Analysis of a poly(ε-decalactone)/silver nanowire composite as an electrically conducting neural interface biomaterial

Krukiewicz et al. BMC Biomedical Engineering https://doi.org/10.1186/s42490-019-0010-3 (2019) 1:9 BMC Biomedical Engineering RESEARCH ARTICLE Open Access Analysis of a poly(ε-decalactone)/silver nanowire composite as an electrically conducting neural interface biomaterial Katarzyna Krukiewicz1,2* , Jorge Fernandez3, Małgorzata Skorupa2, Daria Więcławska2, Anup Poudel1, Jose-Ramon Sarasua4, Leo R. Quinlan5 and Manus J. P. Biggs1 Abstract Background: Advancement in polymer technologies, facilitated predominantly through chemical engineering approaches or through the identification and utilization of novel renewable resources, has been a steady focus of biomaterials research for the past 50 years. Aliphatic polyesters have been exploited in numerous biomedical applications including the formulation of soft-tissue sutures, bone fixation devices, cardiovascular stents etc. Biomimetic ‘soft’ polymer formulations are of interest in the design of biological interfaces and specifically, in the development of implantable neuroelectrode systems intended to interface with neural tissues. Critically, soft polymer formulations have been shown to address the challenges associated with the disregulation of mechanotransductive processes and micro-motion induced inflammation at the electrode/tissue interface. In this study, a polyester-based poly(ε-decalactone)/silver nanowire (EDL:Ag) composite was investigated as a novel electrically active biomaterial with neural applications. Neural interfaces were formulated through spin coating of a polymer/nanowire formulation onto the surface of a Pt electrode to form a biocompatible EDL matrix supported by a percolated network of silver nanowires. As-formed EDL:Ag composites were characterized by means of infrared spectroscopy, scanning electron microscopy and electrochemical methods, with their cytocompatibility assessed using primary cultures of a mixed neural population obtained from the ventral mesencephalon of Sprague-Dawley rat embryos. Results: Electrochemical characterization of various EDL:Ag composites indicated EDL:Ag 10:1 as the most favourable formulation, exhibiting high charge storage capacity (8.7 ± 1.0 mC/cm2), charge injection capacity (84. 3 ± 1.4 μC/cm2) and low impedance at 1 kHz (194 ± 28 Ω), outperforming both pristine EDL and bare Pt electrodes. The in vitro biological evaluation showed that EDL:Ag supported significant neuron viability in culture and to promote neurite outgrowth, which had the average length of 2300 ± 6 μm following 14 days in culture, 60% longer than pristine EDL and 120% longer than bare Pt control substrates. Conclusions: EDL:Ag nanocomposites are shown to serve as robust neural interface materials, possessing favourable electrochemical characteristics together with high neural cytocompatibility. Keywords: Polyesters, Poly(ε-decalactone), Silver nanowires, Neural interfaces, Neural stimulation * Correspondence: 1 Centre for Research in Medical Devices (CURAM), Galway Biosciences Research Building, 118 Corrib Village, Newcastle, Galway, Ireland 2 Department of Physical Chemistry and Technology of Polymers, Silesian University of Technology, M.Strzody 9, 44-100 Gliwice, Poland Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Krukiewicz et al. BMC Biomedical Engineering (2019) 1:9 Background Aliphatic polyesters are among the most widely applied polymeric materials in biomedical engineering [1]. Thanks to their suitable physicochemical properties and ease of fabrication, polyesters have been successfully used as soft-tissue sutures, cardiovascular stents and bone fixation devices [2, 3], as well as advanced drug delivery systems [4, 5]. Additional advantages of polyesters in biomedical engineering stem from their biodegradable and bioresorbable properties which facilitate their use as temporary drug carriers or implants [6]. The most commonly used polyesters, i.e. polylactic acid, poly(lactic-co-glycolic acid), poly(ε-caprolactone) and poly-3-hydroxybutyrate have been exploited in biomedical engineering over the last 50 years, with the first polyester-based medical device being approved by the Food and Drug Administration in 1969 [1]. Since then, much research has been focused on the improvement of polyester technology, mainly through chemical and physical modification of existing polymer formulations [2] or through the identification and utilization of novel renewable sources [7]. ε-Decalactone (εDL) belongs to the class of lactones composed of 10 carbon atoms, which can be polymerized to form a linear polyester [8, 9]. εDL is a commercially available, renewable material produced through fungal technology, and is commonly used in the flavouring and fragrance industries [9]. The structural similarity of εDL with ε-caprolactone indicates this polymer to be a promising candidate for numerous biomedical applications. Consequently, the synthesis and characteristics of several copolymers derived from ε-decalactone have been recently described [8]. Interestingly, incorporation of εDL into these copolymer formulations was shown to significantly decrease the polymer stiffness while not impacting on the material’s mechanical strength. Moreover, the presence of εDL-derived domains hinders the hydrolysis of the copolymer due to a steric effect which results in a mechanically soft and slowly degradable material with assumed biocompatibility. Brain machine interfaces have shown great promises as a way to treat central nervous system disorders such as deafness, paralysis, epilepsy and Parkinson’s disease [10], already reaching notable clinical successes [11]. To facilitate integration with surrounding tissue, neural implants should possess chemical and physical properties analogous to the properties typical of the neural microenvironment, including wettability, roughness and mechanical rigidity [12]. Biomimetic ‘soft’ polymer formulations are of interest in the design of biological interfaces and specifically, in the development of implantable neuroelectrode systems intended to interface with neural tissues. In particular, mechanically soft formulations have been shown to address the challenges associated with the disregulation of mechanotransductive processes [13] and micro-motion induced inflammation at the electrode/tissue interface [14]. Critically, peri-implant Page 2 of 12 glio (...truncated)