Articol Applied Surface Science

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Please cite this article in press as: V. Grumezescu, et al., Functionalized antibiofilm thin coatings based on PLAPVAmicrospheres loaded with

usnic acid natural compounds fabricated byMAPLE, Appl. Surf. Sci. (2013), http://dx.doi.org/10.1016/j.apsusc.2013.09.081

ARTICLE IN PRESSGModel

APSUSC-26364; No.of Pages6

Applied Surface Science xxx (2013) xxxxxx

Contents lists available at ScienceDirect

Applied Surface Science

j ournal homepage : www.elsevier .com/ locate /apsusc

Functionalized antibiofilm thin coatings based on PLAPVAmicrospheres loaded with usnic acid natural compounds fabricatedby MAPLE

Valentina Grumezescua,b, Gabriel Socol a, Alexandru Mihai Grumezescub,, Alina MariaHolban c, Anton Ficaib, Roxana Truscad, Coralia Bleotue, Paul Catalin Balaure f,Rodica Cristescua, Mariana Carmen Chifiriuc c

a National Institute for Lasers, Plasma & Radiation Physics, Lasers Department, PO BoxMG-36, Bucharest-Magurele, Bucharest, Romaniab University Politehnica of Bucharest, Faculty of Applied Chemistry andMaterials Science, Department of Science and Engineering of OxidicMaterials and

Nanomaterials, Polizu Street no 1-7, 011061 Bucharest, Romaniac Faculty of Biology, University of Bucharest,MicrobiologyImmunologyDepartment, AleeaPortocalelor 1-3, Sector 5, 77206Bucharest, Romaniad S.C.Metav-CD S.A., 31Rosetti Str.,020015 Bucharest, Romaniae Stefan S Nicolau Institute of Virology,Bucharest, RomaniafDepartment of Organic Chemistry, Faculty of AppliedChemistry andMaterials Science, Politehnica Universitiy of Bucharest, Polizu Street no 1-7, 011061

Bucharest, Romania

a r t i c l e i n f o

Article history:

Received 29 June 2013

Received in revised form

13 September 2013

Accepted15 September 2013

Available online xxx

Keywords:MAPLE

Microspheres thin coatings

PLAPVA

Usnic acid

Anti-biofilm

Staphylococcus aureus

a b s t r a c t

We report the fabrication of thin coatings ofPLAPVA microspheres loaded with usnic acid by matrixassisted pulsed laser evaporation (MAPLE) onto Ti substrate. The obtained coatings have been physico-

chemically characterized by scanning electronmicroscopy (SEM) and infraredmicroscopy (IRM). In vitro

biological assays have been performed in order to evaluate the influence offabricatedmicrosphere thin

coatings on the Staphylococcus aureus biofilm development as well as their biocompatibility. SEMmicro-graphs have revealed a uniformmorphology ofthin coatings, while IRM investigationshave proved both

the homogeneity and functional groups integrity ofprepared thin coatings. The obtained microsphere-based thin coatingshave proved to be efficient vehicles for usnic acid natural compoundwith antibiofilmactivity, as demonstrated by the inhibitory activity on S. aureusmature biofilm development, opening

new perspectives for the prevention and therapy associated to biofilm related infections. 2013 Elsevier B.V. All rights reserved.

1. Introduction

Biodegradable polymers have attracted increased attention inthe last decade due to the great potential for biomedical applica-

tions [15].Current surface engineering approaches have moved towards

the design ofmicro or nano-platformswithmultifunctional thera-peutic properties [6]. These platforms are intended to concentrate

a synthetic or natural drug, but also to exhibit additional activitiesas complementary therapeutic effects [610].

Due to its good mechanical properties and enhanced biocom-patibility, polylactic acid (PLA) has been extensively studied for

biomedicalapplications includingsutures, bonescrews, drugdeliv-ery systemsor tissue engineering scaffolds [1120].

Corresponding author. Tel.: +40765349326.

E-mail address: [email protected](A.M. Grumezescu).

Polyvinyl alcohol (PVA) has been used in biomedical applica-tions due to a combination of properties such as biocompatibility,availability, relative low price and low toxicity [21,22]. PVA hasbeen frequently combinedwith natural molecules that can be rec-

ognized by cells favoring the preliminary adhesion and thereforethe subsequent colonization of the scaffold [23,24].

It is known that lichens synthesize organic natural compoundsby several biologic pathways [25]. The most extensively stud-ied product is the dibenzofuran derivative usnic acid (UA) [26].

Due to its reported biological characteristics, UA has been usedworldwideasananti-microbial,anti-inflammatory,anti-viral, anti-fungal andanti-mitotic agent [27]. The antimicrobial activity of UAagainsthighlyversatile humanpathogenStaphylococcusaureuswas

already demonstrated [28].

Because of high incidence, associated morbidity, and antimi-crobial resistance, S. aureus infections are a growing concern forclinicians. S. aureus is a common pathogen in skin, soft-tissue,catheter-related, bone, joint, pulmonary, and central nervous

0169-4332/$ see front matter 2013 Elsevier B.V. All rights reserved.

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system infections. S. aureus bacteremias are particularly chal-

lenging because of the high incidence of associated complicatedinfections, including infective endocarditis [29,30]. Approximately20% of healthy persons are persistent carriers ofS. aureus, while60%are intermittent carriers.Colonizationrates arehigh in infants,

hemodialysis patients, illicit injection drugusers, surgical patients,andpatients with insulin-dependent or poorly controlled diabetes[31,32].

Persistent microbial infections, including S. aureus infections

are associated with either biofilms or the occurrence of metaboli-cally modified persister cells, named small colony variants (SCVs).SCVs arenaturallyoccurring subpopulations ofS. aureus that differfrom thenormal-phenotype by their small colonysizes (because of

their slowrate of growth)and also by decreased pigmentation andhemolysis [33]. SCVs are frequently associated with biofilm infec-tionsespeciallyin prosthesizedpatients,wheretheseinfectionsaredifficult to treatbecauseof their increasedresistance [34]. Titanium

implants are routinely used for bone fractures as well as dentalwork. Recent studies have demonstrated that bacteria attach anddevelop biofilms on titanium implants, degrading the prostheticdevice faster and determining an enhanced response in the host

[35]. Actual concern in biomedical and implanteddevice field sup-ports thedevelopment of novel antimicrobial strategies in order to

reduce biofilm formation on prosthetic devices [36].We have explored deposition of thin coatings containing

biopolymers that serve as carriers for antimicrobial natural com-pounds by means of matrix assisted pulsed laser evaporation(MAPLE). MAPLE is a laser technique that is based on a cryogenicapproach for transferring organic and polymeric materials onto a

substrate in a preservedmanner [37,38].This paper reports the MAPLE-deposition of PLAPVAUA

microsphere-based thin coatings with enhanced biocompatibilityand great anti-microbial adherence. The chemical structure was

investigated by IRM, while the surface morphology was tested bySEM. Their inhibitory activity on S. aureus mature biofilm devel-opment was studied. The coatings cytotoxicity was assessed onmesenchymal stem cells cultures.

2. Materials and methods

2.1. Materials

The polylactic acid (PLA), polyvinyl alcohol (PVA), usnic acid

(UA), chloroform and n-hexane were purchased from Sigma-Aldrich. Commercial pure (CP) grade 4 Titanium with 8mmdiameter and both side polished (10 0) silicon were used as sub-strates for theMAPLE coatings.

2.2. Chemical synthesis of PLAPVAUAmicrospheres

PLAPVAUAmicrosphereswerepreparedusing a solventevap-oration method [39,40]. Thus, 400mg PLA and 50mg UA weresolubilized in 3mLCHCl3 by sonication. The organic phase was

emulsified with a sonicator model SONIC-1200WT from MRC for5min, in ON/OFF steps of 5s and 3s with a limitation temper-ature of max 40 C in 5mL aqueous phase containing 2% (w/v)PVA. After sonication, theemulsionwasadded in200mLdeionized

water and stirred for 4h until the CHCl3 was completely evapo-rated. The microsphere emulsion was centrifuged at 6000 rpm for10min. The obtained microspheres were washed four times withultrapurewater, collectedby filtration, andthensubjectedto freeze

drying. PLAPVAAUmicrosphereswere used toprepare thin filmsbyMAPLE technique.

2.3. MAPLE target preparation and deposition of

microsphere-based thin coatings

Hexane solutions of 1% (w/v) PLAPVAUA have been pre-pared. All MAPLE solutions have been poured into a pre-cooled

target holder at 173K and subsequently immersed in liquid nitro-gen for 30min. MAPLE depositions have been performed using aKrF* (=248nm and FWHM =25 ns) laser source COMPexPro 205model, Lambda Physics-Coherent, that was operated at the rep-

etition rate of 10Hz. The laser fluence was within the range of100400mJ/cm2 whereas the laser spot area was set at 38mm2.A laser beam homogenizer was used to improve the energy distri-bution of the laser spot. In order to avoid the target heating and

subsequent drilling, thefrozen targetwas rotatedat a rate of0.4Hzduring coating deposition. Alldepositionswere conducted at roomtemperature into a background pressure of 1 Pa. All coatings weregrown at a target-substrate separation distance of 4 cm by apply-

ing (10,00020,000) subsequent laser pulses. During deposition,the target was kept at a temperature of173K by active liquidnitrogen cooling. Thin coatings were deposited onto CP grade 4Titanium with 8mm diameter, both side polished (10 0) silicon

and glass substrates for IRM, SEM and biological assays. Prior tointroduction inside the deposition chamber, the substrates were

successively cleaned into an ultrasonic bathwith acetone, ethanoland deionized water for 15min, dried in a jet of high purity nitro-

gen and then plasma-cleaned into oxygen atmosphere for 15minwitha plasmasystemtype FEMTO fromDienerelectronic GmbH.For comparison data, a control set of films were prepared by dropcasting on the (10 0) silicon.

2.4. Characterizationmethods

IR mapping were recorded on a Nicolet iN10 MX FT-IR

Microscope with MCT liquid nitrogen cooled detector in themea-surement range 4000600cm1. Spectral collection was made inreflection mode at 4cm1 resolution. For each spectra, 32 scanswere co-added and converted to absorbance using Ominc Picta

software (ThermoScientific).SEManalysiswas performedon a FEIelectronmicroscope,using

secondaryelectronbeamswith energies of 30keV, onsamples cov-eredwith a thin gold layer.

Biofilm formation was analyzed in 6 multi-well plates (Nunc),usinga staticmodel formonospecificbiofilmsdevelopment.Coatedanduncoatedsterile titaniumdiscsweredistributed in6well plates(one perwell). TwomilliliterS. aureus inoculumwithstandardden-

sity (0.5 McFarland) were added in each well, to completely coverthe discs. Samples were incubated for 24h at 37C. Biofilms for-mation was assessed after 24h, 48h and 72h by viable cell countassay.

Viable cell counts (VCCs) analysis of microorganisms grown inbiofilms was assessed following an adapted, previously described

protocol [41]. Briefly, after 24h incubation the culture mediumwas removed and the titanium discs were washed with ster-

ile PBS, in order to remove the unattached bacteria. Titaniumdiscs were placed in fresh medium and incubated for other addi-tional 24h, 48h and 72h. After the incubation, the discs were

gently washed with sterile PBS to remove the non-adherentcells and placed in 1.5mL microcentrifuge tubes containing750L PBS. Samples were vigorously mixed by vortexing for30s and sonicated for 10s in order to disperse biofilm cells

into the suspension. Serial 10-fold dilutions were achieved andplated on LB Agar for viable cell counts assay. Experimentswere performed in triplicate and repeated on three separateoccasions.

The biocompatibility was assessed by cytotoxicity assay using

mesenchymal stem cells. 2

105

mesenchymal cells were seeded
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Fig. 1. Second derivate IR mappings and IR spectra of dropcast surface: intensity distribution of (a) 3500cm1 (OH stretch, end group), (b) 2924cm1 (CH3 stretch), (c)

1750cm1 (C=Ocarbonyl group), (d)1090 (COstretch contributing to alcohols).

Fig. 2. Secondderivate IR mappings and IR spectra of thin coating (F=200mJ/cm2) surface: intensity distribution of (a) 3500cm1 (OH stretch, end group), (b) 2924cm1

(CH3stretch), (c) 1750cm1 (C=Ocarbonyl group), (d)1090 (COstretch contributing to alcohols).




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Fig. 5. SEMmicrographs of dropcasts ((a)(c)) and fabricated thin coatings ((d)(f)).

in eachwell of a 6 well plate (Nunc), containing a 0.5 cmdiameter

(coated/uncoated) titanium disc sterile slide, in triplicate, using-minimal essential medium (GIBCO, USA) supplemented with 10%foetal bovine serum (GIBCO, USA) and 10ng/mL basic fibroblastgrowth factor (bFGF) (Sigma, USA). Plateswere cultured at 37 C in

a humidified atmosphere containing 5% CO2for24h. After incuba-tion, titanium discs containing adherent cells were removed, fixed

in 70% ethanol and stained with 50g/mL FDA (fluorescein diac-etate). The morphology of the stained cells was observed using an

Observer.D1 Carl Zeiss microscope in order to evaluate cytotoxicpotential of testedmaterials.

2.5. Statistical analysis

The statistical significance of the obtained results was ana-lyzed using GraphPad Prism version 5.04 for Windows, GraphPadSoftware, San Diego, CA, USA, www.graphpad.com. We used for

comparison thenumberof CFUmL1 as revealedby the readingsofthree values/experimental variant. Two-way ANOVA and Tukeysmultiple comparison tests were used for revealing significant dif-ferences among the analyzed groups.

3. Results and discussion

The optimum deposition laser fluence was identified usingcomparative IRM analysis (Figs. 14) between PLAPVAUA

microsphere dropcast sample and PLAPVAUA microspheresthin coatings deposited by MAPLE at 200mJ/cm2, 300mJ/cm2

and 400mJ/cm2. Figs. 14 show the second derivative infraredmaps of all PLAPVAUA surfaces involved in this study. Sec-

ond derivative infrared mapping can be used as a quick,easy, reproducible, inexpensive, and non-destructive tool toevaluate the purity and structural integrity of samples [42].Absorbance intensities of IR spectra maps are proportional to

color changes starting with blue (the lowest intensity) and grad-

ually increasing through green, yellow to finally red (the highest

intensity) [43]. Approximately600 spectra were analyzed for each

sample.Analyzing the integrity of IR spectra for each sample deposited

at different laser fluences and the corresponding dropcast coatingwe selected 300mJ/cm2 laser fluence value as the best compro-

mise between the deposition rate and the stoichiometric transferto deposit themicrosphere films for biological assays.

In Fig. 1 (dropcast) and Fig. 3 (microspheres thin films preparedat F=300mJ/cm2), IR spectra are given at different points in plot-

ted maps. The characteristic peaks of the prepared PLAPVAUAmicrospheres drop-cast (reference material) are assigned to: (a)3500cm1 (OH stretch, end group), (b) 2924cm1 (CH3 stretch),(c) 1750cm1 (C=O carbonyl group), (d)1090 (CO stretch con-

tributing to alcohols).As a general remark, typical IR spectra ofMAPLE-deposited thin

coatings at F=300mJ/cm2 show a very close similarity to the cor-respondingdrop-cast IR spectra.

Microsphere dimensions, as well as the integrity of pre-pared microspheres thin films, were given by SEM analysis.PLAPVAUA microspheres and PLAPVAUA microspheres thincoatings have possessed a homogeneous shape, showing no

concavitiesordistortions ontheir surface (Fig.5). Fabricatedmicro-spheres and microsphere-based thin coatings have show a 5maverage diameter. Although a tendency to form aggregates can-

not be observed, the microspheres have maintained their smalldimensions.

Biocompatibility results revealed thatmicrosphere coatings areadequate supports forhuman eukaryotic cells growth, allowing for

the normal development of mesenchymal stem cells (MSC). MSChave exhibiteda normalmorphology andgrowthon both uncoatedand thin film microsphere-based thin coated slides (Fig. 6a and c),demonstratingthat theadditionalmicrospherescoatings have nei-

ther cytotoxic nor inhibitory effects. Micrographs have revealedthat MSCcells adherenormally to plain andmicro-coated titaniumslidesandarestained by FDA, demonstrating their viability (Fig. 6b

and d).
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Fig. 6. Mesenchymal stem cells grown on coatedand uncoated titaniumslides. Typical invertedmicroscopy imagesin visible ((a) and (c)) andUV light ((b) and(d)) (100)

for dropcasts(controls) ((a) and(b)) andthin coatings ((c) and (d)) provedthe usefulness of fabricated thin filmfor thefabrication of biocompatible surfaces forimplantable

prostheses.

Biofilm assays have demonstrated that the newly fabricated

micro-biocoatings have revealed a great antibiofilm effect againstS. aureus biofilm formation. Staphylococcal biofilms are impairedstarting with their initialization, differences observed by viableanalysis after24h ofbiofilmgrowthbeing significant (Fig. 7). These

results demonstrate that the micro-biocoated titanium samplesprovide inappropriate surfaces for adhesion andbiofilmformation.Furthermore, the mature biofilm formation is also altered whenthey are growing on thin-coated titanium slides, S. aureusbiofilms

Fig.7. Graphicrepresentationof viable cell counts analysisafter removingS. aureusbiofilm embedded cells at 24h, 48h and 72h post infection; *p


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