standard an infrared thermal imager (FLIRTM A325SC camera, USA) after an 808 nm laser irradiation. The real-time curve after normalizing to the total protein content. Real-time quantitative reverse transcription-polymerase surface temperature changes of each M S or M S–HA 2 2 scaffold were tested after laser irradiation at different chain reaction (qPCR) was utilized to detect the related osteogenic gene expression of rBMSCs on both types power densities (0.5, 0.75, and 1.0 W/cm ) and in different environmental conditions (in air for dry of scaffolds including genes collagen typeⅠ (COL-1), osteocalcin (OCN), runt-related transcription factor 2 condition and in phosphate buffer solution (PBS) for www.springer.com/journal/40145 1098 J Adv Ceram 2021, 10(5): 1095–1106 (RUNX2), and ALP. The expression level of genes was normalized by the glyceraldehyde-3- phosphate dehydrogenase (GAPDH), and the results were ΔΔCt estimated with reference to 2 method according to Ref. [30]. 2. 6 In vitro photothermal antibacterial ability of scaffolds Staphylococcus aureus (S. aureus) and Escherichia coli (E. coli), as the representative Gram-positive and Fig. 1 Optical photographs of (a) M S and (b) M S–HA 2 2 Gram-negative bacteria, were used to investigate in scaffolds; (c) XRD patterns of M S and M S–HA scaffolds. 2 2 vitro antibacterial ability of M S–HA scaffolds. M S 2 2 scaffolds were used as a control. The antibacterial scaffolds well to form M S–HA scaffolds through a efficiency of M S or M S–HA scaffolds with or 2 2 hydrothermal process. without an 808 nm laser irradiation was determined by To optimize the nucleation and growth state of HA a spread plate counting method [31], and the operation coating on M S scaffolds, the effects of pH value of the procedures were followed as Ref. [12]. reaction solution and hydrothermal temperature on HA coating were subsequently investigated in this study. 2. 7 Statistical analysis Here, Ca(NO ) ·4H O and (NH ) HPO were utilized 3 2 2 4 2 4 The results were expressed as the mean±standard as the Ca and P sources for HA coating by a hydrothermal deviation (SD), which were based on the data from treatment, and the ratio of Ca to P was precisely three rational parallel experiments. The one-way adjusted to be 1.67 which is consistent with natural HA. ANOVA and Student–Newman–Keuls post hoc tests Figure 2 shows the XRD patterns of the M S–HA were used to determine the level of significance and P scaffolds that were hydrothermally treated at 140–200 ℃ values < 0.05 were commonly deemed to be significant. when pH values were from 4 to 10. The HA phase almost could not be observed for M S–HA scaffolds while the reaction condition was set to pH = 6 and 3 Results and discussion hydrothermally treated at 140 ℃, but M S–HA scaffolds that were hydrothermally treated at 160, 180, and 200 ℃ The structure, surface macro/micro morphology, and obviously exhibited the diffraction peaks of HA phase, phase change can be directly reflected by simple physical indicating the HA deposition on M S scaffolds. On the and chemical characterization. Figure 1 shows the other hand, the diffraction peak intensities of HA were representative photographs and XRD patterns of M S similar for M S–HA scaffolds hydrothermally treated and M S–HA scaffolds. It can be seen that M S scaffold 2 2 at 160, 180, and 200 ℃, suggesting that the deposited became rougher and the scaffold color changed from HA with parallel crystallinity could be obtained at the black to gray after HA coating (Figs. 1(a) and 1(b)), hydrothermal temperatures of 160–200 ℃. It can also suggesting the deposition of white HA on M S scaffolds be seen that HA could deposit on M S scaffolds at a was successfully achieved via a simple hydrothermal hydrothermal temperature of 160 ℃ when pH value of process. XRD technique was simultaneously utilized to the reaction solution was adjusted from 4 to 10, which further confirm HA coating on the surface of scaffolds was confirmed by the diffraction peaks of HA phase by analyzing the phases of M S scaffolds before and 2 appeared in M S–HA scaffolds. However, the diffraction after hydrothermal treatments. As shown in Fig. 1(c), peak intensity increased with the increase of pH only the diffraction peaks of forsterite phase (JCPDS value of the reaction solution, suggesting that the pH Card 34-0189) were observed for M S scaffolds; environment could regulate the HA crystallinity during however, the diffraction peaks of HA phase (JCPDS the hydrothermal treatments. Card 09-0432) also appeared on M S–HA scaffolds Figure 3 shows SEM images of the surfaces of the except for the diffraction peaks of forsterite phase. It M S and M S–HA scaffolds treated at different 2 2 obviously revealed that HA could deposit on M S hydrothermal temperatures. It can be observed that no www.springer.com/journal/40145 J Adv Ceram 2021, 10(5): 1095–1106 1099 Fig. 2 XRD patterns of M S–HA scaffolds obtained under different hydrothermal conditions: (a) different hydrothermal temperatures at pH = 6 and (b) different pH values of the reaction solution at a hydrothermal temperature of 160 ℃. Fig. 3 SEM images of the surfaces of (a) M S scaffolds; and M S–HA scaffolds hydrothermally treated at different hydrothermal 2 2 temperatures at (b) 140, (c) 160, (d) 180, and (e) 200 ℃ when the pH value of the reaction solution was set to 6. HA was covered on the surface of the scaffolds like, spherical, or rod-like HA particles on the scaffold hydrothermally treated at 140 ℃, although the surface surface, respectively. Here, during the hydrothermal morphology suffered from a little change due to the process in this study, urea was utilized as an effectual dissolution occurrence by hydrothermal treatment. precipitant to adjust the pH value of the hydrothermal However, different morphological particles were reaction, which promoted the various HA formation. obviously observed on the surfaces of the M S–HA Low hydrothermal temperature (140 ℃) was not able scaffolds hydrothermally treated at 160, 180, and to decompose urea, and thereby did not form HA 200 ℃, which could be identified to be HA particles coating. When the hydrothermal temperature raised, based on the XRD analysis above. Interestingly, the the decomposition rate of urea could be accelerated. regular changes of hydrothermal temperature induced Thus, the pH value of the reaction solution slowly different shapes and structures of HA coatings. It can increased, which contributed to the formation of HA be observed that the hydrothermal temperatures at 160, particles on the surfaces of scaffolds. The higher 180, and 200 ℃ induced the formation of the flower- hydrothermal temperature induced rapid decomposition www.springer.com/journal/40145 1100 J Adv Ceram 2021, 10(5): 1095–1106 of urea, resulting in the rapid increase of alkalinity in To investigate the effects of HA coating on the the solution, which accelerated the nucleus formation S physicochemical and biological performances of M and growth of HA, and thereby formed diverse scaffolds, the M S–HA scaffolds hydrothermally treated morphologies of HA particles on the surfaces of with the reaction solution of pH = 6 and at hydrothermal M S–HA scaffolds. temperature of 160 ℃ were used in this study. The Figure 4 shows SEM images of the surfaces of porosity and compressive strength of the M S scaffolds M S–HA scaffolds hydrothermally treated at 160 ℃ before and after HA coating were summarized in Table 1. with the pH values of the reaction solutions from 4 to The compressive strength of M S–HA scaffolds was 10. HA particles could be observed on the surfaces of determined to be 32.4±4.6 MPa at a porosity of M S–HA scaffolds treated with different pH values of 51.5%±4.3%, and there are no significant decreases in the reaction solutions. However, the morphology of the porosity and compressive strength of the M S HA particles changed from spherical to flower-like and scaffolds after HA coating, indicating that HA coating rod-like. Furthermore, irregular HA particles were process via hydrothermal treatment did not destroy the deposited on the scaffolds when the pH value of the structure of scaffolds. reaction solution was at 4 or 10, suggesting that the Zhu et al. [12] demonstrated that polymer-derived weakly acidic or alkaline environment of the original forsterite scaffolds exhibited excellent photothermal reaction solution facilitates to form regular HA particles, performance due to the embedded free carbon. Here, which was similar to other reported study [32]. On the whether the HA coating on the surface of the scaffold other hand, the M S–HA scaffolds were ultrasonically will affect the photothermal performance was further treated in deionized water bath for 30 s and rinsed with confirmed. Figure 5 shows the influence of HA coating ethanol, and SEM observation confirmed that the on the photothermal effect of scaffolds. It can be seen deposited HA particles have not been dropped off from S and M S–HA scaffolds exhibited excellent that both M 2 2 the scaffolds, suggesting that HA particles could stably photothermal effect under dry (in air) or wet (500 μL bond to the surface of the scaffolds. PBS) condition with an 808 nm laser irradiation, and Fig. 4 SEM images of the surfaces of M S–HA scaffolds hydrothermally treated at different pH values of (a) 4, (b) 6, (c) 8, and (d) 10 when the hydrothermal temperature was set to 160 ℃. www.springer.com/journal/40145 J Adv Ceram 2021, 10(5): 1095–1106 1101 Table 1 Porosity and compressive strength of M S to above 50 ℃. Here, the photothermal effect of the and M S–HA scaffolds M S and M S–HA scaffolds were determined by the 2 2 Scaffold Porosity Compressive strength (MPa) free carbon content in the scaffolds. We have detected MS 52.7%±3.8% 33.8±5.1 2 the carbon element of the cross section of the M S and MS–HA 51.5%±4.3% 32.4±4.6 M S–HA scaffolds by energy disperse spectroscopy 2 2 (EDS) analysis, and the carbon contents were estimated there are negligible changes after HA coating on M S to be 10.37% and 10.68%, respectively. It indicated that HA coating did not influence the photothermal scaffolds. After laser irradiation with an 808 nm laser at a power density of 0.75 W/cm for 5 min, the surface effect of M S scaffolds. Hence, the M S–HA scaffolds 2 2 had photothermal antibacterial ability. Furthermore, the temperatures of both M S and M S–HA scaffolds in 2 2 dry condition increased from room temperature to above temperature of M S–HA scaffolds caused by the photothermal effect increased with the increase of laser 100 ℃, and the solution temperatures of both M S and M S–HA scaffolds in wet condition could still increase power density, suggesting that the photothermal Fig. 5 Photothermal heating curves of both M S and M S–HA scaffolds in (a) dry and (b) wet conditions under an 808 nm 2 2 laser irradiation with a power density of 0.75 W/cm . The photothermal heating curves of M S–HA scaffolds in (c) dry and (d) wet conditions under an 808 nm laser irradiation with different laser power densities (0.5, 0.75, and 1.0 W/cm ). The time–temperature curve of the laser “on–off” cycle (0.75 W/cm ) of M S–HA scaffolds in (e) dry and (f) wet conditions under an 808 nm laser irradiation. www.springer.com/journal/40145 1102 J Adv Ceram 2021, 10(5): 1095–1106 temperature of M S–HA scaffolds could be controlled scaffolds after 3-day culture, which indicated that by adjusting the laser power density to meet the rBMSCs were well adhered on both scaffolds, and the photothermal antibacterial temperature (Figs. 5(c) and interconnected porous structure facilitated cell migration 5(d)). On the other hand, an 808 nm laser with a power and further proliferation. density of 0.75 W/cm was utilized to irradiate the Figure 6(b) shows the proliferation of rBMSCs on M S–HA scaffolds for 5 min (turn on), followed by a S and M S–HA scaffolds for 1, 3, and 7 days. both M 2 2 2 cooling process to room temperature (turn off), and With increasing culture time, the number of rBMSCs three “on–off” cycles were performed. As shown in on both M S and M S–HA scaffolds increased 2 2 Figs. 5(e) and 5(f), the increased temperature of M S–HA significantly. However, both M S and M S–HA scaffolds 2 2 2 scaffolds after each “on–off” cycle did not significantly showed similar level of cell proliferation at each decrease, whatever in dry or wet condition, which culture time point, revealing the good biocompatibility indicated that the M S–HA scaffolds had remarkable for both M S and M S–HA scaffolds. Here, the OD 2 2 2 photothermal stability, and showed a great potential for value for the M S–HA scaffold group showed a little long-term photothermal antibacterial function. decrease compared to that for the M S scaffold group, The cell adhesion and in vitro osteogenic activity of but both groups had no significant difference, suggesting M S–HA scaffolds were investigated to confirm if HA that HA coating did not influence the biocompatibility coating could enhance the bioactivity of M S scaffolds. of the scaffolds. ALP activity of rBMSCs on both M S 2 2 The adhesion of rBMSCs on both M S and M S–HA and M S–HA scaffolds was further evaluated to assess 2 2 2 scaffolds were visualized by confocal laser scanning the early differentiation of osteoblasts. As shown in Fig. microscopy (CLSM). As shown in Fig. 6(a), the dense 6(c), the level of ALP activity increased with culture and uniform layers of rBMSCs with a typical time, and both M S and M S–HA scaffolds showed 2 2 cytoskeleton morphology were distributed on both higher level of ALP activity than the blank group. Fig. 6 In vitro cellular response on the M S and M S–HA scaffolds. (a) CLSM images of rBMSCs seeded on the M S and 2 2 2 M S–HA scaffolds for 3 days (scale bar: 50 μm); (b) proliferation of rBMSCs cultured on the M S and M S–HA scaffolds for 1, 2 2 2 * ** 3, and 7 days; (c) ALP activity of rBMSCs cultured on the M S and M S–HA scaffolds for 7 and 14 days ( P < 0.05, P< 0.01). 2 2 www.springer.com/journal/40145 J Adv Ceram 2021, 10(5): 1095–1106 1103 Furthermore, the ALP activity of rBMSCs on M S–HA related genes. More importantly, M S–HA scaffolds 2 2 scaffolds was much higher than that on M S scaffolds. showed much higher expression level of osteogenic It indicated that HA coating on M S scaffolds could related genes than M S scaffolds, which indicated that 2 2 improve the bioactivity of scaffolds and promote the HA coating on M S scaffolds could improve the early osteogenic differentiation of rBMSCs [33]. osteogenic differentiation. Previous studies also To further evaluate the osteogenic differentiation of demonstrated that HA coating as a bioactive surface rBMSCs on the M S and M S–HA scaffolds, the could enhance cell attachment, proliferation, and 2 2 expression of osteogenic related genes of rBMSCs osteogenic differentiation of stem cells in vitro [34]. (COL-1, OCN, ALP, and RUNX2) on both M S and It has demonstrated that M S scaffolds had excellent 2 2 M S–HA scaffolds was tested in this study. GAPDH photothermal-induced antibacterial activity due to the was used as the internal reference for standardization. embedded free carbon with photothermal effect [12]. Primers (BioTNT, Shanghai, China) used for the Here, using S. aureus and E. coli as Gram-positive and amplification reaction are listed in Table 2. Figure 7 Gram-negative bacteria, respectively, the photothermal- shows the expression of osteogenic related genes of induced antibacterial activity of the M S–HA scaffolds rBMSCs on the scaffolds after 7-day culture. The was also evaluated by dilution plate counting method. expression levels of COL-1, OCN, ALP, and RUNX2 As shown in Fig. 8, after 15 min of irradiation with an genes on the M S and M S–HA scaffolds were much 808 nm laser irradiation, the number of viable bacterial 2 2 higher compared to blank group, suggesting that both colonies of the samples containing M S–HA scaffolds scaffolds could promote the expression of osteogenic on the AGAR plates decreased significantly, and the Table 2 Primer sequences used for qPCR Gene Forward primer sequence (5’-3’) Reverse primer sequence (5’-3’) ALP CAAGGATGCTGGGAAGTCCG CTCTGGGCGCATCTCATTGT RUNX2 CCGAGACCAACCGAGTCATTTA AAGAGGCTGTTTGACGCCAT OCN TCAACAATGGACTTGGAGCCC AGCTCGTCACAATTGGGGTT COL-1 GGAGAGTACTGGATCGACCCTAAC CTGACCTGTCTCCATGTTGCA GAPDH GAAGGTGAAGGTCGGAGTC GAAGATGGTGATGGGATTTC Fig. 7 Osteogenesis-related gene expression of (a) COL-1, (b) OCN, (c) ALP, and (d) RUNX2 for rBMSCs cultured on the * ** M S and M S–HA scaffolds for 7 days by qPCR analysis ( P < 0.05, P < 0.01). 2 2 www.springer.com/journal/40145 1104 J Adv Ceram 2021, 10(5): 1095–1106 Fig. 8 In vitro photothermal-induced antibacterial ability of the M S–HA scaffolds. (a) Optical images of S. aureus and E. coli colonies formed on AGAR plates after different treatments; bacterial colony viability of (b) S. aureus and (c) E. coli after different treatments. antibacterial efficiency increased with increasing the rBMSCs due to the enhanced bioactivity. Hence, laser power density. It can be observed that the M S–HA scaffolds show great potential for bone repair antibacterial efficiencies of M S–HA scaffolds against against bacterial infection. S. aureus and E. coli were 57.7% and 51.9% after 0.5 W/cm laser irradiation for 15 min, respectively. 4 Conclusions However, when the laser power density was increased to 1.0 W/cm , the antibacterial efficiencies of M S–HA In summary, forsterite–HA composite scaffolds with scaffolds against S. aureus and E. coli were significantly photothermal-induced antibacterial ability have been enhanced, even up to 96.1% and 95.6%, respectively, successfully fabricated through HA deposition on which showed similar antibacterial efficiencies for the 3D-printed polymer-derived forsterite scaffolds via a M S and M S–HA scaffolds at the same irradiation 2 2 hydrothermal method. The morphology of HA coating conditions [12]. Therefore, M S–HA scaffolds still had could be regulated by controlling the hydrothermal excellent photothermal antibacterial ability, and the temperature and pH value of the reaction solution. The antibacterial efficiency could be regulated by controlling HA-coated forsterite scaffolds not only dramatically the laser power density. boosted the proliferation and promoted osteogenic HA coating did not influence the photothermal effect differentiation of rBMSCs on the M S–HA, but also of the M S scaffolds, and thereby endowed the M S–HA 2 2 2 maintained excellent photothermal-induced antibacterial scaffolds with excellent photothermal-induced antibacterial ability under an 808 nm laser irradiation. Therefore, activity. On the other hand, HA coating on the M S such HA-coated forsterite scaffolds showed great scaffolds promoted the osteogenic differentiation of www.springer.com/journal/40145 J Adv Ceram 2021, 10(5): 1095–1106 1105 therapy and bone regeneration. Chem Eng J 2020, 382: potential for bacterial infected bone repair. [14] Tavangarian F, Emadi R. Improving degradation rate and Acknowledgements apatite formation ability of nanostructure forsterite. 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On the not included in the article’s Creative Commons licence and your crystallization of hydroxyapatite under hydrothermal intended use is not permitted by statutory regulation or exceeds conditions: Role of sebacic acid as an additive. ACS Omega the permitted use, you will need to obtain permission directly 2020, 5: 27204–27210. from the copyright holder. [33] Cui BC, Zhang RR, Sun FB, et al. Mechanical and To view a copy of this licence, visit http://creativecommons. org/licenses/by/4.0/. biocompatible properties of polymer-infiltrated-ceramic- www.springer.com/journal/40145

Journal

Journal of Advanced CeramicsSpringer Journals

Published: Oct 1, 2021

Keywords: forsterite scaffolds; hydroxyapatite (HA) coating; bone repair; photothermal effect; antibacterial activity

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