Giacomo Favero Daniele Botticelli Giovanni Favero a Brismayda Garc Tomaso Mainetti Niklaus P.

Lang

Alveolar bony crest preservation at implants installed immediately after tooth extraction: an experimental study in the dog

Authors afliations: Giacomo Favero, Giovanni Favero, Brismayda a, Tomaso Mainetti, Faculty of Dentistry, Garc University of Medical Science, Habana, Cuba, Daniele Botticelli, Faculdade de Odontologia de Arac atuba, UNESP - Universidade Estadual Paulista, Sao Paulo, Brazil Daniele Botticelli, Ariminum Odontologica, Oral Surgery Division, ARDEC, Rimini, Italy Daniele Botticelli, Niklaus P. Lang, Prince Philip Dental Hospital, The University of Hong Kong, Hong Kong, China Correspondence author: Dott. Daniele Botticelli lio De Mesquita Universidade Estadual Paulista Ju Filho Campus de Arac atuba Tel.: +55 02118 3636-3209 Fax: 55 02118 3636-3340 e-mail: daniele.botticelli@ardec.it

Key words: animal study, bone healing, collagen membrane, deproteinized bovine bone

mineral,

extraction

socket,

immediate

implants,

implant

dentistry,

osseointegration,

regeneration, ridge preservation, type I installation

Abstract Aim: To evaluate the inuence of deproteinized bovine bone mineral in conjunction with a collagen membrane, at implants installed into sockets in a lingual position immediately after tooth extraction, and presenting initial horizontal residual buccal defects <2 mm. Material and methods: The pulp tissue of the mesial roots of 4P4 was removed in six Labrador dogs, and the root canals were lled with gutta-percha and cement. Flaps were elevated, and the buccal and lingual alveolar bony plates were exposed. The premolars were hemi-sectioned, and the distal roots were removed. Implants were installed in a lingual position and with the margin ush with the buccal bony crest. After installation, defects resulted at about 1.7 mm in width at the buccal aspects, both at the test and control sites. Only in the left site (test), deproteinized bovine bone mineral (DBBM) particles were placed into the defect concomitantly with the placement of a collagen membrane. A non-submerged healing was allowed. Results: After 3 months of healing, one implant was found not integrated and was excluded from the analysis together with the contralateral control implant. All remaining implants were integrated into mature bone. The bony crest was located at the same level of the implant shoulder, both at the test and control sites. At the buccal aspect, the most coronal bone-to-implant contact was located at a similar distance from the implant margin at the test (1.7 1.0 mm) and control (1.6 0.8 mm) sites, respectively. Only small residual DBBM particles were found at the test sites. Conclusion: The placement of an implant in a lingual position into a socket immediately after tooth extraction may favor a low exposure of the buccal implant surface. The use of DBBM particles, concomitantly with a collagen membrane, did not additionally improve the outcome obtained at the control sites.

Date: Accepted 2 October 2011

To cite this article: a B, Mainetti T, Lang Favero G, Botticelli D, Favero G, Garc NP. Alveolar bony crest preservation at implants installed immediately after tooth extraction.: an experimental study in the dog. Clin. Oral Impl. Res. 24, 2013, 712 doi: 10.1111/j.1600-0501.2011.02365.x

The placement of an implant into an alveolus immediately after the extraction has been reported with favorable outcomes (Quirynen et al. 2007; Botticelli et al. 2008; Chen & Buser 2009). It has, however, been demonstrated in a series of clinical (Botticelli et al. 2004; Sanz et al. 2010) as well as experimen jo et al. 2005; Botticelli tal studies (e.g. Arau et al. 2006; Caneva et al. 2010c) that implant installation does not prevent the physiologic resorption of the buccal alveolar bony crest. Several studies tried to limit the resorption of the buccal bony plate mainly by lling or protecting the void that often occurs between the inside of the bony wall of the extraction

socket and the implant surface after installation. In an experiment in dogs (Caneva et al. 2010d), for instance, a wider implant was used to ll the defect, and was compared with a control site, where an implant of reduced diameter was placed into the extraction socket. It was shown that a larger amount of vertical bony crest resorption occurred at the wider implant site. Moreover, ller materials or/and membranes have been used both in clinical (e.g. Lang et al. 1994, 2007; Wilson et al. 1998; Cornelini et al. 2004; Chen et al. 2007) and in experimental studies (Caneva et al. 2010b, 2011a, 2011b; jo et al. 2011). A lower buccal bony Arau

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Favero et al Ridge preservation at immediate implants

crestal resorption at the augmented sites was reported. In particular, in an experimental study in jo et al. 2011), deproteinized dogs (Arau bovine bone mineral (DBBM) collagen was used to ll 12 mm wide buccal defects at immediate implant sites. After 6 months of healing, the buccal bony wall was thicker, and the most coronal bone-to-implant contact located closer to the implant reference at the grafted compared with the control sites. In another study in dogs, where a similar experimental design was adopted (Caneva et al. 2011a), a more limited contribution in preventing resorption was obtained with the use of DBBM particles. The difference in the outcomes may be partly explained by the difference in the width of the buccal defects that were 12 mm in the former and 0.6 mm in the latter study. In fact, in previously published clinical studies (Wilson et al. 1998; Lang et al. 2007), it was suggested to use DBBM to ll defects when the size of the residual defect was at least of 11.5 mm. At immediate implants, the size of the buccal defects and the width of the buccal bone, i.e. both the distance of the buccal surface of the implant from the outer contour of the alveolar bony crest, have been demonstrated to strongly inuence the outcomes regarding the buccal contours (Caneva et al. 2010c, 2010d, 2012; Ferrus et al. 2010; Tomasi et al. 2010). Bone regeneration at standardized buccal defects, close to 2 mm in horizontal dimension, has not been studied sufciently as yet. Hence, the aim of the present study was to evaluate the inuence of deproteinized bovine bone mineral (DBBM), in conjunction with a collagen membrane, at implants installed in a lingual position into sockets immediately after tooth extraction, and presenting initial horizontal residual buccal defects up to 2 mm.

maintained with inhalation with Isourano (Baxter Hospitalar Ltd., Sao Paulo, Brazil) during the surgery. The animals were kept with an intravenous infusion of sterile saline during the procedure. Before surgical treatment, the pulp tissue of the mesial roots of 4P4 was removed, and the root canals lled with gutta-percha and root canal cement (Mtwo, Endopocket, Epll; Sweden & Martina, Due Carrare, Padova, Italy). The crowns were subsequently restored with composite resin (Adonis; Sweden & Martina, Due Carrare, Padova, Italy) . Full thickness aps were elevated in the right side of the mandible, and the buccal and lingual alveolar bony plates were exposed. The forth premolar was hemi-sectioned and the distal root removed, including the corresponding portion of the crown. The buccolingual and mesio-distal dimensions at the coronal margin were measured using calipers (Castroviejo; KLS Martin Group, Umkirch, Germany). The depth of the extraction socket was measured using an UNC 15 probe (HuFriedy, Chigaco, IL, USA), used with the tip of the probe pointed to the apex of the alveolus and inclined toward either the buccal or the lingual aspects. The width of the buccal and lingual bony walls was measured at a 1 and 3 mm distance from the alveolar bony crest using Iwanson calipers (KLS Martin Group, Umkirch, Germany). Recipient sites were subsequently prepared, and a titanium implant with a TiUnite surface (Nobel Biocare Holding AG, Kloten, Switzerland), was

used. A Mark III implant, 11.5 mm long and 3.3 mm wide, was installed into the distal alveolus. The implant was lingually positioned into the alveolus (Fig. 1a), with the margin of the implant placed ush to the alveolar buccal bony crest (Fig. 1b). After implant installation, buccal horizontal defects ranging between 1.5 and 2.0 mm (1.7 0.3 mm) were obtained (Fig. 1c). A healing abutment was afxed to the implant, and the aps were mobilized and sutured to allow a non-submerged healing using interrupted Vicryl 4-0 sutures (Johnson & John dos Campos, Brazil). The same son, Sa o Jose surgical procedures and measurements were performed in the left side of the mandible. A buccal defect of dimensions (1.7 0.3 mm), similar to the contralateral site was obtained. However, deproteinized bovine bone mineral (DBBM) particles with a size of 0.251.0 mm (Bio-Oss;Geistlich Biomaterials, Wolhusen, LU, Switzerland) were placed to ll the remaining defect around the marginal portion of the implant (Fig. 1d). A collagen membrane (Bio-Gide; Geistlich Biomaterials, Wolhusen, LU, Switzerland) was adapted at the buccal aspect around the neck of the implant to cover the experimental region, extending 34 mm beyond the border of the bony defect. The aps were subsequently sutured to allow a non-submerged healing. After the surgeries, the animals were given antibiotics for 10 days (Stomorgyl 10; one tablet/10 Kg daily Merial Saude Animal Ltd., Paulinia, Brazil); anti-inammatory

(a)

(b)

Material and methods

The research protocol was submitted to and approved by the local Ethical Committee for Animal Research (University of the State of Sa o Paolo, Brazil).

(c)

(d)

Clinical procedures

Six Labrador dogs (each approximately 26.5 kg and with a mean age of 1 year) were used. During surgical procedures, the animals were pre-anaesthetized with Acepran 0.2% 0.05 mg/Kg (Univet-vetnil, Sa o Paulo, Brazil), sedated with Zoletil 10 mg/Kg (Virbac, Jurubatuba Santo-Amaro, Sa o Paulo, Brazil), and

Fig. 1. Positioning of the implant at the fourth premolar. (a) Distal extraction socket of the fourth premolar. (b) Implant positioned with the shoulder ush to the buccal bony crest. (c) Occlusal view of the implant, placed in a lingual position. A gap was obtained buccally, similar in dimension at the test and control sites (1.7 0.3 mm). (d) DBBM particles placed to ll the defect.

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drugs for 5 days (Maxicam 2.0 mg, one tablet/20 Kg daily Ouro Fino Saude Animal Ltd., Cravinhos, Brazil), and analgesic for 3 days (Tramal 50 mg, 4.0 mg/Kg subcutaneous, every 8 h Unia o Quimica Farmaceutica Nacional S/A, Pouso Alegre, Brazil). The animals were kept in kennels and on concrete runs at the universitys eld laboratory with free access to water and feed of moistened balanced dogs chow. A daily inspection of the wounds for clinical signs of complications and healing abutment cleaning was performed. The animals were euthanized 3 months after the surgery by applying an overdose of Thiopental (Cristalia Ltd., Campinas, Brazil).
Histologic preparation

about 1 mm, between IS and the apical termination of the implant. Thus, a lattice was superposed over this area.
Data analysis

Mean values and standard deviations as well as 25th, 50th (median), and 75th percentiles were calculated for each outcome variable. The primary variables were IS-C and IS-B. Differences between test and control sites were analyzed using Wilcoxon signed ranks test with PASW Statistics 18 (SPSS Inc. Chicago IL, USA). The level of signicance was set at a = 0.05.

Results
The coronal diameter and depth of extraction sockets as well as the width of the buccal and lingual bony walls at 1 and 3 mm from the alveolar crest are reported in Table 1. After 3 months of healing, all implants were still in situ. During histologic processing, however, one control implant appeared not to be integrated, and consequently, was excluded from the analysis together with the contralateral test implant. Neither artifacts occurred, nor were there any tissue blocks destroyed. Hence, test and control sites yielded an n = 5. All implants evaluated were well integrated into mature mineralized bone (Fig. 3). The alveolar bony crest was located about at the level of the implant shoulder both at the test and control sites (0.1 1.7 and 0.0 1.1 mm, respectively; Table 2). The most coronal bone-to-implant contact (IS-B) presented similar values both at the test and control sites (buccally, 1.7 1.0 and 1.6 0.8 mm, respectively; Table 2). No statistically signicant differences were found for any of the variables analyzed. Remaining buccal and lingual defects of similar depth and 0.60.8 mm in width, were present at both the test and the control sites. The bone located around the implants appeared to be slightly more mineralized at the control than at the test sites (Table 3).

Individual blocks containing the implant and the surrounding soft and hard tissues were xed in 4% formaldehyde solution followed by dehydration in a series of graded alcohol solutions, and nally embedded in resin (LR White hard grade; London Resin Company Ltd, Berkshire, UK). The blocks were cut in a bucco-lingual plane using a diamond band saw tted in a precision slicing machine (Exakt; Apparatebau, Norderstedt, Germany) and then, reduced to a thickness of about 50 lm using a cuttinggrinding device (Exakt; Apparatebau). The histologic slides were stained with toluidine blue and examined under a standard light microscope for histometric analysis.
Histologic evaluation

Fig. 2. Diagram illustrating the landmarks for the histologic evaluation. In red: IS, shoulder of the implant; B, most coronal bone-to-implant contact; C, top of the adjacent bony crest. In green: S, implant surface at the top of the threads; OC, outer contour of the bony tissue at the alveolar crest. The width of the alveolar bony crest was measured (yellow arrows) from S to OC at the IS level (0 mm) and then, apically to it, at each subsequent mm, up to 5 mm (S-OC05).

In a Nikon Eclipse 50i microscope (Nikon Corporation, Tokio, Japan) at a magnication of 9100, the following landmarks were identied (Fig. 2). The shoulder of the implant (IS), the most coronal bone-to-implant contact (B); the top of the adjacent bony crest (C); the implant surface at the buccal aspect at the top of the threads (S); and the outer contour of the alveolar bony crest (OC). The following measurements were performed: (i) the vertical distance, parallel to the longitudinal axis of the implant, between (ii) IS and C (IS-C), IS and B (IS-B), and (iii) the distance between the implant surface (S) and C (S-C). The width of the alveolar bony crest was measured from S to OC (SOC0-5) at the IS level (level 0) and then, apically to it, at each subsequent mm, up to 5 mm (Fig. 2). The density of mineralized bone, non-mineralized tissue, and DBBM particles were determined in a buccal area from the implant surface to a parallel line at a distance of
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However, this difference was not statistically signicant. Only a small amount of DBBM particles was found (4.7 3.2%) at the test sites, partly included into mineralized bone (Fig. 4a, b) or embedded into connective tissue (Fig. 5a, b). The mean values of the thickness of the buccal bone (SOC05), both at the test and control sites after 3 months of healing are reported in Fig. 6. There were no statistically signicant differences between any of the test and control values.

Discussion
The present experiment evaluated the inuence of deproteinized bovine bone mineral (DBBM) particles covered by a collagen membrane on the healing of implants installed in

Table 1. Coronal diameter and depth of extraction sockets and width of the buccal and lingual bone walls at 1 and 3 mm from the alveolar crest. n = 5. Data in millimeters
Coronal diameter m-d PREMOLARS Test Control 5.0 (0.5) 4.9 (0.4) b-l 5.4 (0.4) 5.3 (0.4) Depth b 13.0 (1.4) 12.8 (0.6) l 14.1 (1.3) 13.9 (0.7) Width at 1 mm b 1.1 (0.3) 1.0 (0.3) l 1.5 (0.5) 1.5 (0.5) Width at 3 mm b 1.6 (0.4) 1.4 (0.3) l 2.8 (0.7) 2.7 (0.5)

Mean values and standard deviations (SD) in millimeters. m-d, mesial-distal; b-l, buccal-lingual; b, buccal; l, lingual.

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(a)

(b)

Table 2. Histologic measurements after 3 months of healing at premolar sites. n = 5. Data in millimeters
IS-C b Test Mean and SD Percentiles 25th; 50th; 75th Control Mean and SD Percentiles 25th; 50th; 75th 0.1 (1.7) 1.0; 0.8; 0.3 0.0 (1.1) 0.3; 0.6; 0.7 0.5 (1.2) 1.1; 0.8; 0.0 0.8 (1.7) 1.9; 0.2; 0.3 1.7 (1.0) 0.7; 1.5; 2.7 1.6 (0.8) 1.2; 1.5; 2.0 1.3 (0.4) 0.9; 1.5; 1.6 1.3 (0.3) 1.1; 1.4; 1.5 l IS-B b l

b, buccal; l, lingual; IS, implant shoulder; C, top of the alveolar bony crest; Cbt, top of the most coronal peak of the bulk tissue; B, most coronal bone-to-implant contact; SD, standard deviation. Mean values, SD and 25th, 50th (median), and 75th percentiles. P < 0.05 between control and test.

Table 3. Morphometric measurements after 3 months of healing. Percentage (%) of mineralized tissue, non-mineralized tissue, and DBBM particles around the implants
Bone
Fig. 3. Ground sections representing the results of healing after 3 months from implant installation. (a) Test site. (b) Control site. Toluidine blue stain; original magnication 912.

Bio-oss 4.7 (3.2) 2.6; 5.0; 7.4 0.0 0.0

Non-mineralized 45.6 (9.3) 42.8; 43.5; 44.8 38.2 (16.5) 27.4; 30.0; 41.6

a lingual position into the sockets immediately after tooth extraction. Apparently, no vertical bone resorption was observed both at the test and control sites, as an average width of 1.0 mm of buccal bone was present. However, positive outcomes of DBBM used to ll the residual buccal marginal defects have emerged in several clinical (Cornelini et al. 2004; Chen jo et al. 2007) and experimental studies (Arau et al. 2011; Caneva et al. 2011a, 2011b). In the present experiment, however, the contribution of DBBM was minimal, most probably because of an adequate dimension of 1.0 mm of alveolar buccal bone. Hence, similar outcomes were also observed at the control sites, where no bone augmentation was performed. This outcome may also be explained by the healing pattern of the alveolar crest after tooth extraction. It has been shown that, after tooth extraction, the buccal side of the alveolar process resorbed more extensively than that of the lingual side (e.g. Pietrokov jo & Lindhe 2005). ski & Massler 1967; Arau jo & In an experimental study in dogs (Arau Lindhe 2005), the coronal part of the alveolus was closed by a bridge of mineralized tissue that connected the lingual and the buccal walls after 8 weeks following tooth extraction. The buccal bony crest wall was located 2 mm below the lingual bony crest leaving the bridge of mineralized tissue in an oblique orientation. Moreover, the lingual site was located more coronally compared with the buccal site. A similar pattern of healing may be expected in an alveolus, into which an implant was installed immediately after

Test Mean and SD Percentiles 25th; 50th; 75th Control Mean and SD Percentiles 25th; 50th; 75th

49.7 (11.3) 49.9; 50.2; 56.1 61.8 (16.5) 58.4; 70.0; 72.6

b, buccal; l, lingual; SD, standard deviation. Mean values, SD and 25th, 50th (median), and 75th percentiles. P < 0.05 between control and test.

(a)

(b)

Fig. 4. Ground section of the buccal aspect of a test site. Toluidine blue stain. (a) original magnication 920; (b) larger magnication (original 940) of the microphotograph in a). Particles of DBBM were found in most specimens, however, in small quantity. The particles were partly (yellow arrow) or completely (red arrow) embedded into mature bone.

tooth extraction despite the possible interferences produced by the presence of that implant. Indeed, a higher position of the lingual bony compared with the buccal crest have been reported frequently after healing (e.g. Botticelli et al. 2006; Caneva et al. 2010a, 2010d). This difference was explained by the higher resorption of the buccal compared with the lingual walls owing to the fact that the buccal bony plate was constituted of bundle bone to a higher degree than the lin jo & Lindhe 2005). gual plate (Arau In the present study, the implants were placed in a lingual position in relation to the center axis of the alveolus. This, in turn,

means that the implant outline will have a greater probability to fall within the skeletal envelope and hence, will be covered by alveolar bone to a greater extent than if the implant is placed in the center of the alveolus. The lingual positioning of the implant can be obtained either by a bodily displacement and/or a slight angulation of the implant inclined toward the lingual bony plate (Fig. 7). These assumptions are substantiated using a multivariate multilevel analysis (Tomasi et al. 2010) on data reported in a multicenter randomized clinical study (Sanz et al. 2010) on implants installed into sockets immediately after tooth extraction. It
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(a)

(b)

Fig. 5. Ground section of the buccal aspect of a test site. Toluidine blue stain. (a) original magnication 920; (b) larger magnication (940) of the microphotograph in a). Particles of DBBM were found sometimes not integrated into the bone.

Fig. 6. Graphics representing the mean values of the width of the alveolar bony crest measured after 3 months of healing from S to OC at the IS level (level 0) and then, apically to it, at each subsequent millimeters, up to 5 mm.

was concluded that the more the implant was placed lingually, the less the buccal surface of the implant was exposed after 4 months of healing. This conclusion is also supported by the results from an experiment in dogs (Caneva et al. 2010c). In that study, implants were installed in the distal sockets of the third mandibular premolars in dogs immediately after tooth extraction. In one side, the implant was installed in the center of the alveolus (control) and on the contralateral side, the implant was placed 0.8 mm lingually and 0.8 mm deeper (test). No regenerative procedures were performed for augmentation. After 4 months of healing, the results were superior at the test compared with the control sites, even if the different depths to which the implants were installed were taken into account. Despite the position of the implants in the test sites, however, some exposure of the buccal surface of the implant was observed (0.6 mm). On the contrary, the bony crest was located at the level of the implant margin in the present experiment. Even though the marginal width of the buccal wall was similar in the present study, the buccal defect was larger (1.7 mm) compared with the previ 2011 John Wiley & Sons A/S

ously reported study (1.3 mm). This increased the distance from the implant surface to the outer contour of the alveolar bony crest and allowed the installment of the implant more closely into the skeletal envelope of mineral jo & ized tissue previously described (Arau Lindhe 2005). These ndings also corroborate the results of two experimental studies in dogs (Caneva et al. 2010d, 2012). In both these studies, the distal sockets of the fourth premolars were used for immediate implant installation. In one side, cylindrical implants with a reduced diameter compared with the respective sockets were installed, whereas, in the contralateral side, larger and conical implants were used. At the reduced diameter implant sites, a circumferential gap of about 1 mm was obtained in both studies, whereas, in the contralateral sites, gaps were virtually absent. A lower exposure of the buccal surface of the implant was observed at the cylindrical com-

pared with the conical sites. It was concluded that, when the implant surface was closer to the bony crest, a higher exposure of the buccal implant surface has to be expected. In the current study, teeth were maintained adjacent to the experimental sites, a fact that may have contributed to a better preservation of the bony walls of the sockets (Botticelli et al. 2006, 2008; Favero et al. 2012). In a recent experimental study in dogs (Favero et al. 2012), it was shown that a lower resorption of the alveolar bony crest has to be expected if teeth are present adjacent to an implant installed into extraction sockets immediately after tooth extraction compared with sites without neighboring teeth. In the present study, no improvements of the healing of the hard tissues were observed between test and control sites. This is not in agreement with other studies of similar nat jo et al. 2011; Caneva et al. 2011a, ure (Arau 2011b), in which advantages were found after the use of DBBM and collagen membranes. It has to be understood, however, that, in the present experiment, there was a low chance for the biomaterial to improve the already favorable outcomes obtained at the control sites, where no DBBM and membrane were used. This may be attributable to a buccal bony plate of approximately 1.0 mm and to the large distance between the implant surface and the outer contour of the buccal alveolar bony crest. Furthermore, the results from the present study are in disagreement with another experimental study (Hsu et al. 2010). In that experiment, the fourth premolars of dogs were extracted in one side of the mandible,

Fig. 7. Schematic representation of implants (rectangles in gray) installed into extraction sockets (prole delimited by dark blue lines). The blue dotted lines represent the hypothetic healing slope of the bony crest after 4 month of healing. The red dotted lines represent the projection of the buccal bony wall on the implant shoulder. (a) and (c) Implant installed into the center of the alveolus, with the shoulder ush with the buccal margin of the bony crest. (b) Implant installed more lingually using a bodily displacement. No difference between the two situations is expected in depth of the implant in relation to the lingual bony crest. (d) Implant lingually angulated of 4, using the apex as fulcrum. The implant will result to be positioned slightly deeper in relation to the lingual bony crest compared with the implant in (c), due to the rotation of the projection of 4. The situation illustrated in b and d has more chances to obtain less buccal exposure of the implant surface compared with the situation illustrated in (a) and (c) B, buccal aspect; L, Lingual aspect.

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and an implant was placed in the center of the inter-radicular septum. The remaining defect and the adjacent alveoli were lled with DBBM particles. After 4 months of healing, a micro-CT analysis revealed a mean loss of the buccal bony crest of 4.7 mm. It should be emphasized, however, that at the buccal aspect, a little remaining defect may be expected after implant installation into the septum. Only a small amount of biomaterial was therefore placed at the buccal aspect below the bony crestal level, whereas the majority of the DBBM particles lled the mesial and distal alveoli of the premolars. This fact may have minimized the possible effect of the biomaterial.

In conclusion, within the limits of the present study, due to the small number of implants (n = 5), it was shown that the placement of an implant in a lingual position into a socket immediately after tooth extraction may favor a low exposure of the buccal implant surface. However, most likely owing to the presence of a buccal bony width of 1.0 mm, the use of DBBM particles, concomitantly with a collagen membrane, did not additionally improve the optimal outcome obtained at the control site.

Acknowledgements: This study has been supported by ARDEC, Ariminum

Odontologica SRL, Rimini, Italy. Implants and components were provided by (Nobel Biocare Holding AG, Kloten, Switzerland). DBBM particles and collagen membranes have been kindly provided by Geistlich Biomaterials AG, Wolhusen LU, Switzerland. The competent contributions of Prof. Luiz Antonio Salata and Mr. Sebastia o Bianco (USP Faculty of Dentistry of Ribeira o Preto University of Sa o Paulo, Sa o Paulo, Brazil) in the histologic processing are highly appreciated. All the authors declare to have no conict of interest with the materials used in the present study.

References
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