ieee transactions on plasma science, vol. 35, no. 2, … · 2007-04-20 · ieee transactions on...

IEEE TRANSACTIONS ON PLASMA SCIENCE, VOL. 35, NO. 2, APRIL 2007 181

Plasma-Treated BiomaterialsPaul K. Chu, Fellow, IEEE

(Invited Paper)

Abstract—Atmospheric pressure plasma spraying is currentlyused to fabricate relatively thick ceramic coatings for orthopedicapplications such as hip joints replacements. We have recentlyfabricated bioactive nanostructured titanium oxide coatings thatare bioactive and conducive to the growth of apatite. The materi-als are synthesized by nanoparticle atmospheric pressure plasmaspraying followed by low-pressure plasma immersion ion implan-tation (PIII). Surface bioactivity can also be induced by irradiatingthe nanostructure TiO2 coatings with ultraviolet light instead ofhydrogen plasma ion implantation. PIII is a useful method totreat other types of biomaterials to enhance the surface bioactivity.Recent applications of the technology to modify orthopedic ma-terials as well as biocompatible and antibacterial coatings aredescribed in this invited paper.

Index Terms—Biocompatibility, biomaterials, plasma immer-sion ion implantation (PIII), plasma spraying, plasma surfacemodification.

I. INTRODUCTION

D EVELOPMENT of new biomaterials used in biomedicalimplants and devices usually takes a very long time and

extensive clinical trials. Therefore, shorter and more economi-cal routes to develop novel biomaterials are always welcomedby the biomedical industry. Most current biomaterials sufferfrom drawbacks that can be rectified or improved by surfacemodification. For example, the use of atmospheric or low-pressure plasma processing can effectively enhance the surfaceproperties of a myriad of biomaterials while the favorable bulkattributes such as strength and inertness can be retained [1],[2]. Compared to the time and efforts taken to develop newbiomaterials from scratch, the development time for surfacemodified biomaterials tailored to specific needs can be short-ened significantly. In this paper, our recent research activitieson the use of atmospheric pressure plasma spraying [3], [4]and low-pressure plasma immersion ion implantation (PIII) anddeposition [5], [6] pertaining to biomedical materials researchare reviewed.

Manuscript received July 31, 2006. This work was supported by the HongKong Research Grants Council (RGC) Competitive Earmarked Research Grant(CERG) CityU 112306 and Hong Kong RGC Central Allocation Group Re-search Grant CityU 1/04C.

The author is with the Department of Physics and Materials Science,City University of Hong Kong, Kowloon, Hong Kong (e-mail: [email protected]).

Color versions of one or more of the figures in this paper are available onlineat http://ieeexplore.ieee.org.

Digital Object Identifier 10.1109/TPS.2006.888587

Fig. 1. Schematic diagram of a plasma spray torch [4].

Fig. 2. Surface SEM views of the hydrogen-PIII nano-TiO2 coating aftersoaking in SBF for two weeks [8].

II. PLASMA-SPRAYED BIOMEDICAL COATINGS

Plasma spraying, a subset of thermal spraying, is often usedto form ceramic and oxide coatings. The materials have wideapplications in the aerospace, printing, petrochemical, medical,and electronic industry. Direct-current plasma arc devices cur-rently dominate the commercial market, but radio frequencyor inductively coupled plasmas (ICPs) have also become quitecommon. Plasma spraying includes atmospheric plasma spray-ing and vacuum plasma spraying. The process uses an electricalarc to melt and spray materials onto a surface as illustrated inFig. 1. The high energy and density available in a plasma jethas made plasma spraying one of the popular thermal spraying

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182 IEEE TRANSACTIONS ON PLASMA SCIENCE, VOL. 35, NO. 2, APRIL 2007

Fig. 3. Cross-sectional SEM views and EDS analysis of the hydrogen-PIII nano-TiO2 coating after soaking in SBF for: (a) two weeks and (b) four weeks.

techniques. Almost all materials can be melted in the plasma jetthereby making the technique quite versatile. The advantages ofplasma spraying include high deposition rates (80 g/min), thickdeposits (hundreds of micrometers to several millimeters), andlow costs. In addition, plasma sprayed coatings possess a roughsurface that bodes well for bone growth in orthopedic appli-cations. Therefore, plasma spraying is widely used to preparebiomedical coatings on titanium implants used in orthopedics.

The surface physical, chemical, and biochemical propertiesof the biomaterials control processes such as protein adsorption,cell-surface interaction, and cell/tissue development at the inter-face between the body and the biomaterials. Nanosized surfacetopography may give biomedical implants special and favorableproperties in a biological environment. It has been shownthat nanophase materials that can promote osseointegrationare critical to clinical success for orthopedic/dental implants.Furthermore, osteoblast proliferation has been shown to besignificantly higher on nanophase alumina, titania, and hydrox-yapatite (HA) compared to conventional biomedical ceramicmaterials [7].

Although some types of TiO2 powders and gel-derivedfilms can exhibit bioactivity, plasma-sprayed TiO2 coatings arealways bioinert, thereby hampering wider applications in boneimplants. We have recently produced a bioactive nanostructuredTiO2 surface with grain size smaller than 50 nm using nanopar-ticle plasma spraying followed by hydrogen PIII [8]. Afterimmersion in simulated body fluids (SBFs) for two weeks, thesurface of the hydrogen-PIII nano-TiO2 coating is completelycovered by a newly formed layer, as shown in Fig. 2. At a higher

magnification, the newly formed layer exhibits a subtle netlikestructure consisting of nanosized rods. The cross-sectionalviews of the hydrogen-PIII nano-TiO2 coating soaked in SBFfor two and four weeks show that the newly formed layer isCa and P. The layer has a thickness of about 5 µm after twoweeks and reaches about 25-µm thick after four weeks (Fig. 3).The X-ray diffraction (XRD) and Fourier transform infraredspectroscopy (FTIR) results (not shown here) confirm that thenew layer formed on the hydrogen-PIII nano-TiO2 coatingconsists of carbonate-containing HA [8]. In contrast, in ourcontrol experiments involving the as-sprayed nano-TiO2 andmicro-TiO2 coatings as well as the hydrogen-PIII micro-TiO2

coating and hydrogen-PIII polished nano-TiO2 coating withthe nanostructured surface removed, no new precipitates canbe observed on the surfaces after immersion for two weeks, asshown in Fig. 4.

Our results indicate that only the hydrogen-PIII nano-TiO2

coating with a nanostructured surface (< 50-nm grain size)can induce the formation of carbonate-containing HA. It alsoimplies that the bioactivity of the plasma-sprayed TiO2 dependson two factors: a nanostructured surface composed of enoughsmall particles and hydrogen incorporation. The as-sprayedTiO2 coating is highly oxygen deficient. Although the surfaceof the as-sprayed TiO2 coating is oxidized upon exposure toair [9], the subsurface region remains oxygen deficient. Duringhydrogen PIII, hydrogen ions react with the surface oxygento form Ti–OH bonds. When the hydrogen-PIII TiO2 surfaceis immersed in SBF, Ti–OH reacts with the hydroxyl ion inthe SBF to produce a negatively charged surface with the

CHU: PLASMA-TREATED BIOMATERIALS 183

Fig. 4. SEM micrographs of TiO2 coatings immersed in SBF for two weeks: (a) as-sprayed nano-TiO2 coating, (b) as-sprayed micro-TiO2 coating, (c) hydrogen-PIII micro-TiO2 coating, and (d) hydrogen-PIII polished nano-TiO2 coating with the nanostructured surface removed.

functional group Ti-O−. The formation of a negatively chargedsurface spurs apatite precipitation. Positive calcium ions areattracted from the solution [10], followed by the arrival ofHPO2−

4 resulting in a hydrated precursor cluster consisting ofcalcium hydrogen phosphate. After the precursor clusters areformed, they grow spontaneously by consuming calcium andphosphate ions from the surrounding body fluids.

In addition to a negatively charged surface, the formation of ananostructured surface (< 50 nm) is required for the formationof carbonate-containing HA. The dependence of the adsorptionof molecules and ions on the particle size has been investigated.It has been suggested that finer nanocrystalline particleshave higher surface charge densities than larger ones [11].Peltola et al. [12] have shown that in gel-derived TiO2 coatings,the outermost surface (nanometer scale) promotes apatitenucleation when the peak distance is between 15–50 nm andwhen it is larger than 50 nm, no significant in vitro bioactivityresults. The observed bioactivity of our hydrogen-PIII nano-TiO2 coating is believed to stem from a composite effectencompassing a negatively charged surface after hydrogenPIII as well as enhanced adsorption onto the nanostructuredsurface.

We have also achieved bioactivity enhancement on nano-structured titania using ultraviolet (UV) light irradiation in lieuof hydrogen PIII [13]. After UV light irradiation and immersionin SBF for four weeks, a newly formed layer emerges on the

surface of the plasma-sprayed nanostructured TiO2 [Fig. 5(a)].The energy-dispersive X-ray (EDS) spectrum [top right cornerin Fig. 5(a)] corresponding to the newly formed layer indicatesthat the compound consists of calcium and phosphorus. The Naand Mg signals in the EDS spectra originate from the SBF so-lution. The XRD and FTIR analyses (not shown here) indicatethat the surface compound is carbonate-containing HA (bone-like apatite). On the other hand, as shown in Fig. 5(b), no newprecipitates can be detected on the as-sprayed titania withoutUV illumination. The atomic coordinations on the TiO2 surfacediffer from those in the bulk since the atom arrangements aretruncated on the surface. The perfect surface is built up fromfive-coordinated Ti atoms and two-coordinated O atoms, whichare more energetically reactive than the six-coordinated Ti andthree-coordinated O atoms in the bulk. By UV illumination,oxygen vacancies are created at the two-coordinated bridgingsites, resulting in the conversion of the corresponding Ti4+

sites to Ti3+ sites [14] which dissociate water molecules [15]yielding surface Ti–OH groups. Similar to the situation inhydrogen PIII, the negatively charged surface attracts calciumions from the SBF solution and then the calcium ions in turnattract HPO2−

4 . The calcium phosphate phase that accumulateson the surface of the UV-illuminated titania coatings is initiallyamorphous. It later crystallizes into carbonate-containing HA(bonelike apatite) by incorporating carbonate anions in thesolution.


Fig. 5. Surface SEM views of nanostructured TiO2 coatings after immersionin SBF for four weeks: (a) UV illuminated and (b) as-sprayed.

III. POROUS NICKEL–TITANIUM (NiTi)ORTHOPEDIC MATERIALS

NiTi shape memory alloys are useful orthopedic and ortho-dontic materials due to their superelastic properties and shapememory effects. Recently, porous NiTi has been recognizedas one of the promising biomaterials in surgical implants.Because of the interconnected open pores and large surfacearea, transport of body fluids and in-growth of bone tissuesare possible and the porous materials remain superelastic aftertissue in-growth [16]. Unfortunately, the higher probability ofNi release from the increased surface area of a porous surfacecompared to conventional dense NiTi shape memory alloyscauses more serious health concerns. In order to mitigate leach-ing of harmful Ni ions, a firm barrier layer can be created onthe surface by conducting oxygen PIII (O-PIII) into the porousstructure. The nonline-of-sight capability of PIII allows moreuniform treatment of all exposed areas compared to beam-lineion implantation [17].

Fig. 6 shows the X-ray photoelectron spectroscopy (XPS)depth profiles obtained from four different porous NiTi

samples: (a) O-PIII and immersed in SBF for 28 days,(b) without plasma treatment and immersed in SBF for 28 days,(c) O-PIII and not immersed in SBF, and (d) without plasmatreatment and not immersed in SBF. Comparing the treatedand untreated specimens, the Ni content is greatly reducedin the implanted region due to the higher sputtering rate ofNi compared to Ti during PIII and preferential segregation ofNi from the surface region due to the much stronger Ti–Obond. More importantly, there is very little difference in thedepth profiles between the as implanted and implanted andSBF immersed samples. The data confirm that the barrier layerremains unchanged in a biomimetic environment and there isno obvious chemical reaction between the implanted layer andSBF which is similar to blood plasma. This property is crucialto long term use of the materials in human beings.

The effectiveness of the barrier layer against Ni out-diffusionis assessed by determining the Ni concentrations in the SBFs af-ter immersion tests. Fig. 7 shows the Ni concentrations leachedfrom the untreated and O-PIII dense and porous NiTi materials.The higher Ni concentration from the untreated porous NiTisample compared to that from the dense NiTi arises from thelarger exposed surface area of the porous sample. The amountof Ni leached from the untreated porous sample is at leastthree times higher than that from the treated porous samples.Therefore, the barrier layer is effective in reducing Ni leach-ing. The layer formed by O-PIII also has strong anticorrosionproperties [18], as shown by that the amount of leached Nifrom the untreated dense NiTi is similar to that from theporous O-PIII sample initially but is dramatically higher afterimmersion in SBF for 21 days. Thus, our results unequivocallydemonstrate that PIII is useful in mitigating harmful Ni ionleaching from both dense and porous NiTi. This is due tothe unique nonline-of-sight capability of PIII which has beendemonstrated on much smaller features such as submicrometertrenches in microelectronic devices [19].

IV. MEDICAL POLYMERS

The importance of bacterial adherence and biofilms in noso-comial infection has led to extensive research on antimicrobialagents [20], [21]. Polymers are frequently used in environmen-tal and medical applications and they are commonly surfacemodified for sterilization purposes. Conventional surface mod-ification techniques are usually based on the incorporation ofa leachable antiseptic into a polymeric surface. Unfortunately,these loosely bound antimicrobial agents easily leach into theenvironment and cause side effects to humans as well as theenvironment. A better approach is covalent surface function-alization utilizing antimicrobials that do not leach into theenvironment. It has been found that covalent immobilization ofantimicrobial bronopol or triclosan by PIII can yield excellentmicrobicidal effects on polymer surfaces against both gram pos-itive Staphylococcus aureus and gram-negative Escherichia coli[22], [23]. This approach is relatively simple and produces littlechemical pollution, good surface conformity, and uniformity. Inaddition, PIII does not alter the appearance of polymers suchas polyvinyl chlorine and polyethylene (PE). Here, our recentinvestigation on the microbicidal properties of the plasma-treated PE is described.


Fig. 6. XPS depth profiles of porous NiTi samples: (a) oxygen plasma implanted and immersed in SBF for 28 days, (b) without plasma treatment and immersedin SBF for 28 days, (c) oxygen plasma implanted and not immersed in SBF, and (d) without plasma treatment and not immersed in SBF.

Fig. 7. Nickel concentrations in SBF determined by ICP mass spectrometryfrom dense and porous NiTi samples after immersion tests for 7 to 28 days.

In our plasma process, the medical-grade PE samples are firsttreated under O2 plasma [24]. Subsequently, the samples arethen coated with an antimicrobial agent, triclosan or bronopoland then undergo argon PIII to ensure that the antibacterialreagent bonds well onto the PE surface. In our experiments,sample 1 is the untreated PE (control). Sample 2 is treatedwith oxygen plasma, coated with triclosan, and then treatedwith argon plasma, whereas sample 3 is processed similarlyas sample 2 except that the agent used is bronopol insteadof triclosan. In order to investigate the surface antibacterialproperties, E. coli and S. aureus are chosen as the gram-negativeand gram-positive bacteria in our plate counting tests [22], [23].

Fig. 8(a) shows that before 20 h in the E. coli solution, theamounts of viable bacteria on the plasma-treated samples arehigher than that on sample 1 (control), although samples 2and 3 show antibacterial effects and the bacteria biofilm hasnot formed. This phenomenon can be explained by the betterhydrophilicity on samples 2 and 3 and easier adhesion ofhydrophilic E. coli [24]. After 20 h, the amounts of bacteriaon the modified samples continue to be more than that on thecontrol sample, as the formation of the biofilm on the modifiedsample is easier. On the other hand, Fig. 8(b) indicates that ahigher quantity of S. aureus adheres onto the control samplethan on samples 2 and 3. This is because S. aureus adheres moreeffectively on a more hydrophobic surface. After incubation for20 h, the results are consistent with those in Fig. 8, and theamount of bacteria is significantly larger than that on the controlsample.

Although the antibacterial samples do not inhibit the for-mation of the bacteria biofilm in the high-concentration(1 ∼ 2 × 108 CFU/ml) suspension, the two kinds of bacteriaat the lower concentration (1 ∼ 5 × 106 CFU/ml) exhibit asmaller degree of adherence on samples 2 and 3 than on sample1. As shown in Fig. 9, bacteria adhesion on samples 2 and3 increases initially and then diminishes with time. This isbecause the modified sample surfaces have better hydrophilicityand are rougher resulting in stronger interactions between thebacteria and materials surface [25]. The triclosan and bronopol


Fig. 8. (a) E. coli biofilm evolution on the samples in the cell suspensionwith about 108 CFU/ml of the bacteria. (b) S. aureus biofilm evolution on thesamples in the cell suspension with about 108 CFU/ml of the bacteria.

immobilized on the surface kill or inhibit bacteria by af-fecting the membrane structure and forming a stable ternarycomplex via the interaction with amino acid residues at theenzyme active sites, but they cannot kill all the adhered bacteriaimmediately. Hence, the quantity of adhered bacteria increasesat the beginning. As soon as the bacteria are killed, the numberof adhered viable bacteria starts to decrease.

Our results show that S. aureus can adhere onto the sam-ple surfaces more readily than E. coli. The plasma modifiedsamples can inhibit a range of bacteria concentrations up to106 CFU/ml, but when the concentration exceeds 1 ∼ 2 ×108 CFU/ml, they fail to impede biofilm formation. However, itshould be emphasized that there are very few instances in prac-tice, especially involving human beings, in which the bacteriaconcentrations exceed 106 CFU/ml. Hence, the plasma-treatedPE materials are adequate in most applications.

V. CONCLUSION

Plasma-based technologies are becoming more important inbiomedical research as they provide a fast and economic way to

Fig. 9. (a) Adhered E. coli on the samples in low cell concentration(1 ∼ 5 × 106 CFU/ml) suspensions. (b) Adhered S. aureus on the samplesin low cell concentration (1 ∼ 5 × 106 CFU/ml) suspensions.

selectively modify the surface biological properties of existingbiomaterials to better suit current biomedical needs. In thisinvited paper, our recent work on plasma sprayed and plasmaimplanted biomedical oxide coatings, porous NiTi shape mem-ory alloys, as well as medical polymers is described. Thetechnology is also being applied to other materials and devicesused in orthodontics and cardiovascular treatment.

ACKNOWLEDGMENT

The author would like to thank the contributions of theresearchers in the Plasma Laboratory of City University ofHong Kong and our collaborators.

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Paul K. Chu (M’97–SM’99–F’03) received the B.S.degree in mathematics from Ohio State University,Columbus, in 1977, and the M.S. and Ph.D. degreesin chemistry, from Cornell University, Ithaca, NY, in1979 and 1982.

He is currently Professor (Chair) of MaterialsEngineering with the Department of Physics andMaterials Science at City University of Hong Kong,Kowloon, Hong Kong. His research activities arequite diverse encompassing plasma surface engineer-ing and various types of materials and nanotechnol-

ogy. He is Editor of two books on plasma surface modification and biomaterialsand has written more than ten book chapters, 500 journal papers, 550 confer-ence papers, and is Associate Editor of International Journal of Plasma Scienceand Engineering and a Member of the editorial board of Materials Scienceand Engineering: Reports, Surface and Interface Analysis, and InternationalJournal of Biomolecular Engineering. He has also been granted eight U.S. andthree Chinese patents.

Dr. Chu is a Fellow of AVS (American Vacuum Society) and HKIE (HongKong Institution of Engineers), and Senior Editor of IEEE TRANSACTIONS ON

PLASMA SCIENCE. He is a member of IEEE Plasma Science and ApplicationsCommittee (PSAC).

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