Histologic Evaluation of 2 Human Immediately Loaded and 1 Submerged Titanium Implants Inserted in the Posterior Mandible and Retrieved After 6 Months

HISTOLOGIC EVALUATION OF 2 HUMANIMMEDIATELY LOADED AND 1 SUBMERGEDTITANIUM IMPLANTS INSERTED IN THEPOSTERIOR MANDIBLE AND RETRIEVED AFTER6 MONTHSRESEARCHMarco Degidi, MD, DDSGiovanna Petrone, DDS, PhDGiovanna Iezzi, DDSAdriano Piattelli, MD, DDSKEY WORDSDental implantsHistologyImmediate loadingMarco Degidi, MD, DDS, is a visitingprofessor; Giovanna Petrone, DDS, PhD, andGiovanna Iezzi, DDS, are research fellows;and Adriano Piattelli, MD, DDS, is aprofessor of Oral Medicine and Pathology, aswell as dean and director of Studies andResearch, at the Dental School of theUniversity of Chieti in Chieti, Italy. Addresscorrespondence to Dr Piattelli, Via F. Sciucchi63, 66100, Chieti, Italy (e-mail:[email protected]).Immediate loading can be successfully used in implant dentistry. Many factors arethought to be of importance in obtaining mineralized tissues at the interface. Onesuch factor is the implant surface characteristics. The authors retrieved, after a 6-month loading period, 2 immediately loaded implants and 1 submerged implant,each of which had been inserted in posterior mandibles. Histology showed that, inboth immediately loaded implants, mineralized tissue was present at the interface,and the bone-implant contact percentage was about 65% to 70%. No gaps, fibroustissue, or inflammatory infiltrates were present at the interfaces. In the submerged(control) implant, the bone-implant contact percentage was much lower (about 35%).Our results showed that immediate loading of dental implants, even in the posteriorregions of the jaw bones, hadn't caused untoward effects on the formation ofmineralized tissues at the interface, producing, on the contrary, a higher bone-implantcontact percentage than in the control implant, and thus, immediate loading can bea possible alternative procedure in implant dentistry.INTRODUCTIONstress-free healing periodwas thought to be a prerequisitefor successfulosseointegration and forthe presence of a mineralizedtissue interfacearound dental implants.1,2 A functionalrest of 3 to 4 months in the mandibleand 6 months in the maxilla wasthought to be necessary, and it was believedthat an early loading of dentalimplants could produce a fibrous-tissueencapsulation.3-5 More recently,several clinical and histological reportshave appeared in the literature, showingthat, in man and experimental animals,immediate loading shows promisingclinical results.6-46 Moreover, theJournal of Oral Implantology 223HISTOLOGIC EVALUATIONnecessity for not loading the implantswas empirically based and not experimentallyascertained.12 The classic2-stage protocol is associated with longtreatment time and high treatmentcosts, and elimination of the healingperiod offers advantages in terms ofcost of treatment and convenience topatients,36 and avoiding the need forcomplete dentures while undergoingimplant therapy can be a distinct advantage.44 Complete dentures may createfunctional and psychological problems.43 It has been reported that, withimmediately loaded implants, patientsresumed function quickly and thatmasticatory function was uniformlyjudged to be superior to pretreatmenttime.25 Any reduction in the number ofthe surgical procedures necessary or adecrease in the healing period is certainlyvery well welcomed by cliniciansand patients.45 Chow et al35 reported a1-year follow-up with a 98.3% overallimplant survival rate in 115 immediatelyloaded implants. In Buchs et al36series, the implant survival rate was93.7%. In the Chiapasco et al series,43the cumulative success rate of immediatelyloaded implants supportingmandibular overdentures was 97.5%after 2 years of functional loading.Randow et al10 found that Branemarkimplants can be successfully used inthe interforaminal mandibular areaeven when immediately loaded; moreover,they reported that bone resorptionis similar to that observed around2-stage implants. No failures were reportedby Ericsson et al31 in early loadedimplants and all implants wereworking successfully after 5 years. Branemarket al30 recently reported on amethod for implant therapy of theedentulous mandible; in 50 patients,followed 6 months to 3 years, therewas an overall survival rate of 98% anda prosthetic survival rate of 98%. Jaffinet al27 reported an overall survival rateof 95%, while in a series by Ganeles etal,25 the clinical success rate at the timeof final abutment placement was99.4%. In a Gatti et al29 series, the successrate was 96%. Grunder44 reported224 Vol. XXIX/No. Five/2003an overall success rate of 92.31%. Anotherimportant factor is the characteristicsof the implant surfaces. Occlusalforcetransmission schemes differ anda simple transposition of healing patternsfrom animal to man is not warrantedand should be avoided,12,28 andmoreover, it cannot be assumed apriori that immediately loaded implantswill have identical bone healingand bone-implant interfaces.32 In theposterior areas of the jaws, and especiallyin the maxillae, several demandingpreconditions require consideringinsufficient bone volume, poor bonequality, and high functional forces.40Glauser et al40 believe that the posteriormaxilla should be considered as a riskarea. The aim of the present study wasan evaluation of the peri-implant tissues,in man in 2 immediately loadedimplants and 1 submerged implant insertedin the posterior mandible andretrieved after 6 months.MATERIALS AND METHODSTwo patients participated in this study.One patient was a 53-year-old female,while the other was a 45-year-old male.The protocol was approved by the EthicsCommittee of our University, andboth patients gave their written informedconsent. In the first patient, 8XiVE implants (Friadent, Mannheim,Germany) were inserted in the edentulousmandible (Figures 1 and 2). Itwas planned to remove the most distalimplants (mandibular left 2nd molarregion and mandibular right 2nd molarregion) with a 5-mm trephine aftera 6-month loading period. Both implantswere 3.8- 3 9.5-mm implants.The last drill used for both implantshad a diameter of 3.8 mm and the insertiontorque had been 35 N. A fullarchimmediate provisional prosthesiswas placed and all the implants wereloaded on the same day as the surgery(Figures 3 through 5). The postoperativeperiod was uneventful. Before retrieval,both implants appeared to havebecome clinically osseointegrated,there was no mobility, and periapicalradiographs showed that, in 1 implant,no bone resorption was radiographicallyapparent, while in the other implant,1 to 2 mm of vertical bone resorptionwas visible (Figure 6). Theprovisional temporary crowns wereseparated from the provisional bridgeand the underlying implants were retrieved(Figure 7).In the second patient, an edentulousmandible was rehabilitated with 8XiVE implants, 7 of which were usedfor an immediately loaded provisionalrestoration, while 1 implant was leftsubmerged. This was an 3.8- 3 9.5-mmimplant and had been inserted in theleft mandibular 2nd molar region. Thelast drill used had a diameter of 3.8mm and the insertion torque had been35 N. After a 6-month healing period,this implant was retrieved.Processing of specimensThe implants and the surrounding tissueswere fixed by immediate immersionin 10% buffered formalin and processedto obtain thin ground sectionswith the Precise 1 Automated System(Assing, Rome, Italy).47 The specimenswere dehydrated in an ascending seriesof alcohol rinses and embedded in a glycolmethacrylateresin (Technovit 7200VLC; Kulzer, Wehrheim, Germany). Afterpolymerization, the specimens weresectioned longitudinally along the majoraxis of the implants with a high-precisiondiamond disk at about 150 mm andground down to about 30 mm. Threeslides were obtained for each implant.The slides were stained with acid fuchsinand toluidine blue. A double stainingwas done with von Kossa's and acidfuchsin to evaluate the degree of bonemineralization, and after polishing, 1slide per implant was immersed inAgNO3 for 30 minutes and exposed tosunlight; the slides were then washedunder tap water, dried, immersed in basicfuchsin for 5 minutes, and thenwashed and mounted.HistomorphometryHistomorphometry of bone-implantcontact percentage was done using alight microscope (Laborlux S; Leitz,Marco Degidi et alFIGURES 1-7. FIGURE 1. Postoperative panoramic radiography; 8 implants have been inserted in the mandible for an immediate temporaryrestoration. FIGURE 2. Postoperative view of the implants inserted in the mandible. FIGURE 3. The immediate restoration (frontal view).FIGURE 4. The immediate restoration (occlusal view). FIGURE 5. Periapical X ray (immediately postoperatively). Radiopaque cement is inclose contact with the bone. FIGURE 6. Periapical X ray (6 months later). A crestal bone of about 2 mm is visible. FIGURE 7. One of theretrieved implants.Journal of Oral Implantology 225HISTOLOGIC EVALUATIONFIGURES 8-15. FIGURE 8. Implant 1 (immediately loaded implant at 6 months). There is bone (B) around the entire perimeter of the implant(toluidine blue and acid fuchsin, original magnification 320). FIGURE 9. Implant 1 (immediately loaded implant at 6 months). The newlyformed bone (B) is in close contact with the implant threads (arrows; toluidine blue and acid fuchsin, original magnification 350). FIGURE10. Implant 1 (immediately loaded implant at 6 months). There are no gaps and no fibrous tissue at the implant-bone interface (arrows).At higher magnification, it is possible to observe newly formed bone in contact with the implant surface (B; toluidine blue and acidfuchsin, original magnification 3100). FIGURE 11. Implant 1 (immediately loaded implant at 6 months). The bone around the implantpresents wide marrow spaces (MS; toluidine blue and acid fuchsin, original magnification 350). FIGURE 12. Implant 2 (immediately loadedimplant at 6 months). This implant shows newly formed bone (B) all around its perimeter (toluidine blue and acid fuchsin, originalmagnification 320). FIGURE 13. Implant 2 (immediately loaded implant at 6 months). At higher magnification, a very intimate contactbetween implant and bone can be observed. No gaps are present at the interface (arrows; toluidine blue and acid fuchsin, originalmagnification 350). FIGURE 14. Control submerged implant (6 months). The bone-implant contact percentage is lower than in the immediatelyloaded implants (toluidine blue and acid fuchsin, original magnification 320). FIGURE 15. Control submerged implant (6months).The bone is not in direct contact with the implant surface (arrows; toluidine blue and acid fuchsin, original magnification 350).Wetzlar, Germany) connected to ahigh-resolution video camera (3CCD,JVC KY-F55B) and interfaced to a monitorand personal computer (Intel PentiumIII 1200 MMX). This optical systemwas associated with a digitizingpad (Matrix Vision GmbH) and a histometrysoftware package with imagecapturingcapabilities (Image-Pro Plus226 Vol. XXIX/No. Five/20034.5; Media Cybernetics Inc., Immaginiand Computer Snc, Milano, Italy).RESULTSImplant 1 (immediately loaded)right 2nd mandibular molar regionAt low-power magnification, bone waspresent around the implant (Figure 8).At higher magnification, the bone presentedwide marrow spaces, with afew of these abutting on the implantsurface. In some areas, newly formedbone was present at the interface. Atthe level of the crestal bone, on 1 sideof the implant, there was no evidenceof vertical bone resorption, while onthe other hard, a 1.3-mm (60.2) crestalbone resorption was present. Resorptionsigns were present in the most coronalbone, while no resorption wasseen in the bone at the interface withthe implant. Newly formed bone tendedto grow down into the bottom ofthe threads of the implant (Figure 9).The bone-implant contact percentagewas 72% (62.9%). No gaps or fibroustissue were present at the interface, norwhere there any inflammatory cells(Figure 10), foreign body reaction, orepithelial downgrowth. Bone lamellaeparallel to the threads were found betweenthe threads: in the crestal andmiddle part of the implant, a higherdeposition of new bone was found.Implant 2 (immediately loaded)left2nd mandibular molar regionThe bone was more trabecular, with largemarrow spaces (Figure 11). The bone-implantcontact percentage was 61%(64.2%). A vertical bone resorption ofabout 2.3 mm (60.3) was present on bothsides of the implant. No inflammatorycells or fibrous gaps were present at theinterface (Figures 12 and 13). At the apicalportion of the implants, only a few verythin bone trabeculae covered the metalsurface of the implants.Implant 3 (submerged controlimplant)left 2nd mandibularmolar regionAt low-power magnification, it waspossible to observe that the bone-implantcontact percentage was lowerthan that observed around both loadedimplants (Figure 14): a value of 35.5%(63.9%) was recorded. No bone contactwas observed in a large portion ofthe implant perimeter (Figure 15).DISCUSSIONWhen immediately loaded implantsreach a state of osseointegration clinically,they have a long-term predictabilitysimilar to those of conventionallyloaded implants.25 Moreover, immediateloading shortens the total rehabilitationtime, with increasedpatient satisfaction and the avoidanceof delays in the final rehabilitation withthe accompanying difficulty of wearinga conventional denture during thehealing phase.29 Immediate loading hasbeen used in totally edentulous patientsin order to improve the patienttreatment acceptance and to increasetheir comfort, eliminating the need forremovable dentures in the healing period.46 Immediate loading has beenused mostly with implants inserted betweenthe mental foramina and supportingfixed prosthetic restorations intotally edentulous mandibles.40 Immediatelyloaded implants have also beenused to support successfully implantretainedoverdentures.40 In the anteriormandible, the bone quality is usuallysufficient to achieve primary stability.39The role of bone quality is importantfor successful implant placement,27 andmost of the implant failures tended tooccur in the posterior jaw quadrants.39Glauser et al40 reported a higher failurerate in implants inserted in posteriormaxilla and in implants inserted inbone quality 3 and 4. Thirty-four percentof the implants inserted in theposterior maxilla failed, comparedwith 9% of the other implants insertedin other portions of the jaws.40 Grunder44found that, in his series, all failedimplants were the most distal, andboth implants placed in bone quality 4failed, while 5 failures occurred inbone quality 3. A histologic evidence ofosseointegration is needed for each differentimplant surface,28 and this canbe obtained only by histologic analysisof immediately loaded implants retrievedfrom man.23 Only rarely, however,have human-retrieved immediatelyloaded implants been reported inthe literature.16,21-24,28,33Our histologic data show that osseointegrationcan be obtained in verydemanding situations, such as implantinsertion in the posterior jaws, and thatbone response was not disturbed bythe stresses transmitted at the interfaceunder these mechanical conditions andwas comparable with that foundaround conventional delayed-loadedimplants.41 Implant splinting decreasesthe amount of micromotion during theMarco Degidi et alhealing phase, giving to the implant ahigher tolerance to deleteriousmicromotion.Rigid splinting and minimal lateralforces are critical factors for success.25,43 Primary stability is a key factorin the success of immediately loadedimplants because a high primary stabilityhelps to resist micromotion, thatis, the relative movements between theimplant surface and surrounding boneduring functional loading.39,40 Glauseret al40 reported that primary implantstability is influenced by sufficient implantlength, insertion torque, andbone quality as well as bicortical anchorageand modified surgical techniques.Moreover, the intimacy of initialfit and the percentage of implantsurface in direct contact with bone in-fluences the capability to withstandfunctional loads in early healing situations.40 In our implants, we found thepresence of a crestal bone resorptionradiographically and histologically. Itmust be considered, however, thatSzmukler-Moncler et al12 have pointedout that the authors studying earlyloading did not evaluate the postloadingbone remodeling phase. The previouslyreported differences in boneresorption around early loaded andnonloaded implants must be viewed inlight of this remodeling and, probably,they do not necessarily need to be attributedto the early loading of the implants.12 It must also be pointed outthat, in one of the implants (Figures 5and 6), the margin of the crown wasprobably positioned in a too low position(this is shown by the presence ofthe radiopaque cement) and very nearto the bone. At last, also, the surfaceplays a relevant role in implant longtermsuccess, particularly in very demandingsituations like in immediateloading in posterior jaw regions, andthe roughened surface of the implantsdescribed in this report probably helpsto stabilize the initial blood clot andwound against the titanium surface,and that results in enhanced bone formationon the surface.48 Moreover, thissurface may stimulate cell differentiationof osteoblast-like cells, and theJournal of Oral Implantology 227HISTOLOGIC EVALUATIONlarger dimensions of roughness createdby the sandblasting may provide pocketsof bony ingrowth that may functionas a series of miniretentive grooves.48Striking is the fact that both loaded implantspresented a higher bone-implantcontact percentage than the submerged(control) implant. Our resultsare similar to those reported recentlyby Testori et al,49 who found a boneimplantcontact percentage of 38.9% insubmerged healing and of 64.2% in immediatelyloaded implants. These resultscould be explained by the factthat functional loading stimulatedbone apposition. Wolff formulated histheory according to the idea that thereis a direct link between mechanicalloading and bone formation; Wolff'slaw would imply that increased stressesact as a stimulus to new bone formationwhile reduced stress tends toproduce bone loss.50It must, however, be borne in mindthat the number of specimens that westudied is too small to draw definitiveconclusions on the influence of loading onthe peri-implant bone response.Additionalstudies, with a larger and significantnumber of implants, are certainly needed.ACKNOWLEDGMENTSThis work was partially supported bythe National Research Council (CNR),Rome, Italy, and by the Ministry of Education,University, and Research(MIUR), Rome, Italy.REFERENCES1. Adell R, Lekholm U, Rockler,Branemark PI. A 15 year study of osseointegratedimplants in the treatmentof the edentulous jaw. Int J OralSurg. 1981;10:387-416.2. 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