Maxillary Sinus Floor Augmentation Using Bovine Bone Grafts With Simultaneous Implant Placement: A 5-Year Prospective Follow-Up Study

Abstract

Purpose: 

The aim of this study was to evaluate the 5 year clinical results of maxillary sinus floor augmentation using bovine bone grafts with simultaneous implant placement.

Material and Methods: 

A total of 28 patients were enrolled in the study, and a total of 84 implants were placed into the grafted sites. Unilateral or bilateral sinus augmentation was performed, and implants were inserted into the augmented sinuses. After osseointegration and insertion of the prosthesis, the implants were evaluated by clinical and radiographic parameters.

Results: 

The cumulative implant survival rate after 60 months of loading was 100%. Periimplant bone loss was at clinically acceptable levels (0.146 and 0.34 mm after 1 and 5 years, respectively).

Conclusions: 

Bovine bone grafts used in 1-stage sinus augmentation yields sufficient quality and volume of bone for predictable simultaneous implant placement.

Patients with reduced bone volume or alveolar bone with severe atrophy are a challenge for the surgeon and the prosthodontist. The volume of the maxillary sinus has a natural tendency to increase during life. Especially when the premolars and molars have been extracted, the maxillary sinus extends further downward leaving in some cases only paper thin bone as an alveolar crest of the maxilla.¹ Many authors have used regeneration techniques to increase the volume of new bone to improve the dimension of the residual alveolar ridge before implant placement.^2–4 Other authors have used sinus augmentation procedures to increase the vertical bone heights (VBHs) to permit placement of longer implants.^5–7 Sinus augmentation procedures using autogenous bone and other bone substitutes have been shown to be a safe technique with high predictability. Augmentation of the maxillary sinus floor with an autologous bone graft, first introduced by Boyne and James,⁸ is a commonly used method to increase VBH for immediate or delayed insertion of dental implants. Tatum⁹ introduced intrafracturing the buccal bony wall of the maxillary antrum to oppress the sinus linear membrane gently, followed by bone augmentation. Various bone grafting materials have been used in sinus augmentation.¹ Among these materials, autogenous bone grafts are considered to be the gold standard. Clinical reports in the literature have presented acceptable results with autogenous bone grafts taken from the ileum, tibia, calvarium, and the mandible when applying delayed or simultaneous implant placement.^8,10–15 For augmentation of the bottom of the maxillary sinus, apart from autogenous bone, various bone products or bone substitutes are used.^15–17 One bone substitute evaluated in animal and clinical trials is Bio-Oss, which is a deproteinized bovine bone mineral with a structure similar to human bone.^18–20 Some authors have suggested that the stability in terms of resistance to resorption of deproteinized bovine bone mineral is favorable because the volume of the grafted area is better maintained with time.^21–23 Sinus augmentation procedures in the posterior maxilla is performed in 2 ways: a lateral window technique²³ and an osteotome sinus floor elevation technique.²⁴ Implants can be placed with an osteotome technique with sinus grafting if VBH is at least 5 mm.²³ If the alveolar ridge has a VBH of <5 mm, primary stability of implants may not be achieved. Instead, implants could be placed in a delayed or second-stage surgery after graft remodeling is completed.^23,24 Although these techniques have been used to regenerate lost bone, the factors that contribute to the survival rate of sinus augmentation and dental implant placement are still the subject of discussion. The recent literature concerning sinus grafts has shown differing long-term results depending on which type of bone graft material was used.²⁴

The purpose of this report was to report on the clinical results of a case series study where implants were inserted in the sinus cavities with the sinus floor elevation augmented with bovine bone grafts.

Materials and Methods

Twenty-eight patients with severe atrophy of the maxillary alveolar process as diagnosed by panoramic radiographs were included in the study. Patient selection for sinus floor elevation and immediate implant placement procedure was based on the following criteria: posterior atrophic maxillary ridge, no pathology, and/or repeated sinusitis history in the maxillary sinus.

A sinus augmentation procedure was carried out under local anesthesia using lateral approach technique with simultaneous implant placement. Bovine bone (Bio-Oss; spongious granule, particle size 0.25 to 1 mm; Geistleich Pharmaceutical, Wolhusen, Switzerland) was selected as the grafting material. The sinus area was prepared under local anesthesia in all patients as described.^8,10 A deproteinized bovine bone graft material was mixed with fresh blood from the wounds and inserted in the operation area. Forty-two maxillary sinuses were treated with an augmentation procedure and simultaneous implant placement. Unilateral sinus augmentation was performed in 14 patients and bilateral sinus augmentation was performed in 14 patients simultaneously. A total of 84 titanium implants with roughed surfaces (44 ITI Dental implants [Straumann Inc., Waldenburg, Switzerland] and 40 Camlog [Camlog Bıotechnolgies AG, Basel, Switzerland]) were inserted into the prepared osteotomy sites simultaneously. Forty-four implants were inserted in the right posterior maxilla, and 40 implants were inserted in the left posterior maxilla. Preoperative radiographs were used to assign each position where an implant was placed and to perform implant site classification according to Cawood-Howell.^25,26 Finally, an occlusive bioresorbable membrane (Bio-Guide, Geistlich Pharma AG, Walhusen, Switzerland) was applied. After the healing period, implant-supported fixed partial dentures were constructed. Table 1 shows patient and implant-related parameters investigated in this study. After the prosthetic treatment, patients were recalled after 1 week, 6 months, 12 months, and then annually for evaluation. The implants were evaluated by clinical and radiographic parameters. The following clinical parameters were recorded: (1) Plaque index, (2) Sulcus Bleeding index, (3) periimplant probing depth (4) periimplant marginal bone loss. Mesial and distal periimplant bone measurements were measured in successive radiographs and were digitalized and analyzed at a high magnification (×20). The implant-abutment junction was set as a reference point.

Table 1: Patient and Implant-Related Parameters Investigated in This Study

Standardized radiographs were made before and after implant placement with the long cone paralleling technique at baseline and each recall evaluation.²⁴ A standard film holder (Super-Bite with Ring x-Ray Holders; Kerr, KerrHawe SA, Bioggio, Switzerland) was used to minimize variations in exposure geometry.²⁷

Implants were considered to be successful if radiographic evaluation revealed no more than 1 mm of marginal bone loss during the first year of loading and no more than 0.2 mm resorption per year in subsequent years. The restorations were evaluated by 2 prosthodontists regarding marginal integrity and failure of the ceramic or metal framework.

Four panoramic radiographs were made in each patient: before surgery (T0), directly after maxillary sinus floor elevation and implant placement (T1), 1 year after implant placement (T2), and 5 years after implant placement (T3). These panoramic radiographs were used for morphometric measurements with a tracing of the implant body, residual maxillary bone, original maxillary sinus floor, and grafted sinus floor performed on a tracing paper overlying the radiographs. Maintenance of graft height was measured and calculated with the use of a conversion factor that adjusted for magnification of the panoramic radiograph. To evaluate the change in height of grafted sinus floor for each implant, the variables used were (i) implant length, defined as the distance from the apex to the head of the fixture, and (ii) bone level, defined as the distance from the top of the bone-to-implant contact region to the head of the fixture. To evaluate the change in height of grafted sinus floor in the maxillary sinus, the variables used were (iii) original sinus height (OSH), defined as the distance from the intraoral marginal bone to the lowest point of the original sinus floor, (iv) the VBH (graft height and original maxilla), and (v) grafted sinus height (GSH), defined as the distance from the intraoral marginal bone to the grafted sinus floor directly above the lowest point of the OSH.

Results

No dropout was experienced during the observation period. Six months after the implant insertion, all 84 implants were clinically and radiographically integrated within the graft material. The cumulative implant survival rate after 60 months of loading was 100%. In this study, 70% of implants were placed into the alveolar bone where 4 to 6 mm of residual bone was present (implant site Class C) compared with 30% at implant site Classes B where VBH ranged from 7 to 9 mm. With reference to the Cawood-Howell classification, the greatest number of implants were placed in Class IV sites (60%) (Table 1).

The periimplant tissue health was monitored using periodontal indices and revealed acceptable results. Plaque index (score 1) was found on 28 (8.33%) of the 336 examined surfaces at baseline and on 38 (11.31%) at the first year and 55 (16.37%) at the last follow-up. For Sulcus Bleeding index scores, there was no significant change between baseline and last recall (P = 0.068). At baseline, mean periimplant probing depth value was 1.42 mm and it increased to 1.81 at 5 years. (Table 2). The mean marginal bone loss was 0.146 mm at the first year and 0.34 at the fifth year (Table 3). The prosthodontic follow-up revealed only minor complications, including porcelain fracture in 4 crowns and washout of cement in 6 crowns.

Table 2: Mean Probing Depth Measurements at Baseline and Recall

Table 3: Marginal Bone Level Change at 6 Months and Recall Evaluations

The mean OSH of the native maxilla was 5.2 mm. VBH was 14.34 (±3.12) mm at T1, 13.56 (±2.65) mm at T2, and 12.85 (±2.50) mm at T3. Mean GSH was 6.80 mm at T1, 5.54 mm at T2, and 5.32 mm at T3. Analysis of variance for repeated measures showed that there is a statistically significant reduction over time in VBH and GSH. Post hoc tests (least significant differences) for this variable indicated that there was a reduction between T1 and T2 but not between T2 and T3.

Discussion

During the observation period, all patients included in the study completed the 5 years of follow-up. There were no implant failures. The present study shows that maxillary sinus floor augmentation with Bio-Oss and simultaneous placement of dental implants were successful after an observation period of at least 5 years. Over the past decade, the success of sinus floor augmentation with graft material for the placement of implants has increased significantly, and the procedure has become an excellent choice for treating patients with severely atrophic posterior maxilla.⁶ There is the risk of loss of graft material through possible perforation of the sinus membrane and the chance of graft or sinus infection. It is also surprising that a limited vascularized area between the thin sinus, membrane and the inner cortical surface of caudal sinus, would supply enough nutrition for the inserted bone to survive, let alone remodel, and become a vital environment for osseointegrated implants.^28,29 From the clinical results, it could be concluded that the vascularization, especially from the lateral aspect of the graft, is sufficient.¹⁶ The use of bovine bone grafts delivered successful results in the maxillary sinus area.²² In the present study, 84 implants were successfully placed together with augmentation of the maxillary sinus using bovine bone grafts in the maxilla. Based on the favorable results of this case-controlled clinical study, bovine bone grafts could be advised as bone substitutes considering the bone ridge between 4 and 9 mm. Reconstruction of the posterior maxilla by sinus augmentation procedures has been previously reported in simultaneous and staged implantation approaches.^{11,12,21,22,30–33} Because the primary stability of an inserted implant is decisive for proper osseointegration, the available native bone height plays a vital role. Numerous studies have recommended the 2-step procedure in patients with less than 4 mm alveolar bone height in the posterior maxilla.^13,14 If bone height is less than 4 mm, the primary stability of the implant could be affected. In those cases, before implantation, the vertical dimension must be increased and implants could be placed 4 months after sinus grafting.¹⁸ On the other hand, a survival rate of 94.8% was reported in patients with a residual VBH under the sinus ranging from 6 to 9 mm.⁶ The present study also showed 100% survival rate in patients with a residual VBH under the sinus ranging from 4 to 9 mm. In addition to implant survival rates, the presence of acceptable soft tissue status (periimplant tissue health) influences implant success.³⁴

In this study, implant integration and periodontal health was also successful in all cases. The crestal bone loss in the present investigation was approximately 0.34 mm after 5 years. Ahlqvist et al³⁴ found a bone loss of 1.6 mm after the first year and an additional reduction of 0.1 mm during the next year of loading, and Yerit et al³⁵ reported a mean marginal bone loss of approximately 1.7 mm on the mesial aspect and 1.8 mm on the distal aspect in the extremely atrophied maxilla grafted by autogenous bone blocks. The results of this study are similar to those reported by other authors using a variety of grafting procedures in the maxilla.^34,35 The small reduction of bone around the implants in the present could be the result of slow resorption of deproteinized bovine bone when used as a graft material for sinus augmentation. In the present study, 84 implants were successfully placed together with augmentation of the maxillary sinus using bovine bone grafts in the maxilla. The results of this case series study suggest that bovine grafts used in 1-stage sinus augmentation could yield sufficient quality and volume of bone tissue for predictable simultaneous implant placement in patients with minimum 4 mm of bone height before grafting.

In the present study, most resorption of the graft material took place in the first time period. Thereafter, only minor changes occurred. These findings suggest that implant loading promotes osteogenesis over the long term. This result is in agreement with other studies.^36,37 Hatano et al³⁷ concluded that good long-term results could be achieved using a 2:1 autogenous bone/xenograft mixture for maxillary sinus floor augmentation with simultaneous placement of implants. They reported that the graft height decreased during the first 2 to 3 years after augmentation, but subsequent changes were minimal.

Conclusions

The cumulative implant survival rate after 60 months of loading was 100%, and the greatest number of implants were placed in Class IV sites (60%). Bovine bone grafts used in 1-stage sinus augmentation yields sufficient quality and volume of bone for predictable simultaneous implant placement in patients with a residual VBH under the sinus ranging from 4 to 9 mm (70% of implants were placed into the alveolar bone where 4 to 6 mm of residual bone was present compared with 30% where VBH ranged from 7 to 9 mm) after an observation period of at least 5 years.

Disclosure

The authors claim to have no financial interest in any company or any of the products mentioned in this article.