Titanium Granules for Augmentation of the Maxillary Sinus – A Multicenter Study Ståle Petter Lyngstadaas, DDS, PhD;* Anders Verket, DDS;* Else Marie Pinholt, DDS, PhD;† Christian Mertens, DDS, PhD;‡ Hans Reidar Haanæs, MD, DDS, PhD;§ Gert Wall, DDS, PhD;¶ Mats Wallström, DDS, PhD;** Lars Rasmusson, MD, DDS, PhD**
ABSTRACT Background: Biomaterials are commonly used to augment the maxillary sinus floor prior to or in conjunction with dental implant installation. Recently, porous titanium granules (PTGs) have been used in oral implant surgery to stabilize implants and function as an osteoconductive matrix. Purpose: To evaluate if PTGs can be safely used in a larger population of patients, treated by different surgeons, when sinus floor augmentation was required in conjunction with implant installation. The primary endpoint was 12-month survival rate of the dental implants. Biopsies for histology were taken from the augmented area. Materials and Methods: At five centers, 40 subjects with uni or bilateral posterior edentulism and atrophy of the posterior maxilla (3–6 mm) were enrolled. In a single-stage procedure, PTG and one to three dental implants were installed in each quadrant. In total, 70 implants were included in the study. Results: One immobile implant was removed. The mean marginal bone loss was 0.5 mm and 0.8 mm, on the mesial and distal side, respectively. Histologically, all biopsies demonstrated bone ingrowth. Conclusions: The results suggest that PTG can be safely and effectively used as augmentation material in the sinus floor when used with dental implants in a one-stage procedure. KEY WORDS: biomaterials, bone augmentation, implant survival, maxillary sinus floor elevation
short implants in the posterior maxilla.1–3 There is certainly a need for bone augmentation of the sinus floor if the residual bone height reaches 4 to 5 mm or lower. Different materials have been used with similar outcome for the long-term implant survival rate.4,5 Elevation of the sinus mucosa without any supporting graft has also been evaluated with good clinical outcome,6,7 but this is a more technique-sensitive method. Autologous bone grafts have for long been considered the gold standard for bone augmentation but have disadvantages such as donor site morbidity and the well-known graft resorption.8 Most bone substitutes are to the authors’ knowledge based on hydroxyapatite, which is stable over time or resorbs slowly. A material that is absolutely resistant to resorption, inert, and have good clotting properties is titanium.9 In a proof of concept study, titanium granules were used to augment the sinus floor of 16 patients.10 Both one- and two-stage protocols were used. Three implants (13%) were found mobile and removed during the follow-up period of 12 to 36 months. Two of these three implants
INTRODUCTION Bone graft substitutes are commonly used for augmentation of the maxillary sinus prior to or in conjunction with implant placement. Limitations for the vertical dimensions of the residual bone are not yet fully known, and the literature is inconsistent with regard to the use of *Department of Biomaterials, Faculty of Dentistry, University of Oslo, Oslo, Norway; †Department of Oral and Maxillofacial Surgery, Institute of Odontology, University of Copenhagen, Copenhagen, Denmark; ‡Department of Oral and Maxillofacial Surgery, University Hospital Heidelberg, Heidelberg, Germany; §Department of Oral Surgery and Oral Medicine, Faculty of Dentistry, University of Oslo, Oslo, Norway; ¶Department of Oral and Maxillofacial Surgery, University Hospital Lund, Lund, Sweden; **Department of Oral and Maxillofacial Surgery, The Sahlgrenska Academy, University of Gothenburg, Göteborg, Sweden Corresponding Author: Prof. Lars Rasmusson, Department of Oral and Maxillofacial Surgery, The Sahlgrenska Academy, University of Gothenburg, Box 450, 405 30 Göteborg, Sweden; e-mail: [email protected] © 2015 Wiley Periodicals, Inc. DOI 10.1111/cid.12291
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Titanium Granules for Maxillary Sinus Augmentation
were in the two-stage group. The authors concluded that the material was safe and easy to handle, and observed no radiological signs of migration of the granules. The objective of this prospective multicenter case series was to evaluate if porous titanium granules (PTG) can be safely used in a larger population of patients, treated by different clinicians, when sinus floor augmentation was required in conjunction with implant installation. The primary endpoint was 12-month survival rate of the dental implants. Biopsies for histology were taken from the augmented area for evaluation of possible bone formation around and/or inside the titanium granules. MATERIALS AND METHODS Study Design and Patients In this open prospective multicenter study, a total of 40 patients were included (14 men and 26 women). The mean age was 61 years (range 41–86 years). Main inclusion criteria were uni or bilateral posterior maxillary edentulism and atrophy of the posterior maxillary alveolar process with a residual bone height below the sinus floor between 3 and 6 mm. Exclusion criteria were 3.5 mm. The mean follow-up time for the 37 subjects in the marginal bone loss analysis was 19.7 months (19.4 months) with a range of 12 to 42 months. Sinus Augmentation Height The vertical augmentation with PTG ranged from 3.5 to 11.5 mm, with a mean vertical augmentation of 6.5 mm (12.1 mm). The mean follow-up time was 28 months (19.6 months) with a range of 12 to 42 months. A change in the vertical augmentation was observed in seven out of the 17 analyzed subjects (Table 1). In several subjects, corresponding to those with an observed vertical augmentation change, a condensation
of granules could be observed from the one time point to the other. In particular, this was evident if single or small clusters of PTG were initially located above the principal graft body. These granules were typically observed to be better incorporated with the main graft body at later examinations. Histology In the previous interim study, 18 biopsy specimens retrieved from 17 patients were presented.11 Four additional biopsies were retrieved from four patients. The mean area occupied by new bone and PTG in these four biopsies was 18.9% (17.7 standard deviation [SD]) and 30.7% (11.6 SD), respectively. The area of new bone per specimen ranged from 14.2% to 30.1%. The total mean area occupied by new bone and PTG in all 22 biopsies, representing a total of 21 patients, was 16.6% (19 SD) and 26.8% (15.8 SD), respectively. The new bone was predominantly woven bone. New bone was observed both within and between the PTG (Figure 3) and demonstrated a pattern similar to that of trabecular bone. PTGs located distant from the residual bone were for the most part not surrounded by bone (see Figure 3). The explanted implant with surrounding tissues was subjected to histology. In this specimen, PTGs
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Clinical Implant Dentistry and Related Research, Volume 17, Supplement 2, 2015
Figure 3 Photomicrograph of a histologic section from a biopsy specimen. New bone formation is evident in the grafted area and can be observed both between and within the porous titanium granules (PTG). Bone formation is scarce in the area remote of the original sinus floor.
implants installed in residual bone of 7 to 9 mm and only 29% if the remaining bone height below the sinus floor was 3 mm. The reason behind this was most likely related to lower primary stability of the implant when small amounts of bone remained. Primary stability has been shown to be a determinant factor for implant survival.14 As the implants were installed together with the PTG, one may speculate that the bone substitute supported the implants mechanically already from the start. The survival rate of the implants in the present study, 98.6%, is similar or better compared with previous studies,5,15,16 and there were only few complications related to the augmentation procedure. The number of surgeons involved in the present multicenter study did not seem to influence the consistency of the outcomes, indicating that PTG may be an easy-to-handle material. Rasmusson and colleagues12 reported marginal bone loss of 0.28 mm on TiOblast™ implants after 1 year of loading. Importantly, these implants were not placed in conjunction with sinus augmentation but in pristine bone in both the maxilla and the mandible. The marginal bone loss reported in the present study is more in line with that recently reported by Galindo-Moreno and colleagues17 These authors reported on Astra Tech™ internal connection implants placed in maxillary sinuses grafted with a combination
were visible on both sides of the implant at a level corresponding to the mid-length of the implant and further apically (Figure 4). Apart from the marginal microthreaded portion, the implant was osseointegrated, also at the level corresponding to the grafted area. DISCUSSION The clinical and histomorphometric results from the present study indicate that PTGs can be used as grafting material in the sinus floor simultaneously with implant placement in the edentulous posterior maxilla. The indication for maxillary sinus floor augmentation is of major importance for the clinical outcome. It is suggested that the role of the augmented area for support of the implant becomes more important with reduced height of the residual bone (i.e., the sinus floor). Jensen and Greer13 reported a 100% survival rate for
Figure 4 Photomicrographs of histologic sections from the explanted implant specimen. Porous titanium granules (PTGs) were observed on both sides of the implant. Bone has formed throughout the extent of the implant but is missing in the marginal microthreaded region.
Titanium Granules for Maxillary Sinus Augmentation
of autologous bone and deproteinized bovine bone mineral. A mesial and distal marginal bone loss of 0.47 and 0.54 mm, respectively, was reported 6 months after loading, which corresponds to the follow-up time in the present study. To the best of the authors’ knowledge, this is the first study to evaluate vertical sinus augmentation changes over time for a graft material absolutely resistant to resorption. Previous studies have attributed a change in sinus augmentation height to graft material resorption.18,19 Despite the inherent nonresorptive property of PTG, a reduction in the vertical augmentation was observed for seven subjects. The reduction may be explained by methodological errors, but one may speculate that gravitational and masticatory forces and head movement over time may in fact condensate a graft. However, this must be addressed in future studies. The histomorphometric results obtained from the additional biopsies corresponded to what was reported in the interim study.11 The healing time and the methodologies applied were the same. The histology from the explanted implant demonstrated that the bone formed in the grafted compartment was further capable of implant osseointegration. The mean area of the total grafted area occupied by new mineralized bone in all 22 biopsies, 16.6%, is comparable with what has been reported for other bone graft substitutes in similar healing time. Yildirim and colleagues augmented the maxillary sinus with deproteinized bovine bone mineral mixed with either venous blood20 or autologous bone,21 and reported 14.7% and 18.9% new bone, respectively, after 7 months of healing. Zerbo and colleagues22 reported 17% new bone after 6 months healing using biphasic calcium phosphate for sinus augmentation. A limitation of this study was the use of both orthopantomograms and intraoral radiographs, either digital or analogous. With five centers included, it was not possible to obtain radiographs at standardized conditions. In order to reduce the impact of the radiographic diversity, a single time point only was included in the marginal bone loss analysis. Therefore, the assumption that all implants were installed with the implant neck flush with the margin of the alveolar bone was made, which limits the interpretation of the results, as implants may have been placed either supra or subcrestally.
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CONCLUSIONS Studies of longer observation time and a randomized controlled study is warranted in the future to further assess the significance of PTG as a bone substitute material for sinus augmentation in conjunction with implant placement. The results from the present study suggest that PTG can be effectively used as augmentation material in the sinus floor when used with dental implants in a onestage procedure. ACKNOWLEDGEMENTS Professor Ståle Petter Lyngstadaas is a scientific advisor and board member of Tigran AB. PTG for this study was generously provided by Tigran AB. The implants were kindly provided by Dentsply Implants. The authors appreciate the assistance for clinical monitoring from Ulf Lundgren and Eva Lundberg at Tigran AB. REFERENCES 1. Ferrigno N, Laureti M, Fanali S. Dental implants placement in conjunction with osteotome sinus floor elevation: a 12-year life-table analysis from a prospective study on 588 ITI implants. Clin Oral Implants Res 2006; 17:194–205. 2. Esposito M, Grusovin MG, Rees J, et al. Effectiveness of sinus lift procedures for dental implant rehabilitation: a Cochrane systematic review. Eur J Oral Implantol 2010; 3:7–26. 3. Del Fabbro M, Corbella S, Weinstein T, et al. Implant survival rates after osteotome-mediated maxillary sinus augmentation: a systematic review. Clin Implant Dent Relat Res 2012; 14:e159–e168. 4. Scarano A, Degidi M, Iezzi G, et al. Maxillary sinus augmentation with different biomaterials: a comparative histologic and histomorphometric study in man. Implant Dent 2006; 15:197–207. 5. Aghaloo TL, Moy PK. Which hard tissue augmentation techniques are the most successful in furnishing bony support for implant placement? Int J Oral Maxillofac Implants 2007; 22:49–70. 6. Lundgren S, Andersson S, Gualini F, et al. Bone reformation with sinus membrane elevation: a new surgical technique for maxillary sinus floor augmentation. Clin Implant Dent Relat Res 2004; 6:165–173. 7. Thor A, Sennerby L, Hirsch JM, et al. Bone formation at the maxillary sinus floor following simultaneous elevation of the mucosal lining and implant installation without graft material: an evaluation of 20 patients treated with 44 Astra Tech implants. J Oral Maxillofac Surg 2007; 65:64–72. 8. Dasmah A, Thor A, Ekestubbe A, et al. Particulate vs. block bone grafts: three-dimensional changes in graft volume after
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reconstruction of the atrophic maxilla, a 2-year radiographic follow-up. J Craniomaxillofac Surg 2012; 40:654–659. Hong J, Andersson J, Ekdahl KN, et al. Titanium is a highly thrombogenic biomaterial: possible implications for osteogenesis. Thromb Haemost 1999; 82:58–64. Bystedt H, Rasmusson L. Porous titanium granules used as osteoconductive material for sinus floor augmentation: a clinical pilot study. Clin Implant Dent Relat Res 2009; 11:101–105. Verket A, Lyngstadaas SP, Rasmusson L, et al. Maxillary sinus augmentation with porous titanium granules: a microcomputed tomography and histologic evaluation of human biopsy specimens. Int J Oral Maxillofac Implants 2013; 28:721–728. Rasmusson L, Roos J, Bystedt H. A 10-year follow-up study of titanium dioxide-blasted implants. Clin Implant Dent Relat Res 2005; 7:36–42. Jensen OT, Greer R. Immediate placing of osseointegrating implants into the sinus cavity augmented with mineralized cancellous allograft and Goretex: second-stage surgical and histological findings. In: Laney WR, Tolman DW, eds. Tissue integration in oral orthopedic and maxillofacial reconstruction. Chicago: Quintessence, 1992:321–333. Friberg B, Jemt T, Lekholm U. Early failures in 4641 consecutively placed Brånemark dental implants. Int J Oral Maxillofac Implants 1991; 6:142–146. Blomquist JE, Alberius P, Isaksson S. Two-stage maxillary sinus reconstruction with endosseous implants: a prospective study. Int J Oral Maxillofac Implants 1998; 13:758–766.
16. Del Fabbro M, Testori T, Francetti L, et al. Systematic review of survival for implants placed in the grafted maxillary sinus. Int J Periodontics Restorative Dent 2004; 24:565–577. 17. Galindo-Moreno P, Fernández-Jiménez A, O’Valle F, et al. Marginal bone loss in implants placed in grafted maxillary sinus. Clin Implant Dent Relat Res 2015; 17(2):373–383. 18. Maiorana C, Sigurtà D, Mirandola A, et al. Sinus elevation with alloplasts or xenogenic materials and implants: an up to-to-4-year clinical and radiological follow-up. Int J Oral Maxillofac Implants 2006; 21:426–432. 19. Schmitt C, Karasholi T, Lutz R, et al. Long-term changes in graft height after maxillary sinus augmentation, onlay bone grafting, and combination of both techniques: a long-term retrospective cohort study. Clin Oral Implants Res 2014; 25:e38–e46. 20. Yildirim M, Spiekermann H, Biesterfeld S, et al. Maxillary sinus augmentation using xenogenic bone substitute material Bio-Oss in combination with venous blood. A histologic and histomorphometric study in humans. Clin Oral Implants Res 2000; 11:217–229. 21. Yildirim M, Spiekermann H, Handt S, et al. Maxillary sinus augmentation with the xenograft Bio-Oss and autogenous intraoral bone for qualitative improvement of the implant site: a histologic and histomorphometric clinical study in humans. Int J Oral Maxillofac Implants 2001; 16:23–33. 22. Zerbo IR, Zijderveld SA, de Boer A, et al. Histomorphometry of human sinus floor augmentation using a porous betatricalcium phosphate: a prospective study. Clin Oral Implants Res 2004; 15:724–732.
ABSTRACT Background: Biomaterials are commonly used to augment the maxillary sinus floor prior to or in conjunction with dental implant installation. Recently, porous titanium granules (PTGs) have been used in oral implant surgery to stabilize implants and function as an osteoconductive matrix. Purpose: To evaluate if PTGs can be safely used in a larger population of patients, treated by different surgeons, when sinus floor augmentation was required in conjunction with implant installation. The primary endpoint was 12-month survival rate of the dental implants. Biopsies for histology were taken from the augmented area. Materials and Methods: At five centers, 40 subjects with uni or bilateral posterior edentulism and atrophy of the posterior maxilla (3–6 mm) were enrolled. In a single-stage procedure, PTG and one to three dental implants were installed in each quadrant. In total, 70 implants were included in the study. Results: One immobile implant was removed. The mean marginal bone loss was 0.5 mm and 0.8 mm, on the mesial and distal side, respectively. Histologically, all biopsies demonstrated bone ingrowth. Conclusions: The results suggest that PTG can be safely and effectively used as augmentation material in the sinus floor when used with dental implants in a one-stage procedure. KEY WORDS: biomaterials, bone augmentation, implant survival, maxillary sinus floor elevation
short implants in the posterior maxilla.1–3 There is certainly a need for bone augmentation of the sinus floor if the residual bone height reaches 4 to 5 mm or lower. Different materials have been used with similar outcome for the long-term implant survival rate.4,5 Elevation of the sinus mucosa without any supporting graft has also been evaluated with good clinical outcome,6,7 but this is a more technique-sensitive method. Autologous bone grafts have for long been considered the gold standard for bone augmentation but have disadvantages such as donor site morbidity and the well-known graft resorption.8 Most bone substitutes are to the authors’ knowledge based on hydroxyapatite, which is stable over time or resorbs slowly. A material that is absolutely resistant to resorption, inert, and have good clotting properties is titanium.9 In a proof of concept study, titanium granules were used to augment the sinus floor of 16 patients.10 Both one- and two-stage protocols were used. Three implants (13%) were found mobile and removed during the follow-up period of 12 to 36 months. Two of these three implants
INTRODUCTION Bone graft substitutes are commonly used for augmentation of the maxillary sinus prior to or in conjunction with implant placement. Limitations for the vertical dimensions of the residual bone are not yet fully known, and the literature is inconsistent with regard to the use of *Department of Biomaterials, Faculty of Dentistry, University of Oslo, Oslo, Norway; †Department of Oral and Maxillofacial Surgery, Institute of Odontology, University of Copenhagen, Copenhagen, Denmark; ‡Department of Oral and Maxillofacial Surgery, University Hospital Heidelberg, Heidelberg, Germany; §Department of Oral Surgery and Oral Medicine, Faculty of Dentistry, University of Oslo, Oslo, Norway; ¶Department of Oral and Maxillofacial Surgery, University Hospital Lund, Lund, Sweden; **Department of Oral and Maxillofacial Surgery, The Sahlgrenska Academy, University of Gothenburg, Göteborg, Sweden Corresponding Author: Prof. Lars Rasmusson, Department of Oral and Maxillofacial Surgery, The Sahlgrenska Academy, University of Gothenburg, Box 450, 405 30 Göteborg, Sweden; e-mail: [email protected] © 2015 Wiley Periodicals, Inc. DOI 10.1111/cid.12291
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Titanium Granules for Maxillary Sinus Augmentation
were in the two-stage group. The authors concluded that the material was safe and easy to handle, and observed no radiological signs of migration of the granules. The objective of this prospective multicenter case series was to evaluate if porous titanium granules (PTG) can be safely used in a larger population of patients, treated by different clinicians, when sinus floor augmentation was required in conjunction with implant installation. The primary endpoint was 12-month survival rate of the dental implants. Biopsies for histology were taken from the augmented area for evaluation of possible bone formation around and/or inside the titanium granules. MATERIALS AND METHODS Study Design and Patients In this open prospective multicenter study, a total of 40 patients were included (14 men and 26 women). The mean age was 61 years (range 41–86 years). Main inclusion criteria were uni or bilateral posterior maxillary edentulism and atrophy of the posterior maxillary alveolar process with a residual bone height below the sinus floor between 3 and 6 mm. Exclusion criteria were 3.5 mm. The mean follow-up time for the 37 subjects in the marginal bone loss analysis was 19.7 months (19.4 months) with a range of 12 to 42 months. Sinus Augmentation Height The vertical augmentation with PTG ranged from 3.5 to 11.5 mm, with a mean vertical augmentation of 6.5 mm (12.1 mm). The mean follow-up time was 28 months (19.6 months) with a range of 12 to 42 months. A change in the vertical augmentation was observed in seven out of the 17 analyzed subjects (Table 1). In several subjects, corresponding to those with an observed vertical augmentation change, a condensation
of granules could be observed from the one time point to the other. In particular, this was evident if single or small clusters of PTG were initially located above the principal graft body. These granules were typically observed to be better incorporated with the main graft body at later examinations. Histology In the previous interim study, 18 biopsy specimens retrieved from 17 patients were presented.11 Four additional biopsies were retrieved from four patients. The mean area occupied by new bone and PTG in these four biopsies was 18.9% (17.7 standard deviation [SD]) and 30.7% (11.6 SD), respectively. The area of new bone per specimen ranged from 14.2% to 30.1%. The total mean area occupied by new bone and PTG in all 22 biopsies, representing a total of 21 patients, was 16.6% (19 SD) and 26.8% (15.8 SD), respectively. The new bone was predominantly woven bone. New bone was observed both within and between the PTG (Figure 3) and demonstrated a pattern similar to that of trabecular bone. PTGs located distant from the residual bone were for the most part not surrounded by bone (see Figure 3). The explanted implant with surrounding tissues was subjected to histology. In this specimen, PTGs
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Figure 3 Photomicrograph of a histologic section from a biopsy specimen. New bone formation is evident in the grafted area and can be observed both between and within the porous titanium granules (PTG). Bone formation is scarce in the area remote of the original sinus floor.
implants installed in residual bone of 7 to 9 mm and only 29% if the remaining bone height below the sinus floor was 3 mm. The reason behind this was most likely related to lower primary stability of the implant when small amounts of bone remained. Primary stability has been shown to be a determinant factor for implant survival.14 As the implants were installed together with the PTG, one may speculate that the bone substitute supported the implants mechanically already from the start. The survival rate of the implants in the present study, 98.6%, is similar or better compared with previous studies,5,15,16 and there were only few complications related to the augmentation procedure. The number of surgeons involved in the present multicenter study did not seem to influence the consistency of the outcomes, indicating that PTG may be an easy-to-handle material. Rasmusson and colleagues12 reported marginal bone loss of 0.28 mm on TiOblast™ implants after 1 year of loading. Importantly, these implants were not placed in conjunction with sinus augmentation but in pristine bone in both the maxilla and the mandible. The marginal bone loss reported in the present study is more in line with that recently reported by Galindo-Moreno and colleagues17 These authors reported on Astra Tech™ internal connection implants placed in maxillary sinuses grafted with a combination
were visible on both sides of the implant at a level corresponding to the mid-length of the implant and further apically (Figure 4). Apart from the marginal microthreaded portion, the implant was osseointegrated, also at the level corresponding to the grafted area. DISCUSSION The clinical and histomorphometric results from the present study indicate that PTGs can be used as grafting material in the sinus floor simultaneously with implant placement in the edentulous posterior maxilla. The indication for maxillary sinus floor augmentation is of major importance for the clinical outcome. It is suggested that the role of the augmented area for support of the implant becomes more important with reduced height of the residual bone (i.e., the sinus floor). Jensen and Greer13 reported a 100% survival rate for
Figure 4 Photomicrographs of histologic sections from the explanted implant specimen. Porous titanium granules (PTGs) were observed on both sides of the implant. Bone has formed throughout the extent of the implant but is missing in the marginal microthreaded region.
Titanium Granules for Maxillary Sinus Augmentation
of autologous bone and deproteinized bovine bone mineral. A mesial and distal marginal bone loss of 0.47 and 0.54 mm, respectively, was reported 6 months after loading, which corresponds to the follow-up time in the present study. To the best of the authors’ knowledge, this is the first study to evaluate vertical sinus augmentation changes over time for a graft material absolutely resistant to resorption. Previous studies have attributed a change in sinus augmentation height to graft material resorption.18,19 Despite the inherent nonresorptive property of PTG, a reduction in the vertical augmentation was observed for seven subjects. The reduction may be explained by methodological errors, but one may speculate that gravitational and masticatory forces and head movement over time may in fact condensate a graft. However, this must be addressed in future studies. The histomorphometric results obtained from the additional biopsies corresponded to what was reported in the interim study.11 The healing time and the methodologies applied were the same. The histology from the explanted implant demonstrated that the bone formed in the grafted compartment was further capable of implant osseointegration. The mean area of the total grafted area occupied by new mineralized bone in all 22 biopsies, 16.6%, is comparable with what has been reported for other bone graft substitutes in similar healing time. Yildirim and colleagues augmented the maxillary sinus with deproteinized bovine bone mineral mixed with either venous blood20 or autologous bone,21 and reported 14.7% and 18.9% new bone, respectively, after 7 months of healing. Zerbo and colleagues22 reported 17% new bone after 6 months healing using biphasic calcium phosphate for sinus augmentation. A limitation of this study was the use of both orthopantomograms and intraoral radiographs, either digital or analogous. With five centers included, it was not possible to obtain radiographs at standardized conditions. In order to reduce the impact of the radiographic diversity, a single time point only was included in the marginal bone loss analysis. Therefore, the assumption that all implants were installed with the implant neck flush with the margin of the alveolar bone was made, which limits the interpretation of the results, as implants may have been placed either supra or subcrestally.
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CONCLUSIONS Studies of longer observation time and a randomized controlled study is warranted in the future to further assess the significance of PTG as a bone substitute material for sinus augmentation in conjunction with implant placement. The results from the present study suggest that PTG can be effectively used as augmentation material in the sinus floor when used with dental implants in a onestage procedure. ACKNOWLEDGEMENTS Professor Ståle Petter Lyngstadaas is a scientific advisor and board member of Tigran AB. PTG for this study was generously provided by Tigran AB. The implants were kindly provided by Dentsply Implants. The authors appreciate the assistance for clinical monitoring from Ulf Lundgren and Eva Lundberg at Tigran AB. REFERENCES 1. Ferrigno N, Laureti M, Fanali S. Dental implants placement in conjunction with osteotome sinus floor elevation: a 12-year life-table analysis from a prospective study on 588 ITI implants. Clin Oral Implants Res 2006; 17:194–205. 2. Esposito M, Grusovin MG, Rees J, et al. Effectiveness of sinus lift procedures for dental implant rehabilitation: a Cochrane systematic review. Eur J Oral Implantol 2010; 3:7–26. 3. Del Fabbro M, Corbella S, Weinstein T, et al. Implant survival rates after osteotome-mediated maxillary sinus augmentation: a systematic review. Clin Implant Dent Relat Res 2012; 14:e159–e168. 4. Scarano A, Degidi M, Iezzi G, et al. Maxillary sinus augmentation with different biomaterials: a comparative histologic and histomorphometric study in man. Implant Dent 2006; 15:197–207. 5. Aghaloo TL, Moy PK. Which hard tissue augmentation techniques are the most successful in furnishing bony support for implant placement? Int J Oral Maxillofac Implants 2007; 22:49–70. 6. Lundgren S, Andersson S, Gualini F, et al. Bone reformation with sinus membrane elevation: a new surgical technique for maxillary sinus floor augmentation. Clin Implant Dent Relat Res 2004; 6:165–173. 7. Thor A, Sennerby L, Hirsch JM, et al. Bone formation at the maxillary sinus floor following simultaneous elevation of the mucosal lining and implant installation without graft material: an evaluation of 20 patients treated with 44 Astra Tech implants. J Oral Maxillofac Surg 2007; 65:64–72. 8. Dasmah A, Thor A, Ekestubbe A, et al. Particulate vs. block bone grafts: three-dimensional changes in graft volume after
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reconstruction of the atrophic maxilla, a 2-year radiographic follow-up. J Craniomaxillofac Surg 2012; 40:654–659. Hong J, Andersson J, Ekdahl KN, et al. Titanium is a highly thrombogenic biomaterial: possible implications for osteogenesis. Thromb Haemost 1999; 82:58–64. Bystedt H, Rasmusson L. Porous titanium granules used as osteoconductive material for sinus floor augmentation: a clinical pilot study. Clin Implant Dent Relat Res 2009; 11:101–105. Verket A, Lyngstadaas SP, Rasmusson L, et al. Maxillary sinus augmentation with porous titanium granules: a microcomputed tomography and histologic evaluation of human biopsy specimens. Int J Oral Maxillofac Implants 2013; 28:721–728. Rasmusson L, Roos J, Bystedt H. A 10-year follow-up study of titanium dioxide-blasted implants. Clin Implant Dent Relat Res 2005; 7:36–42. Jensen OT, Greer R. Immediate placing of osseointegrating implants into the sinus cavity augmented with mineralized cancellous allograft and Goretex: second-stage surgical and histological findings. In: Laney WR, Tolman DW, eds. Tissue integration in oral orthopedic and maxillofacial reconstruction. Chicago: Quintessence, 1992:321–333. Friberg B, Jemt T, Lekholm U. Early failures in 4641 consecutively placed Brånemark dental implants. Int J Oral Maxillofac Implants 1991; 6:142–146. Blomquist JE, Alberius P, Isaksson S. Two-stage maxillary sinus reconstruction with endosseous implants: a prospective study. Int J Oral Maxillofac Implants 1998; 13:758–766.
16. Del Fabbro M, Testori T, Francetti L, et al. Systematic review of survival for implants placed in the grafted maxillary sinus. Int J Periodontics Restorative Dent 2004; 24:565–577. 17. Galindo-Moreno P, Fernández-Jiménez A, O’Valle F, et al. Marginal bone loss in implants placed in grafted maxillary sinus. Clin Implant Dent Relat Res 2015; 17(2):373–383. 18. Maiorana C, Sigurtà D, Mirandola A, et al. Sinus elevation with alloplasts or xenogenic materials and implants: an up to-to-4-year clinical and radiological follow-up. Int J Oral Maxillofac Implants 2006; 21:426–432. 19. Schmitt C, Karasholi T, Lutz R, et al. Long-term changes in graft height after maxillary sinus augmentation, onlay bone grafting, and combination of both techniques: a long-term retrospective cohort study. Clin Oral Implants Res 2014; 25:e38–e46. 20. Yildirim M, Spiekermann H, Biesterfeld S, et al. Maxillary sinus augmentation using xenogenic bone substitute material Bio-Oss in combination with venous blood. A histologic and histomorphometric study in humans. Clin Oral Implants Res 2000; 11:217–229. 21. Yildirim M, Spiekermann H, Handt S, et al. Maxillary sinus augmentation with the xenograft Bio-Oss and autogenous intraoral bone for qualitative improvement of the implant site: a histologic and histomorphometric clinical study in humans. Int J Oral Maxillofac Implants 2001; 16:23–33. 22. Zerbo IR, Zijderveld SA, de Boer A, et al. Histomorphometry of human sinus floor augmentation using a porous betatricalcium phosphate: a prospective study. Clin Oral Implants Res 2004; 15:724–732.
