REVUE DE LA LITTÉRATURE / LITERATURE REVIEW Parodontologie /

CURRENT KNOWLEDGE AND FUTURE PERSPECTIVES OF BARRIER MEMBRANES: A BIOMATERIALS PERSPECTIVE

Carole Chakar * | Sara Khalil** | Nadim Mokbel*** | Abdel Rahman Kassir****

Abstract: Periodontal regenerations and augmentations are common procedures practiced on a daily basis worldwide. This had led to the introduction of a wide number of barrier membranes, all aiming at regenerating a sufficient amount of bone while being safe, cost effective and easy to handle. Membranes have different characteristics that may influence their clinical properties and the result obtained. The article aims at presenting an overview of the different barrier membranes commonly used in the oral surgery field, while shedding light on the new advances in the third generation membranes. Keywords: Barrier membrane – periodontal regeneration – bone augmentation. IAJD 2020;11(1):43-50.

CONNAISSANCES ACTUELLES ET PERSPECTIVES D'AVENIR DES MEMBRANES BARRIÈRES

Résumé La régénération parodontale et les chirurgies d’augmentation osseuse sont des procédures courantes pratiquées quotidiennement dans le monde entier. Cela a conduit à l’introduction d’un grand nombre de membranes barrières, toutes visant à régénérer une quantité suffisante d’os tout en étant sûres, rentables et faciles à manipuler. Les membranes ont des caractéristiques différentes qui peuvent influencer leurs propriétés cliniques et le résultat obtenu. L’article vise à présenter un aperçu des différentes membranes barrières couramment utilisées dans le domaine de la chirurgie buccale, tout en mettant en lumière les nouvelles avancées des membranes de troisième génération. Mots-clés: membrane - régénération parodontale - augmentation osseuse. IAJD 2020;11(1):43-50.

* Ass. Prof. ** Masters in Periodontics, Head of Department of Periodontology Department of Periodontology Saint Joseph University, Beirut, Lebanon Saint Joseph University, Beirut, Lebanon [email protected] *** Ass. Prof. **** Masters in Periodontics, Department of Periodontology Department of Periodontology Saint Joseph University, Beirut, Lebanon Saint Joseph University, Beirut, Lebanon 44 IAJD Vol. 11 – Issue 1 Revue delalittérature| ease ofuse/clinical manageability. maintenance, tissue integrationand biocompatibility, cellexclusion,space ria abarriermembraneneeds tofulfill: authors [5-7]describedfivemain crite- the abovementionedfunctions, many progenitor cells[3].Inorderto achieve the mitosisandchemotaxisofosteo- cell populationsandaccommodates which permitsexclusionofundesirable gnized as “compartmentalized healing” for boneregeneration[4]. from thesurroundingtissuesallowing sure fromthetissueflap[3]. and preventsitscollapsebythepres- ted spacefortheorganizingbloodclot [2]. ting formationofanewperiodontium late thecoronalrootsurfacefacilita- dontal ligamentarefavoredtorepopu- sites. from the flap isexcluded from healing interactions. with -root surface apically migratingandinterfering following: of asubgingivalbarrierachievesthe overlying superficialtissues.[1]. nal regeneration of tissues towards the the body;(d)requirementforcoro- sue thatisnotseeninotherpartsof for dentalcementumformation,atis- healing; (c)thespecificrequirement role ofbacterialcontaminationduring periodontal ligament;(b)thepotential formation ofthethreetissues the requirementforcoordinated periodontal tissues.Theseinclude:(a) ticular issues that are unique tothe tissues. Theserequirementsposepar ment interposedbetweenthesetwo functionally orientedperiodontalliga- alveolar bone,dentalcementum,and the coordinatedformationofnew Introduction This phenomenonhasbeenreco- - Particulategraftsareseparated - Themembranecreatesaprotec - Progenitorcellsfromtheperio - Thegingivalconnectivetissue - Epithelialcellsareimpededfrom It isbelievedthattheplacement Periodontal regenerationrequires Literature Review - ingrowth anddoes notelicitaforeign- non-porous, does notallowtissue inertness andbiocompatibility. Itis rocarbon polymer with exceptional 1.2. e-PTFE exfoliation andprematureremoval. clinical applicationduetoreported served itspurpose,itwasnotidealfor fibers. Althoughthistypeofmembrane with insertingperiodontalligament new attachmentofcementum regeneration ofthealveolarboneand 1982. Histologicexaminationshowed acetate asanocclusivemembranein bacterial filterproducedfromcellulose tion attempts,Nymanetal.[9]useda 1.1. Cellulosefilters membranes. cation associatedwithnon-absorbable been afrequentpost-surgicalcompli- of flapsloughingduringhealinghas exposure causedbyvariableamounts procedure [8].Moreover, membrane bidity associatedwithanysurgical tance, time,cost,andpossiblemor nied byconcernsoverpatientaccep- for theirremoval.Thisisaccompa- require asecondsurgicalprocedure left inthetissues.However, they they possessforaslongare integrity, andtheessentialfeatures use. Theymaintaintheirstructural developed andapprovedforclinical first generationofbarriermembranes 1. Non-resorbablemembranes generation membranes. light onthenewadvancesinthird make abetterselectionandshedding surgery field,helpingtheclinician used barriermembranesintheoral an overviewofthemostcommonly situation andhispersonalexperience. can beuseddependingontheclinical combinations of biomaterials that nician hasaconsiderablenumberof and bonereplacementgrafts,thecli- Polytetrafluoroethylene isa fluo- In the first guided tissue regenera- Non-absorbable barrierswerethe The aimofthisarticleistopresent Faced withdifferentmembranes - of non-resorbable membranes[23]. is consideredtodaythe“gold standard” not requiringasecondsurgery [22].It without lifting the mucosal flap, thus, ved easilybypullingonthemembrane preserved [20]andtheycan be remo- the fullwidthofkeratinizedmucosais When noprimaryclosureisrealized remains lowerthane-PTFE[20,21]. brane barrier, andtheriskofinfection it stillactsasanappropriatemem- even if it is exposed to the oral cavity, tion offoodandbacteria,thus, that itcompletelyblocksthepenetra- fact, previousauthorshavereported sue closureisnotmandatory[19].In implant. Furthermore,primarysofttis- the underlyinggraftmaterialand/or augmentation site,whichprotects bacterial infiltrationintothebone membranes [18]. 0.3mm) thanthee-PTFE(around1mm) lower (0.2µm)andarethinner(0.2- porosity ofuptoonehundredtimes permeable. Thesemembraneshavea PTFE, whichisnon-expandedandnon- made ofpuremedical-gradeandinert 1.3. d-PTFE dual probingdepth[17]. attachment level(CAL)gainandresi- positive outcomesregardingclinical with e-PTFEmembranesdemonstrated fact, treatmentofintra-bonylesions in different clinical settings [14-16].In human primatestudies[5,12,13]and been demonstratedincanine,non- support periodontalregenerationhas polytetrafluoroethylene devicesto submerged [9]. e-PTFE membranes;trans-gingivaland 11]. Therearetwoconfigurationsof lar graftmaterialforover20years[10, reactions andhasbeenusedasvascu- exhibits minimalinflammatorytissue in differences in physical structure. It stress duringmanufacturing,resulting trafluoroethylene subjectedtotensile polytetrafluoroethylene isapolyte- body reactionintissue.Expanded These characteristicseliminate The high-densityPTFE(d-PTFE)is The potentialoftheseexpanded 45

Parodontologie / Periodontology

1.4. Titanium mesh / Titanuim-reinforced It appears that neither of the abo- Absorbable materials used for e-PTFE membranes vementioned materials fulfills yet the guided tissue regeneration (GTR) Titanuim reinforced barrier mem- design criteria for a guided tissue rege- or guided bone regeneration (GBR) branes provide advanced mechanical neration device [31]. devices fall into two broad categories: support (increased tent-like effect), Today, as evidence of the effecti- natural products and synthetic mate- which allows a larger space for bone veness of bioresorbable membranes rials [8]. and tissue regrowth. This is of special increases, non-resorbable membranes 2.1. Natural products importance when the defect morpho- are losing importance in clinical Natural membranes are made of logy does not create an adequate space practice and their use is increasingly or chitosan. Successful treat- recognized as important requirement limited to specific indications. Since ment following the use of such barrier for achieving regeneration. However, the use of e-PTFE membranes has materials have been demonstrated, their main disadvantages remain the been documented to result in suc- but the results of studies vary [34]. increased risk of exposure due to their cessful GBR therapy, results obtained stiffness and a more complex secon- using new materials should always be 2.1.1.Collagen barriers dary surgery to remove them [9, 24]. compared with results of e-PTFE mem- Collagen constitutes almost one These membranes consist of a branes [26]. third of all protein in the body and is double layer of e-PTFE with a titanium a major constituent of natural extra- framework interposed [3, 25]. Recent 2. Resorbable membranes cellular matrix. It is (a) physiologically research has demonstrated the suc- Absorbable barriers do not require metabolized, (b) chemotactic for fibro- cessful use of these membranes in ver- additional surgery for removal, which blasts and neutrophils, (c) hemostatic, tical ridge augmentations and in the reduces patient dis- comfort, chair-side (d) a weak immunogen and (e) a scaf- treatment of large defects in the alveo- time and related cost, while elimina- fold for migrating cells [8, 35]. lar process [26]. Some other studies ting potential surgery-related morbi- There are two major types of col- reveal superior regenerative capacity dity. They also offer the advantages of lagen used in the manufacturing [3] and less persistent inflammation having better cost-effectiveness while of membranes, type I and type III, when compared to traditional PTFE causing less complication; they are usually derived from different bovine membranes [27]. quickly resorbed in case of exposure, and porcine tissues (e.g. tendon, thus eliminating the open microstruc- dermis, and small intestine). When 1.5. Other non-resorbable membranes tures that are prone to increased bac- exposed to the oral cavity, periodontal Case reports have documented terial contamination [26, 32]. pathogens (Porphyromonas gingiva- the use of rubber dam [16]. However However, resorbable membranes lis and Bacteroides melaninogenicus) the latter offers little rigidity to assure offer limited control over the length of are capable of producing collagenase, space maintenance, can be tedious application because the disintegration an enzyme that can lead to prema- to manipulate, and exhibits no tissue process starts upon placement in the ture membrane degradation. Collagen integration [8]. tissues, and the ability of each indi- membranes are often used with bone The use of a resin-ionomer barrier vidual patient to degrade a particular grafting material or extra-stabilization has also been reported [28]. It could biomaterial may vary significantly, par- with mini-screws and tacks to compen- have excellent space-making proper- ticularly for materials requiring enzy- sate for their lack of space-making abi- ties; however, it is difficult to fabricate matic degradation [8]. lity [36]. in situ, have the potential to elicit local Several studies have compared 2.1.1.1. Cross-linking of collagen barriers inflammatory reactions and its tis- bioresorbable membranes to non- Collagen membrane goes through sue integration properties, if any, are resorbable membranes made of the process of cross-linking, which unknown [29]. e-PTFE. In situations where no mem- involves the multiplication of natural Cobalt–chromium based alloy has brane exposures were noted, the occurring connections between the col- also been suggested for guided bone results regarding the relative amount lagen molecules, in order to enhance regeneration (GBR). Although this of bone formation were usually more its mechanical properties [37]. This alloy is known to be less biocompa- favorable using the e-PTFE membranes process makes the membranes more tible than titanium and titanium alloy, compared to the bioresorbable ones rigid (increased tensile strength) and it has superior mechanical properties [33]. This is mainly due to the better decelerates enzymatic degradation (e.g. stiffness and toughness). The space-making capacity of e-PTFE and process [38]. Many authors suggested potential use of CoCr alloy for GBR the lack of a resorption process and that the use of cross-linked collagen has been evaluated in a recent animal thus the absence of the resorption membranes brought many benefits to study but it has not yet been docu- products that negatively affect bone guided tissue regeneration (GBR) [36]. mented in any clinical report [30]. formation. 46 IAJD Vol. 11 – Issue 1 Revue delalittérature| GTR [2]. optimal biodegradablematerial for membranes didnotappear to bethe ristics [42].Theyconcludedthat cargile results anddifficulthandlingcharacte- branes. Investigatorsreportedlimited assessing theefficacyofthesemem- ture contains a paucity of information resorb in30-60days[2].Thelitera- gut suturematerial.Itisreportedto chromatized inasimilarmannerto bovine intestineandisprocessed 2.1.3.Cargile membrane were foundintheliterature[41]. papers describingtheclinicalresults table materialsforGBR,nosignificant rimental bonedefectsandaresui- promote boneregenerationinexpe- ting that chitosan-based membranes tion (GTR)techniques. to beusedinguidedtissueregenera- racteristics makethismaterialsuitable and abacteriostaticeffect.Thesecha- biodegradability, lowimmunogenicity, properties, includingbiocompatibility, Chitosan possess important material that ofcollageninhigheranimals[40]. and crab)hasaroleanalogousto crustacean shells(i.e.thatofshrimp of chitin.Thelattermaterialexistsin derived frompartialde-acetylation 2.1.2.Chitosan basedbarriers lagen resorption[31,39]. of bloodvesselsisessentialforcol- since thetransmembranousformation not impaired by its increased thickness tion ofthedoublelayermembranewas improves itsstability. Thevasculariza- a reductionofmicromovementsand ossification. Thesecondlayerachieves and canenablebetterbonedefect time intissue;theydecomposeslowly ter barrierabilityandremainforlonger arranged in several layers, show grea- thickness 2.1.1.2. Membranearchitectureand Cargile membraneisderivedfrom Although thereisevidenceindica- Chitosan isnaturalpolymer Membranes of greaterthickness, Literature Review a similarstructure toextracellular from brown seaweed andachieves polysaccharide thatcanbe obtained 2.1.6.Alginate-based membranes come [8]. ted histologicallyforregenerativeout- exclusion andhasnotbeeninvestiga- provision and/ormaintenance,cell It appearstoofferlimited,ifany, space may possess antibacterial properties. resorbed withoutharmfuleffectsand have demonstratedthatthematerial device [49].Invivoandinvitrostudies used asaguidedtissueregeneration upon incorporatingblood.Ithasbeen that converts to a gelatinous mass lable resorbablehemostaticdressing based product,isacommerciallyavai- 2.1.5.Oxidized cellulose the wound. allow asecondintentionshealingof because itsconsistencyandplasticity regenerations withrisksofexposure [48]. Thus,isparticularlyindicatedin intention healingincaseofexposure facilitating thehandling,andasecond properties andplasticconsistencythus bone formationduetoitsmechanical maintaining thedesiredvolumefor months) [47],notrequiringre-entry, resorbability (approximately5to6 has beendescribedtohaveaslow [46]. space makingeffectinaestheticareas useful whenitisnecessarytoobtaina graft [45].Thispropertyisparticularly semi-rigid coveringtotheunderlying fixated withosteosynthesisscrews,a the defectmorphologycreating,once can beshaped[44]andadaptedto becomes flexibleafterhydrationand cation anddrugs[43].Thefinemodel function asacarrierforcertainmedi- biocompatible, hygroscopic and can cribed asosteoconductive,resorbable, natural heterologousorigins.Itisdes- crystal bonemineralsandcollagenof bone matrixmadeofcarbonatednano- 2.1.4.Cortical lamina Alginate isanaturalbiocompatible Oxidized cellulosemesh,aplant- The collagenatedporcinebarrier The cortical lamina is a cortical sue invasion[31, 51]. bone growthwhilst limitingfibroustis- brane hasbeensuggestedto promote nical properties.Thisparticular mem- in adjusting the thickness and mecha- amnion ECMandhasgood flexibility ral andmechanicalproperties ofthe tic membranepreservesthestructu- and amnion-basedmembranes 2.1.7.3. Humanpericardium,duramater bandage afterosseousresection[9]. of attachedgingivaandasabiologic for mucogingivaldefects,formation currently usedasamembranebarrier, ment ofthirddegreeburnsandare been successfullyusedforthetreat- cular connectivetissue.Theyhave leaving animmunologicallyinertavas- nate the targets of rejection response, zation andde-cellularizationtoelimi- undergone aprocessofde-epitheliali- material (mainly of type-I collagen)has been obtainedfromtissuebanks.The material fromcadaverskinthathas 2.1.7.2. Acellulardermalallografts(ADM) might notbeeasytouse[50]. although ithasbeenreportedthat as resorptiontime)ofthismaterial, is available on other aspects (such bone allograft. Limited information ticulate demineralizedfreeze-dried tion device,inconjunctionwithapar been usedasguidedtissueregenera- sive removaloflipoproteins),hasalso freeze-dried boneallografts(succes- in amannersimilartodemineralized (from calvariumregion),processed 500-µm-thick stripofcorticalbone 2.1.7.1. 2.1.7.Human-derived membranes were foundintheliterature[41]. papers describingtheclinicalresults table materialsforGBR,nosignificant rimental bonedefectsandaresui- promote boneregenerationinexpe- ting thatalginate-basedmembranes tation [18]. may lastseveralmonthsuponimplan- gels. Ithasaslowdegradationrateand matrices whencrosslinkedtohydro- Lyophilized multilayeredamnio- ADM isabioresorbablegrafting Laminar bone,a300-to Although thereisevidenceindica- Laminarbone - 47

Parodontologie / Periodontology

Dura mater, consisting of an irregu- for bone fixation demonstrated that caprilactone)(PLCL) layer surrounded lar network of collagen fibers, is obtai- the material persists for approximately by two composite layers composed ned from cadavers. Clinical reports four to six years [56]. of a gelatin/polymer ternary blend suggest that dura mater has limited At present, there are limited and (PLCL:PLA:GEL). potential to support periodontal rege- contradictory data regarding the effi- neration. Moreover, use of cadaveric cacy of polylactic acid to facilitate 3.2. Antibacterial properties dura mater may represent a risk to regeneration. Additional research is Some antimicrobials, like tetra- acquire Creutzfeldt-Jakob disease not needed to clarify the potential of this cycline for example, which have anti- only for the recipient, but for the ope- material [2]. inflammatory, fibroblast stimulatory rator as well [8]. 2.2.2.PUR membranes properties and collagenase-inhibiting 2.1.7.4. Platelet-concentrate membranes Polyurethanes are organic poly- properties, may improve the regenera- derivatives mers containing the urethane group, tive response because of these proper- Platelet-concentrate membranes encompassing a variety of materials ties, even in the absence of a bacterial are natural autologous membranes with diverse properties [28]. These challenge. Thus integrating these anti- developed through venous blood col- membranes did not result in significant microbials into the membranes can lection and centrifugation protocol regeneration compared with control prolong their degradation time [55]. and/or freezing cycles. The biggest and some clinical complications were The incorporation of metronidazole drawback of these membranes is the described (probable exfoliation of the benzoate (MET) to the layer interfacing short resorption time (generally 10 membranes during early healing) [8]. the epithelial tissue has been deve- days). Thus, it would be most useful 2.2.3.Calcium sulfate loped to reduce the amount of anae- when combined with other grafting These barriers are composed of robic Gram-negative such as materials to take advantage of its hea- medical-grade calcium sulfate and and anae- ling properties rather than serving as can be placed over the bone grafts for robic spore-forming Gram-positive an inherent barrier membrane for GTR clot stabilization and to exclude unde- bacilli [53]. or GBR [52, 53]. sirable tissue. They provide a source Other investigators have also of calcium in the early mineralization focused on the successful incorpora- 2.2. Synthetic products process and aid particle retention. tion of tetracycline hydrochloride and These synthetic resorbable mem- Calcium sulfate dissolves in approxi- metronidazole benzoate (MET) into branes are based on different variants mately 30 days without an inflamma- various membranes [58]. of polyesters (PGA poly-lactic acid, PLA tory reaction, and it does not attract Incorporation of 25% doxycycline poly-lactic acid, PCL poly-caprolac- bacteria or support infection [9]. into a GTR membrane, which was tone) and their copolymers. These are composed of polyglycolic acid and natural metabolites of the body, which 3. An outlook into the future: the polylactic acid, would seem to have a are eliminated through the Krebs cycle third generation membranes beneficial effect on periodontal bone as carbon dioxide and water [54] (52). As the concept of tissue enginee- regeneration in dogs [55]. These materials are biocompatible, but ring has developed, third-generation by definition they are not inert since membranes have evolved, not only 3.3. The incorporation of nanotechnology in some tissue reactions and inflamma- acting as barriers but also as delivery GTR tory response may be expected during devices to release specific agents such The coating or incorporation of degradation [55]. as antibiotics, growth factors, adhe- nano-particles has been shown to 2.2.1.PGA and PLA membranes sion factors, etc., at the wound. Briefly improve other functional characteris- PGA and PLA are manufactured by they may be considered into the fol- tics of the membranes such as stiff- catalytic polymerization of the mono- lowing subdivisions [55]. ness, bioactivity, drug and antimicro- mers and are widely used for sutures bial delivery and protein or molecules and drug controlled-release devices [2, 3.1. Functionally graded and multilayered carriers [36]. (34) 8]. membranes Studies have demonstrated that The main advantages of these types A novel functionally graded mem- the addition of nano-carbonated of polymeric membranes are their brane (FGM) was designed and fabri- hydroxyapatite (nCHAC) improved manageability, processability, tuned cated via multi-layering e-spinning both the biocompatibility and the biodegradation, and drug-encapsula- [57]. The FGM consists of a core-layer osteoconductivity of the membrane. ting ability. However, their degrada- (CL) and two functional surface- The authors demonstrated that cal- tion might elicit a strong inflammatory layers (SL) interfacing bone (nano- cium phosphate nanoparticles played response, leading to resorption of the hydroxyapatite, n-Hap) and epithelial a significant role in terms of improving regenerated bone [31].. In humans, (metronidazole, MET) tissues. The CL membrane bioactivity and facilitating biopsy specimens of PLA screws used comprises a neat poly (D,L-lactide-co- early cell differentiation [55]. 48 IAJD Vol. 11 – Issue 1 Revue delalittérature| . However, utilizing stem predictable regeneration of functional allow better outcomes and a more GTR membranesascellcarriers may either ascellsheetsand/or using the [1]. Relyingonstemcell therapy, b-TCP–extracellular matrix scaffolds lagen matrices,b-TCP, andcombined other matrixmaterial,includingcol- suitable porousscaffoldmaterialor of cells into the wound seeded into a numbers exvivo,andreimplantation or dentaltissues,expansionofcell stem cellsfrombonemarrowstroma rapy is the isolation of mesenchymal vehicle (Cellsheets) 3.5. Membranesasastemcelltherapy ration isnotarealityyet[55]. peutic agentsforperiodontalregene- routine useofgrowthfactorsasthera- evaluation withpromisingresults,the Despite alonghistoryofpreclinical rative efficacy in rat calvarial defects. tially enhanceguidedtissueregene- loaded PLLAmembranemightpoten- studies [26]. activity inexperimentalandclinical found toexhibitveryhighosteogenic human BMP-2(rhBMP-2)hasbeen proteins (BMPs1-15).Recombinant b-FGF), andbonemorphogenetic -b), fibroblastgrowthfactor(a-and ming growthfactorbeta(TGF-aand growth factor(IGF-IandII),transfor growth factor(PDGF),insulin-like mentation includeplatelet-derived periodontal andalveolarridgeaug- currently believedtocontribute the focusofsubstantialresearch[8]. targeted deliveryoftheseproteinsis of extracellularmatrixproteins.The control thesynthesisanddegradation chemotaxis andcellproliferation; and disease,includingangiogenesis, tissue. Theyinfluencetissuerepair produce matrixtowardthedeveloping vide stimulitocellsdifferentiateand modulate thecellularactivityandpro- release 3.4. BarriermembraneswithGrowthFactors The principleofstemcellthe- It wasalsofoundthatPDGF-BB Growth anddifferentiationfactors Growth anddifferentiationfactors Literature Review - ther [1]. branes remains to be investigatedfur cells incombinationwithbarriermem- nical application[32]. tional requirementsinthespecificcli- to thematerialsinrelationfunc- the benefitsandlimitationsinherent based on a thorough understanding of tages, abarriershouldbeselected offers bothadvantagesanddisadvan- periodontal tissueengineering[57]. generation ofGTR/GBRmembranesfor lular matrixcouldsucceedasthenext that mimicscloselythenativeextracel- tionally gradednano-fibrousmaterial active, spatiallydesignedandfunc- can behypothesizedthatabiologically on agraded-biomaterialsapproach,it therapy hasyettobedeveloped.Based for useinperiodontalregenerative Conclusion Until then,sinceeverymembrane It isclearthatthe“ideal”membrane - 49

Parodontologie / Periodontology

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