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Guided Tissue Regeneration AroundDentai impiants in ImmediateExtraction Socl<et$: Comparison ofe-PTFE and a New TitaniumMembrane

Renato Cellefti, MD. DDS'Mithridade Davorpanah. MD, DDS"Daniel Etienne, MD, DDS'"Gabriele Pécora, MD, DDS'""Jean-Francois Tecucianu"Dragaslav Djukanovic"'"Karl Donath, Prof Dr Dr'"""

To evaluate ttie efficacy of guided tissue regeneratior\ around exposedimplant threads, 16 implants were placed Into fresh extroction sockets Inbeagle dogs. Polytetrañuorcefhylene (e-PTFE) membranes and tlfoniummembranes were used tc cover the defects around impiants. A controlgroup did net receive any membranes. Resuits were evaiuated histclogicai-ly. The average gain in bone height wos 2.1 mm for e-PTFE sites, 0.8 mm forItfonium membranes, and 2.9 mm for ccntroi sites. Ttie greatest gain in bonelevels was seen for two sites that received e-PTFE membrones and remoinedcovered for the entire evaluation interval. Within the iimits of this sfudy. clini-cal ond histologie evidence demonstrated fhot, when primary coverage ismaintained, the use of e-PTFE membranes can significantiy enhance bcneregenerotion around implants, (int Periodont Rest Dent 1994; 14:243-253)

'Private Practice, Rome, italy.**Pitie Salpetriere Hospitol, Department Of Periodontoiagy,

University of Poris VL Paris. France.* * • Deportment Of Periodontology, University of Poris Vil, Poris,

Fronce.* * * * Department Of Orai Surgery, University Ot New York ot

Buffolo, Buffalo, New Voik.' * ***Cl in ic For Period o ntoiagy and Oroi Medicine, Faculty ot

Dentistry, University Of Beigtode, Beigrade, Yugoslovio.*****Deportmeni Of Pathology. Eppendorf Hospital, University

of Hamburg, Hamburg, Germany.

Correspondence to: Dott Renato Celletti, Via Ttiailondio 24,0D144Rame, Itaiy.

In the past 20 years, osseointe-grated dental implants havebecome a reliable treatmentmodality for totaiiy edentulouspatients,'-^ The iong-term prog-nosis for endosseous titaniumimplonts is reloted fo the quali-ty and quantity of bone,^ Untilrecently, when presurgiooievaluations revealed an insuffi-cient bone volume, patientshad to be rejected or treotedby graffing procedures. If treat-ment were performed on thesepatients, exposed threads,dehiscences, or bony defectscouid be expecfed fo occur.

In long-term Brônemark ion-gitudinal studies, impiants werecompietely embedded inbone. Therefore, it hos beensuggested that a wall of boneat ieast 1 mm thick shouldcover fhe faciai and the iinguaiaspect of the impiant.^ In thesestudies, extractions were per-formed at least 1 year prior tcimplant plaoement,'-^'' Duringpostextroction heaiing, theedentulous ridge resorbs inwidth and height, which resuits

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in a decrease in theamount ofbone avaiiable for implantsurgery.

Guided bone reconstruc-tive therapy is not a new con-cept, Murray et ai^ and Ling-horne,'' in their studies of woundhealing, have deveioped theprinciples of selective tissuereconstructive therapy. Theyused mechanicai barriers to iso-late bone defects and theblood clot from nonosteogenicextraskeletal connective tissueceils. ' Guided tissue regenera-tion (GTR) has been successfuiiyused to treat various types ofperiodontai defects,^''^ Theprincipie of GTi? is dependentupon the use of occlusivemembranes to isoiate peri-odontai defects frcm gingivaiepitheiium and connective tis-sue. This method seiectiveiyaiiows oeiis from the periodon-tal iigament to repopulote theroot surface and bone defect,resuiting in new attachment.

The principie of GTR hasbeen recently opplied forregeneration of bone tissuearound dental impiants.'""'''Inconsistent bone healingoround exposed implantthreads is due to the ingrowthof fibrous connective tissue intottie wound. Furthermore, whenimplants are placed intoextraction sockets, apicalmigration of epitheiial celisaiong the impiant surface mayprevent osseointegration.

The purpose of this studywas to test the principle ot GTRaround exposed implantthreads. The impiants wereplaoed into fresh extroctionsockets in beagie dogs,Polytetrafiuoroethyiene (e-PTFE)membranes and titanium mem-branes were used to evaluatebone formation around theimplants; untreated control sitesalso were used.

Method ond materiais

Four aduit beagle dogs wereused in this study. The teethwere cleaned with chiorhexi-dine 1 week before the surgicaiprocedures. The animais werepremedicated with Ace Pro-mazine and anesthetized witha combination ot Combalanand Ketamine, Local anesthe-sia (2% lidocaine with epineph-rine 1:100,000) was adminis-tered at the surgicai sites. Anintramuscuiar antibiotic regi-men combining prooaine peni-ciilin (200 mg) and neomycinsulfote (100 mg) was adminis-tered daily for 1 week.

Suioular incisions weremade around teeth P3 and P4 .Buccai and iinguai mucoperi-osteai tiaps were raised ineach mandibular sextant. Forfiap access, two vertical reieas-ing incisions were made on themesiobuccai aspect ot toothP3 and on the distobuccal

aspect of tootj P4, To avoidroot tip fractures, extractions ofteeth P3 and P4 were per-formed using a hemisectiontechnique.^° Granulation tissuewas debrided frcm ttie extrac-tion sockets. For each premo-lar, one extraction socket(mesiai or distai root) was ran-dom iy chosen for implantplacement, A carbide bur wasused to create a dehiscence-type defect of at least 6 mmon the buccai aspect of theselected extraction socket. Atotal ot four implants wereplaced in each dog. A tctai otsixteen 10-mm endosseousimplants (Implant Innovations)were placed according tc theprotocoi described by Adeii etai , ' A varying number ofthreads were left exposed afterimpiant piacement. The dehis-cence-type defect was evalu-ated by five vertical ond tyi/ohorizontai measurements usingPCP 15 periodontal probes (Hu-Friedy)." Vertical measure-ments were taken from thecoronai part of the impiant rimas foliows; coronal aspect ofimplant rim tc the aiveolarcrest, mesially and distally; andto the base of the defect.mesiaily, midbuccaliy, and dis-taily. The width of the defectwas measured horizontally at itsmost coronal and apicaiaspects,

Twc different mechanicalbarriers were evaluated, e-PTFF

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membrane (GTAM. Gore-Texaugmentat ion aaterial, WLGore) and an experimentaltitanium membrane (15 pmthick. A, Hruska). The studydesign inciuded six test e-PTFEsites, six titanium membranesites, and four ccntrci sites,which were not augmented.The flip of a coin determinedtest and control sites. Thematerials (e-PTFE and titaniummembranes) were trimmed tocompletely cover the exposedimpiant threads. The mem-branes were secured to theimpiants with the implant coverscrews. The mucoperiostealflaps were coronally reposi-tioned to attain primary cover-oge and were closed withinterrupted 4-0 e-PTFE sutures.The surgical procedures weredocumented with photo-graphs, ond radiagraphs weretaken during and after surgery(Figs 1 to 7). The dags weremointained on a soft diet fal-lowing surgery. Postoperativecare ccnslsted ot chiorhexidineswobbing on a daily basis for14 weeks. Sutures were re-moved at 10 days.

At 14 weeks, the animaiswere anesthetized, radio-graphs were taken, and surgi-col reentries were performedon 13 sites (Figs 8 to 11). Themembranes were removedand ciinicai measurementswere taken to evaiuatechanges in bone height. The

dogs were killed by an over-dose of scdium pentcthal andblock sections were taken.Vertical slots were made at themidbuccal aspect of fhe im-plant rim to determine a reter-ence point for histologie sec-tions. Soft tissue heaiing wasanalyzed histoiogicaiiy.

At three sites (one e-PTFE,one titanium membrane, andone control) reentry surgerieswere not performed. At thesesites, the implant and ifs sur-rounding tissues were removeden bloc. All specimens werefixed in 10% buffered formalinand processed for histologiesectioning. Tissue sections wereobtained aocording to a saw-ing and grinding techniquedescribed by Donath andBreuner. i

Histologie sections wereexamined under the lightmicroscope to determine thequality and quantity of newbone. Hisfoiogic measurementswere performed aiong the mid-buccal aspect of the implant.Clinical ond histologie bonemeasurements were com-pared to evaluate the amountot regeneration.

Preoperative and postoper-ative measurements were ana-lyzed using difterent statisticalanalysis. The one-way analysisot variance evaluated thecomparability of the preopera-tive measurements, A Pear-son's correlation test was used

to determine if postoperativeclinical and histoiogic mea-surements were related. Apaired Student's t test evaiu-ated ditterences between clini-cal preoperative and histoiogicpostoperative measurementswithin each grcup.

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Fig I test ond control implonts havebeen ploced info fresh extraction sock-ets: typical dehiscence-type defect.

Fig 2 Buccol view of o titanium mem-brone placed aver the defect.

Fig 3 Ciinioal view ot M weeks, beforereentry surgery. Note the exposure oftitanium membrone ond the caverscrews ot the oontroi site

Fig 4 Ah e-PtFE membrane has beensecured to the test site: the control sitewos hot augmented

fig 5 Clinicol measurements ore takenwith POP 15 periadontat probes.

Fig 6 Implont cover sorews secure thee-PTFE membrohes.

Fig 7 Flap clasure is achieved with theuse of e-PTFE sutures.

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Fig 8 (left) At reentry surgery, on e-PTFE membrane tiaO becomeexposed

Fig 9 (right) Clinicol measurements aretoken during the reentry surgery.

Fig W A site that was augmented withtitanium membrane lost bone whencompared to baseline.

Fig 11 Raúiagraphic appearancebefare surgical reentry.

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Table 1 Clinical and histological measurements (mm) for controlsites that received titanium and o-PTFE membranes

Variable

OontrolVCPREVHPOSTDIFV-CH

Titanium

VCPREVHPOSTDiFV-CH

e-PTFE

VCPREVHPOSTDIFV-CH

444

ó66

óÓó

Mean

7,54.72,9

6,8ó.O0,8

6,74.52,1

Standarddeviat ion

G.ó0,90.8

0,81.31,7

0.82.92.4

.005*

•Stotistically significont difference by poited Student's f test.VCPRE = Verticoi ciinical pretfeatment.' VHPOST _ verticoi histoicgic pretreotment;DiFV-CiH - difference between clinicai pietreotment and tiistciogio pcsttreotment.

Results

At 3 weeks postoperativeiy, aiiof the titanium membranes andhalf of fhe e-PTFE membraneswere siightly exposed. For thecontrol sites, three out of fourcover screws were siighfiyexpased. At oii other sites heal-ing was uneventful. At 6 weeks,on additional e-PTFE membranebecame exposed. No titaniumor e-PTFE membranes were lostduring the study. At 14 weeks,macroscopic signs of inflamma-tion were present around ail ex-posed membranes. During sur-gicol reentry the titanium and

exposed e-PTFE membraneswere easily removed, Nanex-posed e-PTFE membranes weretightly adapted to the underly-ing bone. Sites where mem-branes were exposed had aioose type of connective tissuecovering the impiant threads.Ail implants were clinicaiiyImmobiie. Changes in bcneheight were taken after re-moval of all of the granulationtissue. Table 1 presents the ciini-cai and histoiogic measure-ments, Statisticaiiy, all groupswere compared and no statisti-oally significant differenceswere cbserved between ciini-

cal and histoiogic posttreat-ment measurement (P< .05),

The average gain in boneheight for e-PTFE sites was 2,1mm. The gain was 0,8 mm fortitanium membrane sites and2.9 mm far control sites. Themean initial and final defectdepths for the three treatmentgroups can be seen in Fig 12,The initial defect depth for thethree treatment groups wassimiiar, with no signifioant differ-ences between the groups. At14 weeks, the sites that re-ceived the titanium membraneswere not significantiy differentfrom baseline. At 14 weeks thecantroi and e-PTFE sites weresignificantly different from base-line (P < ,05), Chonges in mid-buccai bone ievel for the treot-ment groups can be seen in Fig13, For the three treatmentgroups, there was a widerange of variability in the bonelevéis. There were siight gains inbone levels for the four controisites. These gains ranged from 2to 3 mm. The six sites thatreceived fitonium membranesbecame expased during the14-week evaluation period.Four out of the six e-PTFE sitesalso beoome expased duringthe healing period. The great-est gain in bone ievels wasseen in two sites that receivede-PTFE membranes and re-mained cavered for the entireevaiuation intervai (5.3 and 4,6mm).

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Fig 12 tyieon bane levels (mm) for testand control sites öfter implont place-ment ond at 14 weeks.

Fig 13 Changes in midbucool banelevel (mm).

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Fig 14 Hisfoiagic section affhe fesfsitewifh e-PTFE membrane ih situ. Newbone con be seen aver previouslyexposed implant threads.

Fig Í5 Hisfoiogic section afaneexposed e-PTFE site. Nate the amaunfof exposed imptonf fhreads.

Fig 16 Histology of titanium test site.Nate exposed implant threads.

Histoiogic findings for onenonexposed e-PTFE test sitecan be seen in Fig 14. On thebuccal aspect the distancebetween the impiant rim to thefirst bone contact is 1.4 mm.Lingually, bone covers neariythe entire implant surface.Figure 15 shows a histologiesection of an exposed e-PTFEfest sife. The bone Ievei is accnsiderabie disfonce from theimplant rim. Figure lo shows atitanium test site, Crestal résorp-tion is evident on the buccaiand the iingual aspects of theimplant.

Discussion

The purpose of this sfudy wasto expiore the possibiiity of GTRoround exposed implonfthreads in fresh extractiansockets. Titanium membranesand e-PTFE augmentat ionmaterials were tested on bea-gle dogs. These materials actas mechanicai barriers, isolat-ing the exposed impiantthreads from the gingival con-nective tissue and the epithe-lial cells.

In this study, bone regener-atian in the titanium test sites

was not statistically differenfwhen compared wifh baseiine,in the e-PTFE fest sites theamount ot bone gain wasdirectly related to membroneexposure. When the mucosolseal was maintained, ciinicailysignificant bone regenerationwas a consistent finding, butno significant bone gain wasobserved in sites with exposedmembranes.

The findings in this study aresimiiar to these reported byather authors. Dahiin et ai''^inserted 30 impiants in tibiae ot15 robbits, A varying number of

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impiant threads were exposedin the test and controi sites. Testsites were covered by a poroustefion membrane that isaiotedthe implant from the surround-ing connective tissue. Theperiosteum was sutured overthe membranes. The animalswere divided into three groupsond were kiiled at 6, 9, and 15weeks. For the test sites newbone formation was significant-iy higher (mean of 3.8 mm)when compared with the con-trols (mean of 2.2 mm). Thisconsistent bane regenerationcon be expiained by the com-plete soft tissue coverage ofthese two e-PTFE sites. Becker etol'^ studied bone formation atdehisced implant sites treatedwith e-PTFE membranes in bea-gle dogs. Bone loss wasobserved araund an impiantossociated with eariy mem-brone exposure. In this study,the average gain in baneheight was 1.37 mm for test sitesversus 0.23 mm for controis.

Preliminary findings werereported by Caudili et ai^^ onthe histologie onaiysis ofendosseous impiants that werepiaced in simuiated extractionsockets in three dogs. After 12weei<s. hydroxyapatite-coafedimpiants were inserted into sim-uiated extraction sockets. Hoifof the impiants received over-lay e-PTFE augmentation mate-rioi. and 12 sites served asunougmented controis. In twodogs, primary ciosure wasmointained throughout the

study and healing wasuneventful. In these animalsthe augmented implantsappeared to be fiiied with newbone, whiie controi sites oftenexhibited crestai résorption, inthe third dog, primary ciosurewas not maintained. The con-sistency of the underlying tissuefrom these sites was hémorrag-ie and resembied pooriy differ-entioted granulation tissue.

The results from these stud-iesi4.i7.32 hove presented pre-liminary evidence that prema-ture membrane exposure moybe related to the quantity ofbone regeneration. The resultsfrom our studies tend to sup-port fhe previousiy mentionedstudies. These studies reportedthat membrane exposureaffects new bone formotion, afinding thof is also ossociatedwith bone loss. In this study it isinteresting to note that primaryclasure couid not to be iTiain-tained over the titanium mem-branes and four of the e-PTFFmembranes. Large areas ofmembrane exposure with boneioss was observed in most oftitanium test sites. This couidpossibly be explained by fhestiffness of fhese membranesand by the insufficient voscularsupply due to the nonporoustitanium foil. It would be inter-esting to test fhe principie ofGTR using different titaniummembranes v /ith various poresizes.

Our study cleariy demon-strated that premature expo-

sure of titanium membranesresuits in bone ioss when com-pared to the initial examina-tion. On the other hand, in thetwo sites where e-PTFE mem-branes remained unexposed,the amount of bone regenero-tion was clinicaliy significont.The results of this study demon-strate the importance of main-taining soft tissue coverageover membranes that havebeen used to cover dentaiimpiants.

Within the iimits of thisstudy, ciinicai and histoiogicevidence demonstrated thotwhen primary coverage ismointained, membranes cansignificantiy enhance boneimplants. When early exposureof e-PTFE membranes occurredno significont bone growth wosobserved. The use of titaniummembranes did not enhancebone formation around thetreated sites.

Acknowledgments

The outhors wish to thank Drs ObradZelic, Bozidor Dimitrievic, and PetarKos an o vie for their help with this study.We acknowledge Dr A. Hruska whohelped to provide the titenium foils. Inaddition, we ore gratetui to WL Goreond Associates for their support.Titanium implants were kindly suppliedby Implant Innovotions. A specialther^ks is addressed to Dr WilliamBecker for his help in the preparation afthis manuscript.

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The Internatlonol Jaurnol of Periodontics & Restarative Dentistry