Periimplantitis and Implant Body Roughness: A Systematic Review of Literature by Dr.Niznick

PeriimplantitisandImplantBody Roughness:ASystematicReview ofLiterature

FabienneJordana,MSc,DDS,PhD,*LéaSusbielles,DDS,† andJacquesColat-Parros,MSc,DDS,PhD‡

Periimplantitisisaninfectiousprocessthatoccursafterosseointegrationoftheimplant,thusafter theformationofafunctionalinterface betweentheboneandtheimplant.1

Periimplantinﬂammationaffectsthe surroundinghardandsofttissue.2 Periimplantitisdevelopsprogressivelyfrom inﬂammationaroundtheimplant, whichwillincreaseinthesofttissues, eventuallycausingmarginalboneloss.3

Periimplantitisaffects16%to28%of patientsimplanted,intheshortorlong term.4,5 Bacteriologically,manygerms arefoundintheinfectedperiimplant sitebuttheyaremainlyanaerobes ( Aggregatibacteractinomycetemcomitans , Porphyromonasgingivalis , Prevotellaintermedia , Tannerella forsythia , Treponemadenticola, etc).6–10 Someauthorsthinkthatthis diseaseentityisaforeignbodyreaction ratherthananinfectiveprocess. 11,12 Themultiplecausesofperiimplantitiswarrantbetteranalysis.

Animportantparameterforthe clinicalsuccessofdentalimplantsis theformationofadirectbone-implant

*AssociateProfessor,DentalFaculty,UniversityofNantes, Nantes,France;HospitalPractitioner,DentistryDepartment, UniversityHealthCentre,Nantes,France.

†PrivatePractice,Pau,France.

‡HospitalPractitioner,DentistryDepartment,PellegrinHospital, UniversityHealthCentre,Bordeaux,France;Associate Professor,DentalFaculty,UniversityofBordeaux,Bordeaux, France.

Reprintrequestsandcorrespondenceto:Fabienne Jordana,MSc,DDS,PhD,UniversityofNantes,1Place AlexisRicordeau,BP84215,44042Nantescedex1, France,Phone:+33670580024,Fax:+33240201867, E-mail:fabienne.jordana@univ-nantes.fr

ISSN1056-6163/18/02706-672

ImplantDentistry

Volume27 Number6

DOI:10.1097/ID.0000000000000834

Purpose: Theaimofthissystematicreviewwastoevaluate whetherimplantroughnessisassociatedwithperiimplantitisinhumans.

MaterialsandMethods: An electronicsearchof3databases (MEDLINE,WebofKnowledge,and theCochraneLibrary)wasundertakenuntilOctober2017andwas supplementedbymanualsearching. Prospectivestudieswereincludedif theymetthefollowingcriteria:(1) giveacleardeﬁnitionofperiimplantitisand(2)containoutcomedata (clinicalandradiologicaldata)con-

contact(BIC)thatisdirectlyinﬂuenced bytheimplant’ssurfaceroughness.13 Implantsurfacetopographyatthe micrometerlevelofresolutionhasbeen regardedasthemostimportantfactorfor successfulimplanttreatment.14 Surface topographyinﬂuenceswoundhealing afterimplantationandalsoaffectsosseointegration.15,16 Surfaceroughness measurementisthemeasurementofthe small-scalevariationsintheheightof aphysicalsurface.17 Someparameters, suchasarithmeticmeansurfaceroughness(Sa),thatis,theaverageheightof theanalyzedarea(micrometer),were usedtodescribethesurfacetopography. Sarepresentsthearithmeticmeanofthe roughnessareafromthemeanplane,for theheightofthepeaksandvalleysaccordingtotheISO25178standard.18 Sa expresses,asanabsolutevalue,thedifferenceinheightofeachpointcompared

sideringtheperiimplantitisrate.A systematicreviewwascarriedoutto evaluatetheimpactofroughnesson theperiimplantitisrate.

Results: Of4690potentiallyeligiblearticles,22wereincludedin thequalitativeanalysisandquantitativesynthesis.

Conclusions: Thissystematic reviewsuggeststhatroughnessand surfacetreatmentofdentalimplants areimportantfactorsassociated withperiimplantitis.(ImplantDent 2018;27:672–681)

KeyWords:periimplantdisease, surfaceroughness,implantsurface

tothearithmeticalmeanofthesurface. AccordingtoAlbrektssonandWennerberg,19 implantsmaybeclassiﬁedinto4 typesaccordingtosurfaceroughness: smooth(Sa , 0.5 mm);minimallyrough (Sabetween0.5and1.0 mm),moderately rough(Sabetween1.0and2.0 mm),and rough(Sa . 2.0 mm).

Theaimofthisreviewwasto examinewhetherimplantroughnessis associatedwithperiimplantitisinhumansthroughaliteraturereview.

MATERIALSAND METHODS

ThePreferredReportingItemsfor SystematicReviewsandMeta-Analyses system20,21 wasadoptedforthissystematicreview.

StudyProtocolandCriteria

Theprotocolwasdesignedto answerthefollowingquestion: “In

subjectswithdentalimplants,dothe implantsurfacetreatmentorsurface roughnesscharacteristicsleadtoperiimplantitis?” Itincludedstudiesreporting onatleast15participants,randomized clinicaltrials,prospectivecohortstudies, retrospectivestudies,case-controlstudies,andcross-sectionalstudiesinhumansafterimplantation.Periimplantitis wasdeﬁnedbyHeitz-Mayﬁeld22 asthe radiographicpresenceofboneloss $2mmsincethetimeofprosthetic replacement,positivebleedingonprobing,andprobingdepth $4mm.

Inclusioncriteria. OnlystudiespublishedinEnglishinaninternational peer-reviewedjournalwereincluded. Thestudieshadtodescribesurface treatmentorsurfaceroughnesscharacteristicsthatcanleadtoperiimplantitis. Theyalsohadtogiveacleardeﬁnition ofperiimplantitisorcontainclinicaland radiologicaldata,whichthereviewers couldreliablyrelatetoperiimplantitis. Exclusioncriteria.Invitro studiesand animalstudieswereexcluded.ThefollowingPECO(Population,Exposureto riskfactor,Comparison,Outcome)definitionswereconsideredforsystemic search:

Population:studieshadtoinclude systemicallyhealthypatients withimplanttreatment; Exposure:periimplantdiseasediagnosedunderaclinicalandradiographicexaminationandadhered toapreviouslydescribeddeﬁnition;

Comparison:thespeci ﬁ ccomparisonsinvestigatedweredifferenceseitherinimplantsurface characteristicsorinimplant roughness; Outcomemeasures:theprimaryoutcomevariablewasperiimplantitis.

SearchStrategy

Aliteraturesearchwasperformed inMEDLINEviathePubMeddatabase oftheUSNationalLibraryofMedicine, intheWebofScience,andCochrane Librarydatabasesaswellasahand searchofotherliteraturetoidentify articlesofpotentialrelevance.The

Fig.1. PreferredReportingItemsforSystematicReviewsandMeta-Analyses(PRISMA) ﬂ ow diagramdemonstratingtheresultsofthesystematicliteraturesearch.

Fig.2. Electronicdatabasesusedandjournalssearchedmanuallyforthesystematicliterature search.

searchincludedarticlesacceptedfor publicationfrom2000uptoOctober 2017.Previouslypublishedreview articlesonsimilartopicswerealso analyzedtoassesspotentiallyrelevant publications.

Thefollowingkeywordswereused forthispurpose:

Table1. DesignofSelectedPublications24–45

1117TiOBlast(AstraTech)SandblastedModerately rough 94

Östmanetal37 1146TiUnite(NobelBiocare)AnodicoxidationModerately rough 121

Schliephake etal38 544Osseospeed(AstraTech)Sandblasted+ acid-etched Moderately rough 143

Chappuisetal39 2098Boneﬁ t(Straumann)TPSRough145

Polizzietal40 6–10122BrånemarkSystem(NobelBiocare)MachinedMinimally rough 257500

TiUnite(NobelBiocare)AnodicoxidationModerately rough 243

Ravaldetal41 12–1566TiOblast(AstraTech)SandblastedModerately rough 184371

BrånemarkSystem(NobelBiocare)MachinedMinimally rough 187

Jungneretal42 5103TiUnite(NobelBiocare)AnodicoxidationModerately rough 154287

BrånemarkMKIII(NobelBiocare)MachinedMinimally rough 133

vanVelzenetal43 10250Soft-TissueLevelSLActive (Straumann) Sandblasted+ acid-etched Moderately rough 506

Beckeretal44 12–2392ITITPS(Straumann)TPSRough388 Glauser45 1138TiUniteMKIV(NobelBiocare)AnodicoxidationModerately rough 102

CylindricalInternalGrade31.1ModeratelyroughSandblasted

ConicalInternalTA 6 V 4 z 1.7ModeratelyroughSandblasted+acid-etched

CylindricalExternalGrade10.5MinimallyroughMachined

CylindricalExternalGrade10.7MinimallyroughMachined

CylindricalExternalGrade40.9MinimallyroughMachined

CylindricalExternalGrade41.1ModeratelyroughAnodicoxidation

technologies) † ,32

BrånemarkStandard(NobelBiocare) ‡ ,40

BrånemarkMarkII(NobelBiocare) ‡ ,27,30,40,41

BrånemarkMarkIII(NobelBiocare) ‡ ,40,42

BrånemarkMarkIV(NobelBiocare) ‡ ,40

BrånemarkMarkIIITiUnite(Nobel Biocare) ‡ ,33,37,40,42,45

BrånemarkMarkIVTiUnite(NobelBiocare) ‡ ,37,40,45

ITITPS(Straumann)§ ,24,26,28,44

CylindricalInternal . 2RoughTPS

CylindricalInternalGrade4 . 2RoughTPS Bone ﬁ tTPS(Straumann)§ ,39

CylindricalInternalGrade41.75ModeratelyroughSandblasted+acid-etched

ITISLActive(Straumann)§ ,31,34

SoftTissue-LevelSLActive(Straumann)§ ,43

periimplantitisORperi-implantitis ORperiimplantitisORperiimplantORperiimplantdiseasesORperi-implantdisease ORperiimplantdisease ANDtitaniumORdentalimplant ORimplant AND 1.surfacecharacteristicORsurface roughnessORmaterialcharacteristicORtitaniumsurfaceOR implanttypeORimplantsurface ORsurfacedecontaminationOR surfacetopography.

2.surfacetreatmentORTPSORtitaniumplasma-sprayedORanodic oxidationORSLAORmachined surfaceORturnedsurfaceOR sandblastedandacid-etchedsurfaceORsandblastedsurfaceOR acid-etchedsurface.

QualityAssessment

Qualityassurancewasdeveloped byindependentscreeningby2reviewers (L.S.,F.J.)accordingtoKhanetal.23 Whendisagreementaroseintheselectionandeligibility,itwasresolvedby discussionbetweenthe2reviewers.

DataExtractionandSynthesis

*AstraTechAB,Mölndal,Sweden. † MISImplantTechnologiesLtd,Israël. ‡ NobelBiocareAB,Göteborg,Sweden. §StraumannAG,Waldenburg,SwitzerlandBrånemarkSystem(NobelBiocare) ‡ machined(MKnotidenti ﬁ ed). 25,26

Thesearchgave4690results.Two independentreviewers(L.S.,F.J.)analyzedtitlesandabstractsduringthe first stageofscreening.Irrelevantarticleswere discarded.Additionalmanualsearchingof referencelistsinthearticlesselectedandin anumberofreviewarticleswasperformed tosourcefurtherrelevantpublications (Fig.1).Theimplantologyandperiodontologyjournalsweresearchedmanually between2000and2017: ClinicalImplants DentistryandRelatedResearch, Clinical OralImplantsResearch, EuropeanJournalofOralImplantology, JournalofOral Implantology, ImplantDentistry, InternationalJournalofOralandMaxillofacial Implants, JournalofPeriodontology, JournalofClinicalPeriodontology , andPeriodontology2000 (Fig.2). Ninety-eightfull-textarticleswere assessedforeligibility.Thefulltexts ofthearticleswerereadtodeterminewhetherthestudiesful fi lled thepredeterminedinclusioncriteria. Twenty-twostudiesfulfilledtheinclusion criteriaand76wereexcluded(Fig.1).

Datawerecollatedintotables (Tables1–5)andgroupedaccordingto implantroughnessandsurfacetreatment.Datasynthesiswasperformed basedontheevidencetablesalone, andthedatawerefurtherinterpreted. Statisticalanalyses(Chi2)werecarried outusingXLStat(Addinsoft).

RESULTS

Theinitialsearchoftheliteratureup toOctober2017yielded4690potentiallysuitablearticles.Aftertheexclusionofreviews,animaland invitro studies,andstudiesthatinappropriately identiﬁedperiimplantitisorsurface treatmentorroughnesscharacteristics, 22publicationsremainedfullyeligible forthisreview.Ameta-analysiscould notbeperformedbecauseoftheheterogeneityofthereviewedstudies.

The k valueforintervieweragreementforstudyinclusionwas0.92for titlesandabstractsand1.00forfull-text articles,indicatingstrongagreement.

PeriimplantitisRateandImplant SurvivalRateAccordingtoRoughness

Fortheminimallyroughsurfaces, theSaisbetween0.5and1 mm.The meanperiimplantitisrateobservedis 0.57%(Table3).Of8studiesreferenced,25–27,29,30,40–42 ﬁve25–27,29,30 do notpresentperiimplantitis.Twostudies40,42 presentalowratebetween 0.39%and0.65%.Finally,thestudy byRavaldetal41 indicatesamaximum rateof3.20%for184implants.

Forthemoderatelyroughsurfaces, theSaisbetween1and2 mm.Ourliteraturereviewcovered16studies;periimplantitisratesarebetween0.00%and 7.56%,withameanrateof3.43%.There isahighdispersionofresults.

Fortheroughsurfaces,theSais greaterthan2 mm.Themeanperiimplantitisrateis12.86%,withratesranging between9.76%and20.00%according tothestudies.

Therefore,theminimallyrough surfaceshaveverylowperiimplantitis rates.Theperiimplantitisrateincreases withthemoderatelyroughsurfaces accordingtotheirroughnessandtothe techniqueusedtoobtaintheroughness. Theroughsurfaceshavethehighest periimplantitisrates,whichcanreach 20.00%.

Thestatisticalanalysisisstatisticallysigniﬁcant(P , 10 6)andallows ustosaythatthehighertheroughness is,thehigheristheperiimplantitisrate.

PeriimplantitisRateAccordingto SurfaceTreatment

Theminimallyroughsurfacesare obtainedbymachining.Themoderatelyroughsurfacesareobtainedby sandblasting,sandblasting+acidetching,orbyanodicoxidation(Table4). Theroughsurfacesareobtainedby titaniumplasma-sprayed(TPS).There isastaticallysigni ﬁ cantdifference inthefrequencyofperiimplantitis betweenthedifferentsurfacetreatments( P ¼ 10 6 ).

Inourliteraturereview,all theminimallyroughsurfacesare machined.Theperiimplantitisrates arebetween0.00%and3.20%with themachinedsurfaces. 25 – 27,29,30,40 – 42 Themeanperiimplantitisratewiththe machinedsurfacesis0.57%.

Forthemoderatelyroughimplant surfaces,arelativeheterogeneityof theperiimplantitisratescanbenoted. Thelowestratesareobservedwiththe sandblastedsurfaceswithanSaof 1.1 mm.Themeanperiimplantitisrate withthesandblastedsurfacesis2.38% withratesrangingbetween0.00%and 5.00%.Thesesurfacesseemclinically favorable.Whenthesurfaceisobtained byanodicoxidation,however,theSais also1.1 mm.Themeanperiimplantitis rateis4.14%,withratesranging between1.65%and7.56%.33,37,40,42,45

Thesurfacesobtainedbysandblasting+acidetching(SLA)havean Saof1.75 mm.Themeanperiimplantitisrateis3.41%,withratesranging from1.76%to6.29%.

Thehighestperiimplantitisratesare foundwiththesurfacestreatedbyTPS. TheirSaishigherthan2 mm.Themean periimplantitisrateis12.86%,withrates rangingfrom9.76%to20.00%.

Thesestudiesconﬁrmthatthe periimplantitisrateincreaseswithsurfaceroughness.Theresultsdiffer, however,forthemoderatelyrough surfaces.Thesandblastedsurfaceshave anSaclosetothatoftheminimally roughsurfaces.Thesurfacestreated bysandblasting+acidetchinghave higherperiimplantitisratesthanthe sandblasted-onlysurfaces.TheirSais 1.75 mm.Itisclosetothatoftherough surfaces.However,thesurfacestreated byanodicoxidation,withanSaof 1.1 mm,havehighperiimplantitisrates, withameanrateof4.14%.

PeriimplantitisRateAccording toFollow-up

Sixstudieswerecarriedoutover periodsrangingfrom1to5years (Table5).24–27,38,42 Allthestudiesobserve aperiimplantitisrateof0.11%withtheminimallyroughsurfacesoverperiodsof 1to5years,from1.09%to6.29%for moderatelyroughimplantsandfrom 11.69%to12.28%forroughimplants.

Eightstudies28,31–35,40,43 present afollow-upofbetween6and10years. Theperiimplantitisratesarehigherthan forthestudiescarriedoutovera5-year period.Theperiimplantitisratesobserved withmachinedsurfacesare0.39%and withroughsurfacestreatedbyTPSare 15.40%.28 Theperiimplantitisratesrange from1.76%to6.20%withthemoderatelyroughsurfaces.

Eightstudies29,30,36,37,39,41,44,45 presentingafollow-upofmorethan 11yearswereincludedinthisliterature review.ThelongestisthatofChappuis etal,39 witha20-yearfollow-upofTPS roughsurfaces.Thisstudyindicates a20.00%periimplantitisrate.39 Theminimallyroughsurfaceshaveperiimplantitisratesthatvaryfrom0.00%to 3.20%.Themoderatelyroughsurfaces giveresultsrangingfrom0.00%to 7.56%,withmeanrateof3.21%.The meanperiimplantitisrateislessthan thatofthe5-to10-yearstudies.The studiescarriedoutovermorethan11 yearsconcernimplantswithsurfaces treatedbysandblastingorbyanodic oxidation.Nosigniﬁcantdifference wasfoundwithrespecttothemoderatelyroughsurfacesaccordingto follow-uptime(P ¼ 0.81).Forthemoderatelyroughsurfaces,aperiimplantitis rateof3.04%isobserved,andthenstabilizationisobservedovertime.

Theperiimplantitisratewiththe roughsurfacesincreaseswiththestudy time.Therateofoccurrenceofperiimplantitisis12.04%between1and5 years,15.40%between6and10years. At20years,theperiimplantitisrateis 20%inthestudybyChappuisetal.39 Fortheminimallyroughsurfaces,however,theresultsofthe1-to5-yearstudiesandthe6-to10-yearstudiesare comparable,butthereisastatistically signiﬁcantincreaseintheperiimplantitisrateafter11years(P ¼ 1.2x10 4). However,theperiimplantitisfrequency remainslow.

DISCUSSION

Thereisnoconsensualdefinitionof periimplantitisorofitsclinicalparameters.The6thEuropeanConsensus Conference(2008)gavethefollowing definition: “thelesionofperiimplant mucositisresidesinthesofttissues, periimplantitisalsoaffectsthesupportingbone.”3 Definitionsofperiimplantitis,whichmayincludedifferentclinical andradiologicalthresholds,vary becauseofthevariousthresholdsof bonelossandpocketdepthsusedin theliterature.46 Correctdiagnosisof periimplantdiseaseisessentialto appropriatelymanageperiimplantdisease.32 Weusedthisdefinitionof

periimplantitis:radiographicpresence ofboneloss $2mmsincethetimeof prostheticreplacement,positivebleedingonprobing,andprobingdepth $4mm.22 AccordingtoAlbrektsson andWennerberg,19 implantsmaybe classiﬁedinto4typesaccordingtosurfaceroughness:smooth(Sa , 0.5 mm);minimallyrough(Sabetween 0.5and1.0 mm),moderatelyrough(Sa between1.0and2.0 mm),andrough(Sa . 2.0 mm).Sarepresentsthearithmetic meanoftheroughnessareafromthe meanplane,fortheheightofthepeaks andvalleys.18

The ﬁrstimplantstobeproduced (machinedorturned)arestillconsideredthegoldstandardforimplant surfaces.Theirminimallyroughsurfaces(Satypicallyrangingfrom0.4to 0.8 mm)haveperiodicgrooves.Inthe 2000s,roughersurfacesweresoughtto increasetheBIC,improveimplantstability,andallowearlierimplantloading.47,48 Someauthorsconsideredthat theincreasedsurfaceroughnessofcommerciallypuretitaniumimplantswould improveBICandthemechanicalpropertiesoftheinterface49–53 andthatthe

improvedplateletactivationcouldpositivelyregulatetheosteogenic responses.54

Themajorityofcurrentlymarketed implantsaremoderatelyrough(Sa between1.0and2.0 mm).22 AlbrektssonandWennerberg19 showedthat thereisanoptimumsurfaceroughness windowfrom1to1.5 mm,forwhich thereisacompromisebetweenengineeringandclinicalpractice.Theyconsiderthatahighervalueleadstoaloss ofboneanchoring.19 Quirynenetal55 reportthatimplantswithrelatively smoothsurfacesmustbeusedtopreventbiologicalcomplications.Many studies56–58 showthatroughimplants developsigniﬁcantlymoreperiimplantitis.Espositoetal59 showedthattheuse ofmachinedimplants(minimallyrough surfaces)insteadofroughimplants couldbringa20%reductionintheperiimplantitisrate.Theseauthorsconﬁrm theresultsofourliteraturereview.

Surfacetreatmentsinﬂuenceimplantroughness.Machinedimplants havearelativelysmoothsurface.60 Sandblastingconsistsofforcingsmall gritsofchosenshapeandsizeacross

implantsurfaces,usuallybycompressedair.60 Acidetchingbyimmersioninstrongacidscreatesa microroughnesswithirregularpitsof varyingdepthsonthesurface.60 With theSLAmethod,theimplantsurface is ﬁrstsandblastedwithlargegrit,then theacidetchingformsmicropitsonits surface.TheroughimplantsareallproducedusingtheTPStechnique.TPS dentalimplantshaveacomplexsurface; theparticledensityinthevalleysnormallyappearshigherthanthoseonthe threadpeaks.61 Wehavenotincluded hydroxyapatite-coatedimplantsinour literaturereviewbecausethereare manycontroversiesabouttheirlongtermprognosis.

Thesandblasted+acid-etchedsurfaceshaveanSaof1.75 mm,andthe roughsurfaceshaveanSagreaterthan 2 mm.Inourliteraturereview,themean periimplantitisratewithsurfacestreated bysandblasting+acidetchingis 3.41%.Thebonelossobservedwith themachinedorsandblastedimplants isequivalent,aswiththeoccurrenceof periimplantitisaccordingtoseveralauthors.62–64 BICisevengreaterwith sandblastedsurfacesthanwithmachined surfaces.19,65–67

Inoursystematicreviewofliterature,2studies 29,30 comparesandblastedsurfacesandmachined surfaces.Nosigniﬁcantdifferenceis observed.Theperiimplantitisrateis 0%inboththesestudies.Themeanperiimplantitisratewithsurfacestreatedby anodicoxidation(moderatelyroughsurfaces)is4.14%.ThestudybyPolizzi etal40 concludesthatthesesurfaceshave ahigherperiimplantitisrate(3.7%)than themachinedsurfaces(0.39%).Thesurfacestreatedbyanodicoxidationhave anSaequivalenttothesandblastedsurfaces(1.1 mm);theirperiimplantitisrate is,however,higher.Thedifferenceis duetotheirsurfacetreatment.Thesandblastedsurfaceisobtainedbysubtraction,andthesurfacetreatedbyanodic oxidationisobtainedbyaddition. Finally,implantswithaveryrough TPSsurfacehaveperiimplantitisrates thatcanreach20.00%.Itshouldbenoted thattheperiimplantitisratesobserved withTPSsurfaces(12.86%)are,inour literaturereview,lessertothoseofthe studybyDametal68 (18.00%).

Periimplantitisisoneofthemajor problemsinimplantology.Manyuncertaintiesremainregardingitsetiopathogenesis.Bacterialinfectionisan aggravatingfactor.Also,theroleof theoperatorandthehost’sresponse cannotbeexcluded.Ourliterature reviewshowsthatsurfaceroughness playsamajorroleintheoccurrenceof periimplantitis.

CONCLUSION

Periimplantitisisclearlylinkedwith surfaceroughnessaccordingtotheresultsofoursystematicreviewofliterature.Thehigherthesurfaceroughness, thehigherthemeanperiimplantitisrate. Uptoanarithmeticmeansurfaceroughness(Sa)of1 mm,thereislittleperiimplantitis.PeriimplantitisappearsforSa valuesgreaterthan1.2 mm.

Consideringthereviewedstudies asawhole,itisevidentthatimplant roughnessisassociatedwithperiimplantitis.Althoughacomparisonofthe publishedresultswaslimitedduetothe lackofhomogeneityofthestudies,itis clearthatcliniciansshouldgivepriority totheuseofimplantswithmachinedor evensandblastedsurfaces.

DISCLOSURE

Theauthorsclaimtohaveno ﬁnancialinterest,eitherdirectlyor indirectly,intheproductsorinformationlistedinthearticle.

ROLES/CONTRIBUTIONS

BY AUTHORS

F.Jordanamadesubstantialcontributionstoconceptionanddesign, acquisitionofdata,oranalysisand interpretationofdata;draftedorcriticallyrevisedthemanuscriptforimportantintellectualcontent;andprovided ﬁnalapprovalofthemanuscript.L. Susbiellesmadesubstantialcontributionstoconceptionanddesign,acquisitionofdata,oranalysisand interpretationofdata;draftedorcriticallyrevisedthemanuscriptforimportantintellectualcontent;andprovided ﬁnalapprovalofthemanuscript.J. Colat-Parrosmadesubstantialcontributionstoconceptionanddesign,

acquisitionofdata,oranalysisand interpretationofdata;draftedorcriticallyrevisedthemanuscriptforimportantintellectualcontent;andprovided ﬁnalapprovalofthemanuscript.

ACKNOWLEDGMENTS

F.JordanaandL.Susbiellescontributedequallytothiswork.

REFERENCES

1.MouhyiJ,DohanEhrenfestDM, AlbrektssonT.Theperi-implantitis:Implant surfaces,microstructure,andphysicochemicalaspects. ClinImplantDentRelat Res. 2012;14:170–183.

2.SmeetsR,HenningsenA,JungO, etal.Deﬁnition,etiology,preventionand treatmentofperi-implantitis:Areview. Head FaceMed. 2014;10:34.

3.LindheJ,MeyleJ;GroupDof EuropeanWorkshoponPeriodontology. Peri-implantdiseases:Consensusreport ofthesixthEuropeanWorkshopon Periodontology. JClinPeriodont. 2008; 35:282 – 285.

4.FranssonC,LekholmU,JemtT,etal. Prevalenceofsubjectswithprogressive bonelossatimplants. ClinOralImplants Res. 2005;16:440–446.

5.RinkeS,OhlS,ZiebolzD,etal. Prevalenceofperi-implantdiseaseinpartiallyedentulouspatients:Apracticebased cross-sectionalstudy. ClinOralImplants Res. 2011;22:826–833.

6.PontorieroR,TonelliMP,CarnevaleG, etal.Experimentallyinducedperi-implant mucositis:Aclinicalstudyinhumans. Clin OralImplantsRes. 1994;5:254–259.

7.MombelliA,LangNP.Thediagnosis andtreatmentofperi-implantitis. Periodontology2000. 1998;17:63–76.

8.LeonhardtA,RenvertS,DahlénG. Microbial ﬁndingsatfailingimplants. Clin OralImplantsRes. 1999;10:339–345.

9.TeughelsW,VanAsscheN,Sliepen I,etal.Effectofmaterialcharacteristics and/orsurfacetopographyonbioﬁlm. ClinOralImplantsRes. 2006;17:68–81.

10.HultinM,GustafssonA,Hallström H.Microbiological ﬁndingsandhost responseinpatientwithperi-implantitis. ClinOralImplantsRes. 2012;13:349–358.

11.AlbrektssonT,DahlinC,JemtT, etal.Ismarginalbonelossaroundoral implantstheresultofaprovokedforeign bodyreaction? ClinImplantDentRelat Res. 2014;16:155–165.

12.AlbrektssonT,CanulloL,Cochran D,etal.Peri-implantitis:Acomplicationof aforeignbodyoraman-made “disease.” Factsand ﬁction. ClinImplantDentRelat Res. 2016;18:840–849.

13.RosaMB,AlbrektssonT, FrancischoneCE,etal.Theinﬂuenceof surfacetreatmentontheimplantroughness pattern. JApplOralSci. 2012;20:550–555.

14.WennerbergA,AlbrektssonT. Implantsurfacesbeyondmicronroughness. Experimentalandclinicalknowledgeof surfacetopographyandsurfacechemistry. ApplOsseointegrationRes. 2006;5:40–44.

15.AlbrektssonT,BrånemarkPI, HanssonHA,etal.Osseointegrated titaniumimplants:Requirementsfor ensuringalong-lasting,directbone-toimplantanchorageinman. ActaOrthop. 1981;52:155–170.

16.BauerS,SchmukiP,vonderMark K,etal.Engineeringbiocompatibleimplant surfaces.PartI:Materialsandsurfaces. ProgMaterSci. 2013;58:261–326.

17.ButlerDL.Surfaceroughness measurement.In:LiD,ed. Encyclopedia ofMicroﬂuidicsandNano ﬂuidics.Boston, MA:Springer;2014.

18.InternationalOrganizationforStandardization. ISO25178:GeometricProduct Speciﬁcations(GPS) SurfaceTexture: Areal Part2:Terms,Deﬁnitionsand SurfaceTextureParameters.Geneva, Switzerland;2012:1–47.

19.AlbrektssonT,WennerbergA.Oral implantsurfaces:Part1:Reviewfocusing ontopographicandchemicalpropertiesof differentsurfacesandinvivoresponsesto them. IntJProsthodont. 2004;17:536–543.

20.Transparentreportingofsystematicreviewsandmeta-analyses.Available at:http://www.prisma-statement.org.AccessedOctober21,2017.

21.MoherD,LiberatiA,TetzlaffJ, etal.Preferredreportingitemsfor systematicreviewsandmeta-analyses: ThePRISMAstatement. PLoSMed. 2009;6:e1000097.

22.Heitz-May ﬁeldL.Peri-implant diseases:Diagnosisandriskindicators. JClinPeriodont. 2008;35:292–304.

23.KhanKS,terRietG,PopayJ,etal. StageII:Conductingthereview.Phase5: Studyqualityassessment.In:KhanKS,ter TietG,GlanvillJ,etal,ed. Undertaking SystematicReviewsofResearchon Effectiveness.2nded.York,United Kingdom:UniversityofYork;2001:1–20.

24.BehnekeA,BehnekeN,d’Hoedt B.Thelongitudinalclinicaleffectiveness ofITIsolid-screwimplantsinpartiallyedentulouspatients:A5-yearfollow-upreport. IntJOralMaxillofacImplants. 2000;15: 633–645.

25.EliassonA,PalmqvistS,Svenson B,etal.Five-yearresultswith ﬁxed complete-archmandibularprostheses supportedby4implants. IntJOralMaxillofacImplants. 2000;15:505–510.

26.AstrandP,EngquistB,AnzénB, etal.Athree-yearfollow-upreportof

acomparativestudyofITIDentalImplants andBrånemarkSystemimplantsinthe treatmentofthepartiallyedentulousmaxilla. ClinImplantDentRelatRes. 2004;6: 130–141.

27.AstrandP,EngquistB,DahlgrenS, etal.AstraTechandBrånemarksystem implants:A5-yearprospectivestudyof marginalbonereactions. ClinOralImplants Res. 2004;15:413–420.

28.KaroussisIK,BräggerU,SalviGE, etal.Effectofimplantdesignonsurvival andsuccessratesoftitaniumoral implants:A10-yearprospectivecohort studyoftheITIdentalimplantsystem. Clin OralImplantsRes. 2004;15:8–17.

29.VroomMG,SiposP,deLangeGL, etal.Effectofsurfacetopographyof screw-shapedtitaniumimplantsinhumansonclinicalandradiographicparameters:A12-yearprospectivestudy. Clin OralImplantsRes. 2009;20:1231–1239.

30.JacobsR,PittayapatP,van SteenbergheD,etal.Asplit-mouthcomparativestudyupto16yearsoftwo screw-shapedtitaniumimplantsystems. JClinPeriodont. 2010;37:1119–1127.

31.BuserD,JannerSF,WittnebenJG, etal.10-yearsurvivalandsuccessratesof 511titaniumimplantswithasandblasted andacid-etchedsurface:Aretrospective studyin303partiallyedentulouspatients. ClinImplantDentRelatRes. 2012;14:839–851.

32.CharyevaO,AltynbekovK, ZhartybaevR,etal.Long-termdental implantsuccessandsurvival Aclinical studyafteranobservationperiodupto6 years. SwedDentJ. 2012;36:1–6.

33.DegidiM,NardiD,PiattelliA.10yearfollow-upofimmediatelyloaded implantswithTiUniteporousanodizedsurface. ClinImplantDentRelatRes. 2012; 14:828–838.

34.FischerK,StenbergT.Prospective 10-yearcohortstudybasedonarandomizedcontrolledtrial(RCT)onimplantsupportedfull-archmaxillaryprostheses. Part1:Sandblastedandacid-etchedimplantsandmucosaltissue. ClinImplant DentRelatRes. 2012;14:808–815.

35.GotfredsenK.A10-yearprospectivestudyofsingletoothimplantsplacedin theanteriormaxilla. ClinImplantDentRelat Res. 2012;14:80–87.

36.MertensC,StevelingHG,Stucke K,etal.Fixedimplant-retainedrehabilitationoftheedentulousmaxilla:11-yearresultsofaprospectivestudy. ClinImplant DentRelatRes. 2012;14:816–827.

37.ÖstmanPO,HellmanM,SennerbyL. Tenyearslater.Resultsfromaprospective single-centerclinicalstudyon121oxidized (TiUnite)Brånemarkimplantsin46patients. ClinImplantDentRelatRes. 2012;14:852–860.

38.SchliephakeH,RödigerM,Phillips K,etal.Earlyloadingofsurfacemodiﬁed implantsintheposteriormandible 5-year resultsofanopenprospectivenoncontrolledstudy. JClinPeriodont. 2012; 39:188–195.

39.ChappuisV,BuserR,BräggerU, etal.Long-termoutcomesofdental implantswithatitaniumplasma-sprayed surface:A20-yearprospectivecaseseries studyinpartiallyedentulouspatients. Clin ImplantDentRelatRes. 2013;15:780–790.

40.PolizziG,GualiniF,FribergB.A two-centerretrospectiveanalysisoflongtermclinicalandradiologicdataofTiUnite andturnedimplantsplacedinthesame mouth. IntJProsthodont. 2013;26:350–358.

41.RavaldN,DahlgrenS,TeiwikA, etal.Long-termevaluationofAstraTech andBrånemarkimplantsinpatients treatedwithfull-archbridges.Resultsafter 12to15years. ClinOralImplantsRes. 2013;24:1144–1151.

42.JungnerM,LundqvistP,Lundgren S.Aretrospectivecomparisonofoxidized andturnedimplantswithrespectto implantsurvival,marginalboneleveland peri-implantsofttissueconditionsafterat least5yearsinfunction. ClinImplantDent RelatRes. 2014;16:230–237.

43.vanVelzenFJ,OfecR,Schulten EA,etal.10-yearsurvivalrateandtheincidenceofperi-implantdiseaseof374titaniumdentalimplantswithaSLAsurface:A prospectivecohortstudyin177fullyand partiallyedentulouspatients. ClinOralImplantsRes. 2015;26:1121–1128.

44.BeckerST,Beck-BroichsitterBE, RossmannCM,etal.Long-termsurvival ofstraumanndentalimplantswithTPS surfaces:Aretrospectivestudywith afollow-upof12to23years. ClinImplant DentRelatRes. 2016;18:480–488.

45.GlauserR.Implantswithan oxidizedsurfaceplacedpredominatelyin softbonequalityandsubjectedto immediateocclusalloading:Resultsfrom an11-yearclinicalfollow-up. ClinImplant DentRelatRes. 2016;18:429–438.

46.CharalampakisG,JansåkerE, Roos-JansåkeAM.Deﬁnitionand prevalenceofperi-implantitis. CurrOral HealthRep. 2014;1:239–250.

47.RoccuzzoM,BuninoM,PrioglioF, etal.Earlyloadingofsandblastedand acid-etched(SLA)implants:Aprospective split-mouthcomparativestudy. ClinOral ImplantsRes. 2001;12:572–578.

48.BornsteinMM,LussiA,SchmidB, etal.Earlyloadingofnonsubmerged titaniumimplantswithasandblastedand acid-etched(SLA)surface:3-yearresults ofaprospectivestudyinpartiallyedentu-

louspatients. IntJOralMaxillofacImplants. 2003;18:659–666.

49.CooperLF.Aroleforsurface topographyincreatingandmaintaining boneattitaniumendosseousimplants. JProsthetDent. 2000;84:522–534.

50.ClassL,WilkeHJ,SteinemannS. Theinﬂuenceofvarioustitaniumsurfaces ontheinterfaceshearstrengthbetween implantsandbone. JBiomech. 1991;24: 461.

51.WennerbergA,EktessabiA, AlbrektssonT,etal.A1-yearfollow-up ofimplantsofdifferingsurfaceroughnessplacedinrabbitbone. IntJOral MaxillofacImplants. 1997;12:486 – 494.

52.BuserD,BrogginiN,WielandM, etal.Enhancedboneappositionto achemicallymodiﬁedSLAtitanium surface. JDentRes. 2004;83:529–533.

53.FergusonSJ,BrogginiN,Wieland M,etal.Biomechanicalevaluationofthe interfacialstrengthofachemicallymodiﬁed sandblastedandacid-etchedtitaniumsurface. JBiomedMaterResA. 2006;78: 291–297.

54.ParkJY,GemmellCH,Davies JE.Plateletinteractionswithtitanium: Modulationofplateletactivitybysurface topography. Biomaterials. 2001;22: 2671 – 2682.

55.QuirynenM,DeSoeteM,Van SteenbergheD.Infectiousrisksfororal implants:Areviewoftheliterature. Clin OralImplantsRes. 2002;13:1–19.

56.MobergLE,KöndellPA,Sagulin GB,etal.BrånemarksystemandITI dentalimplantsystemfortreatmentof mandibularedentulism.Acomparative randomizedstudy:3-yearfollow-up. Clin OralImplantsRes. 2001;12:450 – 461.

57.MarroneA,LasserreJ,BercyP, etal.PrevalenceandriskfactorsforperiimplantdiseaseinBelgianadults. ClinOral ImplantsRes. 2013;24:934–940.

58.QuirynenM,AbarcaM,VanAssche N,etal.Impactofsupportiveperiodontal therapyandimplantsurfaceroughnesson implantoutcomeinpatientswithahistoryof periodontitis. JClinPeriodont. 2007;34: 805–815.

59.EspositoM,ArdebiliY,Worthington HV.Interventionsforreplacingmissing teeth:Differenttypesofdentalimplants. CochraneDatabaseSystRev. 2014;22: CD003815.

60.YanGuoC,TinHongTangA, PekkaMatinlinnaJ.Insightsintosurface treatmentmethodsoftitaniumdental implants. JAdhesSciTechnol. 2012;26: 189 – 205.

61.KlokkevoldPR,JohnsonP, DagrostariS,etal.Earlyendosseous integrationenhancedbydualacidetching oftitanium:Atorqueremovalstudyinthe

rabbit. ClinOralImplantsRes. 2001;12: 350–357.

62.WennströmJL,EkestubbeA, GröndahlK,etal.Oralrehabilitationwith implant-supported ﬁxedpartialdentures inperiodontitis-susceptiblesubjects.A5yearprospectivestudy. JClinPeriodont. 2004;31:713–724.

63.ArnhartC,DvorakG,Tre ﬁlC,etal. Impactofimplantsurfacetopography:A clinicalstudywithameanfunctional loadingtimeof85months. ClinOral ImplantsRes. 2013;24:1049–1054.

64.WelanderM,AbrahamssonI, BerglundhT.Subcrestalplacementof two-partimplants. ClinOralImplants Res. 2009;20:226 – 231.

65.ThomasKA,CookSD.An evaluationofvariablesinﬂuencingimplant ﬁxationbydirectboneapposition. JBiomedMaterRes. 1985;19:875–901.

66.BuserD,SchenkRK,Steinemann SG,etal.Inﬂuenceofsurfacecharacteristics onboneintegrationsoftitaniumimplants:A histomorphometricstudyinminiaturepigs. JBiomedMaterRes. 1991;25:889–902.

67.EricssonI,JohanssonCB,Bystedt H,etal.Ahistomorphometricevaluation ofbone-to-implantcontactonmachinepreparedandroughenedtitaniumdentalimplants.Apilotstudyinthedog. ClinOralImplantsRes. 1994;5:202 –206.

68.DamHG,NajmSA,NurdinN,etal. A5-to6-yearradiologicalevaluationof titaniumplasmasprayed/sandblastedand acid-etchedimplants:Resultsfromprivate practice. ClinOralImplantsRes. 2013;25: e159–e165.