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Adsorption of biopolymers and their layer-by-layer assemblies on hydrophilic surfaces
KTH, School of Chemical Science and Engineering (CHE), Chemistry, Surface and Corrosion Science. (avdelningen för yt - och korrosionsvetenskap)
2009 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

It is widely known that surfaces play an important role in numerous biological processes and technological applications. Thus, being able to modify surface properties provides an opportunity to control many phenomena occurring at interfaces. One way of controlling surface properties is to adsorb a polymer film onto the surface, for example through layer-by-layer (LbL) deposition of polyelectrolytes. This simple but versatile technique enables various polymers, proteins, colloidal particles etc. to be incorporated into the film, resulting in a multifunctional coating. Due to recent legislations and a consumer demand for more environmentally friendly products, we have chosen to use natural polymers (biopolymers) from renewable resources. The focus of this thesis has been on the adsorption of biopolymers and their layer-by-layer formation at solid-liquid interfaces; these processes have been studied by a wide range of techniques. The main method was the quartz crystal microbalance with dissipation monitoring (QCM-D), which measures the adsorbed mass, including trapped solvent and the viscoelastic properties of an adsorbed film. This technique was often complemented with an optical method, such as ellipsometry or dual polarization interferometry (DPI), which provided information about the “dry” polymer or protein adsorbed mass. From this combination, the solvent content and density of the layers was evaluated. In addition, the surface force apparatus (SFA), X-ray photoelectron spectroscopy (XPS), total internal reflection fluorescence (TIRF), and fluorescence resonance energy transfer (FRET) were utilized, providing further information about the film structure, chemical composition, and polymer inter-layer diffusion. Adsorption studies of the glycoprotein mucin, which has a key role in the mucousal function, showed that despite the net negative charge of mucin, it adsorbed on negatively charged substrates. The adsorbed layer was highly hydrated and the segment density on the substrate was low. We showed the importance of characterizing the mucin used, since differences in purity, such as the presence of albumin, gave rise to different adsorption behaviours in terms of both adsorbed amount and structure. The adsorbed mucin layer was to a large extent desorbed upon exposure to the anionic surfactant sodium dodecyl sulfate (SDS). In order to prevent desorption, we demonstrated that a protective layer of the cationic polysaccharide chitosan could be adsorbed onto the mucin layer and that the mucin-chitosan complexes resisted the desorption normally induced by association with SDS. Moreover, the association between chitosan and SDS was examined at the solid-liquid interface, in the bulk, and at the air-water interface. In all these environments chitosan-SDS complexes were formed and a net charge reversal of the complexes from positive to negative was observed when the concentration of SDS was increased. Furthermore, the LbL deposition method could be used to form a multilayer-like film by alternate adsorption of mucin and chitosan on silica substrates. The LbL technique was also applied to two proteins, lysozyme and β-casein with the aim of building a multilayer film consisting entirely of proteins. These proteins formed complexes at the solid-liquid interface, resulting in a proteinaceous layer, but the build-up was highly irregular with an increase in adsorbed amount per protein deposition cycle that was far less than a monolayer.Continuing with chitosan, known to have antibacterial properties we assembled multilayers with an anti-adhesive biopolymer, heparin, to evaluate the potential of this system as a coating for medical implants. Multilayers were assembled under various solution deposition conditions and the film structure and dynamics were studied in detail. The chitosan-heparin film was highly hydrated, in the range 60-80 wt-% depending on the deposition conditions. The adsorbed amount and thickness of the film increased exponential-like with the number of deposition steps, which was explained by inter-diffusion of chitosan molecules in the film during the build-up. In a novel approach, we used the distant dependent FRET technique to prove the inter-layer diffusion of fluorescent-labelled chitosan molecules within the film. The diffusion coefficient was insignificantly dependent on the deposition pH and ionic strength, and hence on the film structure. With the use of a pH sensitive dye buried under seven chitosan-heparin bilayers, we showed that the dye remained highly sensitive to the charge of the outermost layer. From complementary QCM-D data, we suggested that an increase in the energy dissipation does not necessarily indicate that the layer structure becomes less rigid.

Abstract [sv]

Det är välkänt att ytor spelar en viktig roll i många biologiska processer och tekniska tillämpningar. Att kunna modifiera en ytas egenskaper ger därför en möjlighet att kunna kontrollera många fenomen som sker på ytor. Ett sätt att kontrollera ytegenskaperna är genom att adsorbera en polymerfilm på ytan, till exempel genom att växelvis adsorbera olika polyelektrolyter (LbL-teknik). Denna enkla men mångsidiga teknik möjliggör att många olika material kan införlivas i filmen, vilket resulterar i en multifunktionell beläggning. På grund av dagens lagstiftning och konsumenters ökade efterfrågan på miljövänliga material beslutade vi oss för att använda biologiska polymerer (biopolymerer) i detta projekt. Fokus i den här avhandlingen har varit på adsorption av biopolymerer och deras LbL-formation på gränsytan vätska-fast fas, där adsorptionsförloppet och det adsorberade skiktet bestående av biopolymerer studerats med en mängd olika tekniker. Huvudtekniken var kvartskristallmikrovåg med energidissipations-registrering (QCM-D), som mäter massan inklusive inkorporerat vatten, samt de viskoelastiska egenskaperna hos ett adsorberat skikt. Som komplement till denna teknik användes ofta optiska metoder, till exempel ellipsometri och ”dubbel polarisationsinterferometri (DPI)”, två tekniker som endast mäter massan av de adsorberade biopolymererna. Genom denna kombination av metoder kunde massan av inkorporerat vatten i filmen och filmens densitet bestämmas. Dessutom användes ytkraftsapparaten (SFA), röntgenfotoelektronspektrometri (XPS), och fluorescens-spektroskopiteknikerna TIRF och FRET i några undersökningar för att erhålla information om skiktens struktur, kemiska sammansättning och polymerernas diffusion inom skiktet.Adsorptionsstudier av glycoproteinet mucin, som har en central roll i funktionen av slemhinnan, avslöjade att trots att mucinet har en negativ nettoladdning adsorberade det ändå på negativt laddade substrat. Det adsorberade lagret var väldigt hydratiserat och hade en låg andel mucin i direkt kontakt med ytan. Vi påvisade vikten av att noga undersöka mucinet som användes, eftersom olika renhet, till exempel i form av förekomsten av albumin gav upphov till olika adsorptionsbeteende gällande både adsorberad mängd och struktur. En stor andel av det adsorberade mucinlagret desorberade när det exponerades för den anjoniska tensiden natriumdodecylsulfat, SDS. Vi visade att ett skyddande lager av den katjoniska polysackariden chitosan kunde adsorberas på mucinet och att mucin-chitosan-komplexen inte desorberade när SDS tillsattes. Därtill studerades växelverkan mellan chitosan och SDS på gränsytan vätska-fast fas, i bulken och på luft-vattengränsytan. Komplex av chitosan-SDS bildades i samtliga miljöer och en nettoladdningsomsvängning från positiv till negativ observerades när koncentrationen av SDS ökades.Vidare kunde LbL-tekniken nyttjas för att skapa ett multilagerlikt skikt genom att alternerande adsorbera mucin och chitosan på kiseldioxidsubstrat. Denna teknik användes även med två proteiner, lysozym och β-kasein, med målet att skapa ett multilager bestående av endast proteiner. Dessa proteiner bildade komplex på gränsytan vätska-fast fas i form av ett blandat proteinlager, men uppbyggnaden var väldigt oregelbunden med en ökning i adsorberad mängd per proteindeponeringscykel som var avsevärt mindre än ett monolager.Inom området för biomaterial utgör de antibakteriella och antihäftande egenskaperna hos chitosan respektive heparin en lovande blandning för beläggningar av medicinska implantat. Baserat på detta konstruerade vi multilagerfilmer av chitosan och heparin med olika deponeringslösningar och undersökte dynamiken och filmens struktur i detalj. Chitosan-heparin-filmen var starkt hydratiserad, bestående av cirka 60-80 vikt-% vatten beroende på deponeringsbetingelserna. Den adsorberade mängden och tjockleken på filmen ökade nästan exponentiellt med antal deponeringar, vilket förklarades med chitosanets förmåga att diffundera genom filmen under uppbyggnaden. Med ett nytt angreppssätt använde vi FRET för att bevisa diffusionen av fluorescerande färgmärkt chitosan i filmen under uppbyggnaden. Diffusionskoefficienten var i princip oberoende av pH och jonstyrka under deponeringen och följaktligen av filmens struktur. Genom att använda ett pH-känsligt färgämne begravt under sju biskikt av chitosan-heparin visade vi att färgämnet i hög grad påverkades av laddningen på det yttersta lagret. Från QCM-D-data lade vi fram teorin om att en ökning av energidissipationen för ett lager inte nödvändigtvis indikerar att lagrets struktur har blivit mindre styvt.

Place, publisher, year, edition, pages
Stockholm: KTH , 2009. , 69 p.
Series
Trita-CHE-Report, ISSN 1654-1081 ; 2009:49
Keyword [en]
Layer-by-layer, multilayer, adsorption, biopolymers, Chitosan, Heparin, Mucin, Albumin, Lysozyme, β-casein, SDS, QCM-D, Ellipsometri, DPI, TIRF, FRET, SFA, layer structure, solvent content, vertical diffusion, exponential growth, solid-liquid interface, deposition conditions
National Category
Physical Chemistry
Identifiers
URN: urn:nbn:se:kth:diva-11058ISBN: 978-91-7415-419-1 (print)OAI: oai:DiVA.org:kth-11058DiVA: diva2:235202
Public defence
2009-10-09, hörsal F3, KTH, Lindstedtsvägen 26, Stockholm, 13:00 (English)
Opponent
Supervisors
Note
QC 20100729Available from: 2009-09-21 Created: 2009-09-14 Last updated: 2011-09-20Bibliographically approved
List of papers
1. Comparison of the Adsorption Kinetics and Surface Arrangement of "As Received" and Purified Bovine Submaxillary Gland Mucin(BSM) on Hydrophilic Surfaces
Open this publication in new window or tab >>Comparison of the Adsorption Kinetics and Surface Arrangement of "As Received" and Purified Bovine Submaxillary Gland Mucin(BSM) on Hydrophilic Surfaces
2009 (English)In: Journal of Colloid and Interface Science, ISSN 0021-9797, E-ISSN 1095-7103, Vol. 336, 30-39 p.Article in journal (Refereed) Published
Abstract [en]

The effect of bovine serum albumin (BSA) as impurity in a commercial bovine submaxillary gland mucin preparation (BSM; Sigma M3895) on the adsorption of BSM to hydrophilic surfaces (mica and silica) has been Studied in terms of adsorption kinetics, amount and structure of the formed adlayer. The Surface Force Apparatus (SFA) was used to gain information about the extended and compressed structure of adsorbed "as received" BSM, purified BSM, BSA extracted from the "as received" BSM and mixtures of the latter Purified proteins. The adsorbed amount was estimated using a combination of X-ray Photoelectron Spectroscopy (XPS), Enzyme-Linked Immuno Sorbent Assay (ELISA), Enzyme-Linked Lectin Assay (ELLA), Dual Polarization Interferometry (DPI) and Quartz Crystal Microbalance (QCM-D) measurements. Under the used conditions, purified BSM showed very low affinity for silica and only small amounts were found to adsorb on mica. Initially, the BSM molecules adopted an extended conformation on the mica surface with tails extending into the bulk phase. These tails were irreversibly compressed into a very thin (10 A) layer upon applying a high load. "As received" BSM formed considerably thicker Compressed layers (35 A); however, the extended layer structure was qualitatively the same. When Mixtures of purified BSM and BSA were coadsorbed on mica, a 9 wt-% albumin content gave a comparable layer thickness as the "as received" BSM and from XPS data we draw the conclusion that the albumin content in the layer adsorbed from "as received" BSM was approximately 5 wt-%. Adsorption from an equal amount of BSM and BSA revealed that even though the amount of BSM is scarce in the mixed layer, the few BSM molecules have a drastic effect on the adsorbed thickness and Structure. Clearly, this study shows the importance of characterizing the mucin used since differences in purity give rise to different adsorption behaviours in terms of both adsorbed amount and layer Structure.

Keyword
Mucin; Albumin; Dual Polarisation Interferometry; Quartz Crystal Microbalance with Dissipation monitoring; Surface Force Apparatus; X-ray Photoelectron Spectroscopy; Enzyme-Linked Immuno Sorbent Assay; Enzyme-Linked Lectin Assay
National Category
Physical Chemistry
Identifiers
urn:nbn:se:kth:diva-11129 (URN)10.1016/j.jcis.2009.03.061 (DOI)000266845400004 ()2-s2.0-67349204509 (Scopus ID)
Note

Tidigare titel: A Comparison of the Adsorption Kinetics and Surface Arrangement of "As Received" and Purified Bovine Submaxillary Gland Mucin(BSM) on Hydrophilic Surfaces QC 20100729 QC20150721

Available from: 2009-09-22 Created: 2009-09-22 Last updated: 2015-07-21Bibliographically approved
2. Mucin−Chitosan Complexes at the Solid−Liquid Interface:  Multilayer Formation and Stability in Surfactant Solutions
Open this publication in new window or tab >>Mucin−Chitosan Complexes at the Solid−Liquid Interface:  Multilayer Formation and Stability in Surfactant Solutions
2005 (English)In: Langmuir, ISSN 0743-7463, E-ISSN 1520-5827, Vol. 21, 9502-9509 p.Article in journal (Refereed) Published
Abstract [en]

The adsorption of a biologically important glycoprotein, mucin, and mucin-chitosan complex layer formation on negatively charged surfaces, silica and mica, have been investigated employing ellipsometry, the interferometric surface apparatus, and atomic force microscopy techniques. Particular attention has been paid to the effect of an anionic surfactant sodium, dodecyl sulfate (SDS), with respect to the stability of the adsorption layers. It has been shown that mucin adsorbs on negatively charged surfaces to form highly hydrated layers. Such mucin layers readily associate with surfactants and are easily removed from the surfaces by rinsing with solutions of SDS at concentrations >= 0.2 cmc (1 cmc SDS in 30 mM NaCl is equal to 3.3 mM). The mucin adsorption layer is negatively charged, and we show how a positively charged polyelectrolyte, chitosan, associates with the preadsorbed mucin to form mucin-chitosan complexes that resist desorption by SDS even at SDS concentrations as high as 1 cmc. Thus, a method of mucin layer protection against removal by surfactants is offered. Further, we show how mucin-chitosan multilayers can be formed.

Keyword
in-situ ellipsometry; force microscopy; charge-density; salivary mucins; adsorbed layers; water-interface; dodecyl-sulfate; gastric mucin; oral cavity; adsorption
National Category
Chemical Engineering
Identifiers
urn:nbn:se:kth:diva-11135 (URN)10.1021/la0511844 (DOI)000232453300022 ()2-s2.0-27144559436 (Scopus ID)
Note
QC 20100729Available from: 2009-09-22 Created: 2009-09-22 Last updated: 2010-12-06Bibliographically approved
3. Interactions between Chitosan and SDS at a Low-Charged Silica Substrate Compared to Interactions in the Bulk: The Effect of Ionic Strength
Open this publication in new window or tab >>Interactions between Chitosan and SDS at a Low-Charged Silica Substrate Compared to Interactions in the Bulk: The Effect of Ionic Strength
2008 (English)In: Langmuir, ISSN 0743-7463, E-ISSN 1520-5827, Vol. 24, no 8, 3814-3827 p.Article in journal (Refereed) Published
Abstract [en]

The effect of ionic strength on association between the cationic polysaccharide chitosan and the anionic surfactant sodium dodecyl sulfate, SDS, has been studied in bulk solution and at the solid/liquid interface. Bulk association was probed by turbidity, clectrophoretic mobility, and surface tension measurements. The critical aggregation concentration, cac, and the saturation binding of surfactants were estimated from surface tension data. The number of associated SDS molecules per chitosan segment exceeded one at both salt concentrations. As a result, a net charge reversal of the polymer-surfactant complexes was observed, between 1.0 and 1.5 mM SDS, independent of ionic strength. Phase separation occurs in the SDS concentration region where low charge density complexes form, whereas at high surfactant concentrations (up to several multiples of cmc SDS) soluble aggregates are formed. Ellipsometry and QCM-D were employed to follow adsorption of chitosan onto low-charged silica substrates, and the interactions between SDS and preadsorbed chitosan layers. A thin (0.5 nm) and rigid chitosan layer was formed when adsorbed from a 0.1 mM NaNO3 solution, whereas thicker (2 nm) chitosan layers with higher dissipation/unit mass were formed from solutions at and above 30 mM NaNO3. The fraction of solvent in the chitosan layers was high independent of the layer thickness and rigidity and ionic strength. In 30 mM NaNO3 Solution, addition of SDS induced a collapse at low concentrations, while at higher SDS concentrations the viscoelastic character of the layer was recovered. Maximum adsorbed mass (chitosan + SDS) was reached at 0.8 times the cmc of SDS, after which surfactant-induced polymer desorption occurred. In 0.1 mM NaNO3. the initial collapse was negligible and further addition of surfactant lead to the formation of a nonrigid, viscoelastic polymer layer until desorption began above a surfactant concentration of 0.4 times the cmc of SDS.

Keyword
sodium dodecyl-sulfate; quartz-crystal microbalance; solid-liquid interface; air-water-interface; x-ray-scattering; anionic surfactant; cationic polyelectrolyte; viscoelastic properties; electrolyte-solutions; air/water interface
National Category
Chemical Engineering
Identifiers
urn:nbn:se:kth:diva-11138 (URN)10.1021/la702653m (DOI)000254647400020 ()2-s2.0-42449149169 (Scopus ID)
Note
QC 20100729Available from: 2009-09-22 Created: 2009-09-22 Last updated: 2010-08-09Bibliographically approved
4. Adsorption of lysozyme, beta-casein and their layer-by-layer formation on hydrophilic surfaces: Effect of ionic strength
Open this publication in new window or tab >>Adsorption of lysozyme, beta-casein and their layer-by-layer formation on hydrophilic surfaces: Effect of ionic strength
2010 (English)In: Colloids and Surfaces B: Biointerfaces, ISSN 0927-7765, E-ISSN 1873-4367, Vol. 77, no 1, 1-11 p.Article in journal (Refereed) Published
Abstract [en]

The adsorbed amount and layer structure of lysozyme, beta-casein and mixed layers of the two proteins were studied on hydrophilic silica and quartz surfaces using the following techniques: ellipsometry, quartz crystal microbalance with dissipation monitoring (QCM-D) and total internal reflection fluorescence (TIRF). Particular emphasis was put on the effect of solution ionic strength on the layer formation. Both lysozyme and beta-casein showed a higher affinity for the silica surface when adsorbed from a solution of low ionic strength even though beta-casein and silica are negatively charged at the pH used. No beta-casein remained adsorbed after rinsing with a 150 mM buffer solution. The adsorbed amount of lysozyme on silica exceeded a monolayer coverage irrespective of the solution conditions and displayed a rigid structure. beta-Casein forms more than a single layer on pre-adsorbed lysozyme; an inner flat layer and an outer layer with an extended structure, which largely desorbs on rinsing. The build-up through sequential adsorption of lysozyme and beta-casein is favoured at intermediate and high ionic strength. The total adsorbed amount increased slightly with each deposition cycle and the mixed lysozyme/beta-casein layers contain higher amounts of protein compared to those of pure lysozyme or beta-casein. Sequential adsorption gives rise to a proteinaceous layer consisting of both lysozyme and beta-casein. The protein layers are probably highly interpenetrated with no clear separation between them.

Keyword
Lysozyme, beta-Casein, Layer-by-layer, Protein adsorption, Multilayers, Ellipsometry, QCM-D, TIRF, Solvent content
National Category
Physical Chemistry
Identifiers
urn:nbn:se:kth:diva-14272 (URN)10.1016/j.colsurfb.2009.12.019 (DOI)000276272100001 ()2-s2.0-77549086167 (Scopus ID)
Note

QC 20100729

Available from: 2010-07-29 Created: 2010-07-29 Last updated: 2016-05-18Bibliographically approved
5. Layer-by-layer assemblies of chitosan and heparin: effect of solution ionic strength and pH
Open this publication in new window or tab >>Layer-by-layer assemblies of chitosan and heparin: effect of solution ionic strength and pH
Show others...
2011 (English)In: Langmuir, ISSN 0743-7463, E-ISSN 1520-5827, Vol. 27, no 12, 7537-7548 p.Article in journal (Refereed) Published
Abstract [en]

The growth of polysaccharide multilayers consisting of positively charged chitosan (CH) and negatively charged heparin (HEP) was monitored in situ by employing a quartz crystal microbalance (QCM-D) and dual-polarization interferometry (DPI). The main focus was on how the physicochemical properties of the solution affect the growth and structure of the resulting multilayer film These results showed that when increasing the ionic strength of the polysaccharide solutions at a fixed pH, both the "dry" (optical) (DPI) mass and wet (QCM) mass of the adsorbed multilayer film increased. The same effect was found when increasing the pH while keeping the ionic strength constant. Furthermore, the growth of multilayers showed an exponential-like behavior independent of the solution conditions that were used in this study. It was also established that chitosan was the predominant species present in the chitosan heparin multilayer film. We discuss the viscoelastic properties of the adsorbed layers and their variation during the multilayer buildup. Interestingly and contrary to common interpretation of the QCM-D results, we found that under one particular solution condition (pH 4.2 and 30 mM NaCl) the increase in the dissipation of oscillation energy from the adsorbed layer was a consequence of layer stiffening rather than indicating a more hydrated and viscous film. On the basis of the widely used Voigt viscoelastic model for an adsorbed layer, we show that it is the film viscosity and shear that define the layer viscoelasticity (structure) of the film and not the absolute value of energy dissipation, which in fact can be very misleading.

Place, publisher, year, edition, pages
American Chemical Society (ACS), 2011
Keyword
QUARTZ-CRYSTAL MICROBALANCE, POLYELECTROLYTE MULTILAYER FILMS, EXPONENTIAL-GROWTH, VISCOELASTIC PROPERTIES, ELECTROLYTE-SOLUTIONS, DISSIPATION, ADSORPTION, SURFACES, WATER, ELLIPSOMETRY
National Category
Chemical Sciences Physical Chemistry
Identifiers
urn:nbn:se:kth:diva-14274 (URN)10.1021/la200441u (DOI)000291500700029 ()2-s2.0-79959202077 (Scopus ID)
Funder
Swedish Research Council
Note

QC 20100729

Updated from manuscript to article in journal. Previous title: Layer-by-layer assemblies of chitosan and heparin: effect of ionic strength and pH.

Available from: 2010-07-29 Created: 2010-07-29 Last updated: 2016-04-29Bibliographically approved
6. Polymer Dynamics in Layer-by-Layer Assemblies of Chitosan and Heparin
Open this publication in new window or tab >>Polymer Dynamics in Layer-by-Layer Assemblies of Chitosan and Heparin
2010 (English)In: Langmuir, ISSN 0743-7463, E-ISSN 1520-5827, Vol. 26, no 5, 3242-3251 p.Article in journal (Refereed) Published
Abstract [en]

The layer-by-layer deposition method has been used to build a multilayer thin film with two polysaccharides, chitosan CH (weak polycation) and heparin HEP (strong polyanion), on planar quartz surfaces. The film structure and dynamics in aqueous Solution were studied with fluorescence resonance energy transfer (FRET) and total internal reflection fluorescence (TIRF). Particular emphasis was placed on the effect of deposition conditions, i.e.. pH and salt concentration, on the out-of-plane (vertical) diffusion of fluorescence labeled chitosan in the chitosan/heparin (CH/HEP) film. FRET analysis showed that CH molecules diffused within the film with a diffusion coefficient that was not significantly sensitive to the deposition pH and Solution ionic strength. A pH-sensitive label bound to CH embedded within the CH/HEP Film wits sensitive to the charge of the outermost polymer layer even when buried under 14 alternate layers of CH and HER A consideration of the results obtained with both fluorescence techniques showed that the structure of the CH/HEP thin film wits highly interpenetrated without clear boundaries between each layer. These results are consistent with the hypothesis that the previously observed exponential-like film growth of CH and HEP in terms of, layer thickness and deposited amount versus deposition cycle can be attributed to out-of-plane diffusion of CH molecules in the multilayer.

Keyword
polyelectrolyte multilayer films, internal-reflection fluorescence, exponential-growth, weak polyelectrolyte, molecular-weight, solid-surfaces, buildup, ph, polycations, adsorption
National Category
Chemical Sciences Physical Chemistry
Identifiers
urn:nbn:se:kth:diva-14277 (URN)10.1021/la902968h (DOI)000274636900041 ()2-s2.0-77749255904 (Scopus ID)
Funder
Swedish Research Council
Note

QC 20100729

Available from: 2010-07-29 Created: 2010-07-29 Last updated: 2016-05-18Bibliographically approved

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