Giacomo Favero Niklaus P. Lang Piero Romanelli Fabio Pantani Marco Caneva Daniele Botticelli
Authors’ affiliations: Giacomo Favero, Daniele Botticelli, Faculty of Dentistry, University of Medical Science, La Habana, Cuba Niklaus P. Lang, Daniele Botticelli, The University of Hong Kong, Prince Philip Dental Hospital, Hong Kong, China Piero Romanelli, Private Practice, Bologna, Italy Fabio Pantani, Private Practice, San Marino, Repubblica di San Marino Marco Caneva, Daniele Botticelli, ARDEC, Ariminum Odontologica, Rimini, Italy Daniele Botticelli, Faculdade de Odontologia de Aracßatuba, UNESP - Universidade Estadual Paulista, S~ ao Paulo, Brasil Corresponding author: Dr. Daniele Botticelli Universidade Estadual Paulista “J ulio de Mesquita Filho” UNESP - Campus de Aracßatuba Rua Jose Bonif acio 1193 16015-050 Aracßatuba, (SP) Brasil Tel.: +55 02118 3636 3209 Fax: +55 02118 3636 3340 e-mail: [email protected]
A digital evaluation of alveolar ridge preservation at implants placed immediately into extraction sockets: an experimental study in the dog
Key words: animal study, bone healing, collagen membrane, deproteinized bovine bone min-
eral, extraction socket, immediate implants, implant dentistry, osseointegration, regeneration, ridge preservation, type I installation Abstract Objective: To compare with pristine sites bone resorption and soft tissue adaptation at implants placed immediately into extraction sockets (IPIES) in conjunction with deproteinized bovine bone mineral (DBBM) particles and a collagen membrane. Material and methods: The mesial root of the third premolar in the left side of the mandible was endodontically treated (Test). Flaps were elevated, the tooth hemi-sectioned, and the distal root removed to allow the immediate installation of an implant into the extraction socket in a lingual position. DBBM particles were placed into the defect and on the outer contour of the buccal bony ridge, concomitantly with the placement of a collagen membrane. A non-submerged healing was allowed. The premolar on the right side of the mandible was left in situ (control). Ground sections from the center of the implant as well as from the center of the distal root of the third premolar of the opposite side of the mandible were obtained. The histological image from the implant site was superimposed to that of the contralateral pristine distal alveolus, and dimensional variation evaluated for the hard tissue and the alveolar ridge. Results: After 3 months of healing, both histological and photographic evaluation revealed a reduction of hard and soft tissue dimensions. Conclusion: The contour augmentation performed with DBBM particles and a collagen membrane at the buccal aspects of implants placed IPIES was not able to maintain the tissue volume.
Date: Accepted 28 October 2013 To cite this article: Favero G, Lang NP, Romanelli P, Pantani F, Caneva M, Botticelli D. A digital evaluation of alveolar ridge preservation at implants placed immediately into extraction sockets. Clin. Oral Impl. Res. 00, 2013, 1–7 doi: 10.1111/clr.12307
After tooth extraction, the alveolar ridge undergoes resorption during the first 3–6 months of healing and reaches a mean horizontal reduction of 3.8 mm and mean vertical reduction of 1.2 mm (Tan et al. 2012). It has been shown that implants placed immediately into extraction sockets (IPIES) are unable to preserve the alveolar bony crest in its entire outline (Botticelli et al. 2004; Ara jo et al. 2005; Sicilia & Botticelli 2012; u Wang & Lang 2012). The positioning of the implant within the extraction socket has been demonstrated to be a determining factor of importance for the final location and volume of the alveolar bony crest (Caneva et al. 2010; Tomasi et al. 2010). The more lingual an implant is installed, the less supra-crestal exposure of the implant will occur. However, such implant placement will not preserve the alveolar bony ridge.
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However, it has been demonstrated that the use of bone substitutes for grafting the alveolus after extraction (Ara ujo et al. 2008; Lindhe et al. 2013) or to fill the remaining defects after immediate implant placement (Ara ujo et al. 2011; Caneva et al. 2011a,b, 2012) may contribute to the preservation of the alveolar ridge. The shrinkage of the alveolar ridge after tooth extraction (Fickl et al. 2008) as well as after IPIES (Caneva et al. 2012; Rossi et al. 2013) has recently been documented using a laser scan on cast models and a software to superpose images taken prior to therapy and after healing. A comparison between IPIES sites and pristine extraction alveoli has been reported (Ara ujo et al. 2005; Vignoletti et al. 2012). Other experimental studies have compared the histological images of grafted alveoli to untreated alveoli and to sites with pristine
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teeth (Ara ujo et al. 2008; Ara ujo & Lindhe 2009, 2011; Lindhe et al. 2013). In these studies, the positions of the apices and axes of the teeth were used as references on the images representing the treated and untreated sites and compared with each other. However, there is a lack of studies that compared IPIES sites with the contralateral pristine sites (teeth). Hence, the aim of this experiment was to compare with pristine sites bone resorption and soft tissue adaptation at implants placed IPIES in conjunction with deproteinized bovine bone mineral (DBBM) particles and a collagen membrane.
Material and methods The research protocol was submitted to and approved by the local Ethical Committee for Animal Research of the University of the State of S~ ao Paolo, Brazil. Clinical procedures
Six Labrador dogs (each approximately 26.5 kg and a mean age of 1 year) were used. During all surgical procedures, the animals were pre-anaesthetized with Acepranâ 0.2% (0.05 mg/kg – Univet-vetnil, S~ao Paulo, Brazil), sedated with Zoletilâ 10 mg/Kg (Virbac, Jurubatuba Santo-Amaro, Brazil), maintained with inhalation with Isofluranoâ (Baxter Hospitalar Ltd., Sao Paulo, Brazil) during the surgery. The animals were kept with an intravenous infusion of sterile saline during the procedures. Local anesthesia was also provided. The pulp tissue of the mesial root of the third premolar at the left side of the mandible (test sites) was removed, the root canal filled with gutta-percha and root canal cement (Mtwoâ, Endopocketâ, Epfillâ, Sweden & Martina, Due Carrare, Padova, Italy). The crown was hemisected, the distal root removed, and the crown restored with composite (Adonisâ, Sweden & Martina, Due Carrare, Padova, Italy). Bucco-lingual fullthickness flaps were elevated, and the buccal and lingual alveolar bony plates exposed. The bucco-lingual dimensions at the coronal margin were measured using calipers (Castroviejoâ; KLS Martin Group, Umkirch, Germany). A recipient site was prepared, and a titanium implant with a TiUniteâ surface (Nobel Biocare Holding AG, Kloten, Switzerland; Mark III Groovy implant, 11.5 mm long and 3.3 mm wide) was installed into the distal alveolus (Fig. 1a). The implants were placed lingually into the alveoli, with the margin of the implants being placed flush with the
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(a)
(b)
Fig. 1. Clinical view of some of the clinical procedures. (a) The implant was placed in a lingual position within the distal alveolus of the third premolar, in the left side of the mandible. A buccal defect about 1 mm wide and 3 mm deep occurred. (b) After the placement of a healing abutment, deproteinized bovine bone mineral particles were placed into the defect and on the buccal bony wall, and a membrane was positioned to cover the site.
alveolar buccal bony crest, and resulting in a buccal gap. The horizontal width (H-GAP; Fig. 1a) and the vertical depth (V-GAP) of the defect between the implant and the bony crest were measured at the buccal aspect using an UNC 15TM probe (Hu-Friedy, Chicago, IL, USA). The implant shoulder (IS) was always located in an apical position in relation to the lingual bony crest. The distance between the top of the bony crest (C-Clinical) and the IS was also measured at the lingual aspect using the same periodontal probe. A healing abutment was affixed to the implant, and DBBM particles (Bio-Ossâ, Granules 0.25–1 mm; Geistlich Biomaterials, Wolhusen, Switzerland) were placed to fill the remaining defect around the marginal portion of the implant and on the buccal bony wall. A collagen membrane (Bio-Gideâ; Geistlich Biomaterials) was adapted to the buccal aspect to cover the experimental region (Fig. 1b). The flaps were subsequently mobilized and sutured to allow a non-submerged healing using interrupted VicrylTM 4-0 sutures (Johnson & Johnson, S~ao Jose dos Campos, Brazil). The third premolar of the right side of the mandible (control sites) was left untreated. After the surgeries, the animals were given antibiotics for 10 days (Stomorgylâ 10, one tablet/10Kg daily – Merial Saude Animal Ltd., Paulinia, Brazil), anti-inflammatory drugs for 5 days (Maxicamâ 2.0 mg, one tablet/20Kg daily – Ouro Fino Saude Animal Ltd., Cravinhos, Brazil), and analgesic for 3 days (Tramalâ 50 mg, 4.0 mg/Kg subcutaneous, every 8 h – Uni~ao Quimica Farmaceutica Nacional S/A, Pouso Alegre, Brazil). The
animals were kept in kennels and on concrete runs at the university’s field 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 abutments cleaning were performed. The animals were euthanized 3 months after the surgery applying an overdose of Thiopentalâ (Cristalia Ltd., Campinas, Brazil). Histological preparation
Individual blocks containing the implant, at the left side, and the tooth, at the right side of the mandible, including the surrounding soft and hard tissues were fixed in 4% formaldehyde solution followed by dehydration in a series of graded alcohol solutions and finally embedded in resin (LR Whiteâ hard grade, London Resin Company Ltd, Berkshire, UK). The blocks were cut following the longitudinal axes in a bucco-lingual plane using a diamond band saw fitted in a precision slicing machine (Exaktâ, Apparatebau, Norderstedt, Germany). The cuts were performed in the center of the implant as well as in the center of the distal root of the third premolar. Subsequently, one slice was obtained from each hemi-blocks and then reduced to a thickness of about 50 lm using a cutting–grinding device (Exaktâ, Apparatebau). The slide representing the most central portion of the implants and teeth was selected from each block and used for histological evaluation. The histological slides were stained with toluidine blue and examined under a standard light microscope for histometric analysis.
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G. Favero et al Ridge preservation
Histological evaluation
In an Eclipse 50i microscope (Nikon Corporation, Tokyo, Japan) equipped with a video camera connected to a computer and using the software NIS-Elements v4.1 (Nikon Corporation), the following landmarks were identified at the test sites (Fig. 2): (IS) the shoulder of the implant, (C) the top of the adjacent bony crest, (Cbt) the most coronal part of the bulky hard tissue (bony crest or DBBM particles), and (B) the most coronal bone-to-implant contact. The following vertical measurements were performed at a magnification of 9100 between the corresponding landmarks: IS-C, IS-Cbt, and IS-B. Photographic evaluation
All histological slides were photographed, and test and control (pristine tooth) images were superimposed. The implants of the test images were positioned on the control images in such a way that the lingual implant surface was parallel to the lingual bony wall of the alveolus. The IS was placed flush to the buccal bony crest leaving a buccal defect
Fig. 2. Diagrams illustrating the landmarks for the histological evaluation. In red: IS, shoulder of the implant; B, most coronal bone-to-implant contact; C, top of the adjacent bony crest; Cbt, the most coronal part of the bulky tissue (bony crest or DBBM particles). DBBM, Deproteinized bovine bone mineral.
width similar to that obtained clinically at the test sites. The alignment was obtained by digital overlapping of the images with the software i-Dixel (J. Morita Mfg. Corp., Kyoto, Japan) according to the fixed landmarks. The measurements were made on a dedicated software (ImageJ 1.34s, Wayne Rasband, National Institute of Health, Bethesda, MD, USA) using unit pixels and converting them to millimeters, applying the implant size as reference for calibration. The following landmarks were identified at the buccal and lingual aspects of the implants/teeth sites (Fig. 3): the IS, the implant surface (S), the top of the periimplant mucosa (PM) and of the gingiva (G), and the bottom of the defect (D). Moreover, the outer contour of the alveolar bony ridge and of the mucosa, as well as the inner contour (IC) of the extraction socket/residual defect and of the mucosa and gingiva, was identified. The vertical distance PM-IS and G-IS was measured. The horizontal distances from S to the outer and inner contours of the hard tissue were measured at the IS level and then apically at each subsequent millimeter up to 4 mm. A similar evaluation was performed for the outer and inner contours of the mucosa at the IS level and then, at each subsequent millimeter, coronally up to 3 mm and apically up to 2 mm. Measurements and analyses were performed for the
Fig. 3. Diagrams illustrating the landmarks for the photographic evaluation. S, Implant surface, G, margin of the gingiva, PM, margin of the peri-implant mucosa, IS, shoulder of the implant; D, bottom of the defect after implant installation. The outer and inner contours of bony crest and mucosa as well as the position of PM, G, and D were measured at the photographic evaluation. Light blue, gingiva; dark blue, peri-implant mucosa; orange, buccal bony wall at tooth; red, buccal bony wall at implant.
© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
buccal aspects, while measurements at the lingual aspect were limited to the coronal regions. Data analysis
Mean values and standard deviations as well as 25th, 50th (median), and 75th percentiles were calculated for each outcome variable. Differences between test (implant) and control (tooth) sites were analyzed using Wilcoxon signed rank test. The level of significance was set at a = 0.05.
Results Clinical evaluations
Table 1 reports the clinical evaluations. The diameter of the extraction sockets was 4.7 0.5 mm, while the horizontal (H-GAP) and the vertical buccal defects (V-GAP) after implant installation were 1.2 0.3 mm and 3.1 1.3 mm, respectively. The IS was located apically in relation to the lingual bony crest by about 0.7 mm. After 3 months of healing, no implants were lost and no obvious signs of inflammation were detected at the time of sacrifice. Histological evaluations
No artifacts occurred during the histological preparation, nor were there any tissue blocks destroyed at the test and control sites. All implants appeared to be integrated into mature mineralized bone. The buccal alveolar bony crest at the test sites was resorbed by 1.7 1.1 mm (Fig. 4a, b; Table 2). At the lingual aspect, the top of the bony crest was located 0.5 0.7 mm apically to the IS. However, taking into account the initial position of the lingual bony crest, the absolute vertical resorption totally reached 1.2 0.5 mm (l-absolute). Deproteinized bovine bone mineral particles were rarely found integrated into newly formed bone. However, a substantial amount of particles included into connective tissue was found above the bony crest and on the outer buccal contour of the bony ridge, sometimes appearing to contribute to maintain coronally the peri-implant mucosal margin (Fig. 5a,b). The distance between IS and the most coronal peak of the hard tissue (bone or DBBM) was 1.1 1.7 mm (IS-Cbt), while the distance IS-B at the buccal aspect was 2.3 1.3 mm. Photographic evaluations
Test and control sites yielded an n = 6. A ground section representing the control sites is depicted in Fig. 6.
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Table 1. Clinical measurements in millimeters performed after implant installation (n = 6)
TEST Mean and standard deviation Percentiles 25th; 50th; 75th
Coronal diameter Bucco-lingual
H-GAP buccal
V-GAP buccal
C-clinical – IS lingual
4.7 (0.5) 4.3; 5.0; 5.0
1.2 (0.3) 1.0; 1.0; 1.4
3.1 (1.3) 2.6; 3.0; 3.0
0.7 (0.4) 0.5; 0.8; 1.0
Mean values, standard deviations and 25th, 50th (median), and 75th percentiles. Horizontal (H-GAP) and vertical (V-GAP) dimensions of the remaining gap at the buccal aspect and vertical distance between the top of the lingual bony crest (C_clinical) and the implant shoulder (IS).The positive values for C_clinical–IS indicate that the bony crest was located coronally to IS.
A shrinkage of both the buccal hard and soft tissues and a reduction of the buccal defects were observed at the analyses on the superimposed images of test and control sites. References are reported in Fig. 3, while data are schematically presented in diagrams illustrated in Fig. 7a–d. The distance IS-D at the buccal aspect, representing the buccal defect present after implant installation, was 4.4 0.7 mm.
Discussion The present experiment evaluated the influence on buccal alveolar bone preservation of DBBM particles placed within marginal defects of about 1.0 mm and on the buccal bony crest wall at IPIES (implant placed immediately into extraction socket) and covered by a collagen membrane. The use of this augmentation procedure within the remaining buccal defects as well as on the outer contour of the buccal bony crest did not maintain the volume of the hard and soft tissues. These results are in agreement with those from other reports on experimental studies on IPIES in dogs that have shown a limited improvement in bony crest preservation compared to untreated sites (Caneva et al. 2012; Favero et al. 2013a). This is, however, in disagreement with another similar experimental study in dogs that demonstrated that no vertical buccal bony crest resorption occurred at overfilled grafted sites (Ara ujo et al. 2011). Despite the fact that the present experiment clearly demonstrated that the augmentation procedures used did not preserve the
hard and soft tissue volumes, it was shown in other experiments that the use of augmentation procedures may limit the shrinkage of tissues at IPIES (for a review see Wang & Lang 2012). The use of DBBM particles has shown to provide better results when placed at small compared to large buccal defects at the time of implant installation. In an experiment (Caneva et al. 2011a), the third premolars were used and buccal defects of about 0.6 mm were obtained. Better buccal bony crest preservation was observed at the treated compared to the untreated sites. In another experiment (Favero et al. 2013a), the buccal defects were of about 1.7 mm, and similar results were obtained between the two sites, treated and untreated. Finally, IPIES was also used in the first molar distal extraction sockets, and buccal defects of about 2.5–2.7 mm were obtained. Better results were observed at the untreated compared to the treated sites, showing a lack of efficacy of the DBBM particles and collagen membranes in preventing bony crest resorption at buccal defects when their dimension exceeds 2 mm (Favero et al. 2013b). In the present study, the buccal defect dimensions were determined clinically and were 1.2 mm in width and 3.1 mm in depth. In the photographic evaluation, the depth of the defect was 4.4 mm. This discrepancy may be at least partially explained by the dimension of the tip of the probe used clinically that did not allow to reach the bottom of the defect. The use of DBBM particles may contribute to maintain also the soft tissue in a more coronal position, as shown in a study in dogs, in which IPIES was used in mandibular third
Fig. 4. Ground section of a control site, represented by a pristine distal root and the corresponding portion of crown of the third premolar of the right side of the mandible. Toluidine blue stain. Original magnification 912.
premolars (Caneva et al. 2012). In one side of the mandible, GBR procedures were applied using DBBM particles and collagen membranes, while no GBR procedures were used on the contralateral side. Impressions of the experimental sites were taken before extractions and after 4 months of healing. The cast models obtained were analyzed using an optical system. The 3D images were superimposed, and the dimensional variation
Table 2. Histological measurements in millimeters of the peri-implant hard tissue levels after 3 months of healing (n = 6) IS-C
TEST Mean and standard deviation Percentiles 25th; 50th; 75th
IS-B
b
l
l-absolute
1.7 (1.1) 1.1; 2.0; 2.5
0.5 (0.7) 0.2; 0.5; 1.0
1.2 (0.5) 1.0; 1.3; 1.5
IS-Cbt b 1.1 (1.7) 0.2; 1.4; 2.5
b
l
2.3 (1.3) 1.3; 2.3; 2.8
1.6 (0.7) 1.0; 1.1; 1.9
Mean values, standard deviations and 25th, 50th (median), and 75th percentiles. IS, Implant shoulder; C, top of the adjacent bony crest; Cbt, top of the adjacent hard bulk tissue; B, coronal end of osseointegration; b, buccal; l, lingual.
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(a)
(b)
Fig. 5. Ground section of a test site. Toluidine blue stain. (a) The implant surface appeared to be, after 3 months of healing, integrated in newly formed bone. DBBM particles are visible in the coronal region of the buccal bony crest. Original magnification 912. (b) Higher magnification of the coronal buccal aspect of the bony crest (originally 940). DBBM particles were mostly embedded into connective tissue. However, the newly formed bone was surrounding the DBBM area. DBBM, Deproteinized bovine bone mineral.
(a)
(b)
Fig. 6. Ground section of a test site. Toluidine blue stain. (a) The buccal bony crest was resorbed. However, DBBM particles were located up to the implant margin, contributing to maintain coronally the mucosal margin of the periimplant mucosa. Original magnification 912. (b) Details of the coronal buccal aspect (original magnification 940). DBBM, deproteinized bovine bone mineral.
© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
between the two periods evaluated. It was shown that sites treated with DBBM particles and a collagen membrane did not maintain the original dimensions. These sites, however, showed a better preservation of the buccal aspect of the alveolar crest compared to untreated contralateral sites. This is also in agreement with clinical studies in which the use of DBBM and membranes at IPIES sites produced better outcomes compared to the use of grafting material alone or no grafting (Cornelini et al. 2004; Chen et al. 2007). Different distances were found in the present study between the IS and the peak of the bulk tissue (Cbt), and between IS and the top of the bony crest (C). This, in turn, means that the top of the hard bulky crest was composed of DBBM particles that the histological analyses revealed to be embedded into connective tissue. This is in agreement with the results of a previous article (Favero et al. 2013b), in which data from a bone regenerative procedure at IPIES at molar regions in dogs were reported. Residual defects >2 mm after implant installation into alveolar sockets were filled with DBBM particles and covered by a collagen membrane and compared to untreated IPIES sites. The hard bulky tissue at the treated sites was located 0.6 mm more coronally compared to the top of the bony crest. This may be related to the resorption of the buccal bony wall after tooth extraction that may interfere with the inclusion of the grafted material into newly formed bone. The presence of DBBM particles above the most coronal top of the bony crest was also analyzed in another experimental study in dogs, in which IPIES was used at the second maxillary incisors, in conjunction with artificial standardized buccal defects treated with DBBM particles or autologous bone and collagen membranes (De Santis et al. 2011). After 2 months of healing, the peak of the bony crest and the peak of DBBM were located at 2 and 0.9 mm apically to IS, respectively. After 4 months of healing, however, the bony crest and the DBBM/hard tissue were located at a similar height (2.5–2.6 mm), denoting that the more coronal location of the DBBM particles found after 2 months was lost after 4 months of healing. It may be speculated that this loss may have been due to resorptive processes that may be very active into the connective tissue (Busenlechner et al. 2012). In the present study, the implant was positioned lingually compared to the center of the alveolus. It was shown that this positioning partially contributes to a less exposure
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(a)
(b)
(c)
(d)
variations were evaluated. The comparison between experimental and pristine sites was already used and described in other articles (Ara ujo & Lindhe 2009, 2011; Lindhe et al. 2013). In those studies, the dimensional variation of extraction sockets filled with different biomaterials was analyzed comparing the original dimension of the alveolar socket at a pristine site (tooth) to that at the extraction sockets. In the experiments mentioned above, while the experimental sites were represented by the distal extraction sockets of premolars, the pristine site was represented by the mesial roots. In the present experiment, instead, both the experimental and the pristine sites were composed by the distal alveolus of premolars that guarantees more similar dimensions among sites at baseline. In conclusion, the contour augmentation performed with DBBM particles and a collagen membrane at the buccal aspects of IPIES sites was not able to maintain the tissue volume.
In the present experiment, histological images from a pristine site (tooth) and the implant site of the opposite side of the jaw were superimposed, and dimensional
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. Sebasti~ ao Bianco (USP - Faculty of Dentistry of Ribeir~ao Preto University of S~ao Paulo, S~ao Paulo, Brazil) in the histological processing are highly appreciated. All the authors declare to have no conflict of interest with the materials used in the present study.
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Fig. 7. Diagrams illustrating the position of soft and hard tissues around teeth and implants. Light blue, gingiva; dark blue, peri-implant mucosa; orange, buccal bony wall at tooth; red, buccal bony wall at implant. (a) Gingiva and peri-implant mucosa; (b) bony crests; (c) gingiva and bony crest at teeth; *P < 0.05; (d) peri-implant mucosa and bony crest at implants.
above the buccal bony crest of the implant surface compared to a more central or buccal positioning (Caneva et al. 2010; Tomasi et al. 2010; Favero et al. 2012).
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Sicilia, A. & Botticelli, D. ; Working Group 3 (2012) Computer-guided implant therapy and soft- and hard-tissue aspects. The Third EAO Consensus Conference 2012. Clinical Oral Implants Research 23(Suppl 6): 157–161. Tan, W.L., Wong, T.L., Wong, M.C. & Lang, N.P. (2012) A systematic review of post-extractional alveolar hard and soft tissue dimensional changes in humans. Clinical Oral Implants Research 23 (Suppl 5): 1–21. Tomasi, C., Sanz, M., Cecchinato, D., Pjetursson, B., Ferrus, J., Lang, N.P. & Lindhe, J. (2010) Bone dimensional variations at implants placed in fresh extraction sockets: a multilevel multivariate analysis. Clinical Oral Implants Research 21: 30–36. Vignoletti, F., Discepoli, N., M€ uller, A., de Sanctis, M., Mu~ noz, F. & Sanz, M. (2012) Bone modelling at fresh extraction sockets: immediate implant placement versus spontaneous healing: an experimental study in the beagle dog. Journal of Clinical Periodontology 39: 91–97. Wang, R. & Lang, N.P. (2012) Ridge preservation after tooth extraction. Clinical Oral Implants Research 23(Suppl 6): 147–156.
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Authors’ affiliations: Giacomo Favero, Daniele Botticelli, Faculty of Dentistry, University of Medical Science, La Habana, Cuba Niklaus P. Lang, Daniele Botticelli, The University of Hong Kong, Prince Philip Dental Hospital, Hong Kong, China Piero Romanelli, Private Practice, Bologna, Italy Fabio Pantani, Private Practice, San Marino, Repubblica di San Marino Marco Caneva, Daniele Botticelli, ARDEC, Ariminum Odontologica, Rimini, Italy Daniele Botticelli, Faculdade de Odontologia de Aracßatuba, UNESP - Universidade Estadual Paulista, S~ ao Paulo, Brasil Corresponding author: Dr. Daniele Botticelli Universidade Estadual Paulista “J ulio de Mesquita Filho” UNESP - Campus de Aracßatuba Rua Jose Bonif acio 1193 16015-050 Aracßatuba, (SP) Brasil Tel.: +55 02118 3636 3209 Fax: +55 02118 3636 3340 e-mail: [email protected]
A digital evaluation of alveolar ridge preservation at implants placed immediately into extraction sockets: an experimental study in the dog
Key words: animal study, bone healing, collagen membrane, deproteinized bovine bone min-
eral, extraction socket, immediate implants, implant dentistry, osseointegration, regeneration, ridge preservation, type I installation Abstract Objective: To compare with pristine sites bone resorption and soft tissue adaptation at implants placed immediately into extraction sockets (IPIES) in conjunction with deproteinized bovine bone mineral (DBBM) particles and a collagen membrane. Material and methods: The mesial root of the third premolar in the left side of the mandible was endodontically treated (Test). Flaps were elevated, the tooth hemi-sectioned, and the distal root removed to allow the immediate installation of an implant into the extraction socket in a lingual position. DBBM particles were placed into the defect and on the outer contour of the buccal bony ridge, concomitantly with the placement of a collagen membrane. A non-submerged healing was allowed. The premolar on the right side of the mandible was left in situ (control). Ground sections from the center of the implant as well as from the center of the distal root of the third premolar of the opposite side of the mandible were obtained. The histological image from the implant site was superimposed to that of the contralateral pristine distal alveolus, and dimensional variation evaluated for the hard tissue and the alveolar ridge. Results: After 3 months of healing, both histological and photographic evaluation revealed a reduction of hard and soft tissue dimensions. Conclusion: The contour augmentation performed with DBBM particles and a collagen membrane at the buccal aspects of implants placed IPIES was not able to maintain the tissue volume.
Date: Accepted 28 October 2013 To cite this article: Favero G, Lang NP, Romanelli P, Pantani F, Caneva M, Botticelli D. A digital evaluation of alveolar ridge preservation at implants placed immediately into extraction sockets. Clin. Oral Impl. Res. 00, 2013, 1–7 doi: 10.1111/clr.12307
After tooth extraction, the alveolar ridge undergoes resorption during the first 3–6 months of healing and reaches a mean horizontal reduction of 3.8 mm and mean vertical reduction of 1.2 mm (Tan et al. 2012). It has been shown that implants placed immediately into extraction sockets (IPIES) are unable to preserve the alveolar bony crest in its entire outline (Botticelli et al. 2004; Ara jo et al. 2005; Sicilia & Botticelli 2012; u Wang & Lang 2012). The positioning of the implant within the extraction socket has been demonstrated to be a determining factor of importance for the final location and volume of the alveolar bony crest (Caneva et al. 2010; Tomasi et al. 2010). The more lingual an implant is installed, the less supra-crestal exposure of the implant will occur. However, such implant placement will not preserve the alveolar bony ridge.
© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
However, it has been demonstrated that the use of bone substitutes for grafting the alveolus after extraction (Ara ujo et al. 2008; Lindhe et al. 2013) or to fill the remaining defects after immediate implant placement (Ara ujo et al. 2011; Caneva et al. 2011a,b, 2012) may contribute to the preservation of the alveolar ridge. The shrinkage of the alveolar ridge after tooth extraction (Fickl et al. 2008) as well as after IPIES (Caneva et al. 2012; Rossi et al. 2013) has recently been documented using a laser scan on cast models and a software to superpose images taken prior to therapy and after healing. A comparison between IPIES sites and pristine extraction alveoli has been reported (Ara ujo et al. 2005; Vignoletti et al. 2012). Other experimental studies have compared the histological images of grafted alveoli to untreated alveoli and to sites with pristine
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teeth (Ara ujo et al. 2008; Ara ujo & Lindhe 2009, 2011; Lindhe et al. 2013). In these studies, the positions of the apices and axes of the teeth were used as references on the images representing the treated and untreated sites and compared with each other. However, there is a lack of studies that compared IPIES sites with the contralateral pristine sites (teeth). Hence, the aim of this experiment was to compare with pristine sites bone resorption and soft tissue adaptation at implants placed IPIES in conjunction with deproteinized bovine bone mineral (DBBM) particles and a collagen membrane.
Material and methods The research protocol was submitted to and approved by the local Ethical Committee for Animal Research of the University of the State of S~ ao Paolo, Brazil. Clinical procedures
Six Labrador dogs (each approximately 26.5 kg and a mean age of 1 year) were used. During all surgical procedures, the animals were pre-anaesthetized with Acepranâ 0.2% (0.05 mg/kg – Univet-vetnil, S~ao Paulo, Brazil), sedated with Zoletilâ 10 mg/Kg (Virbac, Jurubatuba Santo-Amaro, Brazil), maintained with inhalation with Isofluranoâ (Baxter Hospitalar Ltd., Sao Paulo, Brazil) during the surgery. The animals were kept with an intravenous infusion of sterile saline during the procedures. Local anesthesia was also provided. The pulp tissue of the mesial root of the third premolar at the left side of the mandible (test sites) was removed, the root canal filled with gutta-percha and root canal cement (Mtwoâ, Endopocketâ, Epfillâ, Sweden & Martina, Due Carrare, Padova, Italy). The crown was hemisected, the distal root removed, and the crown restored with composite (Adonisâ, Sweden & Martina, Due Carrare, Padova, Italy). Bucco-lingual fullthickness flaps were elevated, and the buccal and lingual alveolar bony plates exposed. The bucco-lingual dimensions at the coronal margin were measured using calipers (Castroviejoâ; KLS Martin Group, Umkirch, Germany). A recipient site was prepared, and a titanium implant with a TiUniteâ surface (Nobel Biocare Holding AG, Kloten, Switzerland; Mark III Groovy implant, 11.5 mm long and 3.3 mm wide) was installed into the distal alveolus (Fig. 1a). The implants were placed lingually into the alveoli, with the margin of the implants being placed flush with the
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(a)
(b)
Fig. 1. Clinical view of some of the clinical procedures. (a) The implant was placed in a lingual position within the distal alveolus of the third premolar, in the left side of the mandible. A buccal defect about 1 mm wide and 3 mm deep occurred. (b) After the placement of a healing abutment, deproteinized bovine bone mineral particles were placed into the defect and on the buccal bony wall, and a membrane was positioned to cover the site.
alveolar buccal bony crest, and resulting in a buccal gap. The horizontal width (H-GAP; Fig. 1a) and the vertical depth (V-GAP) of the defect between the implant and the bony crest were measured at the buccal aspect using an UNC 15TM probe (Hu-Friedy, Chicago, IL, USA). The implant shoulder (IS) was always located in an apical position in relation to the lingual bony crest. The distance between the top of the bony crest (C-Clinical) and the IS was also measured at the lingual aspect using the same periodontal probe. A healing abutment was affixed to the implant, and DBBM particles (Bio-Ossâ, Granules 0.25–1 mm; Geistlich Biomaterials, Wolhusen, Switzerland) were placed to fill the remaining defect around the marginal portion of the implant and on the buccal bony wall. A collagen membrane (Bio-Gideâ; Geistlich Biomaterials) was adapted to the buccal aspect to cover the experimental region (Fig. 1b). The flaps were subsequently mobilized and sutured to allow a non-submerged healing using interrupted VicrylTM 4-0 sutures (Johnson & Johnson, S~ao Jose dos Campos, Brazil). The third premolar of the right side of the mandible (control sites) was left untreated. After the surgeries, the animals were given antibiotics for 10 days (Stomorgylâ 10, one tablet/10Kg daily – Merial Saude Animal Ltd., Paulinia, Brazil), anti-inflammatory drugs for 5 days (Maxicamâ 2.0 mg, one tablet/20Kg daily – Ouro Fino Saude Animal Ltd., Cravinhos, Brazil), and analgesic for 3 days (Tramalâ 50 mg, 4.0 mg/Kg subcutaneous, every 8 h – Uni~ao Quimica Farmaceutica Nacional S/A, Pouso Alegre, Brazil). The
animals were kept in kennels and on concrete runs at the university’s field 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 abutments cleaning were performed. The animals were euthanized 3 months after the surgery applying an overdose of Thiopentalâ (Cristalia Ltd., Campinas, Brazil). Histological preparation
Individual blocks containing the implant, at the left side, and the tooth, at the right side of the mandible, including the surrounding soft and hard tissues were fixed in 4% formaldehyde solution followed by dehydration in a series of graded alcohol solutions and finally embedded in resin (LR Whiteâ hard grade, London Resin Company Ltd, Berkshire, UK). The blocks were cut following the longitudinal axes in a bucco-lingual plane using a diamond band saw fitted in a precision slicing machine (Exaktâ, Apparatebau, Norderstedt, Germany). The cuts were performed in the center of the implant as well as in the center of the distal root of the third premolar. Subsequently, one slice was obtained from each hemi-blocks and then reduced to a thickness of about 50 lm using a cutting–grinding device (Exaktâ, Apparatebau). The slide representing the most central portion of the implants and teeth was selected from each block and used for histological evaluation. The histological slides were stained with toluidine blue and examined under a standard light microscope for histometric analysis.
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G. Favero et al Ridge preservation
Histological evaluation
In an Eclipse 50i microscope (Nikon Corporation, Tokyo, Japan) equipped with a video camera connected to a computer and using the software NIS-Elements v4.1 (Nikon Corporation), the following landmarks were identified at the test sites (Fig. 2): (IS) the shoulder of the implant, (C) the top of the adjacent bony crest, (Cbt) the most coronal part of the bulky hard tissue (bony crest or DBBM particles), and (B) the most coronal bone-to-implant contact. The following vertical measurements were performed at a magnification of 9100 between the corresponding landmarks: IS-C, IS-Cbt, and IS-B. Photographic evaluation
All histological slides were photographed, and test and control (pristine tooth) images were superimposed. The implants of the test images were positioned on the control images in such a way that the lingual implant surface was parallel to the lingual bony wall of the alveolus. The IS was placed flush to the buccal bony crest leaving a buccal defect
Fig. 2. Diagrams illustrating the landmarks for the histological evaluation. In red: IS, shoulder of the implant; B, most coronal bone-to-implant contact; C, top of the adjacent bony crest; Cbt, the most coronal part of the bulky tissue (bony crest or DBBM particles). DBBM, Deproteinized bovine bone mineral.
width similar to that obtained clinically at the test sites. The alignment was obtained by digital overlapping of the images with the software i-Dixel (J. Morita Mfg. Corp., Kyoto, Japan) according to the fixed landmarks. The measurements were made on a dedicated software (ImageJ 1.34s, Wayne Rasband, National Institute of Health, Bethesda, MD, USA) using unit pixels and converting them to millimeters, applying the implant size as reference for calibration. The following landmarks were identified at the buccal and lingual aspects of the implants/teeth sites (Fig. 3): the IS, the implant surface (S), the top of the periimplant mucosa (PM) and of the gingiva (G), and the bottom of the defect (D). Moreover, the outer contour of the alveolar bony ridge and of the mucosa, as well as the inner contour (IC) of the extraction socket/residual defect and of the mucosa and gingiva, was identified. The vertical distance PM-IS and G-IS was measured. The horizontal distances from S to the outer and inner contours of the hard tissue were measured at the IS level and then apically at each subsequent millimeter up to 4 mm. A similar evaluation was performed for the outer and inner contours of the mucosa at the IS level and then, at each subsequent millimeter, coronally up to 3 mm and apically up to 2 mm. Measurements and analyses were performed for the
Fig. 3. Diagrams illustrating the landmarks for the photographic evaluation. S, Implant surface, G, margin of the gingiva, PM, margin of the peri-implant mucosa, IS, shoulder of the implant; D, bottom of the defect after implant installation. The outer and inner contours of bony crest and mucosa as well as the position of PM, G, and D were measured at the photographic evaluation. Light blue, gingiva; dark blue, peri-implant mucosa; orange, buccal bony wall at tooth; red, buccal bony wall at implant.
© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
buccal aspects, while measurements at the lingual aspect were limited to the coronal regions. Data analysis
Mean values and standard deviations as well as 25th, 50th (median), and 75th percentiles were calculated for each outcome variable. Differences between test (implant) and control (tooth) sites were analyzed using Wilcoxon signed rank test. The level of significance was set at a = 0.05.
Results Clinical evaluations
Table 1 reports the clinical evaluations. The diameter of the extraction sockets was 4.7 0.5 mm, while the horizontal (H-GAP) and the vertical buccal defects (V-GAP) after implant installation were 1.2 0.3 mm and 3.1 1.3 mm, respectively. The IS was located apically in relation to the lingual bony crest by about 0.7 mm. After 3 months of healing, no implants were lost and no obvious signs of inflammation were detected at the time of sacrifice. Histological evaluations
No artifacts occurred during the histological preparation, nor were there any tissue blocks destroyed at the test and control sites. All implants appeared to be integrated into mature mineralized bone. The buccal alveolar bony crest at the test sites was resorbed by 1.7 1.1 mm (Fig. 4a, b; Table 2). At the lingual aspect, the top of the bony crest was located 0.5 0.7 mm apically to the IS. However, taking into account the initial position of the lingual bony crest, the absolute vertical resorption totally reached 1.2 0.5 mm (l-absolute). Deproteinized bovine bone mineral particles were rarely found integrated into newly formed bone. However, a substantial amount of particles included into connective tissue was found above the bony crest and on the outer buccal contour of the bony ridge, sometimes appearing to contribute to maintain coronally the peri-implant mucosal margin (Fig. 5a,b). The distance between IS and the most coronal peak of the hard tissue (bone or DBBM) was 1.1 1.7 mm (IS-Cbt), while the distance IS-B at the buccal aspect was 2.3 1.3 mm. Photographic evaluations
Test and control sites yielded an n = 6. A ground section representing the control sites is depicted in Fig. 6.
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Table 1. Clinical measurements in millimeters performed after implant installation (n = 6)
TEST Mean and standard deviation Percentiles 25th; 50th; 75th
Coronal diameter Bucco-lingual
H-GAP buccal
V-GAP buccal
C-clinical – IS lingual
4.7 (0.5) 4.3; 5.0; 5.0
1.2 (0.3) 1.0; 1.0; 1.4
3.1 (1.3) 2.6; 3.0; 3.0
0.7 (0.4) 0.5; 0.8; 1.0
Mean values, standard deviations and 25th, 50th (median), and 75th percentiles. Horizontal (H-GAP) and vertical (V-GAP) dimensions of the remaining gap at the buccal aspect and vertical distance between the top of the lingual bony crest (C_clinical) and the implant shoulder (IS).The positive values for C_clinical–IS indicate that the bony crest was located coronally to IS.
A shrinkage of both the buccal hard and soft tissues and a reduction of the buccal defects were observed at the analyses on the superimposed images of test and control sites. References are reported in Fig. 3, while data are schematically presented in diagrams illustrated in Fig. 7a–d. The distance IS-D at the buccal aspect, representing the buccal defect present after implant installation, was 4.4 0.7 mm.
Discussion The present experiment evaluated the influence on buccal alveolar bone preservation of DBBM particles placed within marginal defects of about 1.0 mm and on the buccal bony crest wall at IPIES (implant placed immediately into extraction socket) and covered by a collagen membrane. The use of this augmentation procedure within the remaining buccal defects as well as on the outer contour of the buccal bony crest did not maintain the volume of the hard and soft tissues. These results are in agreement with those from other reports on experimental studies on IPIES in dogs that have shown a limited improvement in bony crest preservation compared to untreated sites (Caneva et al. 2012; Favero et al. 2013a). This is, however, in disagreement with another similar experimental study in dogs that demonstrated that no vertical buccal bony crest resorption occurred at overfilled grafted sites (Ara ujo et al. 2011). Despite the fact that the present experiment clearly demonstrated that the augmentation procedures used did not preserve the
hard and soft tissue volumes, it was shown in other experiments that the use of augmentation procedures may limit the shrinkage of tissues at IPIES (for a review see Wang & Lang 2012). The use of DBBM particles has shown to provide better results when placed at small compared to large buccal defects at the time of implant installation. In an experiment (Caneva et al. 2011a), the third premolars were used and buccal defects of about 0.6 mm were obtained. Better buccal bony crest preservation was observed at the treated compared to the untreated sites. In another experiment (Favero et al. 2013a), the buccal defects were of about 1.7 mm, and similar results were obtained between the two sites, treated and untreated. Finally, IPIES was also used in the first molar distal extraction sockets, and buccal defects of about 2.5–2.7 mm were obtained. Better results were observed at the untreated compared to the treated sites, showing a lack of efficacy of the DBBM particles and collagen membranes in preventing bony crest resorption at buccal defects when their dimension exceeds 2 mm (Favero et al. 2013b). In the present study, the buccal defect dimensions were determined clinically and were 1.2 mm in width and 3.1 mm in depth. In the photographic evaluation, the depth of the defect was 4.4 mm. This discrepancy may be at least partially explained by the dimension of the tip of the probe used clinically that did not allow to reach the bottom of the defect. The use of DBBM particles may contribute to maintain also the soft tissue in a more coronal position, as shown in a study in dogs, in which IPIES was used in mandibular third
Fig. 4. Ground section of a control site, represented by a pristine distal root and the corresponding portion of crown of the third premolar of the right side of the mandible. Toluidine blue stain. Original magnification 912.
premolars (Caneva et al. 2012). In one side of the mandible, GBR procedures were applied using DBBM particles and collagen membranes, while no GBR procedures were used on the contralateral side. Impressions of the experimental sites were taken before extractions and after 4 months of healing. The cast models obtained were analyzed using an optical system. The 3D images were superimposed, and the dimensional variation
Table 2. Histological measurements in millimeters of the peri-implant hard tissue levels after 3 months of healing (n = 6) IS-C
TEST Mean and standard deviation Percentiles 25th; 50th; 75th
IS-B
b
l
l-absolute
1.7 (1.1) 1.1; 2.0; 2.5
0.5 (0.7) 0.2; 0.5; 1.0
1.2 (0.5) 1.0; 1.3; 1.5
IS-Cbt b 1.1 (1.7) 0.2; 1.4; 2.5
b
l
2.3 (1.3) 1.3; 2.3; 2.8
1.6 (0.7) 1.0; 1.1; 1.9
Mean values, standard deviations and 25th, 50th (median), and 75th percentiles. IS, Implant shoulder; C, top of the adjacent bony crest; Cbt, top of the adjacent hard bulk tissue; B, coronal end of osseointegration; b, buccal; l, lingual.
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G. Favero et al Ridge preservation
(a)
(b)
Fig. 5. Ground section of a test site. Toluidine blue stain. (a) The implant surface appeared to be, after 3 months of healing, integrated in newly formed bone. DBBM particles are visible in the coronal region of the buccal bony crest. Original magnification 912. (b) Higher magnification of the coronal buccal aspect of the bony crest (originally 940). DBBM particles were mostly embedded into connective tissue. However, the newly formed bone was surrounding the DBBM area. DBBM, Deproteinized bovine bone mineral.
(a)
(b)
Fig. 6. Ground section of a test site. Toluidine blue stain. (a) The buccal bony crest was resorbed. However, DBBM particles were located up to the implant margin, contributing to maintain coronally the mucosal margin of the periimplant mucosa. Original magnification 912. (b) Details of the coronal buccal aspect (original magnification 940). DBBM, deproteinized bovine bone mineral.
© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
between the two periods evaluated. It was shown that sites treated with DBBM particles and a collagen membrane did not maintain the original dimensions. These sites, however, showed a better preservation of the buccal aspect of the alveolar crest compared to untreated contralateral sites. This is also in agreement with clinical studies in which the use of DBBM and membranes at IPIES sites produced better outcomes compared to the use of grafting material alone or no grafting (Cornelini et al. 2004; Chen et al. 2007). Different distances were found in the present study between the IS and the peak of the bulk tissue (Cbt), and between IS and the top of the bony crest (C). This, in turn, means that the top of the hard bulky crest was composed of DBBM particles that the histological analyses revealed to be embedded into connective tissue. This is in agreement with the results of a previous article (Favero et al. 2013b), in which data from a bone regenerative procedure at IPIES at molar regions in dogs were reported. Residual defects >2 mm after implant installation into alveolar sockets were filled with DBBM particles and covered by a collagen membrane and compared to untreated IPIES sites. The hard bulky tissue at the treated sites was located 0.6 mm more coronally compared to the top of the bony crest. This may be related to the resorption of the buccal bony wall after tooth extraction that may interfere with the inclusion of the grafted material into newly formed bone. The presence of DBBM particles above the most coronal top of the bony crest was also analyzed in another experimental study in dogs, in which IPIES was used at the second maxillary incisors, in conjunction with artificial standardized buccal defects treated with DBBM particles or autologous bone and collagen membranes (De Santis et al. 2011). After 2 months of healing, the peak of the bony crest and the peak of DBBM were located at 2 and 0.9 mm apically to IS, respectively. After 4 months of healing, however, the bony crest and the DBBM/hard tissue were located at a similar height (2.5–2.6 mm), denoting that the more coronal location of the DBBM particles found after 2 months was lost after 4 months of healing. It may be speculated that this loss may have been due to resorptive processes that may be very active into the connective tissue (Busenlechner et al. 2012). In the present study, the implant was positioned lingually compared to the center of the alveolus. It was shown that this positioning partially contributes to a less exposure
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(a)
(b)
(c)
(d)
variations were evaluated. The comparison between experimental and pristine sites was already used and described in other articles (Ara ujo & Lindhe 2009, 2011; Lindhe et al. 2013). In those studies, the dimensional variation of extraction sockets filled with different biomaterials was analyzed comparing the original dimension of the alveolar socket at a pristine site (tooth) to that at the extraction sockets. In the experiments mentioned above, while the experimental sites were represented by the distal extraction sockets of premolars, the pristine site was represented by the mesial roots. In the present experiment, instead, both the experimental and the pristine sites were composed by the distal alveolus of premolars that guarantees more similar dimensions among sites at baseline. In conclusion, the contour augmentation performed with DBBM particles and a collagen membrane at the buccal aspects of IPIES sites was not able to maintain the tissue volume.
In the present experiment, histological images from a pristine site (tooth) and the implant site of the opposite side of the jaw were superimposed, and dimensional
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. Sebasti~ ao Bianco (USP - Faculty of Dentistry of Ribeir~ao Preto University of S~ao Paulo, S~ao Paulo, Brazil) in the histological processing are highly appreciated. All the authors declare to have no conflict of interest with the materials used in the present study.
implant placement in fresh extraction sockets: an experimental study in the dog. Journal of Clinical Periodontology 32: 645–652. Botticelli, D., Berglundh, T. & Lindhe, J. (2004) Resolution of bone defects of varying dimension and configuration in the marginal portion of the peri-implant bone. An experimental study in the dog. Journal of Clinical Periodontology 31: 309–317. Busenlechner, D., Tangl, S., Arnhart, C., Redl, H., Schuh, C., Watzek, G. & Grube.r, R. (2012) Resorption of deproteinized bovine bone mineral in a porcine calvaria augmentation model. Clinical Oral Implants Research 23: 95–99. Caneva, M., Botticelli, D., Morelli, F., Cesaretti, G., Beolchini, M. & Lang, N.P. (2012) Alveolar process preservation at implants installed immediately into extraction sockets using deproteinized bovine bone mineral – an experimental study in
dogs. Clinical Oral Implants Research 23: 789–796. Caneva, M., Botticelli, D., Pantani, F., Baffone, G.M., Rangel, I.G. Jr & Lang, N.P. (2011a) Deproteinized bovine bone mineral in marginal defects at implants installed immediately into extraction sockets. An experimental study in dogs. Clinical Oral Implants Research 23: 106–112. Caneva, M., Botticelli, D., Stellini, E., Salata, L.A., Souza, S.L.S. & Lang, N.P. (2011b) Magnesiumenriched hydroxyapatite at immediate implants. A histomorphometric study in dogs. Clinical Oral Implants Research 22: 512–517. Caneva, M., Salata, L.A., de Souza, S.S., Baffone, G., Lang, N.P. & Botticelli, D. (2010) Influence of implant positioning in extraction sockets on osseointegration: histomorphometric analyses in dogs. Clinical Oral Implants Research 21: 43– 49.
Fig. 7. Diagrams illustrating the position of soft and hard tissues around teeth and implants. Light blue, gingiva; dark blue, peri-implant mucosa; orange, buccal bony wall at tooth; red, buccal bony wall at implant. (a) Gingiva and peri-implant mucosa; (b) bony crests; (c) gingiva and bony crest at teeth; *P < 0.05; (d) peri-implant mucosa and bony crest at implants.
above the buccal bony crest of the implant surface compared to a more central or buccal positioning (Caneva et al. 2010; Tomasi et al. 2010; Favero et al. 2012).
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G. Favero et al Ridge preservation
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