Abstract
Superelastic (SE) and thermo-activated (TA) nickel–titanium (NiTi) archwires are used in everyday orthodontic practice, based on their acceptable biocompatibility and well-defined shape memory properties. However, the differences in their surface microstructure and cytotoxicity have not been clearly defined, and the standard cytotoxicity tests are too robust to detect small differences in the cytotoxicity of these alloys, all of which can lead to unexpected adverse reactions in some patients. Therefore, we tested the hypothesis that the differences in manufacture and microstructure of commercially available SE and TA archwires may influence their biocompatibility. The archwires were studied as-received and after conditioning for 24 h or 35 days in a cell culture medium under static conditions. All of the tested archwires, including their conditioned medium (CM), were non-cytotoxic for L929 cells, but Rematitan SE (both as received and conditioned) induced the apoptosis of rat thymocytes in a direct contact. In contrast, TruFlex SE and Equire TA increased the proliferation of thymocytes. The cytotoxic effect of Rematitan SE correlated with the higher release of Ni ions in CM, higher concentration of surface Ni and an increased oxygen layer thickness after the conditioning. In conclusion, the apoptosis assay on rat thymocytes, in contrast to the less sensitive standard assay on L929 cells, revealed that Rematitan SE was less cytocompatible compared to other archwires and the effect was most probably associated with a higher exposition of the cells to Ni on the surface of the archwire, due to the formation of unstable oxide layer.
Similar content being viewed by others
References
Es-Souni M, Es-Souni M, Fischer-Brandies H. Assessing the biocompatibility of NiTi shape memory alloys used for medical applications. Anal Bioanal Chem. 2005;381(3):557–67.
Tabish TA, Butt MT, Ali M. Biocompatibility behavior and biomedical applications of Ti-Ni based shape memory alloys: A brief review. J Fac Eng Technol. 2013;19(1):135–40.
Williams DF. Regulatory biocompatibility requirements for biomaterials used in regenerative medicine. J Mater Sci Mater Med. 2015;26(2):89.
Brandal G, Yao YL, Naveed S. Biocompatibility and corrosion response of laser joined NiTi to stainless steel wires. J Manuf Sci Eng. 2015;137(3):031015.
Tomic S, Rudolf R, Bruncko M, Anzel I, Savic V, Colic M. Response of monocyte-derived dendritic cells to rapidly solidified nickel-titanium ribbons with shape memory properties. Eur Cell Mater. 2012;23:58–80.
Tonner R, Waters N. The characteristics of super-elastic Ni-Ti wires in three-point bending. Part l: The effect of temperature. Eur J Orthod. 1994;16(5):409–19.
Evans T, Durning P. Aligning archwires, the shape of things to come? a fourth and fifth phase of force delivery. Br J Orthod. 1996;23(3):269–75.
Kusy RP, Whitley JQ. Thermal and mechanical characteristics of stainless steel, titanium–molybdenum, and nickel–titanium archwires. Am J Orthod Dentofacial Orthop. 2007;131(2):229–37.
Bishara SE, Winterbottom JM, Sulieman A-HA, Rim K, Jakobsen JR. Comparisons of the thermodynamic properties of three nickel–titanium orthodontic archwires. Angle Orthod. 1995;65(2):117–22.
Jian F, Lai W, Furness S, McIntyre GT, Millett DT, Hickman J, et al. Initial arch wires for tooth alignment during orthodontic treatment with fixed appliances. Eur J Orthod. 2003;25:417–21.
Lombardo L, Marafioti M, Stefanoni F, Mollica F, Siciliani G. Load deflection characteristics and force level of nickel titanium initial archwires. Angle Orthod. 2011;82(3):507–21.
Brosens V, Ghijselings I, Voet M, Leemans P, Van Humbeeck J, Willems G. Transformation behaviour, bending properties and surface quality of 22 commercial nickel–titanium wires: a batch-to-batch evaluation. Br J Med Med Res. 2012;2:597–620.
Shabalovskaya SA. On the nature of the biocompatibility and on medical applications of NiTi shape memory and superelastic alloys. Biomed Mater Eng. 1996;6(4):267–89.
Wirth C, Comte V, Lagneau C, Exbrayat P, Lissac M, Jaffrezic-Renault N, et al. Nitinol surface roughness modulates in vitro cell response: a comparison between fibroblasts and osteoblasts. Mater Sci Eng, C. 2005;25(1):51–60.
ISO. Biological evaluation of medical devices Part 5: tests for in vitro cytotoxicity. 10933-52009.
Colic M, Rudolf R, Stamenkovic D, Anzel I, Vucevic D, Jenko M, et al. Relationship between microstructure, cytotoxicity and corrosion properties of a Cu–Al–Ni shape memory alloy. Acta Biomater. 2010;6(1):308–17.
Colic M, Gasic S, Vucevic D, Pavicic L, Popovic P, Jandric D, et al. Modulatory effect of 7-thia-8-oxoguanosine on proliferation of rat thymocytes in vitro stimulated with concanavalin A. Int J Immunopharmacol. 2000;22:203–12.
Shabalovskaya S, Anderegg J. Surface spectroscopic characterization of TiNi nearly equiatomic shape memory alloys for implants. J Vac Sci Technol A. 1995;13:2624–32.
Toker SM, Canadinc D. Evaluation of the biocompatibility of NiTi dental wires: A comparison of laboratory experiments and clinical conditions. Mater Sci Eng C. 2014;40:142–7.
Prymak O, Klocke A, Kahl-Nieke B, Epple M. Fatigue of orthodontic nickel–titanium (NiTi) wires in different fluids under constant mechanical stress. Mater Sci Eng A. 2004;378:110–4.
Lü X, Bao X, Huang Y, Qu Y, Lu H, Lu Z. Mechanisms of cytotoxicity of nickel ions based on gene expression profiles. Biomaterials. 2009;30(2):141–8.
Roediger B, Weninger W. How nickel turns on innate immune cells. Immunol Cell Biol. 2011;89:1.
Ghazal ARA, Hajeer MY, Al-Sabbagh R, Alghoraibi I, Aldiry A. An evaluation of two types of nickel–titanium wires in terms of micromorphology and nickel ions’ release following oral environment exposure. Prog Orthod. 2015;16(1):9.
Mikulewicz M, Chojnacka K, Woźniak B, Downarowicz P. Release of metal ions from orthodontic appliances: an in vitro study. Biol Trace Elem Res. 2012;146(2):272–80.
Wataha J, Lockwood P, Marek M, Ghazi M. Ability of Ni-containing biomedical alloys to activate monocytes and endothelial cells in vitro. J Biomed Mater Res. 1999;45(3):251–7.
Wataha J, Lockwood P, Schedle A. Effect of silver, copper, mercury, and nickel ions on cellular proliferation during extended, low-dose exposures. J Biomed Mater Res. 2000;52(2):360–4.
Eliades T, Pratsinis H, Kletsas D, Eliades G, Makou M. Characterization and cytotoxicity of ions released from stainless steel and nickel–titanium orthodontic alloys. Am J Orthod Dentofac Orthop. 2004;125:24–9.
Spalj S, Mlacovic Zrinski M, Tudor Spalj V, Ivankovic Buljan Z. In-vitro assessment of oxidative stress generated by orthodontic archwires. Am J Orthod Dentofac Orthop. 2012;141:583–9.
Martín-Cameán A, Jos A, Puerto M, Calleja A, Iglesias-Linares A, Solano E, et al. In vivo determination of aluminum, cobalt, chromium, copper, nickel, titanium and vanadium in oral mucosa cells from orthodontic patients with mini-implants by inductively coupled plasma-mass spectrometry (ICP-MS). J Trace Elem Med Biol. 2015;32:13–20.
Taira M, Toguchi M, Hamada Y, Takahashi J, Itou R, Toyosawa S, et al. Studies on cytotoxic effect of nickel ions on three cultured fibroblasts. J Mater Sci Mater Med. 2001;12:373–6.
Ramazanzadeh BA, Ahrari F, Sabzevari B, Habibi S. Nickel ion release from three types of nickel–titanium-based orthodontic archwires in the as-received state and after oral simulation. J Dent Res Dent Clin Dent Prospect. 2014;8:71.
Holsti MA, Raulet D. IL-6 and IL-1 synergize to stimulate IL-2 production and proliferation of peripheral T cells. J Immunol. 1989;143:2514–9.
Schmalz G, Schuster U, Schweikl H. Influence of metals on IL-6 release in vitro. Biomaterials. 1998;19(18):1689–94.
Shabalovskaya SA. Surface, corrosion and biocompatibility aspects of nitinol as an implant material. Biomed Mater Eng. 2002;12:69–109.
Toker S, Canadinc D, Maier H, Birer O. Evaluation of passive oxide layer formation–biocompatibility relationship in NiTi shape memory alloys: geometry and body location dependency. Mater Sci Eng C. 2014;36:118–29.
Huang R, Han Y. The effect of SMAT-induced grain refinement and dislocations on the corrosion behavior of Ti–25Nb–3Mo–3Zr–2Sn alloy. Mater Sci Eng, C. 2013;33:2353–9.
Rahmany MB, Van Dyke M. Biomimetic approaches to modulate cellular adhesion in biomaterials: a review. Acta Biomater. 2013;9(3):5431–7.
Williams D, Williams R. Degradative effects of the biological environment on metals and ceramics. In: Ratner B, Hoffman A, Schoen F, Lemons J, editors. Biomaterials science; an introduction to materials in medicine. San Diego: Academic Press; 1996. p. 260–7.
Fadley C. X-ray photoelectron spectroscopy: progress and perspectives. J Electron Spectrosc. 2010;178:2–32.
Horgnies M, Darque-Ceretti E, Fezai H, Felder E. Influence of the interfacial composition on the adhesion between aggregates and bitumen: investigations by EDX, XPS and peel tests. Int J Adhes Adhes. 2011;31(4):238–47.
Trepanier C, Tabrizian M, Yahia LH, Bilodeau L, Piron DL. Effect of modification of oxide layer on NiTi stent corrosion resistance. J Biomed Mater Res. 1998;43(4):433–40.
Acknowledgments
This work was supported by the International Eureka Programme [ORTO-NITI E! 6788] and the Slovenian Research Agency (ARRS) [L2-5486]. Authors declare that there is no conflict of interests. The authors share gratitude to Dušan A Mihajlović for his kind help in the manuscript preparation.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Čolić, M., Tomić, S., Rudolf, R. et al. Differences in cytocompatibility, dynamics of the oxide layers’ formation, and nickel release between superelastic and thermo-activated nickel–titanium archwires. J Mater Sci: Mater Med 27, 128 (2016). https://doi.org/10.1007/s10856-016-5742-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10856-016-5742-1