immediateimplantsatfresh extractionsockets:bonehealing ... · the distal socket of three p3 and...

Immediate implants at freshextraction sockets: bone healingin four different implant systems

de Sanctis M, Vignoletti F, Discepoli N, Zucchelli G, Sanz M. Immediate implants atfresh extraction sockets: bone healing in four different implant systems. J ClinPeriodontol 2009; 36: 705–711. doi: 10.1111/j.1600-051X.2009.01427.x.

AbstractObjectives: To describe the differences in bone healing, when placing four differentimplant systems in fresh extraction sockets.Material and Methods: Eight beagle dogs received implants randomly installed intothe distal socket of three P3 and four P4. Four-implant systems were evaluated. Eachanimal provided four test implant sites. All animals were sacrificed at 6 weeks afterimplant placement, providing specimens for histo-morphometric analysis of bone toimplant contact (BIC), bone area, new bone formation, as well as histometricmeasurements of the ridge alterations.Results: No statistically significant difference was observed among the four-implantsystems. The mean BIC % ranged between 58.5% and 72.1%. Bone modelling of thebuccal plate was marked and amounted approximately to 2.5mm, independently of thesystem used.Conclusion: This study failed to demonstrate differences in the healing pattern after 6weeks when placing four different implant systems in fresh extraction sockets. In spiteof achieving predictable osteointegration with the four implants studied, theoccurrence of buccal bone resorption may limit the use of this surgical approach.

Key words: buccal crest; fresh extractionsocket; implant surface; immediate implants;osteointegration

Accepted for publication 5 April 2009

In recent years, immediate implant place-ment after tooth extraction has become acommon clinical therapeutic approach,alternative to a staged surgical protocol.The reduction in the number of surgeriesneeded and the advantage of a shortertime to rehabilitate function and aes-thetic has provided an impetus to studieson this surgical approach.

Clinical studies have demonstrated thatthe survival rates for implants placedimmediately, early, delayed or late seemto be similar in short-term follow-ups andrange between 93% and 100%. Schropp

et al. (2003) compared, in 46 patients, thebone healing and crestal bone changesfollowing immediate versus delayed pla-cement of titanium dental implants. In theimmediate group, implants were placed10 days after tooth extraction, while in thedelayed group the placement of theimplant was carried out 3 months afterextraction. The survival rates at the end ofthe study were 91% in the immediategroup and 96% in the delayed group.Covani et al. (2004) reported the resultsfrom a clinical study on 35 implants; 20were placed immediately after toothremoval and 15 were placed between 4and 6 weeks after the extraction. Allimplants were submerged, achieving pri-mary flap closure. At re-entry both groupshealed similarly, achieving a similar bonefill at the coronal portion of the implants(Covani et al. 2004, Ganeles &Wismeijer2004). Ganeles & Wismeijer (2004) pub-

lished a review of the available literatureon this surgical protocol assessing itsoutcome under different loading protocolsand different clinical indications (singletooth versus multiple teeth; bone quality,implants stability, etc.). Combined datafor 1.046 implants yielded a survival rateof 98.2%. Most of the clinical studieshave reported implant survival data wellabove 95%, thus demonstrating clinicaloutcomes similar to the delayed place-ment surgical protocol (Ganeles & Wis-meijer 2004). Few studies have, however,studied the impact of this surgicalapproach on the bone crest in contactwith the implant. Cornelini et al. (2005),in a prospective case series of 22 implantswith a 12-month follow-up, reported amean bone resorption of 0.5mm at 12months. Similarly, Covani et al. (2007)assessed 20 implants positioned in freshextraction sockets resulting at 1 year in

Massimo de Sanctis1, FabioVignoletti2, Nicola Discepoli2,Giovanni Zucchelli3 and MarianoSanz4

1Dipartimento di Scienze, Universita deglistidi di Siena, Odontostomatologiche,Siena,Italy; 2Universidad Complutense of Madrid,Periondotology, Madrid, Spain; 3University ofBologna, Periondotology, Bologna, Italy; and4Faculty of Odontology, UniversidadComplutense of Madrid, Madrid, Spain

Conflict of interest and source offunding statement

The authors declare that there are no con-flict of interests in this study.This study was partially sponsored by aresearch grant from Thommen Medicals.

J Clin Periodontol 2009; 36: 705–711 doi: 10.1111/j.1600-051X.2009.01427.x

705r 2009 John Wiley & Sons A/S

the absence of peri-implant defects andwith a vertical distance between theimplant shoulder and bone crest rangingbetween 0 and 2mm.

Experimental animal studies evaluat-ing this surgical protocol have alsodemonstrated that implants show a simi-lar degree of osseointegration comparedwith delayed inserted implants (Anner-oth et al. 1985, Barzilay et al. 1991,1996a, b, Karabuda et al. 1999). Parrand colleagues studied, in dogs, thebone healing around immediatelyplaced titanium implants in both themandible and the maxilla. At 5 months,the bone to implant contact (BIC) was60.3% in the mandible and 46.3% inthe maxilla. Barzilay et al. (1996a, b)compared the healing of immediateversus delayed implants in monkeys.The differences between both groupsfor BIC were not significant, with BICvalues of 63.97% for the delayedimplants and 56.82% for the immedi-ately placed implants. Karabuda et al.(1999) have investigated the impact ofdifferent implant surfaces, by compar-ing the healing of hydroxyapatite-coatedand titanium plasma-sprayed root-formimplants placed immediately after toothextraction in dogs. At 8 weeks, themean BIC for HA-coated implantswas 61.84%, while the correspondingvalue for the titanium plasma-sprayedimplants was 51.35%.

Consequently, the purpose of thisanimal experiment was to determinewhether the rate and extent of osseoin-tegration is influenced when implantswith different contacting surfaces anddifferent designs are placed in animmediate implant placement surgicalprotocol. Furthermore, the secondaryobjective is to evaluate the influencethat this may have on the modelling ofthe buccal plate.

Material and Methods

This animal experiment was designed asa prospective, randomized controlled,evaluator-blinded study, carried out onadult beagle dogs with a weight rangingbetween 10 and 20 kg.

Study implants

Four-implant systems were evaluated:3i (Biomet 3i, Palm Beach Gdns, Fl,USA, USA) Osseotite Certain straightØ3.25mm/l5 8.5, 11.0mm; Astra (AstraTech, Molndal, Sweden) MicroThreadt-

OsseoSpeedt Ø3.5mm/l5 9.0, 11mm;Thommen (Thommen Medical AG, Wal-denburg, Switzerland) SPI ELEMENTs

Ø3.5mm/l59.5mm; Straumann (Strau-mann AG, Basel, Switzerland) ITI stan-dard plus Ø3.3mm/l5 8, 12mm (Fig.1a–d). All the implants used werecommercially available. Thommen andStraumann implants presented a coronalpolished collar of 1 and 1.8mm, respec-tively.

This experimental animal study wascarried out at the Experimental SurgicalCentre of the Hospital ‘‘Gomez-Ulla’’in Madrid, Spain, once the RegionalEthics Committee for Animal Researchapproved the study protocol.

Eight animals were selected that ful-filled the inclusion criteria. Each animalprovided four-test implant sites. Allanimals were sacrificed 6 weeks afterimplant placement.

Surgical procedure

Animals were sedated and placed undergeneral anaesthesia, using mechanicalrespiration throughout the entire sur-

gery. Induction of sedation wasachieved using propofol. General anaes-thesia was achieved using isofluoranegas, delivered via an endotracheal tube,at concentrations of 0.7–1.5%, achiev-ing a respiratory rate of approximately12 breaths/min. The surgical protocolwas described in detail by Vignolettiet al. (2009). Briefly, once the animalswere anaesthetized, intrasulcular inci-sions were performed and full-thicknessflaps were reflected in order to achieveaccess to the alveolar crest, with care toreduce bone exposition to the minimum.The third and fourth pre-molars werethen extracted with minimal traumaaiming to preserve the walls of thesockets. The distal socket of each two-rooted pre-molar was chosen as theimplant-recipient site. The mesial sock-ets were allowed to fill with blood andheal without intervention.

Implants were then randomized bymeans of scratch-off cards supplied foreach study animal number. The fourimplants were randomly assigned tothe distal sockets of P3 and P4, oneach side of the mandible. The osteo-

Fig. 1. Four implant systems were tested. (a) Thommen 3.5 SPI ELEMENTs. (b) Straumann3.3 ITI Standard. (c) Astra 3.5 Micro Threads OsseoSpeeds. (d) 3i Osseotites MiniplantCertain straight.

Fig. 2. Implant placement. (a) Note the supracrestal position of 1.8mm polished collar of theStraumann implant (black arrow). (b) Note the supracrestal position of 1mm polished collarof the Thommen implant (yellow arrow).

706 de Sanctis et al.

r 2009 John Wiley & Sons A/S

tomies for inserting the different implantsystems were performed according tothe specific implant recommended sur-gical protocols. Hence, only originalinstruments specifically designed andrecommended by the manufacturerswere utilized. These osteotomies were

drilled into the sockets to ensure that theimplant seating platform was placed atthe level of the marginal portion of thebuccal plate for 3i and Astra implant,while Thommen and Straumann im-plants were inserted to a depth thatplaced the coronal margin of the rough

surface at the level of the bone crest andthe polished collars above the alveolarcrest as suggested by the manufacturers(Fig. 2a and b). The depth of the osteot-omy was based on the amount of avail-able bone, with care not to engage thedental nerve or to cause a fenestration.Once the implants were inserted, heal-ing abutments were secured and theflaps were repositioned and suturedwith 4-0 vicryl resorbable sutures.

Post-surgical care

Plaque control was provided using achlorhexidine solution sprayed on allmandibular tooth sites on a 3 days/week regimen. No effort was made touse any abrasive instrument for hygiene.All study implant sites were inspec-ted before the hygienic treatment toevaluate the health of the peri-implantmucosa and document any signs ofinflammation.

Biopsies

Animals were sacrificed with an over-dose of sodium pentothal and perfusedwith a fixative solution (Karnovsky1965) through the carotid arteries. Themandibles were freed from theirattached tissues and cut into halves bymeans of a section between the centralincisors. Each half mandible was placedinto a sealable sample container. Thesample containers were placed in asecure area at the proper temperature(51C) from the time of collection untilthey were shipped for histological pro-cessing.

Histological processing and analysis

The obtained biopsies were processedfor ground sectioning according to themethods described by (Donath & Breu-ner 1982). The blocks were cut in abucco–lingual plane using a cutting–grinding unit (Exakts, Apparatebau,Norderstedt, Germany). From eachimplant site, one central section wasprepared and further reduced to a finalthickness of about 20 mm by microgrinding and polishing using a micro-grinding unit (Exakts). The sectionswere then stained using the Levai Lacz-ko staining method.

Histometric analysis

The degree of osseointegration wasevaluated by linear measurements of

Fig. 3. Ground section representing implant and surrounding tissues. (a) The thin buccalbone crest (Bc) is levelled with the most apical level of the straight polished 1mm collar (p)of the implant. Levai Laczko staining. Original magnification ! 5. (b) Higher magnificationaf (a). Note the woven bone (dark stained areas, WB) in intimate contact with the implantsurface (I) and continuous with the parent bone (PB). (Thommen SPI ELEMENTs implant).Levai Laczko staining. Original magnification ! 10. (c, d). The bone crest (Bc) is observedat different levels apical of the implant shoulder (I). No residual vertical defect is present atthe buccal crest (c). (3i Osseotite Certain straight implant). Levai Laczko staining. Originalmagnification ! 5. I–a, implant–abutment interface.

Immediate implants at fresh extraction sockets 707


the percentage of ‘‘bone to implantcontact’’ (BIC%) assessing the entirelength of the implant surface in directcontact with mineralized bone from thecoronal margin of the rough surface.

Ridge alterations

For assessing the relationship betweenthe alveolar crest and the implant, thefollowing landmarks were identified ineach section and used for linear mea-surements:

I, implant shoulder;Bc, marginal level of the bone crest;B, marginal level of BIC.

The vertical distances between theselandmarks were measured using a direc-tion parallel to the long axis of theimplants.

Histo-morphometric analysis

Newly formed bone area

Measurement of the percentage of new-ly formed bone that occupied the threadarea of each implant.

Total bone area

Measurement of the total hard tissuecomponent that occupied the threadarea of each implant.

Statistical analysis

A one-way analysis of variance test wasused to evaluate the differences amongthe implants used for each independentvariable. A Bonferroni post hoc test waschosen to evaluate the differencesamong implant systems.

ResultsHistological observations

The histological outcomes were similarfor the four-implant systems studied.A marked bone loss was observed atthe buccal aspect of the four-implantsystems. The resorption of the buccalplate ranged between 0.5 and 5mm.The mean position of the marginalbone crest was approximately 2.5mmapical of the shoulder of the implant(Figs 3 and 4).

A gap of various dimensions fre-quently occurred between the socket

walls and the implant surface at thetime of installation. Buccally, this mar-ginal gap healed 6 weeks after implantplacement as a result of a combinedbone resorption and new bone forma-tion. Three different histological out-comes were identified: (i) no marginalgap was present and woven bone wasobserved up to the marginal bone crest,(ii) the most coronal BIC was locatedapical of the bone crest, resulting in aresidual marginal gap of varying dimen-sions and (iii) occasionally newlyformed bone was observed coronal tothe bone crest margin (Figs 3–5).

Remnants of bundle bone were some-times observed in the inner part of thesocket wall. In such cases woven bonewas observed continuous with the bun-dle bone. New bone formation waspronounced, both in intimate contactwith the implant surface and with themature lamellar bone from the bone bed.On some occasions, the newly formedbone was observed on the outer part ofthe bone crest. Extensive areas of boneremodelling were observed both in theparent bone and in the new bone(Fig. 6).

Histometric findings

BIC%

The results for the degree of osseointe-gration achieved by the differentimplant systems at 6 weeks are depictedin Table 1. BIC% presented a highvariability. Values ranged from 39.84%to 78.63% for the 3i implants, from35.78% to 76.58% for the Astra Techimplants, from 58.14% to 83.40% forthe Straumann implants and from50.13% to 86.88% for the Thommenimplants. The mean BIC values were58.5% (11.8), 60.2% (12.2), 72.1% (9.7)and 68.5% (11.5) for 3i, Astra Tech,Straumann and Thommen fixtures,respectively. Although there was a ten-dency towards higher BIC percentagesaround Straumann and Thommen fix-tures, these differences were not statis-tically significant.

Ridge alterations

Histometric results demonstrated that at6 weeks a marked bone remodelling ofthe crest occurred after implant place-ment. Measurements of vertical buccalbone resorption (I–Bc) were performedfrom the coronal edge of the roughsurface, because the machined collars

Fig. 4. Ground section representing implant and surrounding tissues. (a) The buccal bonecrest is slightly apical of the implant–abutment interface. Levai Laczko staining. Originalmagnification ! 2.5. (b) Higher magnification of (a). A residual vertical defect is present atthe buccal crest. Note the woven bone (dark stained areas, WB) at the inner and at the outerpart of the socket wall (Astra MicroThreads-OssesSpeeds implant). Levai Laczko staining.Original magnification ! 5. I, implant surface. PB, parent bone. I–a, implant–abutmentinterface.



of Thommen and Strauman implantswere positioned coronal to the crest ofbone. Measurement demonstrated 2.54(1.39) and 2.95 (1.79)mm of bone lossfor 3i and Straumann implants, respec-tively. Astra Tech and Thommenimplants demonstrated a lower resorp-tion of the buccal bone, averaging 2.06(1.63) and 2.02 (1.27)mm, respectively.These differences, however, were notstatistically significant (Table 2). Themost coronal BIC (B) was identified atvarious positions apical to the implantshoulder (I–B distance). On the buccalside, it was located at approximately3mm, for 3i and Straumann implantsand 2mm for Astra Tech and Thommen.These differences, however, were notstatistically significant. On the lingualside, differences were statistically sig-nificant only between Straumann andAstra Tech implants (Table 2).

The distance Bc–B is representativeof the infra-bony component around theimplant. At the buccal aspect almost noresidual defect was present in allimplants. At the lingual side, a residualgap was more common. In Thommenand Straumann implants, this defectaveraged between 1 and 1.5mm, whilealmost no defect was observed at AstraTech and 3i implants. Still, these differ-ences were not statistically significant.

New bone formation

Results from this outcome variable thatexpresses the percentage of new miner-alized tissue fraction in a selected area(inside the thread) are shown in Table 3.Astra Tech implants showed the highestvalues of new bone formation, aver-aging 54.08% (21.45) of newly formedbone inside the thread 6 weeks afterimplant placement. The results for theother three systems were similar, aver-aging approximately 49% of new miner-alized tissue inside the thread. Thedifferences among the implant systemswere not statistically significant.

Bone area

Results from this histomorphometricoutcome variable that expresses thepercentage of total mineralized tissuefraction inside the thread are shown inTable 3. This percentage was similar inthe four-implant systems, with meanpercentages of 77.68 (12.53), 71.60(16.02), 61.60 (9.78) and 74.49 (13.74)for 3i, Astra Tech, Straumann andThommen implants, respectively.

Fig. 5. Ground section representing implant and surrounding tissues. (a) Woven bone (darkstained areas, WB) is interposed between the implant surface (I) and the socket wall.(Straumann ITI standard implant). Levai Laczko staining. Original magnification ! 5. (b)Detail of (a). Note the woven bone coronal to the marginal bone crest (Bc). Levai Laczkostaining. Original magnification ! 10. I, implant surface; PB, parent bone.

Fig. 6. Ground section representing implant and surrounding tissues. (a) Lingual bone crest(Bc) comprised of parent bone (PB), bundle bone (BB) and woven bone (WB). (I) Implantsurface. Levai Laczko staining. Original magnification ! 5 (Astra MicroThreads

OsseoSpeeds implant). (b) Woven bone continuous with the bundle bone. Levai Laczkostaining. Original magnification ! 10. I, implant surface. PB, parent bone; WB, woven bone(Thommen SPI ELEMENTs implant).



Discussion

The main purpose of this study was tocompare the healing of four differentimplant systems when placed experi-mentally using a specific surgical proto-col (immediate placement in freshextraction sockets). From the four-implant systems tested, Astra Tech, 3iand Thommen were cylindrical-shapedtwo-piece implant designs, althoughthe latter presented a 1mm machinedcollar. Straumann was a cylindrical-shaped one-piece design with a 1.8mmmachined collar.

We used the achieved percentage ofbone to implant contact (BIC%) at 6

weeks as the main outcome variable.For Thommen and Straumann implants,this percentage was close to 70%, whilefor Astra and 3i the achieved meanpercentages were 60.2% and 58.5%,respectively (Fig. 7). These differences,however, were not statistically signifi-cant. These results are consistent withthose reported by Schultes & Gaggl(2001), who reported BIC values of76% after a healing period of 8 monthsusing the same surgical protocol. Simi-lar results, with BIC values around 50%at 2 months and 54% at 4 months werealso reported by Botticelli et al. (2006)in an experimental study in dogs.

The histomorphometric analysis alsoshowed similar results for the four-implant systems studied. In the hardtissues, the percentage of newly formedbone within the thread amounted toapproximately 50% and the total areaof hard-tissue component around theimplants filled between 61% and 77%of the thread area.

The alveolar ridge around the fourtypes of implants showed markedresorption, with a mean bone loss of2.5mm observed at the buccal aspect ofthe crest, indicating that differentimplant surfaces and different geome-tries did not influence the process ofbone remodelling that occurs in thesocket after tooth extraction. These find-ings are in agreement with the observa-tions reported by Araujo et al. (2005) inexperimental beagle dog studies. Theseauthors reported that the level of thebuccal crest was located 2.6 " 0.4mmapical to the most coronal level of thesand-blasted and acid-etched, coated,surface implants. However, a recentsimilar experimental study in the beagledog using the same surgical approachreported significant less vertical resorp-tion of the buccal bone plate, with amean bone loss of 0.63 (0.27)mm 8weeks after the immediate placementof 3.25mm diameter implants (Vigno-letti et al. accepted for publication).Similar results were also reported inanother experimental study in dogs,comparing flap versus flapless surgerywhen placing 3.3mm diameter implants.At 3 months of healing, the verticalbone resorption at the buccal plate was1.33 and 0.8mm in the flapped andthe flapless group, respectively (Blancoet al. 2008). These marked differencesare probably dependent on differentfactors, such as the implant diameter,the width of the alveolar crest and thedimensions of the marginal gap, whichhighlights the importance of being cau-tious while using this surgical protocol.

In conclusion, this comparative ani-mal experimental study has demon-strated that 6 weeks after immediateimplant placement, different implantdesigns and implant surfaces do notsignificantly influence bone healing atfresh extraction sockets.

Acknowledgement

We highly appreciate Prof. FernandoMunoz for his collaboration in the his-tological processing of this material.

Table 1. Results from histometric measurements describing bone to implant contact (BIC) perdog

Dog 3i Astra Tech Straumann Thommen

1 48.20 53.13 68.53 66.482 39.84 62.12 77.47 86.883 54.52 68.14 58.14 68.744 78.63 55.88 82.52 69.495 58.23 64.43 58.83 64.606 60.38 65.64 83.40 81.487 68.42 76.58 76.59 50.138 59.97 35.78 71.41 60.64Total N 8 8 8 8Mean 58.52 60.21 72.11 68.55Minimum 39.84 35.78 58.14 50.13Maximum 78.63 76.58 83.40 86.88Standard deviation 11.82922 12.23288 9.77941 11.50059

Table 2. Results from mean (SD) histomor-phometric measurements reporting the percen-tages of new bone area (NB) and total bonearea (TB) in the thread.

Implant % NB (SD) % TB (SD)

3i 49.01 (19.48) 77.68 (12.53)Astra Tech 54.08 (21.45) 71.60 (16.02)Thommen 49.91 (12.83) 61.60 (9.78)Straumann 49.49 (18.53) 74.49 (13.74)

Table 3. Results from mean (SD) histometric measurements (mm) reporting the distancebetween the various landmarks

Implant I–B buccal I–B lingual I–Bc buccal I–Bc lingual Bc–B buccal Bc–B lingual

3i 3.09 (1.52) 1.9 (0.39) 2.54 (1.39) 1.09 (0.48) 0.29 (0.39) 0.57 (0.87)Astra 2 (0.48) n0.75 (0.36) 2.06 (1.63) 0.68 (0.32) # 0.05 (1.54) 0.08 (0.45)Thommen 1.98 (0.48) 1.61 (1.08) 2.02 (1.27) 0.72 (0.67) 0.09 (0.98) 1.13 (1.30)Straumann 3.18 (1.46) n2.53 (1.08) 2.95 (1.79) 0.75 (1.67) 0.46 (0.55) 1.50 (1.27)

npo0.05.I, implant shoulder (for Straumann and Thommen implant: coronal limit of the treated surface);

B, most coronal contact between the implant surface and bone; Bc, marginal portion of the bone crest.

Fig. 7. Histograms depicting bone toimplant contact (BIC) percentages.



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Address:F. VignolettiFacultad de OdontologıaPlaza Ramon y Cajal s/nMadrid28040 SpainE-mail: [email protected]

Clinical Relevance

Scientific rationale for the study:Immediate implant placement aftertooth extraction is a common surgi-cal protocol in clinical practice.Limited information is available,however, on the possible influencethat different implant designs andsurface modifications may have onthe healing processes and on the finaloutcome of this surgical protocol.It is, therefore, relevant to study

whether using different implantswould influence the healing outcomewhen using this surgical approach.Principal findings: The results fromthe histological outcomes failed todemonstrate significant differencesamong the implant systems studiedafter 6 weeks of healing. The histo-metric measurement of BIC did notreveal any statistically significantdifference. A marked resorption of

the buccal plate was observed inde-pendent of the implant system used.Practical implications: The place-ment of a dental implant immediatelyupon tooth extraction results afterhealing in 2.5mm of mean resorptionof the buccal plate. This finding hasclinical implications that shouldmake the clinician aware of the lim-itations of this surgical protocol,mainly in areas of aesthetic concern.



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