·
REVIEW
·

In silico modelling of the corrosion of biodegradable magnesium-based biomaterials: modelling approaches, validation and future perspectives

Aditya Joshi1 George Dias2 Mark P. Staiger1*
Show Less
1 Department of Mechanical Engineering, University of Canterbury, Christchurch, New Zealand
2 Department of Anatomy, University of Otago, Dunedin, New Zealand
Submitted: 6 September 2021 | Revised: 10 September 2021 | Accepted: 13 September 2021 | Published: 28 September 2021
Copyright © 2021 by the Author(s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution–NonCommercial–ShareAlike 4.0 License.
Abstract

Metallic biomedical implants based on magnesium, zinc and iron alloys have emerged as bioresorbable alternatives to permanent orthopaedic implants over the last two decades. The corrosion rate of biodegradable metals plays a critical role in controlling the compatibility and functionality of the device in vivo. The broader adoption of biodegradable metals in orthopaedic applications depends on developing in vitro methods that accurately predict the biodegradation behaviour in vivo. However, the physiological environment is a highly complex corrosion environment to replicate in the laboratory, making the in vitro-to-in vivo translation of results very challenging. Accordingly, the results from in vitro corrosion tests fail to provide a complete schema of the biodegradation behaviour of the metal in vivo. In silico approach based on computer simulations aim to bridge the observed differences between experiments performed in vitro and vivo. A critical review of the state-of-the-art of computational modelling techniques for predicting the corrosion behaviour of magnesium alloy as a biodegradable metal is presented.

Keywords
biomaterial ; biodegradation ; corrosion ; finite element method ; magnesium ; modelling
References

Below is the content of the Citations in the paper which has been de-formatted, however, the content stays consistent with the original.

1. Geetha, M.; Singh, A. K.; Asokamani, R.; Gogia, A. K. Ti based biomaterials, the ultimate choice for orthopaedic implants – A review. Prog Mater Sci. 2009, 54, 397-425.  
2. Nagels, J.; Stokdijk, M.; Rozing, P. M. Stress shielding and bone resorption in shoulder arthroplasty. J Shoulder Elbow Surg. 2003, 12, 35-39.  
3. Orringer, J. S.; Barcelona, V.; Buchman, S. R. Reasons for removal of rigid internal fixation devices in craniofacial surgery. J Craniofac Surg. 1998, 9, 40-44.  
4. Francel, T. J.; Birely, B. C.; Ringelman, P. R.; Manson, P. N. The fate of plates and screws after facial fracture reconstruction. Plast Reconstr Surg. 1992, 90, 568-573.  
5. Fearon, J. A.; Munro, I. R.; Bruce, D. A. Observations on the use of rigid fixation for craniofacial deformities in infants and young children. Plast Reconstr Surg. 1995, 95, 634-637; discussion 638.  
6. Yu, J. C.; Bartlett, S. P.; Goldberg, D. S.; Gannon, F.; Hunter, J.; Habecker, P.; Whitaker, L. A. An experimental study of the effects of craniofacial growth on the long-term positional stability of microfixation. J Craniofac Surg. 1996, 7, 64-68.  
7. Puleo, D. A.; Huh, W. W. Acute toxicity of metal ions in cultures of osteogenic cells derived from bone marrow stromal cells. J Appl Biomater. 1995, 6, 109-116.  
8. Jacobs, J. J.; Gilbert, J. L.; Urban, R. M. Corrosion of metal orthopaedic implants. J Bone Joint Surg Am. 1998, 80, 268-282.  
9. Lhotka, C.; Szekeres, T.; Steffan, I.; Zhuber, K.; Zweymüller, K. Four-year study of cobalt and chromium blood levels in patients managed with two different metal-on-metal total hip replacements. J Orthop Res. 2003, 21, 189-195.  
10. Jacobs, J. J.; Skipor, A. K.; Patterson, L. M.; Hallab, N. J.; Paprosky, W. G.; Black, J.; Galante, J. O. Metal release in patients who have had a primary total hip arthroplasty. A prospective, controlled, longitudinal study. J Bone Joint Surg Am. 1998, 80, 1447-1458.  
11. Park, J. B.; Kim, Y. K. Metallic Biomaterials. In Biomaterials, Wong, J. Y.; Bronzino, J. D., Eds.; CRC Press: Boca Raton, 2007; pp 1-22.  
12. Gilardino, M. S.; Chen, E.; Bartlett, S. P. Choice of internal rigid fixation materials in the treatment of facial fractures. Craniomaxillofac Trauma Reconstr. 2009, 2, 49-60.  
13. Grünewald, T. A.; Rennhofer, H.; Hesse, B.; Burghammer, M.; Stanzl-Tschegg, S. E.; Cotte, M.; Löffler, J. F.; Weinberg, A. M.; Lichtenegger, H. C. Magnesium from bioresorbable implants: Distribution and impact on the nano- and mineral structure of bone. Biomaterials. 2016, 76, 250-260.  
14. Chen, Y.; Xu, Z.; Smith, C.; Sankar, J. Recent advances on the development of magnesium alloys for biodegradable implants. Acta Biomater. 2014, 10, 4561-4573.  
15. Rahim, M. I.; Ullah, S.; Mueller, P. P. Advances and challenges of biodegradable implant materials with a focus on magnesium-alloys and bacterial infections. Metals. 2018, 8, 532.  
16. Staiger, M. P.; Pietak, A. M.; Huadmai, J.; Dias, G. Magnesium and its alloys as orthopedic biomaterials: a review. Biomaterials. 2006, 27, 1728-1734.  
17. Witte, F.; Fischer, J.; Nellesen, J.; Crostack, H. A.; Kaese, V.; Pisch, A.; Beckmann, F.; Windhagen, H. In vitro and in vivo corrosion measurements of magnesium alloys. Biomaterials. 2006, 27, 1013-1018.  
18. McBride, E. D. Absorbable metal in bone surgery: A further report on the use of magnesium alloys. J Am Med Assoc. 1938, 111, 2464-2467.  
19. Witte, F. Reprint of: The history of biodegradable magnesium implants: A review. Acta Biomater. 2015, 23 Suppl, S28-40.  
20. Badar, M.; Lünsdorf, H.; Evertz, F.; Rahim, M. I.; Glasmacher, B.; Hauser, H.; Mueller, P. P. The formation of an organic coat and the release of corrosion microparticles from metallic magnesium implants. Acta Biomater. 2013, 9, 7580-7589.  
21. Han, P.; Cheng, P.; Zhang, S.; Zhao, C.; Ni, J.; Zhang, Y.; Zhong, W.; Hou, P.; Zhang, X.; Zheng, Y.; Chai, Y. In vitro and in vivo studies on the degradation of high-purity Mg (99.99wt.%) screw with femoral intracondylar fractured rabbit model. Biomaterials. 2015, 64, 57-69.  
22. Plaass, C.; von Falck, C.; Ettinger, S.; Sonnow, L.; Calderone, F.; Weizbauer, A.; Reifenrath, J.; Claassen, L.; Waizy, H.; Daniilidis, K.; Stukenborg-Colsman, C.; Windhagen, H. Bioabsorbable magnesium versus standard titanium compression screws for fixation of distal metatarsal osteotomies - 3 year results of a randomized clinical trial. J Orthop Sci. 2018, 23, 321-327.  
23. Seitz, J.-M.; Lucas, A.; Kirschner, M. Magnesium-based compression screws: a novelty in the clinical use of implants. JOM. 2016, 68, 1177-1182.  
24. Rapetto, C.; Leoncini, M. Magmaris: a new generation metallic sirolimus-eluting fully bioresorbable scaffold: present status and future perspectives. J Thorac Dis. 2017, 9, S903-s913.  
25. Noviana, D.; Paramitha, D.; Ulum, M. F.; Hermawan, H. The effect of hydrogen gas evolution of magnesium implant on the postimplantation mortality of rats. J Orthop Translat. 2016, 5, 9-15.  
26. Loukil, N. Alloying elements of magnesium alloys: a literature review. In Magnesium alloys structure and properties, Tański, T. A.; Jarka, P., eds.; IntechOpen Limited: London, 2021.  
27. Liu, C.; Xin, Y.; Tang, G.; Chu, P. K. Influence of heat treatment on degradation behavior of bio-degradable die-cast AZ63 magnesium alloy in simulated body fluid. Mater Sci Eng A. 2007, 456, 350-357.  
28. Wang, Y.; Liu, G.; Fan, Z. A new heat treatment procedure for rheo-diecast AZ91D magnesium alloy. Scripta Mater. 2006, 54, 903-908.  
29. Zeng, R. C.; Zhang, J.; Huang, W.J.; Dietzel, W.; Kainer, K. U.; Blawert, C.; Ke, W. Review of studies on corrosion of magnesium alloys. Trans Nonfer Metals Soc China. 2006, 16, s763-s771.  
30. Hornberger, H.; Virtanen, S.; Boccaccini, A. R. Biomedical coatings on magnesium alloys - a review. Acta Biomater. 2012, 8, 2442-2455.  
31. Gray, J. E.; Luan, B. Protective coatings on magnesium and its alloys — a critical review. J Alloys Compd. 2002, 336, 88-113.  
32. Gonzalez, J.; Hou, R. Q.; Nidadavolu, E. P. S.; Willumeit-Römer, R.; Feyerabend, F. Magnesium degradation under physiological conditions - Best practice. Bioact Mater. 2018, 3, 174-185.  
33. Barfield, W. R.; Colbath, G.; DesJardins, J. D.; An, Y. H.; Hartsock, L. A. The potential of magnesium alloy use in orthopaedic surgery. Curr Orthop Pract. 2012, 23, 146-150.  
34. Martinez Sanchez, A. H.; Luthringer, B. J.; Feyerabend, F.; Willumeit, R. Mg and Mg alloys: how comparable are in vitro and in vivo corrosion rates? A review. Acta Biomater. 2015, 13, 16-31.  
35. Baino, F.; Yamaguchi, S. The use of simulated body fluid (SBF) for assessing materials bioactivity in the context of tissue engineering: review and challenges. Biomimetics (Basel). 2020, 5, 57.  
36. Song, G. L.; Atrens, A. Corrosion mechanisms of magnesium alloys. Adv Eng Mater. 1999, 1, 11-33.  
37. Zeng, R. C.; Yin, Z. Z.; Chen, X. B.; Xu, D. K. Corrosion Types of Magnesium Alloys. In Magnesium Alloys, Tański, T.; Borek, W.; Król, M., eds.; IntechOpen Limited: London, 2018.  
38. Li, W.; Li, N.; Zheng, Y.; Yuan, G. Fretting properties of biodegradable Mg-Nd-Zn-Zr alloy in air and in Hank’s solution. Sci Rep. 2016, 6, 35803.  
39. Ghali, E.; Dietzel, W.; Kainer, K. U. General and localized corrosion of magnesium alloys: A critical review. J Mater Eng Perform. 2004, 13, 7-23.  
40. Choudhary, L.; Singh Raman, R. K.; Hofstetter, J.; Uggowitzer, P. J. In-vitro characterization of stress corrosion cracking of aluminium-free magnesium alloys for temporary bio-implant applications. Mater Sci Eng C Mater Biol Appl. 2014, 42, 629-636.  
41. Song, R. G.; Blawert, C.; Dietzel, W.; Atrens, A. A study on stress corrosion cracking and hydrogen embrittlement of AZ31 magnesium alloy. Mater Sci Eng A. 2005, 399, 308-317.  
42. Galvin, E.; O’Brien, D.; Cummins, C.; Mac Donald, B. J.; Lally, C. A strain-mediated corrosion model for bioabsorbable metallic stents. Acta Biomater. 2017, 55, 505-517.  
43. Törne, K.; Örnberg, A.; Weissenrieder, J. Influence of strain on the corrosion of magnesium alloys and zinc in physiological environments. Acta Biomater. 2017, 48, 541-550.  
44. Winzer, N.; Atrens, A.; Dietzel, W.; Raja, V. S.; Song, G.; Kainer, K. U. Characterisation of stress corrosion cracking (SCC) of Mg–Al alloys. Mater Sci Eng A. 2008, 488, 339-351.  
45. Snir, Y.; Ben-Hamu, G.; Eliezer, D.; Abramov, E. Effect of compression deformation on the microstructure and corrosion behavior of magnesium alloys. J Alloys Compd. 2012, 528, 84-90.  
46. Sezer, N.; Evis, Z.; Kayhan, S. M.; Tahmasebifar, A.; Koç, M. Review of magnesium-based biomaterials and their applications. J Magnes Alloys. 2018, 6, 23-43.  
47. Kutz, M. Handbook of Materials Selection. John Wiley & Sons, Inc.: 2002.  
48. Song, G.; Atrens, A. Understanding magnesium corrosion—a framework for improved alloy performance. Adv Eng Mater. 2003, 5, 837-858.  
49. Yin Yee Chin, P.; Cheok, Q.; Glowacz, A.; Caesarendra, W. A review of in-vivo and in-vitro real-time corrosion monitoring systems of biodegradable metal implants. Appl Sci. 2020, 10.  
50. Yin Yee Chin, P.; Cheok, Q.; Glowacz, A.; Caesarendra, W. A review of in-vivo and in-vitro real-time corrosion monitoring systems of biodegradable metal implants. Appl Sci. 2020, 10, 3141.  
51. Wang, W.; Wu, H.; Zan, R.; Sun, Y.; Blawert, C.; Zhang, S.; Ni, J.; Zheludkevich, M. L.; Zhang, X. Microstructure controls the corrosion behavior of a lean biodegradable Mg-2Zn alloy. Acta Biomater. 2020, 107, 349-361.  
52. Walter, R.; Kannan, M. B. Influence of surface roughness on the corrosion behaviour of magnesium alloy. Mater Des. 2011, 32, 2350-2354.  
53. Mitchell, J.; Crow, N.; Nieto, A. Effect of surface roughness on pitting corrosion of AZ31 Mg alloy. Metals. 2020, 10, 651.  
54. Jiang, P.; Blawert, C.; Zheludkevich, M. L. The corrosion performance and mechanical properties of Mg-Zn based alloys—a review. Corros Mater Degrad. 2020, 1, 92-158.  
55. Eliezer, A.; Gutman, E. M.; Abramov, E.; Aghion, E. Corrosion fatigue and mechanochemical behavior of magnesium alloys. Corros Rev. 1998, 16, 1-26.  
56. Melchers, R. E.; Jeffrey, R. J. Probabilistic models for steel corrosion loss and pitting of marine infrastructure. Reliab Eng Syst Saf. 2008, 93, 423-432.  
57. Li, S. X.; Yu, S. R.; Zeng, H. L.; Li, J. H.; Liang, R. Predicting corrosion remaining life of underground pipelines with a mechanically-based probabilistic model. J Pet Sci Eng. 2009, 65, 162-166.  
58. Radouani, R.; Echcharqy, Y.; Essahli, M. Numerical simulation of galvanic corrosion between carbon steel and low alloy steel in a bolted joint. Int J Corros. 2017, 2017, 6174904.  
59. Deshpande, K. B. Validated numerical modelling of galvanic corrosion for couples: magnesium alloy (AE44)–mild steel and AE44–aluminium alloy (AA6063) in brine solution. Corros Sci. 2010, 52, 3514-3522.  
60. Xue, Y.; Horstemeyer, M. F.; McDowell, D. L.; El Kadiri, H.; Fan, J. Microstructure-based multistage fatigue modeling of a cast AE44 magnesium alloy. Int J Fatigue. 2007, 29, 666-676.  
61. Saito, K.; Kuniya, J. Mechanochemical model to predict stress corrosion crack growth of stainless steel in high temperature water. Corros Sci. 2001, 43, 1751-1766.  
62. Wenman, M. R.; Trethewey, K. R.; Jarman, S. E.; Chard-Tuckey, P. R. A finite-element computational model of chloride-induced transgranular stress-corrosion cracking of austenitic stainless steel. Acta Mater. 2008, 56, 4125-4136.  
63. da Costa-Mattos, H. S.; Bastos, I. N.; Gomes, J. A. C. P. A simple model for slow strain rate and constant load corrosion tests of austenitic stainless steel in acid aqueous solution containing sodium chloride. Corros Sci. 2008, 50, 2858-2866.  
64. Bolotin, V. V.; Shipkov, A. A. Mechanical aspects of corrosion fatigue and stress corrosion cracking. Int J Solids Struct. 2001, 38, 7297-7318.  
65. Garud, Y. S. Quantitative evaluation of environmentally assisted cracking: a survey of developments and application of modeling concepts. J Pressure Vessel Technol. 1991, 113, 1-9.  
66. Gutman, E. M. Mechanochemistry of materials. Cambridge International Science Publishing Ltd: Cambridge, 1998.  
67. Movchan, T. G.; Esipova, N. E.; Eryukin, P. V.; Uriev, N. B.; Rusanov, A. I. Mechanochemical effects in processes of corrosion of metals. Russ J Gen Chem. 2005, 75, 1681-1686.  
68. Gastaldi, D.; Sassi, V.; Petrini, L.; Vedani, M.; Trasatti, S.; Migliavacca, F. Continuum damage model for bioresorbable magnesium alloy devices - application to coronary stents. J Mech Behav Biomed Mater. 2011, 4, 352-365.  
69. Kachanov, L. M. Introduction to continuum damage mechanics. Springer Netherlands: 1986.  
70. Lévesque, J.; Hermawan, H.; Dubé, D.; Mantovani, D. Design of a pseudo-physiological test bench specific to the development of biodegradable metallic biomaterials. Acta Biomater. 2008, 4, 284-295.  
71. Myrissa, A.; Agha, N. A.; Lu, Y.; Martinelli, E.; Eichler, J.; Szakács, G.; Kleinhans, C.; Willumeit-Römer, R.; Schäfer, U.; Weinberg, A. M. In vitro and in vivo comparison of binary Mg alloys and pure Mg. Mater Sci Eng C Mater Biol Appl. 2016, 61, 865-874.  
72. Antoniac, I.; Adam, R.; Biță, A.; Miculescu, M.; Trante, O.; Petrescu, I. M.; Pogărășteanu, M. Comparative assessment of in vitro and in vivo biodegradation of Mg-1Ca magnesium alloys for orthopedic applications. Materials (Basel). 2020, 14, 84.  
73. Grogan, J. A.; O’Brien, B. J.; Leen, S. B.; McHugh, P. E. A corrosion model for bioabsorbable metallic stents. Acta Biomater. 2011, 7, 3523-3533.  
74. Abdalla, M.; Joplin, A.; Elahinia, M.; Ibrahim, H. Corrosion modeling of magnesium and its alloys for biomedical applications: review. Corros Mater Degrad. 2020, 1, 219-248.  
75. Oppeel, A. Experimental characterisation and finite element modeling of biodegradable magnesium stents. Ghent University: Ghent, 2014.  
76. Debusschere, N.; Segers, P.; Dubruel, P.; Verhegghe, B.; De Beule, M. A Computational framework to model degradation of biocorrodible metal stents using an implicit finite element solver. Ann Biomed Eng. 2016, 44, 382-390.  
77. Amerinatanzi, A.; Mehrabi, R.; Ibrahim, H.; Dehghan, A.; Shayesteh Moghaddam, N.; Elahinia, M. Predicting the biodegradation of magnesium alloy implants: modeling, parameter identification, and validation. Bioengineering (Basel, Switzerland). 2018, 5, 105.  
78. Wu, W.; Gastaldi, D.; Yang, K.; Tan, L.; Petrini, L.; Migliavacca, F. Finite element analyses for design evaluation of biodegradable magnesium alloy stents in arterial vessels. Mater Sci Eng B. 2011, 176, 1733-1740.  
79. Manivasagam, G.; Dhinasekaran, D.; Rajamanickam, A. Biomedical implants: corrosion and its prevention - a review. Recent Patents Corros Sci. 2010, 2, 40-54.  
80. Kasemo, B.; Lausmaa, J. Surface science aspects on inorganic biomaterials. CRC Crit Rev Clin Neurobiol. 1986, 4, 335-380.  
81. Deshpande, K. B. Numerical modeling of micro-galvanic corrosion. Electrochim Acta. 2011, 56, 1737-1745.  
82. Montoya, R.; Iglesias, C.; Escudero, M. L.; García-Alonso, M. C. Modeling in vivo corrosion of AZ31 as temporary biodegradable implants. Experimental validation in rats. Mater Sci Eng C Mater Biol Appl. 2014, 41, 127-133.  
83. Scheiner, S.; Hellmich, C. Stable pitting corrosion of stainless steel as diffusion-controlled dissolution process with a sharp moving electrode boundary. Corros Sci. 2007, 49, 319-346.  
84. Grogan, J. A.; Leen, S. B.; McHugh, P. E. A physical corrosion model for bioabsorbable metal stents. Acta Biomater. 2014, 10, 2313-2322.  
85. Dahms, M.; Höche, D.; Ahmad Agha, N.; Feyerabend, F.; Willumeit-Römer, R. A simple model for long-time degradation of magnesium under physiological conditions. Mater Corros. 2018, 69, 191-196.  
86. Bajger, P.; Ashbourn, J. M. A.; Manhas, V.; Guyot, Y.; Lietaert, K.; Geris, L. Mathematical modelling of the degradation behaviour of biodegradable metals. Biomech Model Mechanobiol. 2017, 16, 227-238.  
87. Birbilis, N.; Easton, M. A.; Sudholz, A. D.; Zhu, S. M.; Gibson, M. A. On the corrosion of binary magnesium-rare earth alloys. Corros Sci. 2009, 51, 683-689.  
88. Shen, Z.; Zhao, M.; Bian, D.; Shen, D.; Zhou, X.; Liu, J.; Liu, Y.; Guo, H.; Zheng, Y. Predicting the degradation behavior of magnesium alloys with a diffusion-based theoretical model and in vitro corrosion testing. J Mater Sci Technol. 2019, 35, 1393-1402.  
89. Ornelas-Tellez, F.; Rico-Melgoza, J. J.; Villafuerte, A. E.; Zavala-Mendoza, F. J. Chapter 3 - Neural networks: a methodology for modeling and control design of dynamical systems. In Artificial neural networks for engineering applications, Alanis, A. Y.; Arana-Daniel, N.; López-Franco, C., eds.; Academic Press: 2019; pp 21-38.  
90. Bulutsuz, A. G.; Yetilmezsoy, K.; Durakbasa, N. Application of fuzzy logic methodology for predicting dynamic measurement errors related to process parameters of coordinate measuring machines. J Intell Fuzzy Syst. 2015, 29, 1619-1633.  
91. Kamrunnahar, M.; Urquidi-Macdonald, M. Prediction of corrosion behaviour of Alloy 22 using neural network as a data mining tool. Corros Sci. 2011, 53, 961-967.  
92. Kirkland, N. T.; Staiger, M. P.; Nisbet, D.; Davies, C. H. J.; Birbilis, N. Performance-driven design of Biocompatible Mg alloys. JOM. 2011, 63, 28-34.  
93. Birbilis, N.; Cavanaugh, M. K.; Sudholz, A. D.; Zhu, S. M.; Easton, M. A.; Gibson, M. A. A combined neural network and mechanistic approach for the prediction of corrosion rate and yield strength of magnesium-rare earth alloys. Corros Sci. 2011, 53, 168-176.  
94. Willumeit, R.; Feyerabend, F.; Huber, N. Magnesium degradation as determined by artificial neural networks. Acta Biomater. 2013, 9, 8722-8729.  
95. Xia, X.; Nie, J. F.; Davies, C. H. J.; Tang, W. N.; Xu, S. W.; Birbilis, N. An artificial neural network for predicting corrosion rate and hardness of magnesium alloys. Mater Des. 2016, 90, 1034-1043.  
96. Alhumade, H.; Rezk, H.; Nassef, A. M.; Al-Dhaifallah, M. Fuzzy logic based-modeling and parameter optimization for improving the corrosion protection of stainless steel 304 by epoxy-graphene composite. IEEE Access. 2019, 7, 100899-100909.  
97. Nava-Dino, C. G.; Orozco-Carmona, V. M.; Monreal-Romero, H. A.; Martínez-García, E. A.; Bautista-Margulis; Neri-Flores, M. A.; Chacón-Nava, J. G.; Martínez-Villafañe, A. Fuzzy sets and electrochemical noise to predict corrosion behavior of Ti alloys. Int J Electrochem Sci. 2013, 8, 4996-5006.  
98. Bahmani, A.; Arthanari, S.; Shin, K. S. Formulation of corrosion rate of magnesium alloys using microstructural parameters. J Magnes Alloys. 2020, 8, 134-149.  
99. Mei, D.; Lamaka, S. V.; Lu, X.; Zheludkevich, M. L. Selecting medium for corrosion testing of bioabsorbable magnesium and other metals – a critical review. Corros Sci. 2020, 171, 108722.  
100. ASTM G31-21. Standard Guide for Laboratory Immersion Corrosion Testing of Metals. ASTM International: West Conshohocken, 2021.  
101. ASTM G1-03(2017)e1. Standard Practice for Preparing, Cleaning, and Evaluating Corrosion Test Specimens. ASTM International: West Conshohocken, 2017.  
102. Song, G.; Atrens, A.; StJohn, D. An hydrogen evolution method for the estimation of the corrosion rate of magnesium alloys. In Magnesium technology, Hryn, J. N., ed. John Wiley & Sons, Inc.: 2001.  
103. Kray, R. H. Modified hydrogen evolution method for metallic magnesium, aluminum, and zinc. Ind Eng Chem Anal Ed. 1934, 6, 250-251.  
104. Sekar, P.; S, N.; Desai, V. Recent progress in in vivo studies and clinical applications of magnesium based biodegradable implants – A review. J Magnes Alloys. 2021, 9, 1147-1163.  
105. Gao, X.; Dai, C. Y.; Jia, Q.; Zhai, C.; Shi, H.; Yang, Y.; Zhao, B. C.; Cai, H.; Lee, E. S.; Jiang, H. B. In vivo corrosion behavior of biodegradable magnesium alloy by MAF treatment. Scanning. 2021, 2021, 5530788.  
106. Kawamura, N.; Nakao, Y.; Ishikawa, R.; Tsuchida, D.; Iijima, M. Degradation and biocompatibility of AZ31 magnesium alloy implants in vitro and in vivo: a micro-computed tomography study in rats. Materials (Basel). 2020, 13, 473.  
107. Xu, Y.; Meng, H.; Yin, H.; Sun, Z.; Peng, J.; Xu, X.; Guo, Q.; Xu, W.; Yu, X.; Yuan, Z.; Xiao, B.; Wang, C.; Wang, Y.; Liu, S.; Lu, S.; Wang, Z.; Wang, A. Quantifying the degradation of degradable implants and bone formation in the femoral condyle using micro-CT 3D reconstruction. Exp Ther Med. 2018, 15, 93-102.  
108. Wang, X.; Shao, X.; Dai, T.; Xu, F.; Zhou, J. G.; Qu, G.; Tian, L.; Liu, B.; Liu, Y. In vivo study of the efficacy, biosafety, and degradation of a zinc alloy osteosynthesis system. Acta Biomater. 2019, 92, 351-361.  
109. Thorngren, K. G. Proceedings of the Swedish Orthopedic Society Helsingborg, June 1-2, 1987. Acta Orthop Scand. 1988, 59, 77-100.  
110. Wang, Z. L.; Yu, S.; Sether, L. A.; Haughton, V. M. Incidence of unfused ossicles in the lumbar facet joints: CT, MR, and cryomicrotomy study. J Comput Assist Tomogr. 1989, 13, 594-597.  
111. Kapadia, R. D.; Stroup, G. B.; Badger, A. M.; Koller, B.; Levin, J. M.; Coatney, R. W.; Dodds, R. A.; Liang, X.; Lark, M. W.; Gowen, M. Applications of micro-CT and MR microscopy to study pre-clinical models of osteoporosis and osteoarthritis. Technol Health Care. 1998, 6, 361-372.  
112. Ding, M.; Odgaard, A.; Hvid, I. Accuracy of cancellous bone volume fraction measured by micro-CT scanning. J Biomech. 1999, 32, 323-326.  
113. Salmon, P. Micro-CT 3D image analysis techniques for orthopedic applications: metal implant-to-bone contact surface and porosity of biomaterials. In A practical manual for musculoskeletal research, World Scientific: 2008; pp 583-603.  
114. Rhee, Y.; Hur, J. H.; Won, Y. Y.; Lim, S. K.; Beak, M. H.; Cui, W. Q.; Kim, K. G.; Kim, Y. E. Assessment of bone quality using finite element analysis based upon micro-CT images. Clin Orthop Surg. 2009, 1, 40-47.  
115. Suen, P. K.; Zhu, T. Y.; Chow, D. H.; Huang, L.; Zheng, L. Z.; Qin, L. Sclerostin antibody treatment increases bone formation, bone mass, and bone strength of intact bones in adult male rats. Sci Rep. 2015, 5, 15632.  
116. Wang, J.; Bi, L.; Bai, J. P.; Lyu, R.; Yang, B. K. Comparative study of micro-CT and histological section in bone morphometry. Zhongguo Jiaoxing Waike Zazhi. 2009, 17, 381-384.  
117. Buie, H. R.; Campbell, G. M.; Klinck, R. J.; MacNeil, J. A.; Boyd, S. K. Automatic segmentation of cortical and trabecular compartments based on a dual threshold technique for in vivo micro-CT bone analysis. Bone. 2007, 41, 505-515.  
118. Doepke, A.; Kuhlmann, J.; Guo, X.; Voorhees, R. T.; Heineman, W. R. A system for characterizing Mg corrosion in aqueous solutions using electrochemical sensors and impedance spectroscopy. Acta Biomater. 2013, 9, 9211-9219.  
119. Wang, J.; Jang, Y.; Wan, G.; Giridharan, V.; Song, G. L.; Xu, Z.; Koo, Y.; Qi, P.; Sankar, J.; Huang, N.; Yun, Y. Flow-induced corrosion of absorbable magnesium alloy: In-situ and real-time electrochemical study. Corros Sci. 2016, 104, 277-289.  
120. Zhao, D.; Wang, T.; Nahan, K.; Guo, X.; Zhang, Z.; Dong, Z.; Chen, S.; Chou, D. T.; Hong, D.; Kumta, P. N.; Heineman, W. R. In vivo characterization of magnesium alloy biodegradation using electrochemical H(2) monitoring, ICP-MS, and XPS. Acta Biomater. 2017, 50, 556-565.  
121. Zhao, D.; Wang, T.; Kuhlmann, J.; Dong, Z.; Chen, S.; Joshi, M.; Salunke, P.; Shanov, V. N.; Hong, D.; Kumta, P. N.; Heineman, W. R. In vivo monitoring the biodegradation of magnesium alloys with an electrochemical H2 sensor. Acta Biomater. 2016, 36, 361-368.  
122. Zhao, D.; Wang, T.; Hoagland, W.; Benson, D.; Dong, Z.; Chen, S.; Chou, D. T.; Hong, D.; Wu, J.; Kumta, P. N.; Heineman, W. R. Visual H(2) sensor for monitoring biodegradation of magnesium implants in vivo. Acta Biomater. 2016, 45, 399-409.  
123. Boutry, C. M.; Chandrahalim, H.; Streit, P.; Schinhammer, M.; Hänzi, A. C.; Hierold, C. Towards biodegradable wireless implants. Philos Trans R Soc A Math Phys Eng Sci. 2012, 370, 2418-2432.  
124. Su Natasha, M.; Malon, R. S. P.; Wicaksono, D. H. B.; Córcoles, E. P.; Hermawan, H. Monitoring magnesium degradation using microdialysis and fabric-based biosensors. Sci China Mater. 2018, 61, 643-651.  
125. Ulrich, A.; Ott, N.; Tournier-Fillon, A.; Homazava, N.; Schmutz, P. Investigation of corrosion behavior of biodegradable magnesium alloys using an online-micro-flow capillary flow injection inductively coupled plasma mass spectrometry setup with electrochemical control. Spectrochim Acta Part B At Spectrosc. 2011, 66, 536-545.  
126. Witte, F.; Kaese, V.; Haferkamp, H.; Switzer, E.; Meyer-Lindenberg, A.; Wirth, C. J.; Windhagen, H. In vivo corrosion of four magnesium alloys and the associated bone response. Biomaterials. 2005, 26, 3557-3563.  
127. Ma, S.; Zhou, B.; Markert, B. Numerical simulation of the tissue differentiation and corrosion process of biodegradable magnesium implants during bone fracture healing. Z Angew Math Mech. 2018, 98, 2223-2238.  
128. Mehboob, H.; Chang, S. H. Evaluation of healing performance of biodegradable composite bone plates for a simulated fractured tibia model by finite element analysis. Compos Struct. 2014, 111, 193-204.  
129. Costantino, M. D.; Schuster, A.; Helmholz, H.; Meyer-Rachner, A.; Willumeit-Römer, R.; Luthringer-Feyerabend, B. J. C. Inflammatory response to magnesium-based biodegradable implant materials. Acta Biomater. 2020, 101, 598-608.  
130. Jin, L.; Wu, J.; Yuan, G.; Chen, T. In vitro study of the inflammatory cells response to biodegradable Mg-based alloy extract. PLoS One. 2018, 13, e0193276.  
131. Tsakiris, V.; Tardei, C.; Clicinschi, F. M. Biodegradable Mg alloys for orthopedic implants – A review. J Magnes Alloys. 2021. doi:10.1016/j.jma.2021.06.024.  
132. Walker, J.; Shadanbaz, S.; Kirkland, N. T.; Stace, E.; Woodfield, T.; Staiger, M. P.; Dias, G. J. Magnesium alloys: predicting in vivo corrosion with in vitro immersion testing. J Biomed Mater Res B Appl Biomater. 2012, 100, 1134-1141.  
133. Baroncelli, G. I. Quantitative ultrasound methods to assess bone mineral status in children: technical characteristics, performance, and clinical application. Pediatr Res. 2008, 63, 220-228.  
134. Gao, Y.; Wang, L.; Li, L.; Gu, X.; Zhang, K.; Xia, J.; Fan, Y. Effect of stress on corrosion of high-purity magnesium in vitro and in vivo. Acta Biomater. 2019, 83, 477-486.  

Conflict of interest
The authors declare they have no competing interests.
Share
Back to top