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Bone level change of extraction sockets with Bio-Oss collagen and implant placement: A clinical study
Annals of Anatomy 194 (2012) 508–512
Contents lists available at SciVerse ScienceDirect
Annals of Anatomy journal homepage: www.elsevier.de/aanat
Bone level change of extraction sockets with Bio-Oss collagen and implant placement: A clinical study Friedhelm Heinemann a,∗,1, Istabrak. Hasan b,1, Christian Schwahn a, Christoph Bourauel b, Torsten Mundt a a b
Department of Prosthodontics, Gerodontology and Biomaterials, University of Greifswald, Rotgerberstr. 8, 17475 Greifswald, Germany Endowed Chair of Oral Technology, University of Bonn, Welschnonnenstr 17, 53111 Bonn, Germany
a r t i c l e
i n f o
Article history: Received 16 October 2011 Received in revised form 19 November 2011 Accepted 24 November 2011
Keywords: Bio-Oss collagen Socket preservation Alveolar bone Bone level change
a b s t r a c t Aims: To compare the reaction of the alveolar bone to the preservation of the extraction socket by BioOss Collagen with and without combination of implant treatment. To evaluate whether early implant insertion 8–10 weeks thereafter could be a suitable time point for long term bone stability around the implant. Methods: A total of 25 patients were divided into three groups: The first group (seven patients) received Bio-Oss Collagen after extraction and 8–10 weeks later an implant, the second group (eight patients) received only Bio-Oss Collagen without implantation thereafter, while the third group was considered as a control (eleven patients), where the sockets healed without any treatment. The change in the vertical bone level of the alveolar crests were measured from panoramic radiographs and statistically analysed. Results: Bone level change was significantly less for Group 1 than Group 3 (P < 0.001), while was not significantly different for Group 2 and Group 3 (P = 0.23). However, the rate of bone level change per year was statistically smaller for Group 1 compared to Group 3 (P = 0.019) and as well as for Group 1 than for Group 2 (P = 0.003), whereas the change per year was not significantly different for Group 2 vs. Group 3 (P = 0.122). Conclusion: Bone level preservation of extraction sockets using Bio-Oss Collagen with implantation is significantly better compared to using Bio-Oss Collagen only and untreated sockets. Implant insertion 8–10 weeks after extraction is a suitable time point after socket augmentation. © 2011 Elsevier GmbH. All rights reserved.
1. Introduction Alveolar bone resorption after tooth extraction is accelerated in the first 6 months after extraction and followed by a gradual remodelling that includes changes in size and shape. About 40% height and 60% width of alveolar bone is lost (Atwood and Coy, 1971; Araújo and Lindhe, 2009). The height and width reduction of the alveolar ridge complicates the implant placement thereafter, especially in the anterior maxilla, where bone volume is important for functional and aesthetic reasons (Seibert, 1993). Early extraction socket healing is expected to decrease the alveolar ridge by 2–4 mm horizontally and 1 mm vertically. This change is time dependent; by the end of the first year postextraction, nearly 6 mm of buccal loss can be expected (Lekovic et al., 1997, 1998; Iasella et al., 2003; Fernandes et al., 2011).
∗ Corresponding author at: Im Hainsfeld 29, 51597 Morsbach, Germany. Tel.: +49 2294992010. E-mail address: [email protected] (F. Heinemann). 1 First two authors claim for equal authorship. 0940-9602/$ – see front matter © 2011 Elsevier GmbH. All rights reserved. doi:10.1016/j.aanat.2011.11.012
Adequate volumes of alveolar bone are necessary to provide favourable aesthetic and successful long-term outcomes for dental implants. Therefore, in order to preserve the original ridge dimensions following tooth extraction and promote bone regeneration of the residual alveolar socket, various bone grafts and substitutes used in combination with or without barriers for guided tissue regeneration (GTR) have been suggested (Froum et al., 2002; Feuille et al., 2003; Iasella et al., 2003; Serino et al., 2003; Barone et al., 2008). Among these grafting materials, bovine bone mineral xenografts were able to promote bone regeneration and preserve the pre-extraction alveolar ridge dimensions when grafted in immediate extraction sockets, especially when combined with collagen (Artzi et al., 2000; Araújo and Lindhe, 2009; Carmagnola et al., 2003). The use of xenografts, especially bovine bone, has increased not only in ridge preservation, but also in other bone augmentation procedures. The important benefits of xenograft bone are a reduction in the drawbacks associated with autografts and their unlimited availability. Some studies have found that bovine bone grafted sites demonstrated good outcome and indicated this material could be a good bone substitute for bone augmentation before implant
F. Heinemann et al. / Annals of Anatomy 194 (2012) 508–512
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Table 1 Inclusion and exclusion criteria of the patients. Patients inclusion criteria
Patients exclusion criteria
Patients with need for single tooth extraction and subsequent implant placement.
• Severe renal or liver disease. • History of radiotherapy in the head region. • Chemotherapy at the time of surgical procedure. • Non-compensated diabetes mellitus symptoms of maxillary sinus disease. • Pregnancy. • Active periodontal disease. • Poor oral hygiene.
installation (Hammerle et al., 1998; Artzi and Nemcovsky, 1998; Artzi et al., 2000). Furthermore, a randomised controlled clinical radiographic trial demonstrated that the postextraction alveolar ridge resorption was significantly reduced when the extraction sockets were grafted with a deproteinised bovine bone in comparison with the sockets that were left to heal without any grafting (Nevins et al., 2006). However, the disadvantages of the use of bovine bone include its slow resorption and healing with fibrous encapsulation (Artzi et al., 2000, 2001; Carmagnola et al., 2003) that leads to very protracted or even no remodelling in the central part of the augmented socket. As an alternative to socket preservation, collagen materials have shown proangiogenic qualities (Twardowski et al., 2007) and acceleration of ingrowth, proliferation and maturation of endothelial cells (Breithaupt-Faloppa et al., 2006) that encourage physiological bone regeneration. However, recent histological studies on a collagenous bovine bone matrix showed different results. While Araújo et al. (2011) reported an improved formation of new bone for sockets that were grafted with collagenous bovine bone matrix (Bio-Oss Collagen), the clinical study by Heberer et al. (2011a,b) reported smaller bone regeneration in grafted extraction sockets with Bio-Oss Collagen compared to the control extraction socket after 6–8 weeks of healing period. The aim of this study was to radiographically evaluate whether implant placement 8–10 weeks after socket augmentation with Bio-Oss Collagen is a proper time protocol concerning implant success and bone stability. 2. Materials and methods The present clinical study was performed according to principles outlined by the Declaration of Helsinki on experimentation involving human subjects and was approved by the University of Greifswald ethical committee (BB 13/11b). Patients requiring one tooth extraction in the maxillary anterior or premolar region were included in this study. A total of 26 patients were included, 16 females and 10 males. All were non-smokers and in good general health. Patients were enrolled in the study according to specific exclusion and inclusion criteria (Table 1). The patients were divided into three groups (Table 2): Group 1: In seven patients, the sockets were filled with Bio-Oss® Collagen (Geistlich Biomaterials, Baden-Baden, Germany) after tooth extraction and implants were inserted after a 8–10 weeks healing period. Group 2: In eight patients, the sockets were filled with Bio-Oss® Collagen after tooth extraction without implant treatment thereafter. Group 3: Eleven patients were selected as a control group in which the sockets were left to heal without further treatment.
Fig. 1. Reference points and measurement methods of the bone level for the three groups: (a) Group 1, Group 2, and (b) Group 3.
2.1. Treatment procedure For Group 1 and Group 2, the affected tooth was extracted using a flapless atraumatic technique. The socket was thoroughly curetted to remove granulation tissue and copiously irrigated with normal saline solution. The socket was then augmented with BioOss Collagen (Geistlich, Pharma AG, Wolhusen, Switzerland). No effort was made to extend the graft beyond the preexisting dimension of the socket. The marginal gingiva was then gently adapted and fixed with suture without total closure. A custom-made provisional fixed partial denture was cemented on the adjacent teeth. The provisional fixed partial denture included an ovate pontic to stabilise the graft and support buccal soft tissue. Oral hygiene at the surgical site was limited to soft brushing for the first 2 weeks. Regular brushing in the rest of the mouth and twice daily rinsing with 0.12% chlorhexidine was prescribed for 2 weeks. Patients were recalled weekly for monitoring within the first month. Group 1 underwent reopening after 8–10 weeks. The provisional fixed partial denture was removed and a re-entry procedure was performed. Preoperative antibiotic prophylaxis was carried out and a full-thickness flap was raised. An adequate implant in length and diameter (tioLogic© , Dentaurum Implants, Ispringen, Germany) was inserted. If necessary, missing sufficient local bone augmentation procedures and soft tissue management were performed according to standard protocols. The amount of the augmentation material was controlled. Single interrupted 5.0 monofilament sutures were used for flap adaptation in both groups. Ten to fourteen days later, the sutures were removed. Four to six months after implant placement, the definitive restorations were seated. 2.2. Bone level change measurement The change in the alveolar bone level in panoramic X-ray images was evaluated at different time intervals (length of observation period, Table 2). It was attempted to maintain an identical head position for each patient for the follow-up panoramic X-rays. A cephalostat device was used to hold the head within the same plane of occlusion. In all groups, the nearest (most mesial or most distal edge, respectively) of two neighbouring teeth were connected as a reference line. From this line, the bone level was measured at a 90◦ angle. For the X-rays of Group 1, the bone level around the implants to the reference line was measured mesially and distally (Fig. 1a). For X-rays of Group 2 and Group 3, corresponding bone levels were measured 2 mm mesial and 2 mm distal to the middle of the
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Table 2 Baseline characteristics.
Male Age at baseline, mean ± SD Length of observation period Mean ± SD Min–Max Baseline bone level, mean ± SE Non-smoking patients
Group 1 (n = 7)
Group 2 (n = 8)
Group 3 (n = 11)
Total (n = 26)
3 53.8 ± 11.9
4 55.3 ± 12.5
3 52.1 ± 10.2
10 53.5 ± 11.0
1.5 ± 1.0 0.6–3.4 11.8 ± 0.4 7
2.4 ± 1.6 0.6–4.7 13.9 ± 0.5 8
4.9 ± 3.1 0.3–10.9 12.8 ± 0.3 11
3.2 ± 2.7 0.3–10.9 12.8 ± 0.3 26
For clustered observations, SE = standard error instead of SD = standard deviation is given.
Table 3a Linear combinations (95% CI) for the initial status and the rate of change in the groups, adjusted for sex and age.
Baseline bone level Rate of change per year
Group 1 (n = 7)
Group 2 (n = 7)
Group 3 (n = 7)
11.5 (10.8–12.3) 0.292 + −0.411 = −0.119 (−0.449–0.211)
14.1 (13.3–14.8) 0.292 + 0.189 = 0.481 (0.262–0.700)
13.5 (12.9–14.1) 0.292 (reference) = 0.292 (0.194–0.390)
neighbouring teeth. The measurements were performed at a 90◦ angle to the same reference line (Fig. 1b). 2.2.1. Statistical analysis The change in bone levels over time was estimated with linear mixed models. Mixed models use all available data, properly accounting for correlation between repeated measurements in patients, in teeth, and in sites and appropriately handle missing data if it meets random (MAR) assumption. The change in bone levels was fitted by a linear slope model as described in “Applied Longitudinal Data Analysis” (ALDA, Singer and Willett, 2003). To estimate the initial status, the final model included sex (reference: female), age at baseline, the intercept (baseline value), and group (reference: Group 3, Table 2). To estimate the rate of change, the final model included the intercept (continuous time [years]) and the interaction between the intercept (continuous time) and group as fixed effects, and continuous time and the intercept as random effects or variance components. For the variance components an unstructured error covariance matrix was assumed on patient level (which herein corresponds to the tooth level). By centring, the intercept of the initial status can directly be interpreted as the baseline value for the reference category (Group 3) in females (reference category for sex) aged 53.6 years. The intercept for the rate of change (continuous time) can directly be interpreted as the rate of change in the reference group. Analyses were performed with STATA/MP software, version 10.1 (StataCorp LP, College Station, Texas, USA). For the computation of linear mixed models, we used the “xtmixed” procedure. Furthermore, smoothed scatter plots were used to show the relationships between bone levels and time in more detail (Fig. 2). The smoothing was generated with the STATA procedure lowess. For the amount of smoothing we chose a bandwidth = 0.8, meaning that 80% of the data are used in smoothing each point. Note that the smoothing procedure assumes independent observations. The three groups differ in the length of the observation period, which is reflected in the corresponding smoothing figures.
data for bone level changes per year. A significant difference was observed between Group 1 and Group 3 (P < 0.001), while no significant difference was observed between Group 2 and Group 3 (P = 0.23). However, the rate of bone level change per year was statistically significant for Group 1 vs. Group 3 (P = 0.019) and Group
3. Results 3.1. Bone level change The baseline bone level according to the measurement protocol of this study was +11.5 mm, +14.1 mm, and +13.5 mm for Group 1, Group 2, and Group 3, respectively (Table 3a). According to the measured bone level from the panoramic X-rays, the level of the bone was estimated for the three groups (Table 3b). The statistical method used in the study allowed the interposition of the
Fig. 2. Smooth scatter plots for the association between bone levels and time. The scale of 10–18 mm for the bone level was used to present the distance of the bone level to the reference point; i.e. the higher the value, the more resorption of the bone. From above: Group 1, Group 2, and Group 3.
F. Heinemann et al. / Annals of Anatomy 194 (2012) 508–512 Table 3b Mean bone level to the reference point over time of the three groups, adjusted for sex and age. Year
Group 1 (n = 7)
Group 2 (n = 8)
Group 3 (n = 11)
0 (baseline) 1 2 3
11.5 mm 11.4 mm 11.3 mm 11.2 mm
14.1 mm 14.6 mm 15.1 mm 15.5 mm
13.5 mm 13.8 mm 14.1 mm 14.4 mm
Table 4 P values of the three groups (26 patients, 26 teeth, 174 observations). P value Initial status Intercept (baseline for Group 3) Group 1 (vs. Group 3) Group 2 (vs. Group 3) Rate of change per year Intercept (change for Group 3) Group 1 (vs. change for Group 3) Group 2 (vs. change for Group 3) Group 1 (vs. change for Group 2)
<0.001 <0.001 0.24 <0.001 0.02 0.12 0.003
1 vs. Group 2 as well (P = 0.003), while the change per year was not significantly different for Group 2 vs. Group 3 (P = 0.122, Table 4). 4. Discussion Socket preservation procedures aim to graft the extraction sockets immediately after extraction. This serves to prevent alveolar ridge atrophy and maintain adequate bone dimensions which in turn facilitates implant placement in prosthetically driven positions or to maintain an acceptable ridge contour in areas of aesthetic concern. The use of collagenous xenografts helps to stabilise soft tissue contour. At reopening of the extraction site 8–10 weeks later, new bone is not expected to be found but more or less integrated small granules in a connective-tissue-like matrix. This tissue is usually removed during the preparation for implant placing in this region. The lost hard tissue of the deeper site of the drilling is substituted by grafting material. The large benefit then is the availability of a sufficient amount of soft tissue for stress-free socket closure and, consequently, their preservation. In this study, extraction sockets grafted with Bio-Oss Collagen with and without implant insertion were evaluated and compared to control sockets allowing for healing without further introductions. The change in bone level relative to a reference point was followed radiographically for the three groups. Heberer et al. (2011a,b) compared extraction sockets that were grafted with Bio-Oss Collagen and ungrafted extraction sites. They observed that the rate of new bone formation in ungrafted human extraction sockets was significantly higher when compared to sockets grafted with Bio-Oss Collagen after 12 weeks, and suggested a delay of bone formation in the grafted sites without signs of inflammation. Artzi et al. (2000) observed only slightly higher rates of bone in human extraction sockets filled with bovine bone mineral investigated after a healing period of 3 months than after a 6-week healing period. These results are in agreement with those obtained in this study. In the first 6–8 months from socket augmentation, 0.1 mm bone apposition was observed in Group 1 where implants were inserted after 8–10 months from the augmentation. Bone resorption of 0.5 mm and 0.3 mm were obtained for Group 2 and Group 3, respectively. After the first year and up to three years, further bone apposition was shown for Group 1 (0.2 mm), while bone resorption continued to be detected in Group 2 (0.9 mm) which was greater than that observed in the control group (0.6 mm, Fig. 2).
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Moreover, the rate of bone level change per year was significantly different for Group 1 vs. Group 3 (P = 0.019) and Group 1 vs. Group 2 as well (P = 0.003), while the change per year was not significantly different for Group 2 vs. Group 3 (P = 0.122, Table 4). According to the results of the present study, a healing period of 8–10 months after tooth extraction and socket augmentation can be used for implantation protocol. Long-term investigations of the change in the cervical alveolar bone around the implants are necessary to confirm our preliminary results. One of the limitations of the present study was the small group number. However, the primary results of this study can help for further study of Bio-Oss collagen as an augmentation material.
References Araújo, M.G., Lindhe, J., 2009. Ridge alterations following tooth extraction with and without flap elevation: an experimental study in the dog. Clin. Oral Implants Res. 20, 545–549. Araújo, M.G., Linder, E., Lindhe, J., 2011. Bio-Oss collagen in the buccal gap at immediate implants: a 6-month study in the dog. Clin. Oral Implants Res. 22, 1–8. Artzi, Z., Tal, H., Dayan, D., 2000. Porous bovine bone mineral in healing of human extraction sockets. Part 1: histomorphometric evaluations at 9 months. J. Periodontol. 71, 1015–1023. Artzi, Z., Tal, H., Dayan, D., 2001. Porous bovine bone mineral in healing of human extraction sockets: 2. Histochemical observations at 9 months. J. Periodontol. 72, 152–159. Artzi, Z., Nemcovsky, C.E., 1998. The application of deproteinized bovine bone mineral for ridge preservation prior to implantation. Clinical and histological observations in a case report. J. Periodontol. 69, 1062–1067. Atwood, D.A., Coy, W.A., 1971. Clinical, cephalometric, and densitometric study of reduction of residual ridges. J. Prosthet. Dent. 26, 280–295. Barone, A., Aldini, N.N., Fini, M., Giardino, R., Calvo Guirado, J.L., Covani, U., 2008. Xenograft versus extraction alone for ridge preservation after tooth removal: a clinical and histomorphometric study. J. Periodontol. 79, 1370–1377. Breithaupt-Faloppa, A.C., Kleinheinz, J., Crivello, O.J.R., 2006. Endothelial cell reaction on a biological material. J. Biomed. Mater. Res. B. Appl. Biomater. 76, 49–55. Carmagnola, D., Adriaens, P., Berglundh, T., 2003. Healing of human extraction sockets filled with Bio-Oss. Clin. Oral Implants Res. 14, 137–143. Fernandes, P.G., Novaes A.B. Jr., de Queiroz, A.C., de Souza, S.L., Taba M. Jr., Palioto, D.B., Grisi, M.F., 2011. Ridge preservation with acellular dermal matrix and anorganic bone matrix cell-binding peptide P-15 after tooth extraction in humans. J. Periodontol. 82, 72–79. Feuille, F., Knapp, C.I., Brunsvold, M.A., Mellonig, J.T., 2003. Clinical and histologic evaluation of bone replacement grafts in the treatment of localized alveolar ridge defects. Part 1: mineralized freeze-dried bone allograft. Int. J. Periodontics Restorative Dent. 23, 29–35. Froum, S., Cho, S.C., Rosenberg, E., Rohre, M., Tarnow, D., 2002. Histological comparison of healing extraction sockets implanted with bioactive glass or demineralized freeze-dried bone allograft: a pilot study. J. Periodontol. 73, 94–102. Hammerle, C.H., Chiantella, G.C., Karring, T., Lang, N.P., 1998. The effect of a deproteinized bovine bone mineral on bone regeneration around titanium dental implants. Clin. Oral Implants Res. 9, 151–162. Heberer, S., Al-Chawaf, B., Jablonski, C., Nelson, J.J., Lage, H., Nelson, K., 2011a. Healing of ungrafted and grafted extraction sockets after 12 weeks: a prospective clinical study. Int. J. Oral Maxillofac. Implants 26, 385–392. Heberer, S., Wustlich, A., Lage, H., Nelson, J.J., Nelson, K., 2011b. Osteogenic potential of mesenchymal cells embedded in the provisional matrix after a 6-week healing period in augmented and non-augmented extraction sockets: an immunohistochemical prospective pilot study in humans. Clin. Oral Implants Res. (Epub ahead of print). Iasella, J.M., Greenwell, H., Miller, R.L., Hill, M., Drisko, C., Bohra, A.A., Scheetz, J.P., 2003. Ridge preservation with freeze-dried bone allograft and a collagen membrane compared to extraction alone for implant site development: a clinical and histologic study in humans. J. Periodontol. 74, 990–999. Lekovic, V., Kenney, E.B., Weinlaender, M., Han, T., Klokkevold, P., Nedic, M., Orsini, M., 1997. A bone regenerative approach to alveolar ridge maintenance following tooth extraction. Report of 10 cases. J. Periodontol. 68, 563–570. Lekovic, V., Camargo, P.M., Klokkevold, P.R., Weinlaender, M., Kenney, E.B., Dimitrijevic, B., Nedic, M., 1998. Preservation of alveolar bone in extraction sockets using bioabsorbable membranes. J. Periodontol. 69, 1044–1049. Nevins, M., Camelo, M., De Paoli, S., Friedland, B., Schenk, R.K., Parma-Benfenati, S., Simion, M., Tinti, C., Wagenberg, B., 2006. A study of the fate of the buccal wall of extraction sockets of teeth with prominent roots. Int. J. Periodontics Restorative Dent. 26, 19–29.
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Seibert, J.S., 1993. Treatment of moderate localized alveolar ridge defects. Preventive and reconstructive concepts in therapy. Dent. Clin. North Am. 37, 265–280. Serino, G., Biancu, S., Iezzi, G., Piattelli, A., 2003. Ridge preservation following tooth extraction using a polylactide and polyglycolide sponge as space filler: a clinical and histological study in humans. Clin. Oral Implants Res. 14, 651–668.
Singer, J.D., Willett, J.B., 2003. Applied Longitudinal Data Analysis: Modeling Change and Event Occurrence. Oxford University Press, London. Twardowski, T., Fertala, A., Orgel, J.P., San Antonio, J.D., 2007. Type I collagen and collagen mimetics as angiogenesis promoting superpolymers. Curr. Pharm. 13, 3608–3621.
Contents lists available at SciVerse ScienceDirect
Annals of Anatomy journal homepage: www.elsevier.de/aanat
Bone level change of extraction sockets with Bio-Oss collagen and implant placement: A clinical study Friedhelm Heinemann a,∗,1, Istabrak. Hasan b,1, Christian Schwahn a, Christoph Bourauel b, Torsten Mundt a a b
Department of Prosthodontics, Gerodontology and Biomaterials, University of Greifswald, Rotgerberstr. 8, 17475 Greifswald, Germany Endowed Chair of Oral Technology, University of Bonn, Welschnonnenstr 17, 53111 Bonn, Germany
a r t i c l e
i n f o
Article history: Received 16 October 2011 Received in revised form 19 November 2011 Accepted 24 November 2011
Keywords: Bio-Oss collagen Socket preservation Alveolar bone Bone level change
a b s t r a c t Aims: To compare the reaction of the alveolar bone to the preservation of the extraction socket by BioOss Collagen with and without combination of implant treatment. To evaluate whether early implant insertion 8–10 weeks thereafter could be a suitable time point for long term bone stability around the implant. Methods: A total of 25 patients were divided into three groups: The first group (seven patients) received Bio-Oss Collagen after extraction and 8–10 weeks later an implant, the second group (eight patients) received only Bio-Oss Collagen without implantation thereafter, while the third group was considered as a control (eleven patients), where the sockets healed without any treatment. The change in the vertical bone level of the alveolar crests were measured from panoramic radiographs and statistically analysed. Results: Bone level change was significantly less for Group 1 than Group 3 (P < 0.001), while was not significantly different for Group 2 and Group 3 (P = 0.23). However, the rate of bone level change per year was statistically smaller for Group 1 compared to Group 3 (P = 0.019) and as well as for Group 1 than for Group 2 (P = 0.003), whereas the change per year was not significantly different for Group 2 vs. Group 3 (P = 0.122). Conclusion: Bone level preservation of extraction sockets using Bio-Oss Collagen with implantation is significantly better compared to using Bio-Oss Collagen only and untreated sockets. Implant insertion 8–10 weeks after extraction is a suitable time point after socket augmentation. © 2011 Elsevier GmbH. All rights reserved.
1. Introduction Alveolar bone resorption after tooth extraction is accelerated in the first 6 months after extraction and followed by a gradual remodelling that includes changes in size and shape. About 40% height and 60% width of alveolar bone is lost (Atwood and Coy, 1971; Araújo and Lindhe, 2009). The height and width reduction of the alveolar ridge complicates the implant placement thereafter, especially in the anterior maxilla, where bone volume is important for functional and aesthetic reasons (Seibert, 1993). Early extraction socket healing is expected to decrease the alveolar ridge by 2–4 mm horizontally and 1 mm vertically. This change is time dependent; by the end of the first year postextraction, nearly 6 mm of buccal loss can be expected (Lekovic et al., 1997, 1998; Iasella et al., 2003; Fernandes et al., 2011).
∗ Corresponding author at: Im Hainsfeld 29, 51597 Morsbach, Germany. Tel.: +49 2294992010. E-mail address: [email protected] (F. Heinemann). 1 First two authors claim for equal authorship. 0940-9602/$ – see front matter © 2011 Elsevier GmbH. All rights reserved. doi:10.1016/j.aanat.2011.11.012
Adequate volumes of alveolar bone are necessary to provide favourable aesthetic and successful long-term outcomes for dental implants. Therefore, in order to preserve the original ridge dimensions following tooth extraction and promote bone regeneration of the residual alveolar socket, various bone grafts and substitutes used in combination with or without barriers for guided tissue regeneration (GTR) have been suggested (Froum et al., 2002; Feuille et al., 2003; Iasella et al., 2003; Serino et al., 2003; Barone et al., 2008). Among these grafting materials, bovine bone mineral xenografts were able to promote bone regeneration and preserve the pre-extraction alveolar ridge dimensions when grafted in immediate extraction sockets, especially when combined with collagen (Artzi et al., 2000; Araújo and Lindhe, 2009; Carmagnola et al., 2003). The use of xenografts, especially bovine bone, has increased not only in ridge preservation, but also in other bone augmentation procedures. The important benefits of xenograft bone are a reduction in the drawbacks associated with autografts and their unlimited availability. Some studies have found that bovine bone grafted sites demonstrated good outcome and indicated this material could be a good bone substitute for bone augmentation before implant
F. Heinemann et al. / Annals of Anatomy 194 (2012) 508–512
509
Table 1 Inclusion and exclusion criteria of the patients. Patients inclusion criteria
Patients exclusion criteria
Patients with need for single tooth extraction and subsequent implant placement.
• Severe renal or liver disease. • History of radiotherapy in the head region. • Chemotherapy at the time of surgical procedure. • Non-compensated diabetes mellitus symptoms of maxillary sinus disease. • Pregnancy. • Active periodontal disease. • Poor oral hygiene.
installation (Hammerle et al., 1998; Artzi and Nemcovsky, 1998; Artzi et al., 2000). Furthermore, a randomised controlled clinical radiographic trial demonstrated that the postextraction alveolar ridge resorption was significantly reduced when the extraction sockets were grafted with a deproteinised bovine bone in comparison with the sockets that were left to heal without any grafting (Nevins et al., 2006). However, the disadvantages of the use of bovine bone include its slow resorption and healing with fibrous encapsulation (Artzi et al., 2000, 2001; Carmagnola et al., 2003) that leads to very protracted or even no remodelling in the central part of the augmented socket. As an alternative to socket preservation, collagen materials have shown proangiogenic qualities (Twardowski et al., 2007) and acceleration of ingrowth, proliferation and maturation of endothelial cells (Breithaupt-Faloppa et al., 2006) that encourage physiological bone regeneration. However, recent histological studies on a collagenous bovine bone matrix showed different results. While Araújo et al. (2011) reported an improved formation of new bone for sockets that were grafted with collagenous bovine bone matrix (Bio-Oss Collagen), the clinical study by Heberer et al. (2011a,b) reported smaller bone regeneration in grafted extraction sockets with Bio-Oss Collagen compared to the control extraction socket after 6–8 weeks of healing period. The aim of this study was to radiographically evaluate whether implant placement 8–10 weeks after socket augmentation with Bio-Oss Collagen is a proper time protocol concerning implant success and bone stability. 2. Materials and methods The present clinical study was performed according to principles outlined by the Declaration of Helsinki on experimentation involving human subjects and was approved by the University of Greifswald ethical committee (BB 13/11b). Patients requiring one tooth extraction in the maxillary anterior or premolar region were included in this study. A total of 26 patients were included, 16 females and 10 males. All were non-smokers and in good general health. Patients were enrolled in the study according to specific exclusion and inclusion criteria (Table 1). The patients were divided into three groups (Table 2): Group 1: In seven patients, the sockets were filled with Bio-Oss® Collagen (Geistlich Biomaterials, Baden-Baden, Germany) after tooth extraction and implants were inserted after a 8–10 weeks healing period. Group 2: In eight patients, the sockets were filled with Bio-Oss® Collagen after tooth extraction without implant treatment thereafter. Group 3: Eleven patients were selected as a control group in which the sockets were left to heal without further treatment.
Fig. 1. Reference points and measurement methods of the bone level for the three groups: (a) Group 1, Group 2, and (b) Group 3.
2.1. Treatment procedure For Group 1 and Group 2, the affected tooth was extracted using a flapless atraumatic technique. The socket was thoroughly curetted to remove granulation tissue and copiously irrigated with normal saline solution. The socket was then augmented with BioOss Collagen (Geistlich, Pharma AG, Wolhusen, Switzerland). No effort was made to extend the graft beyond the preexisting dimension of the socket. The marginal gingiva was then gently adapted and fixed with suture without total closure. A custom-made provisional fixed partial denture was cemented on the adjacent teeth. The provisional fixed partial denture included an ovate pontic to stabilise the graft and support buccal soft tissue. Oral hygiene at the surgical site was limited to soft brushing for the first 2 weeks. Regular brushing in the rest of the mouth and twice daily rinsing with 0.12% chlorhexidine was prescribed for 2 weeks. Patients were recalled weekly for monitoring within the first month. Group 1 underwent reopening after 8–10 weeks. The provisional fixed partial denture was removed and a re-entry procedure was performed. Preoperative antibiotic prophylaxis was carried out and a full-thickness flap was raised. An adequate implant in length and diameter (tioLogic© , Dentaurum Implants, Ispringen, Germany) was inserted. If necessary, missing sufficient local bone augmentation procedures and soft tissue management were performed according to standard protocols. The amount of the augmentation material was controlled. Single interrupted 5.0 monofilament sutures were used for flap adaptation in both groups. Ten to fourteen days later, the sutures were removed. Four to six months after implant placement, the definitive restorations were seated. 2.2. Bone level change measurement The change in the alveolar bone level in panoramic X-ray images was evaluated at different time intervals (length of observation period, Table 2). It was attempted to maintain an identical head position for each patient for the follow-up panoramic X-rays. A cephalostat device was used to hold the head within the same plane of occlusion. In all groups, the nearest (most mesial or most distal edge, respectively) of two neighbouring teeth were connected as a reference line. From this line, the bone level was measured at a 90◦ angle. For the X-rays of Group 1, the bone level around the implants to the reference line was measured mesially and distally (Fig. 1a). For X-rays of Group 2 and Group 3, corresponding bone levels were measured 2 mm mesial and 2 mm distal to the middle of the
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Table 2 Baseline characteristics.
Male Age at baseline, mean ± SD Length of observation period Mean ± SD Min–Max Baseline bone level, mean ± SE Non-smoking patients
Group 1 (n = 7)
Group 2 (n = 8)
Group 3 (n = 11)
Total (n = 26)
3 53.8 ± 11.9
4 55.3 ± 12.5
3 52.1 ± 10.2
10 53.5 ± 11.0
1.5 ± 1.0 0.6–3.4 11.8 ± 0.4 7
2.4 ± 1.6 0.6–4.7 13.9 ± 0.5 8
4.9 ± 3.1 0.3–10.9 12.8 ± 0.3 11
3.2 ± 2.7 0.3–10.9 12.8 ± 0.3 26
For clustered observations, SE = standard error instead of SD = standard deviation is given.
Table 3a Linear combinations (95% CI) for the initial status and the rate of change in the groups, adjusted for sex and age.
Baseline bone level Rate of change per year
Group 1 (n = 7)
Group 2 (n = 7)
Group 3 (n = 7)
11.5 (10.8–12.3) 0.292 + −0.411 = −0.119 (−0.449–0.211)
14.1 (13.3–14.8) 0.292 + 0.189 = 0.481 (0.262–0.700)
13.5 (12.9–14.1) 0.292 (reference) = 0.292 (0.194–0.390)
neighbouring teeth. The measurements were performed at a 90◦ angle to the same reference line (Fig. 1b). 2.2.1. Statistical analysis The change in bone levels over time was estimated with linear mixed models. Mixed models use all available data, properly accounting for correlation between repeated measurements in patients, in teeth, and in sites and appropriately handle missing data if it meets random (MAR) assumption. The change in bone levels was fitted by a linear slope model as described in “Applied Longitudinal Data Analysis” (ALDA, Singer and Willett, 2003). To estimate the initial status, the final model included sex (reference: female), age at baseline, the intercept (baseline value), and group (reference: Group 3, Table 2). To estimate the rate of change, the final model included the intercept (continuous time [years]) and the interaction between the intercept (continuous time) and group as fixed effects, and continuous time and the intercept as random effects or variance components. For the variance components an unstructured error covariance matrix was assumed on patient level (which herein corresponds to the tooth level). By centring, the intercept of the initial status can directly be interpreted as the baseline value for the reference category (Group 3) in females (reference category for sex) aged 53.6 years. The intercept for the rate of change (continuous time) can directly be interpreted as the rate of change in the reference group. Analyses were performed with STATA/MP software, version 10.1 (StataCorp LP, College Station, Texas, USA). For the computation of linear mixed models, we used the “xtmixed” procedure. Furthermore, smoothed scatter plots were used to show the relationships between bone levels and time in more detail (Fig. 2). The smoothing was generated with the STATA procedure lowess. For the amount of smoothing we chose a bandwidth = 0.8, meaning that 80% of the data are used in smoothing each point. Note that the smoothing procedure assumes independent observations. The three groups differ in the length of the observation period, which is reflected in the corresponding smoothing figures.
data for bone level changes per year. A significant difference was observed between Group 1 and Group 3 (P < 0.001), while no significant difference was observed between Group 2 and Group 3 (P = 0.23). However, the rate of bone level change per year was statistically significant for Group 1 vs. Group 3 (P = 0.019) and Group
3. Results 3.1. Bone level change The baseline bone level according to the measurement protocol of this study was +11.5 mm, +14.1 mm, and +13.5 mm for Group 1, Group 2, and Group 3, respectively (Table 3a). According to the measured bone level from the panoramic X-rays, the level of the bone was estimated for the three groups (Table 3b). The statistical method used in the study allowed the interposition of the
Fig. 2. Smooth scatter plots for the association between bone levels and time. The scale of 10–18 mm for the bone level was used to present the distance of the bone level to the reference point; i.e. the higher the value, the more resorption of the bone. From above: Group 1, Group 2, and Group 3.
F. Heinemann et al. / Annals of Anatomy 194 (2012) 508–512 Table 3b Mean bone level to the reference point over time of the three groups, adjusted for sex and age. Year
Group 1 (n = 7)
Group 2 (n = 8)
Group 3 (n = 11)
0 (baseline) 1 2 3
11.5 mm 11.4 mm 11.3 mm 11.2 mm
14.1 mm 14.6 mm 15.1 mm 15.5 mm
13.5 mm 13.8 mm 14.1 mm 14.4 mm
Table 4 P values of the three groups (26 patients, 26 teeth, 174 observations). P value Initial status Intercept (baseline for Group 3) Group 1 (vs. Group 3) Group 2 (vs. Group 3) Rate of change per year Intercept (change for Group 3) Group 1 (vs. change for Group 3) Group 2 (vs. change for Group 3) Group 1 (vs. change for Group 2)
<0.001 <0.001 0.24 <0.001 0.02 0.12 0.003
1 vs. Group 2 as well (P = 0.003), while the change per year was not significantly different for Group 2 vs. Group 3 (P = 0.122, Table 4). 4. Discussion Socket preservation procedures aim to graft the extraction sockets immediately after extraction. This serves to prevent alveolar ridge atrophy and maintain adequate bone dimensions which in turn facilitates implant placement in prosthetically driven positions or to maintain an acceptable ridge contour in areas of aesthetic concern. The use of collagenous xenografts helps to stabilise soft tissue contour. At reopening of the extraction site 8–10 weeks later, new bone is not expected to be found but more or less integrated small granules in a connective-tissue-like matrix. This tissue is usually removed during the preparation for implant placing in this region. The lost hard tissue of the deeper site of the drilling is substituted by grafting material. The large benefit then is the availability of a sufficient amount of soft tissue for stress-free socket closure and, consequently, their preservation. In this study, extraction sockets grafted with Bio-Oss Collagen with and without implant insertion were evaluated and compared to control sockets allowing for healing without further introductions. The change in bone level relative to a reference point was followed radiographically for the three groups. Heberer et al. (2011a,b) compared extraction sockets that were grafted with Bio-Oss Collagen and ungrafted extraction sites. They observed that the rate of new bone formation in ungrafted human extraction sockets was significantly higher when compared to sockets grafted with Bio-Oss Collagen after 12 weeks, and suggested a delay of bone formation in the grafted sites without signs of inflammation. Artzi et al. (2000) observed only slightly higher rates of bone in human extraction sockets filled with bovine bone mineral investigated after a healing period of 3 months than after a 6-week healing period. These results are in agreement with those obtained in this study. In the first 6–8 months from socket augmentation, 0.1 mm bone apposition was observed in Group 1 where implants were inserted after 8–10 months from the augmentation. Bone resorption of 0.5 mm and 0.3 mm were obtained for Group 2 and Group 3, respectively. After the first year and up to three years, further bone apposition was shown for Group 1 (0.2 mm), while bone resorption continued to be detected in Group 2 (0.9 mm) which was greater than that observed in the control group (0.6 mm, Fig. 2).
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Moreover, the rate of bone level change per year was significantly different for Group 1 vs. Group 3 (P = 0.019) and Group 1 vs. Group 2 as well (P = 0.003), while the change per year was not significantly different for Group 2 vs. Group 3 (P = 0.122, Table 4). According to the results of the present study, a healing period of 8–10 months after tooth extraction and socket augmentation can be used for implantation protocol. Long-term investigations of the change in the cervical alveolar bone around the implants are necessary to confirm our preliminary results. One of the limitations of the present study was the small group number. However, the primary results of this study can help for further study of Bio-Oss collagen as an augmentation material.
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