The Effects of Biodegradation on the Cytocompatibility of Bioresorbable Fe-Based Scaffolds: A Review

Abstract:

This work aims to review current trends in research within the field of iron-based scaffolds for orthopaedic applications. Current research is trapped in a ‘see-saw’ type problem where an increase in corrosion rate of the base metal is required to accelerate the degradation process making the resorption time compatible with the healing time. This is done via several methods including porosity control, cathodic element addition and/or patterning and alloying. In turn, this increase in corrosion rate causes the local concentration of metallic ions to increase beyond the toxicity limit for osteoblast type cells, thus negatively effecting cytocompatibility. This is most pronounced when considering the orthopaedic environment, in which static conditions provide for increased local ion concentrations, resulting in local toxicity. However, research from the medical field of Thalassemia may help solve this dilemma by providing chelation medicine for patients undergoing implantation of resorbable orthopaedic scaffolds, throughout the resorption period. Excretion of iron would then be provided mainly through bowel movement and urination.

• Periodical: Journal of Biomimetics, Biomaterials and Biomedical Engineering (Volume 42)
• Pages: 22-38
• DOI: https://doi.org/10.4028/www.scientific.net/JBBBE.42.22
• Online since: July 2019
• Authors: Malcolm Caligari Conti*, Daphne Anne Pollacco
• Keywords: Biodegradable, Cytocompatibility, Deferasirox, Orthopaedic, Scaffold

References

[1] H. Hermawan, Updates on the research and development of absorbable metals for biomedical applications,, Progress in biomaterials, pp.1-18, (2018).

[2] J. Lévesque, H. Hermawan, D. Dubé, and D. Mantovani, Design of a pseudo-physiological test bench specific to the development of biodegradable metallic biomaterials,, Acta biomaterialia, vol. 4, pp.284-295, (2008).

DOI: 10.1016/j.actbio.2007.09.012

[3] D. Tatkare, World Medical Implants Market Opportunities and Forecasts,, Allied Market Research, Portland, United States, (2016).

[4] D. Adamovic, B. Ristic, and F. Zivic, Review of existing biomaterials—Method of material selection for specific applications in orthopedics,, in Biomaterials in Clinical Practice, ed: Springer, 2018, pp.47-99.

DOI: 10.1007/978-3-319-68025-5_3

[5] S. Bose, M. Roy, and A. Bandyopadhyay, Recent advances in bone tissue engineering scaffolds,, Trends in biotechnology, vol. 30, pp.546-554, (2012).

DOI: 10.1016/j.tibtech.2012.07.005

[6] M. Peuster, P. Beerbaum, F.-W. Bach, and H. Hauser, Are resorbable implants about to become a reality?,, Cardiology in the Young, vol. 16, pp.107-116, (2006).

DOI: 10.1017/s1047951106000011

[7] J. R. Parsons, Resorbable materials and composites: New concepts in orthopedic biomaterials,, Orthopedics, vol. 8, pp.907-915, (1985).

DOI: 10.3928/0147-7447-19850701-17

[8] G. Guillemin, J.-L. Patat, and A. Patel, Biodegradable implant useable as a bone prosthesis,, ed: Google Patents, (1982).

[9] K. de Groot, Bioceramics consisting of calcium phosphate salts,, Biomaterials, vol. 1, pp.47-50, (1980).

DOI: 10.1016/0142-9612(80)90059-9

[10] A. Sáenz, E. Rivera, W. Brostow, and V. M. Castaño, Ceramic biomaterials: an introductory overview,, Journal of Materials Education, vol. 21, pp.267-276, (1999).

[11] E. Schmitt and R. Polistina, Patent 3,463,158, 1969.(b) Frazza, EJ; Schmitt,, in J. Biomed. Mater. Res. Symp, 1971, p.13.

[12] A. R. Santos Jr, Bioresorbable polymers for tissue engineering,, in Tissue engineering, ed: IntechOpen, (2010).

[13] J. C. Middleton and A. J. Tipton, Synthetic biodegradable polymers as orthopedic devices,, Biomaterials, vol. 21, pp.2335-2346, (2000).

DOI: 10.1016/s0142-9612(00)00101-0

[14] G. Govindasamy, S. Vijayakumar, P. Kavya, M. Ranganayaki, and M. Sangavi, Fabrication of biodegrdable bone plates using polymer and nanocomposite matrix.,.

[15] E. D. McBride, Absorbable metal in bone surgery: a further report on the use of magnesium alloys,, Journal of the American Medical Association, vol. 111, pp.2464-2467, (1938).

DOI: 10.1001/jama.1938.02790530018007

[16] M. Seelig, A study of magnesium wire as an absorbable suture and ligature material,, Archives of Surgery, vol. 8, pp.669-680, (1924).

DOI: 10.1001/archsurg.1924.01120050210011

[17] M. P. Staiger, A. M. Pietak, J. Huadmai, and G. Dias, Magnesium and its alloys as orthopedic biomaterials: a review,, Biomaterials, vol. 27, pp.1728-1734, (2006).

DOI: 10.1016/j.biomaterials.2005.10.003

[18] M. Peuster, P. Wohlsein, M. Brügmann, M. Ehlerding, K. Seidler, C. Fink, et al., A novel approach to temporary stenting: degradable cardiovascular stents produced from corrodible metal—results 6–18 months after implantation into New Zealand white rabbits,, Heart, vol. 86, pp.563-569, (2001).

DOI: 10.1136/heart.86.5.563

[19] M. Peuster, C. Fink, C. Von Schnakenburg, and G. Hausdorf, Dissolution of tungsten coils does not produce systemic toxicity, but leads to elevated levels of tungsten in the serum and recanalization of the previously occluded vessel,, Cardiology in the Young, vol. 12, pp.229-235, (2002).

DOI: 10.1017/s1047951102000513

[20] B. Heublein, R. Rohde, V. Kaese, M. Niemeyer, W. Hartung, and A. Haverich, Biocorrosion of magnesium alloys: a new principle in cardiovascular implant technology?,, Heart, vol. 89, pp.651-656, (2003).

DOI: 10.1136/heart.89.6.651

[21] H. Hermawan, D. Dubé, and D. Mantovani, Development of degradable Fe-35Mn alloy for biomedical application,, in Advanced Materials Research, 2007, pp.107-112.

DOI: 10.4028/www.scientific.net/amr.15-17.107

[22] B. Liu and Y. Zheng, Effects of alloying elements (Mn, Co, Al, W, Sn, B, C and S) on biodegradability and in vitro biocompatibility of pure iron,, Acta biomaterialia, vol. 7, pp.1407-1420, (2011).

DOI: 10.1016/j.actbio.2010.11.001

[23] J. Farack, C. Wolf-Brandstetter, S. Glorius, B. Nies, G. Standke, P. Quadbeck, et al., The effect of perfusion culture on proliferation and differentiation of human mesenchymal stem cells on biocorrodible bone replacement material,, Materials Science and Engineering: B, vol. 176, pp.1767-1772, (2011).

DOI: 10.1016/j.mseb.2011.06.004

[24] P. Sharma and P. M. Pandey, Corrosion behaviour of the porous iron scaffold in simulated body fluid for biodegradable implant application,, Materials Science and Engineering: C, vol. 99, pp.838-852, (2019).

DOI: 10.1016/j.msec.2019.01.114

[25] B. Wegener, B. Sievers, S. Utzschneider, P. Müller, V. Jansson, S. Rößler, et al., Microstructure, cytotoxicity and corrosion of powder-metallurgical iron alloys for biodegradable bone replacement materials,, Materials Science and Engineering: B, vol. 176, pp.1789-1796, (2011).

DOI: 10.1016/j.mseb.2011.04.017

[26] P. P. Mueller, S. Arnold, M. Badar, D. Bormann, F. W. Bach, A. Drynda, et al., Histological and molecular evaluation of iron as degradable medical implant material in a murine animal model,, Journal of Biomedical Materials Research Part A, vol. 100, pp.2881-2889, (2012).

DOI: 10.1002/jbm.a.34223

[27] F. Witte, V. Kaese, H. Haferkamp, E. Switzer, A. Meyer-Lindenberg, C. Wirth, et al., In vivo corrosion of four magnesium alloys and the associated bone response,, Biomaterials, vol. 26, pp.3557-3563, (2005).

DOI: 10.1016/j.biomaterials.2004.09.049

[28] M. Yazdimamaghani, M. Razavi, D. Vashaee, K. Moharamzadeh, A. R. Boccaccini, and L. Tayebi, Porous magnesium-based scaffolds for tissue engineering,, Materials Science and Engineering: C, vol. 71, pp.1253-1266, (2017).

DOI: 10.1016/j.msec.2016.11.027

[29] R. Oriňáková, A. Oriňák, L. M. Bučková, M. Giretová, L. Medvecký, E. Labbanczová, et al., Iron based degradable foam structures for potential orthopedic applications,, Int. J. Electrochem. Sci, vol. 8, pp.12451-12465, (2013).

[30] C. S. Obayi, R. Tolouei, C. Paternoster, S. Turgeon, B. A. Okorie, D. O. Obikwelu, et al., Influence of cross-rolling on the micro-texture and biodegradation of pure iron as biodegradable material for medical implants,, Acta biomaterialia, vol. 17, pp.68-77, (2015).

DOI: 10.1016/j.actbio.2015.01.024

[31] H. Hermawan, D. Dubé, and D. Mantovani, Degradable metallic biomaterials: design and development of Fe–Mn alloys for stents,, Journal of Biomedical Materials Research Part A, vol. 93, pp.1-11, (2010).

DOI: 10.1002/jbm.a.32224

[32] A. H. Yusop and H. Hermawan, Synthesis and development of polymers-infiltrated porous iron for temporary medical implants: A preliminary result,, in Advanced Materials Research, 2013, pp.331-335.

DOI: 10.4028/www.scientific.net/amr.686.331

[33] D. L. Millis, Responses of musculoskeletal tissues to disuse and remobilization,, in Canine Rehabilitation and Physical Therapy (Second Edition), ed: Elsevier, 2014, pp.92-153.

DOI: 10.1016/b978-1-4377-0309-2.00007-7

[34] M. Schinhammer, A. C. Hänzi, J. F. Löffler, and P. J. Uggowitzer, Design strategy for biodegradable Fe-based alloys for medical applications,, Acta biomaterialia, vol. 6, pp.1705-1713, (2010).

DOI: 10.1016/j.actbio.2009.07.039

[35] D. A. Algren, Review of oral iron chelators (deferiprone and deferasirox) for the treatment of iron overload in pediatric patients,, World Health Organization [on line], pp.1-22, (2010).

[36] H. Hermawan, A. Purnama, D. Dube, J. Couet, and D. Mantovani, Fe–Mn alloys for metallic biodegradable stents: degradation and cell viability studies,, Acta biomaterialia, vol. 6, pp.1852-1860, (2010).

DOI: 10.1016/j.actbio.2009.11.025

[37] O. E. Barcia and O. R. Mattos, The role of chloride and sulphate anions in the iron dissolution mechanism studied by impedance measurements,, Electrochimica Acta, vol. 35, pp.1003-1009, (1990).

DOI: 10.1016/0013-4686(90)90035-x

[38] N. M. Daud, N. B. Sing, A. H. Yusop, F. A. A. Majid, and H. Hermawan, Degradation and in vitro cell–material interaction studies on hydroxyapatite-coated biodegradable porous iron for hard tissue scaffolds,, Journal of Orthopaedic Translation, vol. 2, pp.177-184, (2014).

DOI: 10.1016/j.jot.2014.07.001

[39] H. Pickering and R. Frankenthal, On the mechanism of localized corrosion of iron and stainless steel I. Electrochemical studies,, journal of the Electrochemical Society, vol. 119, pp.1297-1304, (1972).

DOI: 10.1149/1.2403983

[40] P. Quadbeck, R. Hauser, K. Kümmel, G. Standke, G. Stephani, B. Nies, et al., Iron based cellular metals for degradable synthetic bone replacement,, in PM2010 World Congress, Florenz, Italy, (2010).

[41] P. Sotoudehbagha, S. Sheibani, M. Khakbiz, S. Ebrahimi-Barough, and H. Hermawan, Novel antibacterial biodegradable Fe-Mn-Ag alloys produced by mechanical alloying,, Materials Science and Engineering: C, vol. 88, pp.88-94, (2018).

DOI: 10.1016/j.msec.2018.03.005

[42] P. S. Bagha, M. Khakbiz, S. Sheibani, and H. Hermawan, Design and characterization of nano and bimodal structured biodegradable Fe-Mn-Ag alloy with accelerated corrosion rate,, Journal of Alloys and Compounds, vol. 767, pp.955-965, (2018).

DOI: 10.1016/j.jallcom.2018.07.206

[43] T. Huang and Y. Zheng, Uniform and accelerated degradation of pure iron patterned by Pt disc arrays,, Scientific reports, vol. 6, p.23627, (2016).

DOI: 10.1038/srep23627

[44] K. Ralston, N. Birbilis, and C. Davies, Revealing the relationship between grain size and corrosion rate of metals,, Scripta Materialia, vol. 63, pp.1201-1204, (2010).

DOI: 10.1016/j.scriptamat.2010.08.035

[45] A. Böcker, H. Klein, and H. Bunge, Development of cross-rolling textures in Armco-Iron,, Texture, Stress, and Microstructure, vol. 12, pp.103-123, (1990).

DOI: 10.1155/tsm.12.103

[46] Y. Feng, N. Gaztelumendi, J. Fornell, H. Zhang, P. Solsona, M. Baró, et al., Mechanical properties, corrosion performance and cell viability studies on newly developed porous Fe-Mn-Si-Pd alloys,, Journal of Alloys and Compounds, vol. 724, pp.1046-1056, (2017).

DOI: 10.1016/j.jallcom.2017.07.112

[47] A. Vahidgolpayegani, C. Wen, P. Hodgson, and Y. Li, Production methods and characterization of porous Mg and Mg alloys for biomedical applications,, in Metallic Foam Bone, ed: Elsevier, 2017, pp.25-82.

DOI: 10.1016/b978-0-08-101289-5.00002-0

[48] Q. L. Loh and C. Choong, Three-dimensional scaffolds for tissue engineering applications: role of porosity and pore size,, Tissue Engineering Part B: Reviews, vol. 19, pp.485-502, (2013).

DOI: 10.1089/ten.teb.2012.0437

[49] T. L. Nguyen, M. P. Staiger, G. J. Dias, and T. B. Woodfield, A novel manufacturing route for fabrication of topologically‐ordered porous magnesium scaffolds,, Advanced Engineering Materials, vol. 13, pp.872-881, (2011).

DOI: 10.1002/adem.201100029

[50] C. Yang, Z. Huan, X. Wang, C. Wu, and J. Chang, 3D printed Fe scaffolds with HA nanocoating for bone regeneration,, ACS Biomaterials Science & Engineering, vol. 4, pp.608-616, (2018).

DOI: 10.1021/acsbiomaterials.7b00885

[51] Y. Li, H. Jahr, K. Lietaert, P. Pavanram, A. Yilmaz, L. Fockaert, et al., Additively manufactured biodegradable porous iron,, Acta biomaterialia, vol. 77, pp.380-393, (2018).

DOI: 10.1016/j.actbio.2018.07.011

[52] M. Caligari Conti, G. Xerri, F. Peyrouzet, P. S. Wismayer, E. Sinagra, D. Mantovani, et al., Optimisation of fluorapatite coating synthesis applied to a biodegradable substrate,, Surface Engineering, vol. 35, pp.255-265, (2019).

DOI: 10.1080/02670844.2018.1491510

[53] E. Tenekecioglu, V. Farooq, C. V. Bourantas, R. C. Silva, Y. Onuma, M. Yılmaz, et al., Bioresorbable scaffolds: a new paradigm in percutaneous coronary intervention,, BMC cardiovascular disorders, vol. 16, p.38, (2016).

DOI: 10.1186/s12872-016-0207-5

[54] J. S. McLaren, L. White, H. Cox, W. Ashraf, C. Rahman, G. Blunn, et al., A biodegradable antibiotic-impregnated scaffold to prevent osteomyelitis in a contaminated in vivo bone defect model,, European Cells and Materials, vol. 27, pp.332-349, (2014).

DOI: 10.22203/ecm.v027a24

[55] W.-J. Lin, D.-Y. Zhang, G. Zhang, H.-T. Sun, H.-P. Qi, L.-P. Chen, et al., Design and characterization of a novel biocorrodible iron-based drug-eluting coronary scaffold,, Materials & Design, vol. 91, pp.72-79, (2016).

DOI: 10.1016/j.matdes.2015.11.045

[56] Y. Qi, H. Qi, Y. He, W. Lin, P. Li, L. Qin, et al., Strategy of metal–polymer composite stent to accelerate biodegradation of iron-based biomaterials,, ACS applied materials & interfaces, vol. 10, pp.182-192, (2017).

DOI: 10.1021/acsami.7b15206

[57] J. Wu, X. Lu, L. Tan, B. Zhang, and K. Yang, Effect of hydrion evolution by polylactic‐co‐glycolic acid coating on degradation rate of pure iron,, Journal of Biomedical Materials Research Part B: Applied Biomaterials, vol. 101, pp.1222-1232, (2013).

DOI: 10.1002/jbm.b.32934

[58] H. Chen, E. Zhang, and K. Yang, Microstructure, corrosion properties and bio-compatibility of calcium zinc phosphate coating on pure iron for biomedical application,, Materials Science and Engineering: C, vol. 34, pp.201-206, (2014).

DOI: 10.1016/j.msec.2013.09.010

[59] M. Hrubovčáková, M. Kupkova, M. Džupon, M. Giretova, Ľ. Medvecký, and R. Džunda, Biodegradable polylactic acid and polylactic acid/hydroxyapatite coated iron foams for bone replacement materials,, Int. J. Electrochem. Sci, vol. 12, pp.11122-11136, (2017).

DOI: 10.20964/2017.12.53

[60] J. He, F.-L. He, D.-W. Li, Y.-L. Liu, Y.-Y. Liu, Y.-J. Ye, et al., Advances in Fe-based biodegradable metallic materials,, RSC Advances, vol. 6, pp.112819-112838, (2016).

DOI: 10.1039/c6ra20594a

[61] L. Aissani, M. Fellah, L. Radjehi, C. Nouveau, A. Montagne, and A. Alhussein, Effect of annealing treatment on the microstructure, mechanical and tribological properties of chromium carbonitride coatings,, Surface and Coatings Technology, vol. 359, pp.403-413, 2019/02/15/ 2019. https://doi.org/10.1016/j.surfcoat.2018.12.099.

DOI: 10.1016/j.surfcoat.2018.12.099

[62] M. Fellah, L. Aissani, M. A. Samad, S. Mechacheti, M. Z. Touhami, A. Montagne, et al., Characterisation of RF magnetron sputtered Cr-N, Cr-Zr-N and Zr-N coatings,, Transactions of the IMF, vol. 95, pp.261-268, (2017).

DOI: 10.1080/00794236.2017.1339464

[63] J. Weber, L. Atanasoska, and T. Eidenschink, Corrosion resistant coatings for biodegradable metallic implants,, ed: Google Patents, (2007).

[64] I. S. Organisation, ISO 5832-1:2016: Implants for surgery -- Metallic materials -- Part 1: Wrought stainless steel,, ed, (2016).

[65] D. Paramitha, M. F. Ulum, D. Noviana, S. Estuningsih, and H. Hermawan, Assessment on the inflammatory reaction during the implantation of biodegradable metal implants in mice,, Frontiers in Bioengineering and Biotechnology. 10.3389/conf.FBIOE.2016.01.00782.

DOI: 10.1063/1.4930726

[66] T. Kraus, F. Moszner, S. Fischerauer, M. Fiedler, E. Martinelli, J. Eichler, et al., Biodegradable Fe-based alloys for use in osteosynthesis: Outcome of an in vivo study after 52 weeks,, Acta biomaterialia, vol. 10, pp.3346-3353, (2014).

DOI: 10.1016/j.actbio.2014.04.007

[67] M. Traverson, M. Heiden, L. A. Stanciu, E. A. Nauman, Y. Jones-Hall, and G. J. Breur, In vivo Evaluation of Biodegradability and Biocompatibility of Fe30Mn Alloy,, Veterinary and Comparative Orthopaedics and Traumatology, vol. 31, pp.010-016, (2018).

DOI: 10.3415/vcot-17-06-0080

[68] F. Nie, Y. Zheng, S. Wei, C. Hu, and G. Yang, In vitro corrosion, cytotoxicity and hemocompatibility of bulk nanocrystalline pure iron,, Biomedical Materials, vol. 5, p.065015, (2010).

DOI: 10.1088/1748-6041/5/6/065015

[69] S. Zhu, N. Huang, L. Xu, Y. Zhang, H. Liu, H. Sun, et al., Biocompatibility of pure iron: in vitro assessment of degradation kinetics and cytotoxicity on endothelial cells,, Materials Science and Engineering: C, vol. 29, pp.1589-1592, (2009).

DOI: 10.1016/j.msec.2008.12.019

[70] J. He, F.-L. He, D.-W. Li, Y.-L. Liu, and D.-C. Yin, A novel porous Fe/Fe-W alloy scaffold with a double-layer structured skeleton: preparation, in vitro degradability and biocompatibility,, Colloids and Surfaces B: Biointerfaces, vol. 142, pp.325-333, (2016).

DOI: 10.1016/j.colsurfb.2016.03.002

[71] J. Cheng, T. Huang, and Y. Zheng, Microstructure, mechanical property, biodegradation behavior, and biocompatibility of biodegradable Fe–Fe2O3 composites,, Journal of Biomedical Materials Research Part A, vol. 102, pp.2277-2287, (2014).

DOI: 10.1002/jbm.a.34882

[72] W. Lin, G. Zhang, P. Cao, D. Zhang, Y. Zheng, R. Wu, et al., Cytotoxicity and its test methodology for a bioabsorbable nitrided iron stent,, Journal of Biomedical Materials Research Part B: Applied Biomaterials, vol. 103, pp.764-776, (2015).

DOI: 10.1002/jbm.b.33246

[73] Y. Yang, Surface Modification of Biodegradable Metallic Materials with Focus on Magnesium and Iron,, (2017).

[74] E. M. Sussman, B. J. Casey, D. Dutta, and B. J. Dair, Different cytotoxicity responses to antimicrobial nanosilver coatings when comparing extract‐based and direct‐contact assays,, Journal of Applied Toxicology, vol. 35, pp.631-639, (2015).

DOI: 10.1002/jat.3104

[75] M. W. Hentze, M. U. Muckenthaler, B. Galy, and C. Camaschella, Two to tango: regulation of Mammalian iron metabolism,, Cell, vol. 142, pp.24-38, (2010).

DOI: 10.1016/j.cell.2010.06.028

[76] M. Schinhammer, I. Gerber, A. C. Hänzi, and P. J. Uggowitzer, On the cytocompatibility of biodegradable Fe-based alloys,, Materials Science and Engineering: C, vol. 33, pp.782-789, (2013).

DOI: 10.1016/j.msec.2012.11.002

[77] A. K. Mishra and A. Tiwari, Iron overload in beta thalassaemia major and intermedia patients,, Maedica, vol. 8, p.328, (2013).

[78] G. Faa and G. Crisponi, Iron chelating agents in clinical practice,, Coordination Chemistry Reviews, vol. 184, pp.291-310, (1999).

DOI: 10.1016/s0010-8545(99)00056-9

[79] M. D. Cappellini, A. Cohen, A. Piga, M. Bejaoui, S. Perrotta, L. Agaoglu, et al., A phase 3 study of deferasirox (ICL670), a once-daily oral iron chelator, in patients with β-thalassemia,, Blood, vol. 107, pp.3455-3462, (2006).

DOI: 10.1182/blood-2005-08-3430

[80] M. D. Cappellini and P. Pattoneri, Oral iron chelators,, Annual review of medicine, vol. 60, pp.25-38, (2009).

DOI: 10.1146/annurev.med.60.041807.123243

[81] A. Piga, R. Galanello, G. L. Forni, M. D. Cappellini, R. Origa, A. Zappu, et al., Randomized phase II trial of deferasirox (Exjade, ICL670), a once-daily, orally-administered iron chelator, in comparison to deferoxamine in thalassemia patients with transfusional iron overload,, haematologica, vol. 91, pp.873-880, (2006).

DOI: 10.1182/blood.v108.11.1768.1768

[82] L. H. Alparslan and B. N. Weissman, Chapter 15 - Imaging Findings of Drug-Related Musculoskeletal Disorders,, in Imaging of Arthritis and Metabolic Bone Disease, B. N. Weissman, Ed., ed Philadelphia: W.B. Saunders, 2009, pp.264-279.

DOI: 10.1016/b978-0-323-04177-5.00015-x