Enhancement of hydroxyapatite dissolution through structure modification by Krypton ion irradiation

doi:10.1016/j.jmst.2019.03.048

Abstract

Abstract:

Hydroxyapatite (HA) synthesized by a wet chemical route was subjected to heavy ion irradiation, using 4 MeV Krypton ion (Kr¹⁷⁺) with ion fluence ranging from 1 × 10¹³ to 1 × 10¹⁵ ions/cm². Glancing incidence X-ray diffraction (GIXRD) results confirmed the phase purity of irradiated HA with a moderate contraction in lattice parameters, and further indicated the irradiation-induced structural disorder, evidenced by broadening of the diffraction peaks. High-resolution transmission electron microscopy (HRTEM) observations indicated that the applied Kr irradiation induced significant damage in the hydroxyapatite lattice. Specifically, cavities were observed with their diameter and density varying with the irradiation fluences, while a radiation-induced crystalline-to-amorphous transition with increasing ion dose was identified. Raman and X-ray photoelectron spectroscopy (XPS) analysis further indicated the presence of irradiation-induced defects. Ion release from pristine and irradiated materials following immersion in Tris (pH 7.4, 37 ℃) buffer showed that dissolution in vitro was enhanced by irradiation, reaching a peak at 0.1dpa. We examined the effects of irradiation on the early stages of the mouse osteoblast-like cells (MC3T3-E) response. A cell counting kit-8 assay (CCK-8 test) was carried out to investigate the cytotoxicity of samples, and viable cells can be observed on the irradiated materials.

Key words: High energy heavy ion irradiation, Hydroxyapatite, HRTEM, Crystal defects, In vitro dissolution, Cell compatibility

Zhu Hui, Guo Dagang, Zang Hang, A.H. Hanaor Dorian, Yu Sen, Schmidt Franziska, Xu Kewei. Enhancement of hydroxyapatite dissolution through structure modification by Krypton ion irradiation[J]. J. Mater. Sci. Technol., 2020, 38: 148-158.

Figures/Tables 12

Fig. 1. (a) 3D surface morphology gradient map of a typical HA coating on a fused silica substrate. (b) Sample fixing setup for ion irradiation. (c) A diagram of irradiation process.

Fig. 2. SRIM simulation of the irradiation induced damage variations and Kr ion distribution with depth. Irradiation on the Cu foil and bulk Cu sample. Pink areas in the figures represent the 100-nm TEM foils and yellow areas represent the 2 μm HA coatings.

Table 1 Correspondence of dpa to ion fluences.

Sample label	Displacements-per-atom	Ion fluence
S0	0	0
S1	0.005 dpa	1 × 10¹³ ions/cm²
S2	0.01 dpa	2 × 10¹³ ions/cm²
S3	0.05 dpa	1 × 10¹⁴ ions/cm²
S4	0.1 dpa	2 × 10¹⁴ ions/cm²
S5	0.5 dpa	1 × 10¹⁵ ions/cm²

Fig. 3. GIXRD spectra of the irradiated and unirradiated HA coatings. Ion fluence: (a) 1 × 1013 to (f) 1 × 1015 ions/cm2.

Fig. 4. (a) Cavities formation and evolution in the HA nanoparticles after irradiation with 4 MeV Kr17+ ions with increasing irradiation fluence at room temperature. (b) Cavity size variations upon the heavy ion fluence from TEM observations. (c) EDS spectrum taken from S0. (d) EDS spectrum taken from S3.

Fig. 5. Typical TEM images of the HA nanoparticles before and after Kr irradiation. (a) unirradiated, (b) 1 × 1013 ions/cm2 (0.005 dpa) and (c) its inverse fast fourier transform, (d) and (e) 2 × 1013 ions/cm2 (0.01 dpa), (f) 1 × 1014 ions/cm2 (0.05 dpa), (g) 2 × 1014 ions/cm2 (0.1 dpa), (h) 1 × 1015 ions/cm2 (0.5 dpa), (i) SAED patterns of the sampels irradiated with various fluences.

Fig. 6. Raman analysis: Spectra of samples irradiated at different doses are shown (a) over the full range of shifts, and in the shift ranges of (b) 350 to 650 cm-1, (c) 890 to 1000 cm-1, (d) 1000 to 1150 cm-1, (e) 3500 to 3650 cm-1. Decay of this band’s intensity, change of its position, and the increase of its breadth as indicated by FWHMs are plotted as a function of ion fluence in (f), (g) and (h) respectively. (i) the area ratio of the radiation-induced broad ν1b band (950 cm-1) to the ν1 band (962 cm-1).

Fig. 7. XPS O 1s spectra for samples with increasing irradiation dose. (a) unirradiated, (b) 1 × 1013 ions/cm2 (0.005 dpa), (c) 2 × 1013 ions/cm2 (0.01 dpa), (d) 1 × 1014 ions/cm2 (0.05 dpa), (E) 2 × 1014 ions/cm2 (0.1 dpa), (f) 1 × 1015 ions/cm2 (0.5 dpa). In each subfigure, black markers show the data points, the solid red line shows the fitted profile and the two shaded areas show the deconvoluted contributions of the two binding energies.

Fig. 8. (a) Calcium and (b) phosphate ions released in Tris-buffer solution from HA discs irradiated by 4 MeV Kr17+ ions with different fluences, with respect to immersion duration. Insets: enlarged view from 30 min to 8 h immersion. (c) Comparison of the ion release of pristine sample and 0.1 dpa irradiated samples. (d) HRTEM pictures of the pristine and 0.1 dpa irradiated samples after immersion for 1 and 2 weeks. Arrows indicate the dissolution starting points.

Fig. 9. Selected SEM images of cultured specimens ((a)-(f) 1 × 1013 to 1 × 1015 ions/cm2) at 24 h after MC3T3-E1 were seeded on their surfaces; (g) cell adhesion of MC3T3-E1 cells on the specimens at 24 h; (h) cell proliferation after cell seeding for 1, 3 and 7 days. The modified OD values at 3 and 7 days were normalized to those at 1 day. * denote p < 0.05.

Table 2 A summary of irradiation damage progression of HA nanoparticles after irradiation.

Irradiation dose	HA crystal stuructures
0	Perfect lattice arrangement
0.005 dpa	Few dislocations and small mottled contrast
0.01 dpa	Grain boundaries and numerous dislocation lines. Considerable number of disorders
0.05 dpa	The original single crystal is broken into isolated crystallites with continuous amorphous phase.
0.1 dpa	Few crystalline regions embedded in the amorphous matrix. Lattice fringe are still visable
0.5 dpa	Completely amorphous HA particles.

Fig. 10. Contact angle measurement of pristine and irradiated specimens with increasing irradiation fluences ((a)-(f) 1 × 1013 to 1 × 1015 ions/cm2).

References

[1]	L.L. Hench, J.M. Polak, Science 295 (2002) 1014-1017.
[2]	T. Thamaraiselvi, S. Rajeswari, Carbon 24 (2004) 172.
[3]	P. Ducheyne, J.M. Cuckler, Clin. Orthop. Relat. Res. 276 (1992) 102-114.
[4]	F.B. Bagambisa, U. Joos, W. Schilli, J. Biomed. Mater. Res. 27 (1993) 1047-1055.
[5]	R.Z. LeGeros, Clin. Orthop.Relat. Res. 395 (2002) 81-98.
[6]	M. Nagano, T. Nakamura, T. Kokubo, M. Tanahashi, M. Ogawa, Biomaterials 17 (1996) 1771-1777.
[7]	J. Lu, M. Descamps, J. Dejou, G. Koubi, P. Hardouin, J. Lemaitre, J.P. Proust, J. Biomed. Mater. Res. 63 (2002) 408-412.
[8]	H. Zhu, D. Guo, W. Qi, K. Xu,Biomed. Mater. 12 (2017), 015016.
[9]	S. Takagi, L.C. Chow, J. Mater. Sci. Mater. Med. 12 (2001) 135-139.
[10]	B.S. Chang, C.K. Lee, K.S. Hong, H.J. Youn, H.S. Ryu, S.S. Chung, K.W. Park, Biomaterials 21 (2000) 1291-1298.
[11]	H. Wang, L. Jong-Kook, M. Amr, J.J. Lannutti, J. Biomed. Mater. Res. A 67A (2003) 599-608.
[12]	W. Xue, L.X. Zheng, J. Biomed. Mater. Res. A 74A (2010) 553-561.
[13]	A.E. Porter, C.M. Botelho, M.A. Lopes, J.D. Santos, S.M. Best, W. Bonfield, J. Biomed. Mater. Res. A 69 (2004) 670-679.
[14]	A.E. Porter, S.M. Best, W. Bonfield, J. Biomed. Mater. Res. A 68 (2004) 133-141.
[15]	A.E. Porter, N. Patel, J.N. Skepper, S.M. Best, W. Bonfield, Biomaterials 24 (2003) 4609-4620.
[16]	G. Daculsi, B. Kerebel, J. Biol. Buccale 5 (1977) 203-218.
[17]	A. Krajewski, A. Ravaglioli, S. Wen, J. Feng, J. Appl. Crystallogr. 25 (1992) 465-470.
[18]	G. Daculsi, B. Kerebel, L.M. Kerebel, Caries Res. 13 (1979) 277-289.
[19]	S. Kuriakose, D. Avasthi, S. Mohapatra, Beilstein J. Nanotechnol. 6 (2015) 928.
[20]	B.D. Begg, N.J. Hess, W.J. Weber, R. Devanathan, J.P. Icenhower, S. Thevuthasan, B.P. McGrail, J. Nucl.Mater. 288 (2001) 208-216.
[21]	A.R. Ananda Sagari, P. Rahkila, M. Väisänen, R. Lehto, T. Sajavaara, S. Gorelick, M. Laitinen, M. Putkonen, S. Sangyuenyongpipat, J. Timonen, S. Cheng, H.J. Whitlow, Nucl. Instrum. Methods Phys. Res. B 266 (2008) 2515-2519.
[22]	K. Elayaraja, P. Rajesh, M.I. Ahymah Joshy, V. Sarath Chandra, R.V. Suganthi, J. Kennedy, P.K. Kulriya, I. Sulania, K. sokan, D. Kanjilal, D.K. Avasthi, H.K. Varma, S. Narayana Kalkura, Mater. Chem. Phys. 134 (2012) 464-477.
[23]	C.M. Lopatin, T.L. Alford, V.B. Pizziconi, M. Kuan, T. Laursen, Nucl. Instrum. Methods Phys. Res. B 145 (1998) 522-531.
[24]	V. Nelea, H. Pelletier, D. Müller, N. Broll, P. Mille, C. Ristoscu, I.N. Mihailescu, Appl. Surf. Sci. 186 (2002) 483-489.
[25]	K. Elayaraja, M.I.A. Joshy, R.V. Suganthi, S.N. Kalkura, M. Palanichamy, M. Ashok, V.V. Sivakumar, P.K. Kulriya, I. Sulania, D. Kanjilal, K. Asokan, Appl. Surf. Sci. 257 (2011) 2134-2141.
[26]	R.V. Suganthi, S. Prakash Parthiban, K. Elayaraja, E.K. Girija, P. Kulariya, Y.S. Katharria, F. Singh, K. Asokan, D. Kanjilal, S. Narayana Kalkura, J. Mater. Sci. Mater. Med. 20 (2008) 271.
[27]	D. Guo, Y.Z. Hao, H.Y. Li, C.Q. Fang, L.J. Sun, H. Zhu, J. Wang, X.F. Huang, P.F. Ni, K.W. Xu, J. Biomed. Mater. Res. Part B Appl.Biomater. 101 (2013) 1275-1283.
[28]	G.S. Was, J. Mater. Res. 30 (2015) 1158-1182.
[29]	B.J.P. Ziegler J F, 2008 Program TRIM. <.
[30]	L.M. Wang, R.C. Ewing, M. Cameron, W.J. Weber, In situ observation of radiation induced amorphization of crystals with apatite structure, Spring Meeting Mater. Res. Soc. (1993).
[31]	O. Lehtinen, T. Nikitin, A.V. Krasheninnikov, L.T. Sun, F. Banhart, L. Khriachtchev, J. Keinonen, New J. Phys. 13 (2011) 19.
[32]	J.X. Xue, G.J. Zhang, L.P. Guo, H.B. Zhang, X.G. Wang, J. Zou, S.M. Peng, X.G. Long, J. Eur. Ceram. Soc. 34 (2013) 633-639.
[33]	C.N.S.M.C.AQSIQ GB/T16886.14-2003 Medical Biological Evaluation, Part 14: Degradation Product of Pottery and Porcelain Qualitative and Quantitative, Standards Press of China, 2003.
[34]	W. Gong, L. Wang, R. Ewing, J. Appl. Phys. 84 (1998) 4204-4208.
[35]	P. Houllé, J.C. Voegel, P. Schultz, P. Steuer, F.J. Cuisinier, J. Dent. Res. 76 (1997) 895-904.
[36]	P. Comodi, Y. Liu, M.L. Frezzotti, Phys. Chem. Miner. 28 (2001) 225-231.
[37]	S. Miro, J. Costantini, J. Bardeau, D. Chateigner, F. Studer, E. Balanzat, J. Raman Spectrosc. 42 (2011) 2036-2041.
[38]	C. Weikusat, U.A. Glasmacher, B. Schuster, C. Trautmann, R. Miletich, R. Neumann, Phys. Chem. Miner. 38 (2011) 293-303.
[39]	F. Villa, M. Grivet, M. Rebetez, C. Dubois, A. Chambaudet, N. Chevarier, G. Blondiaux, T. Sauvage, M. Toulemonde, Nucl. Instrum. Methods Phys. Res. B 168 (2000) 72-77.
[40]	M. Toulemonde, Applied Radiation, Isotopes. 46 (1995) 375-381.
[41]	J. Liu, U.A. Glasmacher, M. Lang, C. Trautmann, K.O. Voss, R. Neumann, G.A. Wagner, R. Miletich, Appl. Phys. A 91 (2008) 17-22.
[42]	M.A. Baker, S.L. Assis, O.Z. Higa, I. Costa, Acta Biomater. 5 (2009) 63-75.
[43]	R.S. Lubna, A. Bakhtyar, Z. Hao, W.G. Wang, Y.Q. Song, H.W. Zhang, S.I. Shah, J.Q. Xiao,J. Phys. Condens.Matter 21 (2009), 486004.
[44]	J.F. Ziegler, J.P. Biersack, M.D. Ziegler, SRIM : The Stopping and Range of Ions in Matter, SRIM, Chester (Md.), 2008.
[45]	J. Reyes-Gasga, R. Garcia-Garcia, E. Brès, Physica B Condens. Matter 404 (2009) 1867-1873.
[46]	M. Fell, S.M. Murphy, J. Nucl. Mater. 172 (1990) 1-12.
[47]	B. Bharti, S. Kumar, H.-N. Lee, R. Kumar, Sci. Rep. 6 (2016) 32355.
[48]	K.I. Maslakov, Y.A. Teterin, A.J. Popel, A.Y. Teterin, K.E. Ivanov, S.N. Kalmykov, V.G. Petrov, P.K. Petrov, I. Farnan, Appl. Surf. Sci. 448 (2018) 154-162.
[49]	S.T. Rosinski, M.L. Grossbeck, T.R. Allen, A.S. Kumar, Effects of Radiation on Materials: 20th International Symposium, ASTM International, 2001.
[50]	T. Lu, L. Lin, X. Zu, S. Zhu, L. Wang, Nucl. Instrum. Methods Phys. Res. B 218 (2004) 111-116.
[51]	S. Zinkle, S. Kojima, Nucl. Instrum. Methods Phys. Res. B 46 (1990) 165-170.
[52]	X. Yan, Y. Li, J. Zhao, Y. Li, G. Bai, S. Zhu,Appl. Phys. Lett. 108 (2016), 033108.
[53]	L. Wang, W. Weber, Philos. Mag. A 79 (1999) 237-253.
[54]	K. Elayaraja, P. Rajesh, M.A. Joshy, V.S. Chandra, R. Suganthi, J. Kennedy, P. Kulriya, I. Sulania, K. Asokan, D. Kanjilal, Mater. Chem. Phys. 134 (2012) 464-477.
[55]	I. De Wolf, Semicond. Sci. Technol. 11 (1996) 139.
[56]	Z. Mohammadi, A. Ziaei-Moayyed, A.S.-M. Mesgar,Biomed. Mater. 3 (2008), 015006.
[57]	J. Arends, W.L. Jongebloed, Caries Res. 11 (1977) 186-188.
[58]	S.V. Dorozhkin, Prog. Cryst. Growth Charact.Mater. 44 (2002) 45-61.
[59]	S.C. Cox, P. Jamshidi, L.M. Grover, K.K. Mallick, J. Mater. Sci. Mater. Med. 25 (2014) 37-46.
[60]	S. Samavedi, A.R. Whittington, A.S. Goldstein, Acta Biomater. 9 (2013) 8037-8045.
[61]	T.J. Webster, L.S. Schadler, R.W. Siegel, R. Bizios, Tissue Eng. 7 (2001) 291-301.