Filling bone defects with β-TCP in maxillofacial surgery: A review

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GENERAL REVIEW

Filling bone defects with ␤ -TCP in maxillofacial surgery: A review

Comblement osseux par ␤ -TCP en chirurgie maxillofaciale : revue des indications

B. Guillaume

^a^,^b^,∗

aCollègeFranc¸aisd’Implantologie(CFI),6,ruedeRome,75005Paris,France

bGroupeÉtudesRemodelageOsseuxetbioMatériaux(GEROM),InstitutdeBiologieenSanté(IRIS-IBS), LUNAMUniversité,CHUd’Angers,49933Angerscedex,France

Availableonline29May2017

KEYWORDS

Tricalciumphosphate;

␤-TCP;

Bonegraft;

Sinuslift;

Biomaterial

Summary Reconstructionofbonedefectspriortoimplantplacementnowinvolvessynthetic substitutessuchas␤-TCPbecauseofitsabilitytopromoteboneremodeling.Itscapacityto beprogressivelysubstitutedbythepatient’sboneallowstoregenerateadensebonevolume.

Inaddition,itsavailabilityinlargequantities,avoidingthemorbidityobservedwithharvest- ing autogenous bone, widens the operative indications. In this paper,the main indications of␤-TCPin maxillofacialsurgery(dentistry, parodontology anddental implantsurgery) are reviewed.Theyincludeperiodontalbonedisease,bonedisjunction,pre-implantsurgery(sinus ﬂoorelevationandlateralizationoftheinferioralveolarnerve).

MOTSCLÉS

␤-TCP; Biomatériau; Greffeosseuse; Sinuslift;

Tricalciumphosphate

Résumé Lareconstructiondesdéﬁcitsosseuxavantlaposed’implantfaitappeldésormaisà desmatériauxdesubstitutionsynthétiquecommele␤-TCPdeparsescapacitésàfavoriserle remodelageosseux.Ilestprogressivementsubstituéparl’osdupatientpermettantderégénérer unvolumeosseuxdense.Enﬁn,sadisponibilitéengrandequantité,évitantlamorbiditéliée à unsite deprélèvement d’autogreffe, élargit les indicationsopératoires. Dansce travail, les principalesindications d’utilisationdu ␤-TCP enchirurgiemaxillofaciale (chirurgie dentaire, parodontologie et implantation dentaire)sont revues. Elles comprennent la maladie osseuseparodontale, ladisjonctionosseuse,la chirurgiepré-implantaire (élévationdesinus etlatéralisationdunerfalvéolaireinférieur).

∗6,ruedeRome,75005Paris,France.

E-mailaddress:doct.guillaume@wanadoo.fr

Introduction

In dental and maxillofacial surgery, the repair of bone defectsaimsatrecreating a bonysitethat issuitable for http://dx.doi.org/10.1016/j.morpho.2017.05.002

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Figure 1 Scanning electron microscopic image of beta- tricalciumphosphate(␤-TCP).A.A scaffoldsuitablefor bone graftingwithaninterconnectedmacroporosity.B.Highmagni- ﬁcationofthesurfaceofa wallofthisscaffold showingthe typicalsurfaceofsinteredgrainswithmicroporosity(arrows).

morphological,prostheticor implant-prostheticrehabilita- tion[1,2].Causesofbonedeﬁciencyarenumerous:genetic, post-traumatic, secondary totooth removal,infectious or iatrogenic.Thevolumeofbonetoreconstructvariesaccord- ingtotheanatomicalsituation.Thecharacteristics ofthe

Figure2 Fillingabonesocketandreconstructionofthecorti- calsidewithbeta-tricalciumphosphate(␤-TCP)granulesafter atoothextraction.Insert:CTanalysisofthereconstructedbone severalmonthsafterthegraft,notethehighbonedensity.

graftdependonthevolumestobefilled(alveolararea)orto berestored(verticalorhorizontalridgeinsufficiency,bone cyst or sinus lifting). The volumeand form of the defect influence the choice ofthe grafting material. Aconsider- ablenumberofpossibilitiesareavailable:e.g.,harvesting autologousboneparticlestofillapost-extractionsocket[3], thickeningofathinridgecausedbyhypodontia[4],bonedisjunction[5],sinuslifting[6]orlateralizationoftheinferior alveolarnerve[7].Surgicaltechniquesalsousevarioussur- gicalprotocolswithalocalorageneralanesthesia;itshould benoticedthatlocalanesthesiaisbeingpracticedmoreand morefrequently.Althoughautologousbonegraftsandallo- graftshavebeenarecognizedsurgicalmodalityforseveral decades,theuseofsyntheticbiomaterialshascontinuedto developassubstituteproducts,especiallyinthecontextof pre-implantsurgery.

Deﬁnitions of graft-related criteria

A bone substitute must be biocompatible and ﬁll several criteria: bio-inertia is deﬁnedas the absence of physico- chemical reaction of the product in direct contact with bone.Bioactivityisthecapacitytodevelopreactionsfavor- ingosseointegrationoftheproductandtheadaptationofthe

Figure 3 A. Disjunction on a premolar zone. B. Beta- tricalcium phosphate (␤-TCP) granules (1000—2000␮m) with highporosityareinsertedinthegapcreatedbetweenthetwo cortices.

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Boneﬁllingwith␤-TCP 115 receivingtissue.Osteoinductionisdeﬁnedastheabilityto

induceboneformationinanextra-skeletalarea.Osteocon- ductionistheabilityoftherecipientbonecellstocolonize thegraft.Anevolutioninthechoiceofmaterialstofillbone defectsoccurredinthepastfewyears.Autologousgraftis consideredasthe‘‘goldstandard’’intermsofosteogenic- itybutitsmaindisadvantageis thatobtaininga sufficient volumeofboneissometimesaproblem(exceptwhenlarge bonesamplesareharvestedbutwithasignificantincrease inmorbidity)[8,9].So,duetothejustifiedreluctancetouse extra-oralbonegraftsandthemedicolegalconstraints,the interestforsyntheticbonesubstitutesisincreasinglygrow- ing.Mostsurgicalteamsseektorestoresufficientamounts of high qualitybone allowing implant placementby using biomaterials to restore a part or the whole bone. Beta- tricalciumphosphate(␤-TCP)isnowoneofthemostused synthetic materials for bone reconstructionin orthopedic andmaxillofacial surgeryand nowin pre-implantsurgery.

In implantology, the resorbable or non-resorbable nature ofthegraftedmaterialappearsoftheupmostimportance.

Some materialsareresorbable butthereareconsiderable differences in termof disappearance upon time,some of themcanpersistindeﬁnitely.Theuseofabiomaterialina maxillaryormandibularsiteafteratoothextractionmust allowimplantplacementinasecondsurgicaltime.Inaddi- tion,syntheticbiomaterialspreservethemacroarchitecture

oftheimplantedareasandtheycanbeproduced inlarge quantitiesbyindustry.

Characteristics of ␤ -TCP

␤-TCP - Ca3(POH4)2 - belongs tothe family of tricalcium phosphatesinthebetaphase.Beingconsiderablymuchmore resorbablethan hydroxyapatite, this biomaterialis highly biocompatible when implanted in bone; it is resorbable within6 to 9 monthsas shown in animal andhuman histological studies [10]. One of the main characteristics of the biomaterial is to be commercially available as scaf- foldswitha macroporosityof 100 to600␮m that ensures osteoconductionandcanreach85%ofthetotalmassofthe graftedmaterial(Fig.1A).␤-TCPhas alsoa microporosity (<100␮m)duetosinteringofelementarygrains,whichfacil- itatestheexchangeofextracellularﬂuxesofCa²⁺andPO43−

ions (Fig. 1B). This ensures an optimal bone remodeling withincreased osteoblastic apposition and the apposition oflamellarbone.Itsbiocompatibility,itsbioresorptionand osteoconductiveproperties fromthe recipient bone make it a reliable material particularly adapted to ﬁll alveolar sockets of variablesizes. In addition,reconstruction of a maxillarysinusinapre-implantationstepcanalsobeeasily obtained.␤-TCPcanalsobepreparedintheformofplates

Figure4 Sinusliftelevation.A.Thesinusmembraneisgentlypushedaway.B.Thespaceavailableforgraftingisthenexposed.

C.Beta-tricalciumphosphate(␤-TCP)granules(1000—2000␮m)withahighporosityareusedtoﬁllthisarea.D.Implantshavebeen placedinthegraftedarea9monthslater,notetheincreasedensityofthegraftedzone.

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toﬁllthesinusceiling.Suchplatesalsoallowtodensifythe underlyinggraftwithgranulesandcanbeusedtoprotectthe sinusmucosa(Schneider’smembrane)incaseofperforation.

Clinical indications of bone ﬁlling biomaterials

Periodonticsandpre-implantsurgery

Periodontalbonedisease

It has been proposed for more than 15 years to fillperi- odontal pockets with biomaterial granules. Loss of the peri-radicularbonetissueinducesmobilityofthedentalroot andcancauselossofthetooth.Underlocalanesthesia,the procedureconsistsindetachingthefullthicknessofthegin- givatoscraptheinflammatorytissuesandcementumalong therootandtofillthedefect.␤-TCPisavailableinvarious granulesizesvaryingfrom550—1000␮mto1000—2000␮m.

Figure 5 Histological analysis of a bone biopsy harvested in a patient six months after grafting with beta-tricalcium phosphate(␤-TCP) granules. A. Mineralized bone isapposed directlyontothe biomaterialsurfaces. (Goldner’s trichrome, calciﬁedboneisingreenosteoid tissueinred). B.Remodel- ingofimplanted␤-TCPgranulesbyosteoclasts.Histoenzymatic identiﬁcation of these cells by their tartrate resistant acid phosphatase(TRAcP)content;osteoclastsareinbrown,newly- apposed bone is counterstained in blue and ␤-TCP remains unstained.

Thecharacteristicsof␤-TCPscaffoldspreparedwithahigh porosity by industry are to promote reconstruction with lamellar bone. In case of apicoectomyand elimination of thecystictissuesattheapexofthetooth,abonelossmay occurwithavariablevolumerangingfromafewmm³to1 or2cm³.Thecystictissueisremovedbyacarefulcurettage and1000—2000␮mgranulesofhighporosity␤-TCPareused toﬁllthecavity.

Pre-implantsurgery

Increasing the volume of the dental arch will allow the placementofdentalimplants.Inimplantsurgery,itisoften mandatory to respect the healing time necessary for the graftedareatoberemodeledbeforeplacinganimplantin a bone environment that is sufﬁcient in volume and will remain stableover time.Post-extractionsockets, asperi- odontalpockets,canbeneﬁtfromtheuseof␤-TCPgranules tosupportbonereconstruction(Fig.2).

Bonedisjunction

Whetheratthemaxillaorthemandible,insufﬁcientthick- nessof theridgeimposestorecreate the bonethickness.

Appositiongraft isanalternativetechniquebut requiresa secondsitetoharvesttheautogenousbone;sometimesthis isnotpossibleorrejectedbythepatient.Bonedisjunction representsin facta greenstickfracture[11]. Withabone chiselorwithaﬁssureburr,verticalsectionsaredoneatthe desiredheight(Fig.3A).Similarly,acleavageplaneismade inthewholethicknessoftheridge.Finally,thecorticalbone isgraduallymovedawaywhilemaintainingitsapicalinser- tion. The gap (4 to 5mm in thickness) is then ﬁlledwith

␤-TCP1000—2000␮mgranules,thispreventsthevestibular corticalbonefromreturninginplace(Fig.3B).Thisallows boneremodelingandosseointegrationofthebiomaterialby osteoconductionin8to9months.

Sinusﬂoorelevation

Placementofanimplantintheposteriorzoneoftheupper jaw is often challenging because bone loss is observed in mostpatientswithedentulationandthicknessofthesinus ﬂoor maybe reduced up to5 to6mm. It is evident that such areduced vertical bone heightlimits implantplace- mentsincean8to10mmofboneheightisrequiredtoallow implant placement.Thus,elevationof themaxillarysinus ﬂoorisarecentlydescribedsolutiontorestoreasuitable5 to10mm heightofavailable bonefor implantplacement.

Sinus liftingwasfirstreportedbyBoyne andJamesin the 1960s[12].Sinus floorelevationfor dentalimplantplace- mentisobtainedbydetachmentofthesinusmucosausing alateralmaxillarywindowapproach(lateralanthrotomy,in mostcases)orbythecrestalroute,followedbythefillingby agraftingmaterial[13—15].Acrestalincisionofthemax- illaismadeonthealveolar ridgewithaverticaldischarge incisioninthecanineregionandoppositetotheposterior tuberosity.Thegingivalflapisthenreclinedtoensuregood visibilityoftheanteriorsurfaceofthesinusandallowthe realizationof a bone window whose upperlimit is 15mm fromthecrest. The bonewindow isdone withadiamond roundbur underirrigation(Fig.4A).The central trapdoor of corticalbone ispreserved tomaintainabone layerfor

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Boneﬁllingwith␤-TCP 117 themucosaduringtheothersurgicalsteps.Thesinusmem-

braneisthengentlyraisedfromthebonefloortodelimita sufficientvolume.Atthisstage,oneshouldcarefullycheck thepresenceofanyperforationofthemembranebecause they can leadto complications at the time of placement ofthebiomaterial(Fig.4B).Asuture maybedone witha 6/0threadora␤-TCPplate(Sinus-up^TM,Kasios,France)to ensureacomplete closureofthesinus.The cavityisthen filledwithabiomaterialthatwilllatterprovidethebonybed suitableforimplantplacement.Autogenousbonechipshave longbeenconsideredasthegoldstandardduetotheirpre- sumptivemaintenanceofcellularviability[12].Thechoice ofabiomaterialmust fulfillseveralqualities:itshouldbe biocompatible in the grafted site and should not induce aninflammatoryreactionofthesinusmucosa,whichcould bedeleterioustothewholesurgicalprocedure.Itmustbe integratedwithinthegraftedareasbycombiningitsresorp- tion and its substitution by new bone. Resorption should be progressive to allow bone remodeling with apposition oflamellarbone.Non-resorbablehydroxyapatiteshouldbe avoided[16].Macroporosityofthegraftedbiomaterialplays akeyrolein boneosteoconductionbecauseit determines theinvasionofvascularandcellularsprouts[17,18].Lastly, thegraftingmaterialmustbeprovidedinsufficientvolume toallowaneasyadaptationinthesecomplexsurgicalareas tofillvolumesup3to6cm³.Overtheyears,severaltypes of materialsincluding allograftsandxenografts of various

originshavebeenusedeitheraloneormixedwithmorcel- lizedautogenicbone[19].␤-tricalciumphosphatewasthe firstsyntheticbonesubstitutetobeproposedforsinusfloor elevation[14].The useof 1000—2000␮m granulesof high porosity␤-TCPHPisrecommendednowadays[20].Anthral fillingbeginsbyplacinggranulesontheposteriorwallthen on the latero-anterior and anteroposterior walls without excessive compression of the biomaterial (Fig. 4C). The anteriorwallisthenfilledandaresorbableSurgicel^TMmem- brane (Ethicon, Johnson and Johnson) to avoid migration ofgranulesandsuturedwithVicryl5/0^TM thread(Ethicon, JohnsonandJohnson).Acomputedtomographicanalysisis usuallydone8monthslater.Thereisamarkeddensification ofthegraftedareafilledbythebiomaterialandnoedema ofthesinusmembranecanbeevidenced(Fig.4D).

Thegraftedareaappearstobemoreradio-opaquethan thesurroundbonetissue(duetothegreatercalciumcontent of ␤-TCP). The density willprogressively decrease asthe biomaterialis replacedby bone [21]. Histologicalanalysis conﬁrmed the direct bonding of mineralized bone matrix to␤-TCPgranulestogetherwiththebiomaterialresorption (Fig.5A)[10,22,23].Dependingonthearea,thebonehasa matrixoflamellarornon-lamellartexture.Thedetectionof akeyenzymepresentintheosteoclasts(tartrateresistant acidphosphatase[TRAcP])evidencesthesecellsatthesur- faceofthenewlyformedboneandatthesurfaceof␤-TCP granules(Fig.5B).

Figure6 Loweralveolarnerve(IAN)lateralization.A.X-rayofapatientwithanincludedcaninewhoseablationwillcreatea largebonedefect.B.AsigniﬁcantbonedefectisobtainedandtheemergenceoftheIANisevidenced.C.Beta-tricalciumphosphate (␤-TCP)granules(1000—2000␮m)withahighporosityareusedtoﬁllthisarea.D.X-rayofthepatientafterlateralizationofthe IANandplacementoffourimplantsisnowpossible.

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Lateralizationoftheinferioralveolarnerve(IAN) Vertical atrophy of alveolar ridge is encountered at the mandibleasasequelaofdentalextractions(Fig.6A)orin patientswitha longhistory of wearingaremovable pros- thesis. An onlay graft allows bone reconstruction in the verticaldirectionbut requiresthe useautologouscortico- trabecular bone harvested at the calvarium, iliac crest, tibiaormandibularsymphysis,retromolararea,mandibular ramus [24]. The use of allogenic or xenogenic bone particles has also been suggested. In all cases, the graft is maintainedtothealveolarridgebyosteosynthesisusingtita- niumscrews.TheIANremains oneofthemain anatomical limitation to the placement of implants in the poste- riormandibular zone. Another alternative is to move the IAN laterally from its canal by nerve lateralization and repositioning toprovide a bone area suitable for implant placement[25].The displacement of the IANcan bepro- posedin severalsituations: in case of compression ofthe nervesheathfollowingatrauma,whenaremovableprosthe- sisexertscompressivestrainsontheIANorwhenanimplant apexdirectly compressesthe nerve [7,11,26]. Lateraliza- tionoftheIANradicallychangesthenatureoftheprosthetic conceptwhereonlytheanteriorregionisusuallyconcerned.

Displacementofthenerveallowstheplacementofimplants intheposteriorzonewitharemovableprosthesiswithanO- ringsystemoraposteriorbar.Inﬁxeddentalprosthesis,the posteriorimplantsincrease the holdingof anoverdenture oraﬁxedbridgebyprovidingsupportingpillars.Incaseofa removableprosthesis,attachmentoftheprosthesisiscon- siderablyimprovedwhenanO-ringsystemoraposteriorbar isused.

Thesurgicaltechniqueisbasedonavestibularosteotomy ofthe external corticalbone in front ofthe mental foramen,andextendedbyfashioningofaboneflaptowardsthe rear[27—29].Thecortico-trabecularboneblockisremoved togain accessto the nerveand to gently tease it out of the mandible (Fig. 6B). The bone block is both removed intotoormorcellizedandkeptuntiltheendoftheinter- vention.Replacementofthebonyflapallowsanunderlying bonegrowthandpreventsthenervefromreturningtothe mandibular canal. Nevertheless, displacement of the IAN creates abone void. It can befilled with␤-TCP particles (Fig.6C)heldinplacewithaSurgicel^TMmembrane.Compact blocksof ␤-TCP can alsobe implanted.After an 8-month bonehealingperiod,themandibularbonehasbeen recon- stituted and offers a suitable site for implant placement (Fig.6D). Highporosity ␤-TCP granules playsan essential roleinthelocalremodelingofbonevolumeandleadtothe formationofaqualitysite.

Conclusion

Boneremodelingisanessentialstepinthehealingprocess ofagraftedarea.Thecontributionofsyntheticbiomaterials is now conﬁrmed and guarantees an optimal reconstruc- tionthatallows implantplacementin a second step.The availability of ␤-TCP in the form of granules or compact slabs offers newtherapeutic perspectives in maxillofacial andpre-implantsurgery.

Disclosure of interest

Theauthordeclaresthathehasnocompetinginterest.

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