- Email: [email protected]
Biocompatibility and functionalization of diamond for neural applications
Available online at www.sciencedirect.com
ScienceDirect
Current Opinion in
Biomedical Engineering
Biocompatibility and functionalization of diamond for neural applications Kai-Hung Yang1,2 and Roger J. Narayan1 Abstract
Diamond has been studied as an interface between medical devices and the body because of its wide potential window, chemical inertness, mechanical hardness, capability for surface modification, tunable electrical conductivity, and biocompatibility. Diamond coatings have been considered for use in a variety of medical device applications, including protective coatings, biointerfaces, and biosensors. For example, diamond has been investigated for use in neural stimulation because it exhibits not only stability but also a wide potential window. This manuscript reviews the development of neural interfaces on the basis of diamond coatings, which can provide an improved quality of life for individuals suffering from many types of medical conditions. Addresses 1 Joint Department of Biomedical Engineering, University of North Carolina and North Carolina State University, Raleigh, NC, USA 2 Department of Materials Science & Engineering, North Carolina State University, Raleigh, NC, USA Corresponding author: Narayan, Roger J. ([email protected])
Current Opinion in Biomedical Engineering 2019, 10:60–68 This review comes from a themed issue on Biomaterials: Biomaterials and Biocompatibility Edited by Masayuki Yamato and Masoud Mozafari
https://doi.org/10.1016/j.cobme.2019.03.002 2468-4511/© 2019 Elsevier Inc. All rights reserved.
Keywords Diamond, Thin film, Medical device, Neural stimulation.
Background Diamond has been studied as an interface between medical devices and the human body for several decades because of its wide potential window [1,2], chemical inertness [3,4], mechanical hardness [5e7], capability for surface modification [8e10], tunable electrical conductivity [11], and biocompatibility [12e14]. Based on grain size, diamond coatings can be classified into microcrystalline diamond, nanocrystalline diamond (NCD), and ultrananocrystalline diamond (UNCD) (Figure 1a) [7]. NCD and UNCD, which exhibit small grain sizes and low roughness values, may be used in microelectromechanical systems and other tribological applications [5,15].
Current Opinion in Biomedical Engineering 2019, 10:60–68
Raman spectroscopy is commonly used for examining the bonding of carbon atoms in diamond [16,17]. The Raman peak at 1140 cm 1 is sometimes noted in diamond coatings with small grain size (<0.1 mm). The 1140 cm 1 peak has been associated with NCD coatings or sp2bonded carbon atoms in NCD coatings. The peak at 1332 cm 1 has been associated with sp3-bonded carbon atoms and is attributed to the zone center optical phonon mode, which exhibits F2g symmetry. This peak has a narrower full width at a half maximum value (2 cm 1) and a higher peak intensity in highly tetrahedral materials such as natural diamond. Broadening of this peak is observed in diamond coatings with large amounts of amorphous carbon and small grain sizes. The broad hump at 1580 cm 1 is called the graphite (G) band; it is the optically allowed E2g zone center mode that is associated with crystalline graphite. The small shoulder at 1350 cm 1 region is the A1g mode of graphite; it is known as the disordered (D) band. These two features are found in sp2-bonded amorphous carbon. The peak at 1470 cm 1 is also associated with amorphous carbon. An example of a Raman spectrum showing features associated with diamond and other forms of carbon is illustrated in Figure 2 [18]. Other characterization techniques such as near-edge X-ray absorption fine structure spectroscopy and electron energy loss spectroscopy can be used to determine the sp2/sp3 ratio in diamond coatings [19]. Diamond can be synthesized using cost-efficient chemical vapor deposition (CVD) methods, including hot filament CVD and microwave plasma CVD (MPCVD) [4,20e22]. MPCVD is widely used in laboratory and industry settings. MPCVD can provide a high-density plasma and a high concentration of active species, enabling deposition at low temperature and low pressure. Additionally, MPCVD enables high-quality NCD or UNCD coatings be grown in the absence of contamination from the filament materials [23]. A schematic diagram of the CVD approach is shown in Figure 1b.
Electrical stimulation and biocompatibility NCD and UNCD have been considered for use in a variety of medical device applications, including protective coatings, biointerfaces, and biosensors [24e28]. The mechanical strength and wear resistance of diamond coatings make them a proper candidate as protective coating for heart valve and joint prostheses. Anchoring of proteins, cells, or DNA on the surface of diamond coatings may facilitate uses of these materials as biointerfaces and biosensors. Intrinsic diamond is a www.sciencedirect.com
Biocompatibility and functionalization of diamond Yang and Narayan
61
Figure 1
(a) Scanning electron microscopy images showing typical surface morphology of microcrystalline, nanocrystalline, and ultrananocrystalline diamond from left to right. Reprinted from Ref. [7] with permission from the publisher. (b) Schematic diagram of microwave CVD. CVD, chemical vapor deposition.
semiconductor material with a wide bandgap. The conductivity of diamond can be greatly increased with boron (p-type) or nitrogen (n-type) doping [11]; doping can increase conductivity to around 200 U 1cm 1 [5].
Field emission by hydrogen-terminated diamond with negative electron affinity has also been demonstrated [29,30]. Under electrical stimulation, charge was delivered in the leading phase to depolarize the membranes
Figure 2
Raman spectrum of diamond and other carbon features. Reprinted from Ref. [18] with permission from the publisher. www.sciencedirect.com
Current Opinion in Biomedical Engineering 2019, 10:60–68
62 Biomaterials: biomaterials and biocompatibility
of excitable cells by either the capacitive injection mechanism or the faradaic injection mechanism [31]. The most commonly used conventional materials are titanium nitride [32,33], platinum [34e36], and iridium oxide [37e39] with capacitive injection, pseudocapacitive injection, and faradaic injection approaches, respectively. Among them, faradaic injection is not favored because it may change local environment such as water electrolysis, change in the pH value, protein reduction, or oxidation; these processes may be detrimental to cells. Dissolution of the electrode, delamination, and breakdown of the passivation film may also impair function. Poly(3,4-ethylenedioxythiophene), an electrically conductive polymer, has also been studied as electrode material [40e42]; however, the long-term stability of this material is uncertain. Diamond is a promising material for neural stimulation that exhibits not only stability but also a wide potential window to avoid the electrolysis of water. In the previous studies, diamond has been demonstrated to have a potential window of around 3e3.2 V, which is higher than that of all the materials mentioned previously. The mechanical integrity and chemical inertness provided by diamond make it an appropriate material for long-term use. One of the concerns for application of NCD or UNCD as a biointerface for neural stimulation or recording is biocompatibility. Because NCD is doped with boron to give tunable electrical conductivity, it might demonstrate cytotoxicity with higher doping concentration (1021 cm 3 or higher). Surface termination and hydrophilicity were also important for determining cellular attachment, differentiation, and proliferation. In 2004, Specht et al. [12] demonstrated ordered growth of neurons on a diamond single crystal. In recent years, Taylor et al. [13] showed that human neural stem cells are able to attach and proliferate on NCD and borondoped NCD surfaces that exhibit high levels of boron doping (w1021 cm 3). For long-term stability and compatibility, Nistor et al. [14] examined differentiation and function of neurons; they demonstrated that borondoped diamond (BDD) can support pluripotent stem cellederived human neurons after long-term culture. Neural stimulation and brainemachine interfaces can not only act as neural prostheses but also treat medical conditions. In neural stimulation, a microelectrode is often used to provide sufficient charge density injection over a small surface area [31]. These devices can be used for selected stimulation of tissues with good spatial resolution. Electrodes with high relative surface areas may have enhanced attachment of neuron cells; rough surfaces have been shown to provide better cell attachment than flat surfaces (Figure 3) [43]. Too high or too low of roughness might have adverse effect. As shown in Figure 4, nanoporous membranes have also Current Opinion in Biomedical Engineering 2019, 10:60–68
been demonstrated to provide cellular anchoring [44]. This study indicates that many types of microscale and nanoscale structures may have appropriate functionality to serve as biointerfaces.
Surface functionalization After the demonstration of cochlear implants for hearing loss [45,46] and deep brain stimulation devices for Parkinson’s disease [47,48], visual prostheses [1,49e51] are being investigated for providing blind patients with capabilities for text reading, facial recognition, and sense of direction. A microelectrode array (MEA) with at least 600 pixels is commonly used in visual prostheses [52]. From an engineering side of view, a ground grid configuration is recommended to give better electrode resolution compared with distant ground, bipolar [53], and hexapolar return electrode configurations [49]. Additionally, 3D nanostructured electrodes can provide higher resolution compared with their planar counterparts [51]. To create effective neural prostheses, studies on the behavior of both retinal neurons and glial cells are necessary because adhesion of glial cell and gliosis can affect the interaction between the electrode and the cells and long-term efficacy. Surface termination is an important factor for controlling the attachment of cells to the diamond surface because neural cells tend to have stronger attachment to hydrophilic surfaces. Surface treatments were usually achieved through plasma [8,9,54e57] or photochemical reactions [10,58,59]. Four common surface termination approaches that have been demonstrated include hydrogen termination, oxygen termination, fluorine termination, and amino termination. These four terminations gave distinct surface hydrophilicity and water contact angle (F-termination>H-termination>NH2-termination>O-termination) attributes. Although NH2 termination is relatively unstable when stored in air, NH2 termination can be retained to a significant extent for up to three months if properly stored under reduced pressure [60,61]. Most as-grown diamond surfaces are H-terminated because the film growth involves the CH3* radical [7]; however, nitrogen-incorporated UNCD is not intrinsically Hterminated. The growth of nitrogen-incorporated UNCD film was shown to be based on C2 radical, so additional hydrogen plasma treatment is required to impart H-termination to the surface. In recent years, Bendali et al. [62] showed that both retinal bipolar neurons and retinal ganglion cell neurons grew on unmodified O-terminated NCD, whereas glial cells demonstrated low survival with O-termination. The results suggested that O-termination can be applied on the tip of the penetrating electrode to facilitate neuroneelectrode interaction while preventing glial cell growth. O-termination is preferred at the base of the electrode to facilitate rapid sealing. This further underlined the importance of patterning the surface with different types of termination [63]. An in vivo www.sciencedirect.com
Biocompatibility and functionalization of diamond Yang and Narayan
63
Figure 3
The growth of human neurons followed the NCD pillars. (a, b) SEM pictures showing the growth of the regenerating human Scarpa’s ganglion neurites grown on the NCD pillar tops when the spacing was 4 mm. (c, d) When the spacing was increased to 9 mm, the axons still followed the structures but anchored on both the NCD pillar tops and silicon pillar bodies. Reprinted from Ref. [39] with permission from the publisher. NCD, nanocrystalline diamond; SEM, scanning electron microscope.
experiment demonstrated the stability of implanted diamond electrodes for 8 weeks in a rodent model [51]. In another study, biocompatibility of diamond MEAs in the rat cortex was observed after implantation for six months; magnetic resonance imaging showed no alteration of brain tissue [64]. In addition, few artifacts were observed because of the low magnetic susceptibility of carbon; this result suggests that diamond MEAs may be appropriate for functional imaging to investigate brain tissue. For MEAs, a foreign body reaction can induce fibrous encapsulation; this phenomenon not only affects the recorded signal from microelectrodes but also increases the threshold for stimulation by formation of a fibrous connective tissue. The encapsulation layer increases the distance between the microelectrode and the target tissue; it also increases the distance between microelectrodes during recording. The compromised signal quality, and requirement for increased charge injection may cause safety issues; furthermore, the highpower consumption is not favorable for clinical use. Alcaide et al. [65] demonstrated a thinner encapsulation layer for BDD electrodes compared with TiN electrodes after implantation for two and four weeks. Lower levels of inflammatory reaction were also observed on the BDD electrodes. The BDD electrodes demonstrated better biofouling resistance than the TiN electrodes [66]. A stable electrochemical response was demonstrated over six weeks of implantation. Garrett et al. implanted www.sciencedirect.com
diamond films into the back muscle of a guinea pig; they demonstrated that the median encapsulation thickness after implantation followed the trend NUNCD
Charge injection capacity and charge storage capacity To characterize the capability of microelectrodes to stimulate neural responses, charge injection capacity (CIC) or charge storage capacity (CSC) were usually measured using voltage transient and cyclic voltammetry (CV) approaches, respectively; these approaches serve as predictors for successful neural stimulation when comparing with the threshold charge density required for use in a neural prosthesis [31]. CIC is defined as the amount of charge delivered per unit area. There are a few mechanisms in the literature to derive it. One approach was based on the slope of voltage excursion in voltage transient [50] or the scan rate of CV [2] to obtain the capacitance of the electrode. Injection capacity was obtained by multiplying capacitance with scan range of voltage. The other way was through direct measurement of injected current to get CIC [50]. The numbers obtained with each method can be quite different. The CSC was defined as the amount of charge Current Opinion in Biomedical Engineering 2019, 10:60–68
64 Biomaterials: biomaterials and biocompatibility
Figure 4
SEM images: SK-N-SH cell attached to (a,b) poly-lysine-coated glass, (c) a solid portion of the N-UNCD membrane with 400 nm pores, (d) a 400 nm nanoporous region, (e) a solid portion of the N-UNCD membrane with 100 nm pores, and (f) a nanoporous region of the N-UNCD membrane with 100 nm pores. Reprinted from [40] with permission from the publisher.
available for the device. However, not all the charges available can be injected to give a stimulation pulse [68]. As such, CIC data cannot be replaced by CSC data. CSC data are usually obtained by performing a CV scan under a slow scan rate, which is not similar to the neural stimulation pulse; the neural stimulation pulse is typically performed at a high rate and with a high current density. Before use in electrochemical applications, an activation pretreatment is usually carried out to enhance charge Current Opinion in Biomedical Engineering 2019, 10:60–68
injection by electrochemical or plasma treatment [69,70]. Cleaning of surface contaminants and roughening the surface provided sites for rapid electron transfer and additional higher injection capacity. In addition to a change in morphology, surface termination can also play an important role. Electrochemical pretreatment with a CV scan was demonstrated to induce changes in the distribution of functional groups on the surface. After activation, CIC values ranging from 250 to 300 mC cm 2 [50] were reported with capacitive injection. Hydrogen plasma was used for activation, which rendered the www.sciencedirect.com
Biocompatibility and functionalization of diamond Yang and Narayan
Figure 5
Capacitance values for the growth sides of N-UNCD after oxygen plasma treatment for various lengths of time (red bars). Capacitance of the smooth, seeded side of the N-UNCD after 0 and 180 min of oxygen plasma (green bars). Also indicated are the capacitance of a 180 min oxygen plasma–treated sample after a further 1 min in hydrogen plasma (purple dashed line) and the previously reported capacitance of electrochemical activated N-UNCD [35] (purple dashed line). Error bars are the standard deviation calculated from at least five measurements each from two sample electrodes. Reprinted from Ref. [2] with permission from the publisher. UNCD, ultrananocrystalline diamond.
65
The ability to use NCD or UNCD as a recording electrode was assessed by electrochemical impedance spectroscopy; in this approach, a high electrode impedance corresponds to a low signal-to-noise ratio [64,66,74]. The impedance was usually measured under a frequency of 1 kHz because that value is the fundamental frequency of a neuronal action potential [75]. It was expected that the primary component of the electrode impedance may interfere with the recording signal at a frequency of 1 kHz. Piret et al. recently demonstrated an impedance value of around 103 kU for BDD electrode; a 3D nanostructured BDD MEA exhibited an impedance around 50 kU; this value is comparable to that of state-of-the-art neural electrode materials [74]. The median noise level of the 3D nanostructured BDD MEA was 3.1 mV, which was lower than the value for Pt microelectrodes (6.9 mV). However, the impedance of the conventional BDD microelectrodes was slightly higher (10.7 mV). The low noise level of the 3D nanostructured BDD MEA enabled a detection limit of 10e20 mV for the local field potential. Despite this, sometimes it may fail to measure the action potential in neurons. Cai et al. [43] demonstrated the absence of the differentiation marker for Scarpa’s ganglion neurons on an NCD surface, which could indicate immature growth of neurons or exposure to stress.
Future perspectives and challenges surface H-terminated and increased the surface conductivity. Recently, Tong et al. [71] demonstrated that oxygen plasma increases oxygen coverage, which in turn increases the hydrophilicity and double-layer capacitance properties. This caused a dramatic increase of CIC from 20 mC cm 2 of the as-grown film to 1.18 mC cm 2 after a 180-min treatment (Figure 5) [2]. Cell density, neurites per neuron, and neurite length values were high, indicating that the oxygen plasma treatment can be optimized to facilitate neuron growth. Additional hydrogen plasma treatment after oxygen plasma was shown to push the CIC to a higher value.
Use as a recording electrode Hebert et al. showed that CSC of diamond MEA was carried out with 435 mC cm 2 in phosphate-buffered saline, which was comparable with CSC of Pt electrodes. This CSC can be further improved by applying carbon nanotubes (CNTs) as a scaffold for BDD growth. By using this 3D nanostructure, Piret et al. demonstrated a CSC of 6.8 mC cm 2 in phosphate-buffered saline. However, the nickel used in CNT fabrication is carcinogenic. Metal impurities in diamond nanoparticles were reported to be cytotoxic [72]. In addition, the release of reactive oxygen species from CNTs has been reported to cause cell death [73]. Complete encapsulation of CNTs by diamond is necessary to avoid this adverse effect.
www.sciencedirect.com
The recent development of neural interfaces based on NCD or UNCD can provide an improved quality of life for individuals suffering from many types of health conditions. A diamond interface can be used to treat patients suffering from spinal cord injury, stroke, hearing loss, visual impairment, epilepsy, Parkinson’s disease, or paralysis by providing stimulation and recording functionalities. Additional research efforts are necessary to understand the in vivo performance of these materials. Improving the long-term stability of these materials on the basis of new electrode designs, changes in morphology, changes in surface termination, changes in patterns, and composite materials may be worthy of further consideration. Nanostructured features and chemistry can dramatically affect charge injection. Patterning, doping, and surface treatments provide a mechanism to create conductive and insulating regions on a single structure. Composite materials or hybrid structures may give improvements to electrochemical properties and biocompatibility. In addition, the waveform of current injection and the leakage of current with increased contact area may affect the threshold for stimulation.
Acknowledgement The authors would like to acknowledge support from US National Science Foundation Grant Number 1836767.
Conflict of interest statement Nothing declared.
Current Opinion in Biomedical Engineering 2019, 10:60–68
66 Biomaterials: biomaterials and biocompatibility
References Papers of particular interest, published within the period of review, have been highlighted as: * of special interest * * of outstanding interest 1.
2.
Ganesan K, Garrett DJ, Ahnood A, Shivdasani MN, Tong W, Turnley AM, Fox K, Meffin H, Prawer S: An all-diamond, hermetic electrical feedthrough array for a retinal prosthesis. Biomaterials 2014, 35:908–915. https://doi.org/10.1016/ j.biomaterials.2013.10.040. Tong W, Fox K, Zamani A, Turnley AM, Ganesan K, Ahnood A, Cicione R, Meffin H, Prawer S, Stacey A, Garrett DJ: Optimizing growth and post treatment of diamond for high capacitance neural interfaces. Biomaterials 2016, 104:32–42. https://doi.org/ 10.1016/j.biomaterials.2016.07.006.
3. *
Iman S, Javaherian Z, Minai-tehrani D, Ghasemi R: Antibacterial properties of fl uorinated diamond-like carbon fi lms deposited by direct and remote plasma. Mater Lett 2017, 188:84–87. https://doi.org/10.1016/j.matlet.2016.10.102. The author related the power of RF and MW plasma to the coverage of F atoms, roughness and antibacterial activity against E.coli. A clear diffference of results was demonstrated with two different mode of plasma. 4.
Nemanich RJ, Carlisle JA, Hirata A, Haenen K: CVD diamond research, applications, and challenges. MRS Bull 2014, 39: 490–494. https://doi.org/10.1557/mrs.2014.97.
5.
Auciello O, VSumant A: Status review of the science and technology of ultrananocrystalline diamond ( UNCD TM ) fi lms and application to multifunctional devices. Diam Relat Mater 2010, 19:699–718. https://doi.org/10.1016/ j.diamond.2010.03.015.
6.
7.
Konicek AR, Grierson DS, VSumant A, Friedmann TA, Sullivan JP, Gilbert PUPA, Sawyer WG, Carpick RW: Influence of surface passivation on the friction and wear behavior of ultrananocrystalline diamond and tetrahedral amorphous carbon thin films. Phys Rev B 2012, 155448:1–13. https:// doi.org/10.1103/PhysRevB.85.155448. VSumant A, Auciello O, Carpick RW, Srinivasan S, Butler JE: Ultrananocrystalline and nanocrystalline diamond thin films for MEMS/NEMS applications. MRS Bull 2010, 35:281–288.
8. *
Budil J, Matyska P, Artemenko A, Ukraintsev E, Gordeev I, Beranová J, Konopásek I, Kromka A: Anti-adhesive properties of nanocrystalline diamond fi lms against Escherichia coli bacterium: in fluence of surface termination and cultivation medium. Diam Relat Mater 2018, 83:87–93. https://doi.org/ 10.1016/j.diamond.2018.02.001. The author studied the adhesive property of E. coli with different cultivation and suggested that the NCD films can be used as the reference platform for biofilm-related experiments.
neurons on diamond - a substrate for neurodegeneration research and therapy. Biomaterials 2015, 61:139–149. https:// doi.org/10.1016/j.biomaterials.2015.04.050. 15. X.Wang, L.E.Ocola, R.S.Divan, Nanopatterning of ultrananocrystalline diamond nanowires, (n.d.). doi:10.1088/09574484/23/7/075301. 16. Prawer Steven, Nemanich Robert J: Raman spectroscopy of diamond and doped diamond. Phil Trans R Soc Lond A 2004, 362:2537–2565. https://doi.org/10.1098/rsta.2004.1451. 17. Solin SA, Ramdas AK: Raman spectrum of diamond. Phys Rev B 1970, 1:1687–1698. https://doi.org/10.1103/PhysRevB.1.1687. 18. Carvalho AF, Holz T, Santos NF, Ferro MC, Fernandes JS, Silva RF, Costa FM, Martins MA: Simultaneous CVD synthesis of graphene-diamond hybrid fi lms. Carbon N Y 2016, 98: 99–105. https://doi.org/10.1016/j.carbon.2015.10.095. 19. Butler BJE, VSumant A: The CVD of nanodiamond materials. Chem Vap Depos 2008, 14:145–160. https://doi.org/10.1002/ cvde.200700037. 20. Lux H, Edling M, Siemroth P, Schrader S: Fast and costeffective synthesis of high-quality arc evaporation. Materials (Basel) 2018, 11:804. https://doi.org/10.3390/ma11050804. 21. Nistor PA, May PW: Diamond thin films: giving biomedical applications a new shine. J R Soc Interface 2017, 14:20170382. 22. Saravanan MSS, Babu SPK, Sivaprasad K, Jagannatham M: Techno-economics of carbon nanotubes produced by open air arc discharge method. Int J Eng Sci Technol 2010, 2: 100–108. 23. Yang J, Zhang Y: Nanocrystalline diamond films grown by * * microwave plasma chemical vapor deposition and its biocompatible property. Adv Mater Phys Chem 2018, 08: 157–176. https://doi.org/10.4236/ampc.2018.84011. This review article covered a broad content of properties and structure of diamond. General biocompatible application was mentioned. 24. Majchrowicz D, Ficek M, Baran T, Wasowicz M, Majchrowicz D, * Ficek M, Baran T, Wasowicz M, StrukÎ P: Diamond-based proÎ tective layer for optical biosensors. Proc SPIE 2017, 9929. https://doi.org/10.1117/12.2240115. Diamond film was studied as protective coating for biosensor due to optiocal transparency and other attractive properties. Biocompatibility was demonstrated with whole human blood samples. 25. Briones M, Casero E, Petit-domínguez MD, Ruiz MA, Parraalfambra AM: Biosensors and Bioelectronics Diamond nanoparticles based biosensors for efficient glucose and lactate determination. Biosens Bioelectron J 2015, 68:521–528. https:// doi.org/10.1016/j.bios.2015.01.044. 26. Nebel CE, Rezek B, Shin D: Diamond for bio-sensor applications. J Phys D Appl Phys Rev 2007, 40:6443–6466. https:// doi.org/10.1088/0022-3727/40/20/S21.
Jin W, Chu PK: Surface functionalization of biomaterials by plasma and ion beam. Surf Coat Technol 2018, 336:2–8. https:// doi.org/10.1016/j.surfcoat.2017.08.011.
27. Knickerbocker T, Strother T, Schwartz MP, Russell JN, Butler J, Smith LM, Hamers RJ: DNA-modified diamond surfaces. Langmuir 2003, 19:1938–1942.
10. Wang C, Huang N, Zhuang H, Yang B, Zhai Z, Jiang X: Photochemical functionalization of diamond films using a short carbon chain acid. Chem Phys Lett J 2016, 646: 87 – 90.
28. Yang W, Auciello O, Butler JE, Cai WEI, Carlisle JA, Gerbi JE, Gruen DM, Knickerbocker T, Lasseter TL, Russell JN, Smith LM, Hamers RJ: DNA-modified nanocrystalline diamond thinfilms as stable, biologically active substrates. Nat Mater 2003, 1:253–258. https://doi.org/10.1038/nmat779.Diamond.
9.
11. Ikeda T, Teii K, Casiraghi C, Robertson J, Ferrari AC: Effect of the s p2 carbon phase on n -type conduction in nanodiamond films. J Appl Phys 2008, 104:1–7. https://doi.org/10.1063/ 1.2990061. 12. Specht CG, Williams OA, Jackman RB, Schoepfer R: Ordered growth of neurons on diamond. Biomaterials 2004, 25: 4073–4078. https://doi.org/10.1016/j.biomaterials.2003.11.006. 13. Taylor AC, Vagaska B, Edgington R, Hébert C, Ferretti P, Bergonzo P, Jackman RB: Biocompatibility of nanostructured boron doped diamond for the attachment and proliferation of human neural stem cells. J Neural Eng 2015, 12:66016. https:// doi.org/10.1088/1741-2560/12/6/066016. 14. Nistor PA, May PW, Tamagnini F, Randall AD, Caldwell MA: Long-term culture of pluripotent stem-cell-derived human Current Opinion in Biomedical Engineering 2019, 10:60–68
29. Taylor A, Fendrych F, Mandys V: Epithelial cell morphology and adhesion on diamond films deposited and chemically modified by plasma processes. Biointerphases 2014, 9: 031012. https://doi.org/10.1116/1.4890471. 30. Khanna P, Villagra A, Kim S, Seto E, Jaroszeski M, Kumar A, Bhansali S: Use of nanocrystalline diamond for microfluidic lab-on-a-chip. Diam Relat Mater 2006, 15:2073–2077. https:// doi.org/10.1016/j.diamond.2006.05.014. 31. Cogan SF: Neural stimulation and recording electrodes. Annu Rev Biomed Eng 2008, 10:275–309. https://doi.org/10.1146/ annurev.bioeng.10.061807.160518. 32. Meijs S, Fjorback M, Jensen C, Sørensen S: Electrochemical properties of titanium nitride nerve stimulation electrodes: an www.sciencedirect.com
Biocompatibility and functionalization of diamond Yang and Narayan
in vitro and in vivo study. Front Neurosci 2015, 9:1–11. https:// doi.org/10.3389/fnins.2015.00268. 33. Weiland JD, Anderson DJ, Humayun MS: In vitro electrical properties for iridium oxide versus titanium nitride stimulating electrodes. IEEE Trans Biomed Eng 2002, 49: 1574–1579. 34. Brummer SB, Turner MJ: Electrochemical considerations for safe electrical stimulation of the nervous system with platinum electrodes. IEEE Trans Biomed Eng BME 1977, 24:59–63. https://doi.org/10.1109/TBME.1977.326218. 35. Rozman J, Pec P: Electrochemical performance of platinum electrodes within the multi-electrode spiral nerve cuff. Australas Phys Eng Sci Med 2014, 37:525–533. https://doi.org/ 10.1007/s13246-014-0282-9. 36. Hudak EM, Mortimer JT, Martin HB: Platinum for neural stimulation: voltammetry considerations. J Neural Eng 2010, 7: 026005. https://doi.org/10.1088/1741-2560/7/2/026005. 37. Cogan SF, Ehrlich J, Plante TD, Smirnov A, Shire DB, Gingerich M, Rizzo JF: Sputtered iridium oxide films for neural stimulation electrodes. J Biomed Mater Res B Appl Biomater 2008:353–361. https://doi.org/10.1002/jbm.b.31223. 38. Eick S, Wallys J, Hofmann B, VanOoyen A, Schnakenberg U, Ingebrandt S, Anderson DJ: Iridium oxide microelectrode arrays for in vitro stimulation of individual rat neurons from dissociated cultures. Front Neuroeng 2009, 2:1–12. https:// doi.org/10.3389/neuro.16.016.2009. 39. Cogan SF, Troyk PR, Ehrlich J, Gasbarro CM, Plante TD: The influence of electrolyte composition on the in vitro chargeinjection limits of activated iridium oxide ( AIROF ) stimulation electrodes. J Neural Eng 2007, 4:79–86. https://doi.org/ 10.1088/1741-2560/4/2/008. 40. Cui X, Martin DC: Electrochemical deposition and characterization of poly (3, 4-ethylenedioxythiophene ) on neural microelectrode arrays. Sensor Actuator B 2003, 89:92–102. 41. Joseph D, Ludwig KA, Uram JD, Yang J, Martin DC, Kipke DR: Chronic neural recordings using silicon microelectrode arrays electrochemically deposited with a poly (3, 4ethylenedioxythiophene ) ( PEDOT ) film *. J Neural Eng 2006, 3:59–70. https://doi.org/10.1088/1741-2560/3/1/007. 42. Wilks SJ, Richardson-burns SM, Hendricks JL, Martin DC, Otto KJ: Poly (3, 4-ethylenedioxythiophene ) as a micro-neural interface material for electrostimulation. Front Neuroeng 2009, 2:1–8. https://doi.org/10.3389/neuro.16.007. 43. Cai Y, Edin F, Jin Z, Alexsson A, Gudjonsson O, Liu W, RaskAndersen H, Karlsson M, Li H: Strategy towards independent electrical stimulation from cochlear implants: guided auditory neuron growth on topographically modified nanocrystalline diamond. Acta Biomater 2016, 31:211–220. https:// doi.org/10.1016/j.actbio.2015.11.021. 44. Yang K-H, Nguyen AK, Goering PL, VSumant A, Narayan RJ: * Ultrananocrystalline diamond-coated nanoporous membranes support SK-N-SH neuroblastoma endothelial cell attachment. Interface Focus 2018, 8. http://rsfs. royalsocietypublishing.org/content/8/3/20170063.abstract. Neuroblastoma cell attachment on diamond nanoporous membrane was demonstrated. This inverse structure to rough surface or surface with island structure. 45. Blake S, Charles C: Better speech recognition with cochlear implants. Nature 1991, 352:236–238. 46. Fallon B, Leary SJO, Richardson RR, Mcdermott HJ: Principles of design and biological approaches for improving the selectivity of cochlear implant electrodes. J Neural Eng 2009, 6. https://doi.org/10.1088/1741-2560/6/5/055002. 47. Lebedev MA, Nicolelis MAL: Brain – machine interfaces : past , present and future. Trends Neurosci 2006, 29:536–546. https:// doi.org/10.1016/j.tins.2006.07.004. 48. Wei XF, Grill WM: Impedance characteristics of deep brain stimulation electrodes in vitro and in vivo. J Neural Eng 2009, 6. https://doi.org/10.1088/1741-2560/6/4/046008.
www.sciencedirect.com
67
49. Matteucci PB, Chen SC, Tsai D, Dodds CWD, Dokos S, Morley JW, Lovell NH, Suaning GJ: Current steering in retinal stimulation via a quasimonopolar stimulation paradigm. Investig Ophthalmol Vis Sci 2013, 54:4307–4320. https://doi.org/ 10.1167/iovs.13-11653. 50. Hadjinicolaou AE, Leung RT, Garrett DJ, Ganesan K, Fox K, Nayagam DAX, Shivdasani MN, Meffin H, Ibbotson MR, Prawer S, O’Brien BJ: Electrical stimulation of retinal ganglion cells with diamond and the development of an all diamond retinal prosthesis. Biomaterials 2012, 33:5812–5820. https:// doi.org/10.1016/j.biomaterials.2012.04.063. 51. Bendali A, Rousseau L, Lissorgues G, Scorsone E, Djilas M, Dégardin J, Dubus E, Fouquet S, Benosman R, Bergonzo P, Sahel JA, Picaud S: Synthetic 3D diamond-based electrodes for flexible retinal neuroprostheses: model, production and in vivo biocompatibility. Biomaterials 2015, 67:73–83. https:// doi.org/10.1016/j.biomaterials.2015.07.018. 52. Sommerhalder J, Rappaz B, DeHaller R, Fornos AP, Safran AB, Pelizzone M: Simulation of artificial vision: II. Eccentric reading of full-page text and the learning of this task. Vision Res 2004, 44:1693–1706. https://doi.org/10.1016/ j.visres.2004.01.017. 53. Joucla S, Yvert B: Improved focalization of electrical microstimulation using microelectrode arrays: a modeling study. PLoS One 2009, 4. https://doi.org/10.1371/journal.pone.0004828. 54. Voss A, Wei H, Zhang Y, Turner S, Ceccone G, Peter J, Stengl M, Popov C: Strong attachment of circadian pacemaker neurons on modified ultrananocrystalline diamond surfaces. Mater Sci Eng C 2016, 64:278–285. https://doi.org/10.1016/ j.msec.2016.03.092. 55. Chen Y, Tsai C, Lee C, Lin I: In vitro and in vivo evaluation of ultrananocrystalline diamond as an encapsulation layer for implantable microchips. Acta Biomater 2014, 10:2187–2199. https://doi.org/10.1016/j.actbio.2014.01.014. 56. Arnault JC, Girard HA: Hydrogenated nanodiamonds: synthe* * sis and surface properties. Curr Opin Solid State Mater Sci 2017, 21:10–16. https://doi.org/10.1016/j.cossms.2016.06.007. This paper present state of art hydrogenation treatments on nanodiamond and further functionalization and reactivity. The photoelectric property cound open new field of application for hydrogenated diamond. 57. Zhao Y, Yeung KWK, Chu PK: Functionalization of biomedical materials using plasma and related technologies. Appl Surf Sci 2014, 310:11–18. https://doi.org/10.1016/ j.apsusc.2014.02.168. 58. Shintani Y, Ibori S, Igarashi K, Naramura T: Polycrystalline boron-doped diamond with an oxygen-terminated surface channel as an electrolyte-solution-gate fi eld-effect transistor for pH sensing. Electrochim Acta 2016, 212:10–15. 59. Miksovsky J, Voss A, Kozarova R, Kocourek T, Pisarik P, Ceccone G: Cell adhesion and growth on ultrananocrystalline diamond and diamond-like carbon films after different surface modifications. Appl Surf Sci 2014, 297:95–102. https:// doi.org/10.1016/j.apsusc.2014.01.085. 60. Voss A, Mozafari M, Popov C, Ceccone G, Kulisch W, * * Reithmaier JP: Surface & Coatings Technology Stability of the surface termination of differently modi fi ed ultrananocrystalline diamond/amorphous carbon composite fi lms *. Surf Coating Technol J 2012, 209:184–189. https:// doi.org/10.1016/j.surfcoat.2012.08.049. This paper brought out preferential attachment of cells and guided growth on UNCD surface. The applicability of surface patterning was demonstrated. 61. Sen FG, Qi Y, Alpas AT: Surface stability and electronic structure of hydrogen and fluorine terminated diamond surfaces: a first principles investigation surface stability and electronic structure of hydrogen- and fluorine-terminated diamond surfaces: a first principles invest. J Mater Res 2009, 24:2461–2470. https://doi.org/10.1557/JMR.2009.0309. 62. Bendali A, Agnès C, Meffert S, Forster V, Bongrain A, Arnault JC, Sahel JA, Offenhäusser A, Bergonzo P, Picaud S: Distinctive glial and neuronal interfacing on nanocrystalline diamond. PLoS One 2014, 9. https://doi.org/10.1371/journal.pone.0092562. Current Opinion in Biomedical Engineering 2019, 10:60–68
68 Biomaterials: biomaterials and biocompatibility
63. Voss A, Stateva SR, Reithmaier JP, Apostolova MD, Popov C: Patterning of the surface termination of ultrananocrystalline diamond films for guided cell attachment and growth. Surf Coating Technol 2017, 321:229–235. https://doi.org/10.1016/ j.surfcoat.2017.04.066. 64. Hébert C, Warnking J, Depaulis A, Garçon LA, Mermoux M, Eon D, Mailley P, Omnès F: Microfabrication, characterization and in vivo MRI compatibility of diamond microelectrodes array for neural interfacing. Mater Sci Eng C 2015, 46:25–31. https://doi.org/10.1016/j.msec.2014.10.018. 65. Alcaide M, Taylor A, Fjorback M, Zachar V, Pennisi CP: Borondoped nanocrystalline diamond electrodes for neural interfaces: in vivo biocompatibility evaluation. Front Neurosci 2016, 10:1–9. https://doi.org/10.3389/fnins.2016.00087. 66. Meijs S, Alcaide M, Sørensen C, McDonald M, Sørensen S, Rechendorff K, Gerhardt A, Nesladek M, Rijkhoff NJM, Pennisi CP: Biofouling resistance of boron-doped diamond neural stimulation electrodes is superior to titanium nitride electrodes in vivo. J Neural Eng 2016, 13:1–12. https://doi.org/ 10.1088/1741-2560/13/5/056011. 67. Garrett DJ, Saunders AL, McGowan C, Specks J, Ganesan K, Meffin H, Williams RA, Nayagam DAX: In vivo biocompatibility of boron doped and nitrogen included conductivediamond for use in medical implants. J Biomed Mater Res B Appl Biomater 2016, 104:19 –26. https://doi.org/10.1002/ jbm.b.33331. 68. Ganji M, Tanaka A, Gilja V, Halgren E, Dayeh SA: Scaling effects on the electrochemical stimulation performance of Au , Pt , and PEDOT: PSS electrocorticography arrays. Adv Funct Mater 2017, 1703019. https://doi.org/10.1002/adfm.201703019. 69. Boris Duran GMS, Brocenschi Ricardo F, France Marion, Galligan James J: Electrochemical activation of diamond
Current Opinion in Biomedical Engineering 2019, 10:60–68
microelectrodes: implications for the in vitro measurement of serotonin in the bowel. Analyst 2014, 139:3160–3166. https:// doi.org/10.1002/bmb.20244.DNA. 70. Garrett DJ, Ganesan K, Stacey A, Fox K, Meffin H, Prawer S: Ultra-nanocrystalline diamond electrodes: optimization towards neural stimulation applications. J Neural Eng 2012, 9. https://doi.org/10.1088/1741-2560/9/1/016002. 71. Kim YT, Ito Y, Tadai K, Mitani T, Kim US, Kim HS, Cho BW: Drastic change of electric double layer capacitance by surface functionalization of carbon nanotubes. Appl Phys Lett 2005, 87:1–3. https://doi.org/10.1063/1.2139839. 72. Keremidarska M, Ganeva A, Mitev D, Hikov T, Presker R, Pramatarova L, Krasteva N: Comparative study of cytotoxicity of detonation nanodiamond particles with an osteosarcoma cell line and primary mesenchymal stem cells. Biotechnol Biotechnol Equip 2014, 28:733–739. https://doi.org/10.1080/ 13102818.2014.947704. 73. Alarifi S, Ali D, Verma A, Almajhdi FN, Al-Qahtani AA: Singlewalled carbon nanotubes induce cytotoxicity and DNA damage via reactive oxygen species in human hepatocarcinoma cells. In Vitro Cell Dev Biol Anim 2014, 50:714–722. https://doi.org/10.1007/s11626-014-9760-3. 74. Piret G, Hébert C, Mazellier JP, Rousseau L, Scorsone E, Cottance M, Lissorgues G, Heuschkel MO, Picaud S, Bergonzo P, Yvert B: 3D-nanostructured boron-doped diamond for microelectrode array neural interfacing. Biomaterials 2015, 53:173–183. https://doi.org/10.1016/ j.biomaterials.2015.02.021. 75. Williams JC, Hippensteel JA, Dilgen J, Shain W, Kipke DR: Complex impedance spectroscopy for monitoring tissue responses to inserted neural implants. J Neural Eng 2007, 4: 410–423. https://doi.org/10.1088/1741-2560/4/4/007.
www.sciencedirect.com
ScienceDirect
Current Opinion in
Biomedical Engineering
Biocompatibility and functionalization of diamond for neural applications Kai-Hung Yang1,2 and Roger J. Narayan1 Abstract
Diamond has been studied as an interface between medical devices and the body because of its wide potential window, chemical inertness, mechanical hardness, capability for surface modification, tunable electrical conductivity, and biocompatibility. Diamond coatings have been considered for use in a variety of medical device applications, including protective coatings, biointerfaces, and biosensors. For example, diamond has been investigated for use in neural stimulation because it exhibits not only stability but also a wide potential window. This manuscript reviews the development of neural interfaces on the basis of diamond coatings, which can provide an improved quality of life for individuals suffering from many types of medical conditions. Addresses 1 Joint Department of Biomedical Engineering, University of North Carolina and North Carolina State University, Raleigh, NC, USA 2 Department of Materials Science & Engineering, North Carolina State University, Raleigh, NC, USA Corresponding author: Narayan, Roger J. ([email protected])
Current Opinion in Biomedical Engineering 2019, 10:60–68 This review comes from a themed issue on Biomaterials: Biomaterials and Biocompatibility Edited by Masayuki Yamato and Masoud Mozafari
https://doi.org/10.1016/j.cobme.2019.03.002 2468-4511/© 2019 Elsevier Inc. All rights reserved.
Keywords Diamond, Thin film, Medical device, Neural stimulation.
Background Diamond has been studied as an interface between medical devices and the human body for several decades because of its wide potential window [1,2], chemical inertness [3,4], mechanical hardness [5e7], capability for surface modification [8e10], tunable electrical conductivity [11], and biocompatibility [12e14]. Based on grain size, diamond coatings can be classified into microcrystalline diamond, nanocrystalline diamond (NCD), and ultrananocrystalline diamond (UNCD) (Figure 1a) [7]. NCD and UNCD, which exhibit small grain sizes and low roughness values, may be used in microelectromechanical systems and other tribological applications [5,15].
Current Opinion in Biomedical Engineering 2019, 10:60–68
Raman spectroscopy is commonly used for examining the bonding of carbon atoms in diamond [16,17]. The Raman peak at 1140 cm 1 is sometimes noted in diamond coatings with small grain size (<0.1 mm). The 1140 cm 1 peak has been associated with NCD coatings or sp2bonded carbon atoms in NCD coatings. The peak at 1332 cm 1 has been associated with sp3-bonded carbon atoms and is attributed to the zone center optical phonon mode, which exhibits F2g symmetry. This peak has a narrower full width at a half maximum value (2 cm 1) and a higher peak intensity in highly tetrahedral materials such as natural diamond. Broadening of this peak is observed in diamond coatings with large amounts of amorphous carbon and small grain sizes. The broad hump at 1580 cm 1 is called the graphite (G) band; it is the optically allowed E2g zone center mode that is associated with crystalline graphite. The small shoulder at 1350 cm 1 region is the A1g mode of graphite; it is known as the disordered (D) band. These two features are found in sp2-bonded amorphous carbon. The peak at 1470 cm 1 is also associated with amorphous carbon. An example of a Raman spectrum showing features associated with diamond and other forms of carbon is illustrated in Figure 2 [18]. Other characterization techniques such as near-edge X-ray absorption fine structure spectroscopy and electron energy loss spectroscopy can be used to determine the sp2/sp3 ratio in diamond coatings [19]. Diamond can be synthesized using cost-efficient chemical vapor deposition (CVD) methods, including hot filament CVD and microwave plasma CVD (MPCVD) [4,20e22]. MPCVD is widely used in laboratory and industry settings. MPCVD can provide a high-density plasma and a high concentration of active species, enabling deposition at low temperature and low pressure. Additionally, MPCVD enables high-quality NCD or UNCD coatings be grown in the absence of contamination from the filament materials [23]. A schematic diagram of the CVD approach is shown in Figure 1b.
Electrical stimulation and biocompatibility NCD and UNCD have been considered for use in a variety of medical device applications, including protective coatings, biointerfaces, and biosensors [24e28]. The mechanical strength and wear resistance of diamond coatings make them a proper candidate as protective coating for heart valve and joint prostheses. Anchoring of proteins, cells, or DNA on the surface of diamond coatings may facilitate uses of these materials as biointerfaces and biosensors. Intrinsic diamond is a www.sciencedirect.com
Biocompatibility and functionalization of diamond Yang and Narayan
61
Figure 1
(a) Scanning electron microscopy images showing typical surface morphology of microcrystalline, nanocrystalline, and ultrananocrystalline diamond from left to right. Reprinted from Ref. [7] with permission from the publisher. (b) Schematic diagram of microwave CVD. CVD, chemical vapor deposition.
semiconductor material with a wide bandgap. The conductivity of diamond can be greatly increased with boron (p-type) or nitrogen (n-type) doping [11]; doping can increase conductivity to around 200 U 1cm 1 [5].
Field emission by hydrogen-terminated diamond with negative electron affinity has also been demonstrated [29,30]. Under electrical stimulation, charge was delivered in the leading phase to depolarize the membranes
Figure 2
Raman spectrum of diamond and other carbon features. Reprinted from Ref. [18] with permission from the publisher. www.sciencedirect.com
Current Opinion in Biomedical Engineering 2019, 10:60–68
62 Biomaterials: biomaterials and biocompatibility
of excitable cells by either the capacitive injection mechanism or the faradaic injection mechanism [31]. The most commonly used conventional materials are titanium nitride [32,33], platinum [34e36], and iridium oxide [37e39] with capacitive injection, pseudocapacitive injection, and faradaic injection approaches, respectively. Among them, faradaic injection is not favored because it may change local environment such as water electrolysis, change in the pH value, protein reduction, or oxidation; these processes may be detrimental to cells. Dissolution of the electrode, delamination, and breakdown of the passivation film may also impair function. Poly(3,4-ethylenedioxythiophene), an electrically conductive polymer, has also been studied as electrode material [40e42]; however, the long-term stability of this material is uncertain. Diamond is a promising material for neural stimulation that exhibits not only stability but also a wide potential window to avoid the electrolysis of water. In the previous studies, diamond has been demonstrated to have a potential window of around 3e3.2 V, which is higher than that of all the materials mentioned previously. The mechanical integrity and chemical inertness provided by diamond make it an appropriate material for long-term use. One of the concerns for application of NCD or UNCD as a biointerface for neural stimulation or recording is biocompatibility. Because NCD is doped with boron to give tunable electrical conductivity, it might demonstrate cytotoxicity with higher doping concentration (1021 cm 3 or higher). Surface termination and hydrophilicity were also important for determining cellular attachment, differentiation, and proliferation. In 2004, Specht et al. [12] demonstrated ordered growth of neurons on a diamond single crystal. In recent years, Taylor et al. [13] showed that human neural stem cells are able to attach and proliferate on NCD and borondoped NCD surfaces that exhibit high levels of boron doping (w1021 cm 3). For long-term stability and compatibility, Nistor et al. [14] examined differentiation and function of neurons; they demonstrated that borondoped diamond (BDD) can support pluripotent stem cellederived human neurons after long-term culture. Neural stimulation and brainemachine interfaces can not only act as neural prostheses but also treat medical conditions. In neural stimulation, a microelectrode is often used to provide sufficient charge density injection over a small surface area [31]. These devices can be used for selected stimulation of tissues with good spatial resolution. Electrodes with high relative surface areas may have enhanced attachment of neuron cells; rough surfaces have been shown to provide better cell attachment than flat surfaces (Figure 3) [43]. Too high or too low of roughness might have adverse effect. As shown in Figure 4, nanoporous membranes have also Current Opinion in Biomedical Engineering 2019, 10:60–68
been demonstrated to provide cellular anchoring [44]. This study indicates that many types of microscale and nanoscale structures may have appropriate functionality to serve as biointerfaces.
Surface functionalization After the demonstration of cochlear implants for hearing loss [45,46] and deep brain stimulation devices for Parkinson’s disease [47,48], visual prostheses [1,49e51] are being investigated for providing blind patients with capabilities for text reading, facial recognition, and sense of direction. A microelectrode array (MEA) with at least 600 pixels is commonly used in visual prostheses [52]. From an engineering side of view, a ground grid configuration is recommended to give better electrode resolution compared with distant ground, bipolar [53], and hexapolar return electrode configurations [49]. Additionally, 3D nanostructured electrodes can provide higher resolution compared with their planar counterparts [51]. To create effective neural prostheses, studies on the behavior of both retinal neurons and glial cells are necessary because adhesion of glial cell and gliosis can affect the interaction between the electrode and the cells and long-term efficacy. Surface termination is an important factor for controlling the attachment of cells to the diamond surface because neural cells tend to have stronger attachment to hydrophilic surfaces. Surface treatments were usually achieved through plasma [8,9,54e57] or photochemical reactions [10,58,59]. Four common surface termination approaches that have been demonstrated include hydrogen termination, oxygen termination, fluorine termination, and amino termination. These four terminations gave distinct surface hydrophilicity and water contact angle (F-termination>H-termination>NH2-termination>O-termination) attributes. Although NH2 termination is relatively unstable when stored in air, NH2 termination can be retained to a significant extent for up to three months if properly stored under reduced pressure [60,61]. Most as-grown diamond surfaces are H-terminated because the film growth involves the CH3* radical [7]; however, nitrogen-incorporated UNCD is not intrinsically Hterminated. The growth of nitrogen-incorporated UNCD film was shown to be based on C2 radical, so additional hydrogen plasma treatment is required to impart H-termination to the surface. In recent years, Bendali et al. [62] showed that both retinal bipolar neurons and retinal ganglion cell neurons grew on unmodified O-terminated NCD, whereas glial cells demonstrated low survival with O-termination. The results suggested that O-termination can be applied on the tip of the penetrating electrode to facilitate neuroneelectrode interaction while preventing glial cell growth. O-termination is preferred at the base of the electrode to facilitate rapid sealing. This further underlined the importance of patterning the surface with different types of termination [63]. An in vivo www.sciencedirect.com
Biocompatibility and functionalization of diamond Yang and Narayan
63
Figure 3
The growth of human neurons followed the NCD pillars. (a, b) SEM pictures showing the growth of the regenerating human Scarpa’s ganglion neurites grown on the NCD pillar tops when the spacing was 4 mm. (c, d) When the spacing was increased to 9 mm, the axons still followed the structures but anchored on both the NCD pillar tops and silicon pillar bodies. Reprinted from Ref. [39] with permission from the publisher. NCD, nanocrystalline diamond; SEM, scanning electron microscope.
experiment demonstrated the stability of implanted diamond electrodes for 8 weeks in a rodent model [51]. In another study, biocompatibility of diamond MEAs in the rat cortex was observed after implantation for six months; magnetic resonance imaging showed no alteration of brain tissue [64]. In addition, few artifacts were observed because of the low magnetic susceptibility of carbon; this result suggests that diamond MEAs may be appropriate for functional imaging to investigate brain tissue. For MEAs, a foreign body reaction can induce fibrous encapsulation; this phenomenon not only affects the recorded signal from microelectrodes but also increases the threshold for stimulation by formation of a fibrous connective tissue. The encapsulation layer increases the distance between the microelectrode and the target tissue; it also increases the distance between microelectrodes during recording. The compromised signal quality, and requirement for increased charge injection may cause safety issues; furthermore, the highpower consumption is not favorable for clinical use. Alcaide et al. [65] demonstrated a thinner encapsulation layer for BDD electrodes compared with TiN electrodes after implantation for two and four weeks. Lower levels of inflammatory reaction were also observed on the BDD electrodes. The BDD electrodes demonstrated better biofouling resistance than the TiN electrodes [66]. A stable electrochemical response was demonstrated over six weeks of implantation. Garrett et al. implanted www.sciencedirect.com
diamond films into the back muscle of a guinea pig; they demonstrated that the median encapsulation thickness after implantation followed the trend NUNCD
Charge injection capacity and charge storage capacity To characterize the capability of microelectrodes to stimulate neural responses, charge injection capacity (CIC) or charge storage capacity (CSC) were usually measured using voltage transient and cyclic voltammetry (CV) approaches, respectively; these approaches serve as predictors for successful neural stimulation when comparing with the threshold charge density required for use in a neural prosthesis [31]. CIC is defined as the amount of charge delivered per unit area. There are a few mechanisms in the literature to derive it. One approach was based on the slope of voltage excursion in voltage transient [50] or the scan rate of CV [2] to obtain the capacitance of the electrode. Injection capacity was obtained by multiplying capacitance with scan range of voltage. The other way was through direct measurement of injected current to get CIC [50]. The numbers obtained with each method can be quite different. The CSC was defined as the amount of charge Current Opinion in Biomedical Engineering 2019, 10:60–68
64 Biomaterials: biomaterials and biocompatibility
Figure 4
SEM images: SK-N-SH cell attached to (a,b) poly-lysine-coated glass, (c) a solid portion of the N-UNCD membrane with 400 nm pores, (d) a 400 nm nanoporous region, (e) a solid portion of the N-UNCD membrane with 100 nm pores, and (f) a nanoporous region of the N-UNCD membrane with 100 nm pores. Reprinted from [40] with permission from the publisher.
available for the device. However, not all the charges available can be injected to give a stimulation pulse [68]. As such, CIC data cannot be replaced by CSC data. CSC data are usually obtained by performing a CV scan under a slow scan rate, which is not similar to the neural stimulation pulse; the neural stimulation pulse is typically performed at a high rate and with a high current density. Before use in electrochemical applications, an activation pretreatment is usually carried out to enhance charge Current Opinion in Biomedical Engineering 2019, 10:60–68
injection by electrochemical or plasma treatment [69,70]. Cleaning of surface contaminants and roughening the surface provided sites for rapid electron transfer and additional higher injection capacity. In addition to a change in morphology, surface termination can also play an important role. Electrochemical pretreatment with a CV scan was demonstrated to induce changes in the distribution of functional groups on the surface. After activation, CIC values ranging from 250 to 300 mC cm 2 [50] were reported with capacitive injection. Hydrogen plasma was used for activation, which rendered the www.sciencedirect.com
Biocompatibility and functionalization of diamond Yang and Narayan
Figure 5
Capacitance values for the growth sides of N-UNCD after oxygen plasma treatment for various lengths of time (red bars). Capacitance of the smooth, seeded side of the N-UNCD after 0 and 180 min of oxygen plasma (green bars). Also indicated are the capacitance of a 180 min oxygen plasma–treated sample after a further 1 min in hydrogen plasma (purple dashed line) and the previously reported capacitance of electrochemical activated N-UNCD [35] (purple dashed line). Error bars are the standard deviation calculated from at least five measurements each from two sample electrodes. Reprinted from Ref. [2] with permission from the publisher. UNCD, ultrananocrystalline diamond.
65
The ability to use NCD or UNCD as a recording electrode was assessed by electrochemical impedance spectroscopy; in this approach, a high electrode impedance corresponds to a low signal-to-noise ratio [64,66,74]. The impedance was usually measured under a frequency of 1 kHz because that value is the fundamental frequency of a neuronal action potential [75]. It was expected that the primary component of the electrode impedance may interfere with the recording signal at a frequency of 1 kHz. Piret et al. recently demonstrated an impedance value of around 103 kU for BDD electrode; a 3D nanostructured BDD MEA exhibited an impedance around 50 kU; this value is comparable to that of state-of-the-art neural electrode materials [74]. The median noise level of the 3D nanostructured BDD MEA was 3.1 mV, which was lower than the value for Pt microelectrodes (6.9 mV). However, the impedance of the conventional BDD microelectrodes was slightly higher (10.7 mV). The low noise level of the 3D nanostructured BDD MEA enabled a detection limit of 10e20 mV for the local field potential. Despite this, sometimes it may fail to measure the action potential in neurons. Cai et al. [43] demonstrated the absence of the differentiation marker for Scarpa’s ganglion neurons on an NCD surface, which could indicate immature growth of neurons or exposure to stress.
Future perspectives and challenges surface H-terminated and increased the surface conductivity. Recently, Tong et al. [71] demonstrated that oxygen plasma increases oxygen coverage, which in turn increases the hydrophilicity and double-layer capacitance properties. This caused a dramatic increase of CIC from 20 mC cm 2 of the as-grown film to 1.18 mC cm 2 after a 180-min treatment (Figure 5) [2]. Cell density, neurites per neuron, and neurite length values were high, indicating that the oxygen plasma treatment can be optimized to facilitate neuron growth. Additional hydrogen plasma treatment after oxygen plasma was shown to push the CIC to a higher value.
Use as a recording electrode Hebert et al. showed that CSC of diamond MEA was carried out with 435 mC cm 2 in phosphate-buffered saline, which was comparable with CSC of Pt electrodes. This CSC can be further improved by applying carbon nanotubes (CNTs) as a scaffold for BDD growth. By using this 3D nanostructure, Piret et al. demonstrated a CSC of 6.8 mC cm 2 in phosphate-buffered saline. However, the nickel used in CNT fabrication is carcinogenic. Metal impurities in diamond nanoparticles were reported to be cytotoxic [72]. In addition, the release of reactive oxygen species from CNTs has been reported to cause cell death [73]. Complete encapsulation of CNTs by diamond is necessary to avoid this adverse effect.
www.sciencedirect.com
The recent development of neural interfaces based on NCD or UNCD can provide an improved quality of life for individuals suffering from many types of health conditions. A diamond interface can be used to treat patients suffering from spinal cord injury, stroke, hearing loss, visual impairment, epilepsy, Parkinson’s disease, or paralysis by providing stimulation and recording functionalities. Additional research efforts are necessary to understand the in vivo performance of these materials. Improving the long-term stability of these materials on the basis of new electrode designs, changes in morphology, changes in surface termination, changes in patterns, and composite materials may be worthy of further consideration. Nanostructured features and chemistry can dramatically affect charge injection. Patterning, doping, and surface treatments provide a mechanism to create conductive and insulating regions on a single structure. Composite materials or hybrid structures may give improvements to electrochemical properties and biocompatibility. In addition, the waveform of current injection and the leakage of current with increased contact area may affect the threshold for stimulation.
Acknowledgement The authors would like to acknowledge support from US National Science Foundation Grant Number 1836767.
Conflict of interest statement Nothing declared.
Current Opinion in Biomedical Engineering 2019, 10:60–68
66 Biomaterials: biomaterials and biocompatibility
References Papers of particular interest, published within the period of review, have been highlighted as: * of special interest * * of outstanding interest 1.
2.
Ganesan K, Garrett DJ, Ahnood A, Shivdasani MN, Tong W, Turnley AM, Fox K, Meffin H, Prawer S: An all-diamond, hermetic electrical feedthrough array for a retinal prosthesis. Biomaterials 2014, 35:908–915. https://doi.org/10.1016/ j.biomaterials.2013.10.040. Tong W, Fox K, Zamani A, Turnley AM, Ganesan K, Ahnood A, Cicione R, Meffin H, Prawer S, Stacey A, Garrett DJ: Optimizing growth and post treatment of diamond for high capacitance neural interfaces. Biomaterials 2016, 104:32–42. https://doi.org/ 10.1016/j.biomaterials.2016.07.006.
3. *
Iman S, Javaherian Z, Minai-tehrani D, Ghasemi R: Antibacterial properties of fl uorinated diamond-like carbon fi lms deposited by direct and remote plasma. Mater Lett 2017, 188:84–87. https://doi.org/10.1016/j.matlet.2016.10.102. The author related the power of RF and MW plasma to the coverage of F atoms, roughness and antibacterial activity against E.coli. A clear diffference of results was demonstrated with two different mode of plasma. 4.
Nemanich RJ, Carlisle JA, Hirata A, Haenen K: CVD diamond research, applications, and challenges. MRS Bull 2014, 39: 490–494. https://doi.org/10.1557/mrs.2014.97.
5.
Auciello O, VSumant A: Status review of the science and technology of ultrananocrystalline diamond ( UNCD TM ) fi lms and application to multifunctional devices. Diam Relat Mater 2010, 19:699–718. https://doi.org/10.1016/ j.diamond.2010.03.015.
6.
7.
Konicek AR, Grierson DS, VSumant A, Friedmann TA, Sullivan JP, Gilbert PUPA, Sawyer WG, Carpick RW: Influence of surface passivation on the friction and wear behavior of ultrananocrystalline diamond and tetrahedral amorphous carbon thin films. Phys Rev B 2012, 155448:1–13. https:// doi.org/10.1103/PhysRevB.85.155448. VSumant A, Auciello O, Carpick RW, Srinivasan S, Butler JE: Ultrananocrystalline and nanocrystalline diamond thin films for MEMS/NEMS applications. MRS Bull 2010, 35:281–288.
8. *
Budil J, Matyska P, Artemenko A, Ukraintsev E, Gordeev I, Beranová J, Konopásek I, Kromka A: Anti-adhesive properties of nanocrystalline diamond fi lms against Escherichia coli bacterium: in fluence of surface termination and cultivation medium. Diam Relat Mater 2018, 83:87–93. https://doi.org/ 10.1016/j.diamond.2018.02.001. The author studied the adhesive property of E. coli with different cultivation and suggested that the NCD films can be used as the reference platform for biofilm-related experiments.
neurons on diamond - a substrate for neurodegeneration research and therapy. Biomaterials 2015, 61:139–149. https:// doi.org/10.1016/j.biomaterials.2015.04.050. 15. X.Wang, L.E.Ocola, R.S.Divan, Nanopatterning of ultrananocrystalline diamond nanowires, (n.d.). doi:10.1088/09574484/23/7/075301. 16. Prawer Steven, Nemanich Robert J: Raman spectroscopy of diamond and doped diamond. Phil Trans R Soc Lond A 2004, 362:2537–2565. https://doi.org/10.1098/rsta.2004.1451. 17. Solin SA, Ramdas AK: Raman spectrum of diamond. Phys Rev B 1970, 1:1687–1698. https://doi.org/10.1103/PhysRevB.1.1687. 18. Carvalho AF, Holz T, Santos NF, Ferro MC, Fernandes JS, Silva RF, Costa FM, Martins MA: Simultaneous CVD synthesis of graphene-diamond hybrid fi lms. Carbon N Y 2016, 98: 99–105. https://doi.org/10.1016/j.carbon.2015.10.095. 19. Butler BJE, VSumant A: The CVD of nanodiamond materials. Chem Vap Depos 2008, 14:145–160. https://doi.org/10.1002/ cvde.200700037. 20. Lux H, Edling M, Siemroth P, Schrader S: Fast and costeffective synthesis of high-quality arc evaporation. Materials (Basel) 2018, 11:804. https://doi.org/10.3390/ma11050804. 21. Nistor PA, May PW: Diamond thin films: giving biomedical applications a new shine. J R Soc Interface 2017, 14:20170382. 22. Saravanan MSS, Babu SPK, Sivaprasad K, Jagannatham M: Techno-economics of carbon nanotubes produced by open air arc discharge method. Int J Eng Sci Technol 2010, 2: 100–108. 23. Yang J, Zhang Y: Nanocrystalline diamond films grown by * * microwave plasma chemical vapor deposition and its biocompatible property. Adv Mater Phys Chem 2018, 08: 157–176. https://doi.org/10.4236/ampc.2018.84011. This review article covered a broad content of properties and structure of diamond. General biocompatible application was mentioned. 24. Majchrowicz D, Ficek M, Baran T, Wasowicz M, Majchrowicz D, * Ficek M, Baran T, Wasowicz M, StrukÎ P: Diamond-based proÎ tective layer for optical biosensors. Proc SPIE 2017, 9929. https://doi.org/10.1117/12.2240115. Diamond film was studied as protective coating for biosensor due to optiocal transparency and other attractive properties. Biocompatibility was demonstrated with whole human blood samples. 25. Briones M, Casero E, Petit-domínguez MD, Ruiz MA, Parraalfambra AM: Biosensors and Bioelectronics Diamond nanoparticles based biosensors for efficient glucose and lactate determination. Biosens Bioelectron J 2015, 68:521–528. https:// doi.org/10.1016/j.bios.2015.01.044. 26. Nebel CE, Rezek B, Shin D: Diamond for bio-sensor applications. J Phys D Appl Phys Rev 2007, 40:6443–6466. https:// doi.org/10.1088/0022-3727/40/20/S21.
Jin W, Chu PK: Surface functionalization of biomaterials by plasma and ion beam. Surf Coat Technol 2018, 336:2–8. https:// doi.org/10.1016/j.surfcoat.2017.08.011.
27. Knickerbocker T, Strother T, Schwartz MP, Russell JN, Butler J, Smith LM, Hamers RJ: DNA-modified diamond surfaces. Langmuir 2003, 19:1938–1942.
10. Wang C, Huang N, Zhuang H, Yang B, Zhai Z, Jiang X: Photochemical functionalization of diamond films using a short carbon chain acid. Chem Phys Lett J 2016, 646: 87 – 90.
28. Yang W, Auciello O, Butler JE, Cai WEI, Carlisle JA, Gerbi JE, Gruen DM, Knickerbocker T, Lasseter TL, Russell JN, Smith LM, Hamers RJ: DNA-modified nanocrystalline diamond thinfilms as stable, biologically active substrates. Nat Mater 2003, 1:253–258. https://doi.org/10.1038/nmat779.Diamond.
9.
11. Ikeda T, Teii K, Casiraghi C, Robertson J, Ferrari AC: Effect of the s p2 carbon phase on n -type conduction in nanodiamond films. J Appl Phys 2008, 104:1–7. https://doi.org/10.1063/ 1.2990061. 12. Specht CG, Williams OA, Jackman RB, Schoepfer R: Ordered growth of neurons on diamond. Biomaterials 2004, 25: 4073–4078. https://doi.org/10.1016/j.biomaterials.2003.11.006. 13. Taylor AC, Vagaska B, Edgington R, Hébert C, Ferretti P, Bergonzo P, Jackman RB: Biocompatibility of nanostructured boron doped diamond for the attachment and proliferation of human neural stem cells. J Neural Eng 2015, 12:66016. https:// doi.org/10.1088/1741-2560/12/6/066016. 14. Nistor PA, May PW, Tamagnini F, Randall AD, Caldwell MA: Long-term culture of pluripotent stem-cell-derived human Current Opinion in Biomedical Engineering 2019, 10:60–68
29. Taylor A, Fendrych F, Mandys V: Epithelial cell morphology and adhesion on diamond films deposited and chemically modified by plasma processes. Biointerphases 2014, 9: 031012. https://doi.org/10.1116/1.4890471. 30. Khanna P, Villagra A, Kim S, Seto E, Jaroszeski M, Kumar A, Bhansali S: Use of nanocrystalline diamond for microfluidic lab-on-a-chip. Diam Relat Mater 2006, 15:2073–2077. https:// doi.org/10.1016/j.diamond.2006.05.014. 31. Cogan SF: Neural stimulation and recording electrodes. Annu Rev Biomed Eng 2008, 10:275–309. https://doi.org/10.1146/ annurev.bioeng.10.061807.160518. 32. Meijs S, Fjorback M, Jensen C, Sørensen S: Electrochemical properties of titanium nitride nerve stimulation electrodes: an www.sciencedirect.com
Biocompatibility and functionalization of diamond Yang and Narayan
in vitro and in vivo study. Front Neurosci 2015, 9:1–11. https:// doi.org/10.3389/fnins.2015.00268. 33. Weiland JD, Anderson DJ, Humayun MS: In vitro electrical properties for iridium oxide versus titanium nitride stimulating electrodes. IEEE Trans Biomed Eng 2002, 49: 1574–1579. 34. Brummer SB, Turner MJ: Electrochemical considerations for safe electrical stimulation of the nervous system with platinum electrodes. IEEE Trans Biomed Eng BME 1977, 24:59–63. https://doi.org/10.1109/TBME.1977.326218. 35. Rozman J, Pec P: Electrochemical performance of platinum electrodes within the multi-electrode spiral nerve cuff. Australas Phys Eng Sci Med 2014, 37:525–533. https://doi.org/ 10.1007/s13246-014-0282-9. 36. Hudak EM, Mortimer JT, Martin HB: Platinum for neural stimulation: voltammetry considerations. J Neural Eng 2010, 7: 026005. https://doi.org/10.1088/1741-2560/7/2/026005. 37. Cogan SF, Ehrlich J, Plante TD, Smirnov A, Shire DB, Gingerich M, Rizzo JF: Sputtered iridium oxide films for neural stimulation electrodes. J Biomed Mater Res B Appl Biomater 2008:353–361. https://doi.org/10.1002/jbm.b.31223. 38. Eick S, Wallys J, Hofmann B, VanOoyen A, Schnakenberg U, Ingebrandt S, Anderson DJ: Iridium oxide microelectrode arrays for in vitro stimulation of individual rat neurons from dissociated cultures. Front Neuroeng 2009, 2:1–12. https:// doi.org/10.3389/neuro.16.016.2009. 39. Cogan SF, Troyk PR, Ehrlich J, Gasbarro CM, Plante TD: The influence of electrolyte composition on the in vitro chargeinjection limits of activated iridium oxide ( AIROF ) stimulation electrodes. J Neural Eng 2007, 4:79–86. https://doi.org/ 10.1088/1741-2560/4/2/008. 40. Cui X, Martin DC: Electrochemical deposition and characterization of poly (3, 4-ethylenedioxythiophene ) on neural microelectrode arrays. Sensor Actuator B 2003, 89:92–102. 41. Joseph D, Ludwig KA, Uram JD, Yang J, Martin DC, Kipke DR: Chronic neural recordings using silicon microelectrode arrays electrochemically deposited with a poly (3, 4ethylenedioxythiophene ) ( PEDOT ) film *. J Neural Eng 2006, 3:59–70. https://doi.org/10.1088/1741-2560/3/1/007. 42. Wilks SJ, Richardson-burns SM, Hendricks JL, Martin DC, Otto KJ: Poly (3, 4-ethylenedioxythiophene ) as a micro-neural interface material for electrostimulation. Front Neuroeng 2009, 2:1–8. https://doi.org/10.3389/neuro.16.007. 43. Cai Y, Edin F, Jin Z, Alexsson A, Gudjonsson O, Liu W, RaskAndersen H, Karlsson M, Li H: Strategy towards independent electrical stimulation from cochlear implants: guided auditory neuron growth on topographically modified nanocrystalline diamond. Acta Biomater 2016, 31:211–220. https:// doi.org/10.1016/j.actbio.2015.11.021. 44. Yang K-H, Nguyen AK, Goering PL, VSumant A, Narayan RJ: * Ultrananocrystalline diamond-coated nanoporous membranes support SK-N-SH neuroblastoma endothelial cell attachment. Interface Focus 2018, 8. http://rsfs. royalsocietypublishing.org/content/8/3/20170063.abstract. Neuroblastoma cell attachment on diamond nanoporous membrane was demonstrated. This inverse structure to rough surface or surface with island structure. 45. Blake S, Charles C: Better speech recognition with cochlear implants. Nature 1991, 352:236–238. 46. Fallon B, Leary SJO, Richardson RR, Mcdermott HJ: Principles of design and biological approaches for improving the selectivity of cochlear implant electrodes. J Neural Eng 2009, 6. https://doi.org/10.1088/1741-2560/6/5/055002. 47. Lebedev MA, Nicolelis MAL: Brain – machine interfaces : past , present and future. Trends Neurosci 2006, 29:536–546. https:// doi.org/10.1016/j.tins.2006.07.004. 48. Wei XF, Grill WM: Impedance characteristics of deep brain stimulation electrodes in vitro and in vivo. J Neural Eng 2009, 6. https://doi.org/10.1088/1741-2560/6/4/046008.
www.sciencedirect.com
67
49. Matteucci PB, Chen SC, Tsai D, Dodds CWD, Dokos S, Morley JW, Lovell NH, Suaning GJ: Current steering in retinal stimulation via a quasimonopolar stimulation paradigm. Investig Ophthalmol Vis Sci 2013, 54:4307–4320. https://doi.org/ 10.1167/iovs.13-11653. 50. Hadjinicolaou AE, Leung RT, Garrett DJ, Ganesan K, Fox K, Nayagam DAX, Shivdasani MN, Meffin H, Ibbotson MR, Prawer S, O’Brien BJ: Electrical stimulation of retinal ganglion cells with diamond and the development of an all diamond retinal prosthesis. Biomaterials 2012, 33:5812–5820. https:// doi.org/10.1016/j.biomaterials.2012.04.063. 51. Bendali A, Rousseau L, Lissorgues G, Scorsone E, Djilas M, Dégardin J, Dubus E, Fouquet S, Benosman R, Bergonzo P, Sahel JA, Picaud S: Synthetic 3D diamond-based electrodes for flexible retinal neuroprostheses: model, production and in vivo biocompatibility. Biomaterials 2015, 67:73–83. https:// doi.org/10.1016/j.biomaterials.2015.07.018. 52. Sommerhalder J, Rappaz B, DeHaller R, Fornos AP, Safran AB, Pelizzone M: Simulation of artificial vision: II. Eccentric reading of full-page text and the learning of this task. Vision Res 2004, 44:1693–1706. https://doi.org/10.1016/ j.visres.2004.01.017. 53. Joucla S, Yvert B: Improved focalization of electrical microstimulation using microelectrode arrays: a modeling study. PLoS One 2009, 4. https://doi.org/10.1371/journal.pone.0004828. 54. Voss A, Wei H, Zhang Y, Turner S, Ceccone G, Peter J, Stengl M, Popov C: Strong attachment of circadian pacemaker neurons on modified ultrananocrystalline diamond surfaces. Mater Sci Eng C 2016, 64:278–285. https://doi.org/10.1016/ j.msec.2016.03.092. 55. Chen Y, Tsai C, Lee C, Lin I: In vitro and in vivo evaluation of ultrananocrystalline diamond as an encapsulation layer for implantable microchips. Acta Biomater 2014, 10:2187–2199. https://doi.org/10.1016/j.actbio.2014.01.014. 56. Arnault JC, Girard HA: Hydrogenated nanodiamonds: synthe* * sis and surface properties. Curr Opin Solid State Mater Sci 2017, 21:10–16. https://doi.org/10.1016/j.cossms.2016.06.007. This paper present state of art hydrogenation treatments on nanodiamond and further functionalization and reactivity. The photoelectric property cound open new field of application for hydrogenated diamond. 57. Zhao Y, Yeung KWK, Chu PK: Functionalization of biomedical materials using plasma and related technologies. Appl Surf Sci 2014, 310:11–18. https://doi.org/10.1016/ j.apsusc.2014.02.168. 58. Shintani Y, Ibori S, Igarashi K, Naramura T: Polycrystalline boron-doped diamond with an oxygen-terminated surface channel as an electrolyte-solution-gate fi eld-effect transistor for pH sensing. Electrochim Acta 2016, 212:10–15. 59. Miksovsky J, Voss A, Kozarova R, Kocourek T, Pisarik P, Ceccone G: Cell adhesion and growth on ultrananocrystalline diamond and diamond-like carbon films after different surface modifications. Appl Surf Sci 2014, 297:95–102. https:// doi.org/10.1016/j.apsusc.2014.01.085. 60. Voss A, Mozafari M, Popov C, Ceccone G, Kulisch W, * * Reithmaier JP: Surface & Coatings Technology Stability of the surface termination of differently modi fi ed ultrananocrystalline diamond/amorphous carbon composite fi lms *. Surf Coating Technol J 2012, 209:184–189. https:// doi.org/10.1016/j.surfcoat.2012.08.049. This paper brought out preferential attachment of cells and guided growth on UNCD surface. The applicability of surface patterning was demonstrated. 61. Sen FG, Qi Y, Alpas AT: Surface stability and electronic structure of hydrogen and fluorine terminated diamond surfaces: a first principles investigation surface stability and electronic structure of hydrogen- and fluorine-terminated diamond surfaces: a first principles invest. J Mater Res 2009, 24:2461–2470. https://doi.org/10.1557/JMR.2009.0309. 62. Bendali A, Agnès C, Meffert S, Forster V, Bongrain A, Arnault JC, Sahel JA, Offenhäusser A, Bergonzo P, Picaud S: Distinctive glial and neuronal interfacing on nanocrystalline diamond. PLoS One 2014, 9. https://doi.org/10.1371/journal.pone.0092562. Current Opinion in Biomedical Engineering 2019, 10:60–68
68 Biomaterials: biomaterials and biocompatibility
63. Voss A, Stateva SR, Reithmaier JP, Apostolova MD, Popov C: Patterning of the surface termination of ultrananocrystalline diamond films for guided cell attachment and growth. Surf Coating Technol 2017, 321:229–235. https://doi.org/10.1016/ j.surfcoat.2017.04.066. 64. Hébert C, Warnking J, Depaulis A, Garçon LA, Mermoux M, Eon D, Mailley P, Omnès F: Microfabrication, characterization and in vivo MRI compatibility of diamond microelectrodes array for neural interfacing. Mater Sci Eng C 2015, 46:25–31. https://doi.org/10.1016/j.msec.2014.10.018. 65. Alcaide M, Taylor A, Fjorback M, Zachar V, Pennisi CP: Borondoped nanocrystalline diamond electrodes for neural interfaces: in vivo biocompatibility evaluation. Front Neurosci 2016, 10:1–9. https://doi.org/10.3389/fnins.2016.00087. 66. Meijs S, Alcaide M, Sørensen C, McDonald M, Sørensen S, Rechendorff K, Gerhardt A, Nesladek M, Rijkhoff NJM, Pennisi CP: Biofouling resistance of boron-doped diamond neural stimulation electrodes is superior to titanium nitride electrodes in vivo. J Neural Eng 2016, 13:1–12. https://doi.org/ 10.1088/1741-2560/13/5/056011. 67. Garrett DJ, Saunders AL, McGowan C, Specks J, Ganesan K, Meffin H, Williams RA, Nayagam DAX: In vivo biocompatibility of boron doped and nitrogen included conductivediamond for use in medical implants. J Biomed Mater Res B Appl Biomater 2016, 104:19 –26. https://doi.org/10.1002/ jbm.b.33331. 68. Ganji M, Tanaka A, Gilja V, Halgren E, Dayeh SA: Scaling effects on the electrochemical stimulation performance of Au , Pt , and PEDOT: PSS electrocorticography arrays. Adv Funct Mater 2017, 1703019. https://doi.org/10.1002/adfm.201703019. 69. Boris Duran GMS, Brocenschi Ricardo F, France Marion, Galligan James J: Electrochemical activation of diamond
Current Opinion in Biomedical Engineering 2019, 10:60–68
microelectrodes: implications for the in vitro measurement of serotonin in the bowel. Analyst 2014, 139:3160–3166. https:// doi.org/10.1002/bmb.20244.DNA. 70. Garrett DJ, Ganesan K, Stacey A, Fox K, Meffin H, Prawer S: Ultra-nanocrystalline diamond electrodes: optimization towards neural stimulation applications. J Neural Eng 2012, 9. https://doi.org/10.1088/1741-2560/9/1/016002. 71. Kim YT, Ito Y, Tadai K, Mitani T, Kim US, Kim HS, Cho BW: Drastic change of electric double layer capacitance by surface functionalization of carbon nanotubes. Appl Phys Lett 2005, 87:1–3. https://doi.org/10.1063/1.2139839. 72. Keremidarska M, Ganeva A, Mitev D, Hikov T, Presker R, Pramatarova L, Krasteva N: Comparative study of cytotoxicity of detonation nanodiamond particles with an osteosarcoma cell line and primary mesenchymal stem cells. Biotechnol Biotechnol Equip 2014, 28:733–739. https://doi.org/10.1080/ 13102818.2014.947704. 73. Alarifi S, Ali D, Verma A, Almajhdi FN, Al-Qahtani AA: Singlewalled carbon nanotubes induce cytotoxicity and DNA damage via reactive oxygen species in human hepatocarcinoma cells. In Vitro Cell Dev Biol Anim 2014, 50:714–722. https://doi.org/10.1007/s11626-014-9760-3. 74. Piret G, Hébert C, Mazellier JP, Rousseau L, Scorsone E, Cottance M, Lissorgues G, Heuschkel MO, Picaud S, Bergonzo P, Yvert B: 3D-nanostructured boron-doped diamond for microelectrode array neural interfacing. Biomaterials 2015, 53:173–183. https://doi.org/10.1016/ j.biomaterials.2015.02.021. 75. Williams JC, Hippensteel JA, Dilgen J, Shain W, Kipke DR: Complex impedance spectroscopy for monitoring tissue responses to inserted neural implants. J Neural Eng 2007, 4: 410–423. https://doi.org/10.1088/1741-2560/4/4/007.
www.sciencedirect.com