Implant stability after sinus floor augmentation with deproteinized bovine bone mineral particles of different sizes: a prospective, randomized and controlled split-mouth clinical trial


The aim of this study was to compare implant stability after maxillary sinus floor augmentation using small- or large-sized particles of Bio-Oss. Ten partially edentulous patients requiring bilateral maxillary sinus floor augmentation were enrolled. The subjects were assigned randomly to one of two experimental groups: maxillary sinus was filled with 0.25–1 mm particle size (small particles) and the contralateral side was filled with 1–2 mm particle size (large particles). After 8 months, a total of 25 implants were placed in the two maxillary sinuses. Primary implant stability was measured immediately after implant placement (T0) using a torque controller and resonance frequency analysis (RFA). Six months after implant placement (T1), the implant stability was measured again. There were no postoperative complications in either particle size group, and the success rate for implant survival was 100%. All implants showed good primary stability as evidenced by high torque for the implant insertion in both groups. RFA revealed high ISQ values for all implants installed in both groups at T0 and T1. These results indicate that the size of the Bio-Oss particles (small and large) did not influence implant stability in the maxillary sinus. Indeed, small and large particles of Bio-Oss presented optimal properties, supporting their possible use as osteoconductive grafts.

The use of osseointegrated implants to restore function and patient aesthetics provides predictable treatment outcomes, and these implants have a high survival rate. However, crestal bone resorption after tooth extraction and/or pneumatization of the maxillary sinus leads to insufficient vertical and horizontal bone dimensions for the rehabilitation of posterior missing teeth with osseointegrated implants. Sinus floor augmentation with autogenous bone or bone substitutes is a surgical approach that allows the installation of implants of a suitable length: the sinus membrane is elevated, enabling the interposition of bone graft materials before or simultaneously with implant placement, increasing the bone height in the posterior edentulous maxilla for long-term implant stability.

A variety of bone substitutes and autogenous bone grafts are used to fill the newly formed space in the maxillary sinus. The autogenous bone graft still represents the gold standard for grafting materials because of its osteogenic, osteoconductive, and osteoinductive proprieties. However, it presents some drawbacks mainly related to the high morbidity associated with graft harvesting, limited availability, and the need for two or more surgical sites in the case of bilateral sinus augmentation. Consequently, bone materials that could replace the use of autogenous bone are required. Autogenous bone has gradually been associated with and/or substituted by different types of biomaterial, with the aim of increasing patient acceptance and minimizing patient morbidity. These materials include deproteinized bovine bone mineral (DBBM), human deproteinized bone matrix, tricalcium phosphate, hydroxyapatite, and bioactive glass particles.

DBBM is a material widely used for sinus floor augmentation due to its similarity to human bone, predictable treatment outcomes, and promising rate of bone formation. The deproteinization process results in the removal of protein and organic components, thus preventing immunological rejection of the DBBM after placement; the remaining material is mainly hydroxyapatite, and this acts as a scaffold for new bone formation, characterizing it as an osteoconductive material. Several human studies reported in the literature have shown the use of DBBM for maxillary sinus floor augmentation to be histologically associated with active bone neoformation. Previous studies have also recommended a healing period of 8 months for this type of material when used as the only grafting material in the maxillary sinus. Optimal outcomes in terms of implant survival have been demonstrated for implants placed in the maxillary sinus filled with DBBM, and this material can be considered a safe and predictable graft material for sinus floor augmentation. However, only a few studies have compared different sizes of DBBM for sinus floor augmentation, and no study appears to have used resonance frequency analysis (RFA) to evaluate implant stability following the use of different particle sizes of DBBM.

RFA is a commonly used method to evaluate implant osseointegration and is indicative of treatment success. This is a non-invasive method of measuring dental implant stability that can be used for routine periodical evaluations. The implant stability quotient (ISQ) is calculated. This has a value that ranges between 0 and 100, where a high ISQ value indicates greater stability and a low value indicates a reduced integration between the implant and the surrounding bone. This measurement is achieved with the RFA apparatus and the technique has been designed to reflect the bone–implant interface. Estimates of implant stability using RFA are highly correlated with maximum insertion torque.

The aim of this prospective, randomized and controlled split-mouth clinical trial was to compare the stability of implants placed in the maxillary sinus after sinus floor augmentation using small-sized (0.25–1 mm) and large-sized (1–2 mm) particles of Bio-Oss, by means of RFA, immediately after implant placement (T0) and at 6 months (T1) after implant installation. The working hypothesis was that there would be a statistically significant difference in implant stability, relative to the parameters examined, between augmentations using the large particles of Bio-Oss and those using the small particles, due to the expected larger spaces between the granules with the larger particles; these spaces could favour the formation of more bone between the DBBM particles when compared to the small particles.

Materials and methods

This prospective, randomized and controlled split-mouth clinical trial was conducted in accordance with the Consolidated Standards of Reporting Trials (CONSORT) Statement. The protocol was approved by the institutional ethics committee on human research before patient enrolment. Each subject was fully informed about the treatment and its implications, and written informed consent was obtained from all patients prior to the commencement of treatment.

Patient characteristics

A total of 10 partially edentulous patients presenting to the implantology department were enrolled in this study; six were male and four were female, and they ranged in age from 30 to 65 years (average age 48.34 years). For inclusion in the study, the patient had to require bilateral maxillary sinus floor augmentation and have a residual alveolar bone crest height of 2–4 mm (based on panoramic images), for implant placement in a two-stage approach. Patients were excluded if they had a compromised general health condition or any condition known to modify bone metabolism that would primarily affect bone and soft tissue healing, including chemotherapy and uncontrolled diabetes. Smokers and alcohol and drug abusers, and any subject suffering from any pathology in the maxillary sinus, were also excluded from the study.

The patients included in this study were assigned randomly (by a random table created by panoramic radiography before the surgical procedures) to two experimental groups to be grafted with two different particle sizes of DBBM (Bio-Oss; Geistlich Pharma AG, Wolhusen, Switzerland). One maxillary sinus was filled with small particles (particle size 0.25–1 mm) and the contralateral side with large particles (particle size 1–2 mm).

Maxillary sinus floor augmentation procedure

Prior to the sinus lifting surgery, conventional panoramic radiographs were obtained to evaluate the maxillary sinus and the residual vertical bone height. The procedure was performed under local anaesthesia (mepivacaine 2% and epinephrine 1:100,000; DFL, Rio de Janeiro, RJ, Brazil). A crestal incision was made in the maxillary edentulous area, followed by two vertical incisions extending both mesial and distal to the lateral sinus wall, as described previously. The mucoperiosteal flap was detached to fully expose the maxillary lateral sinus wall. A lateral window approach was accomplished according to the technique first described by Boyne and James. Briefly, an oval window was created, the cortical bone wall was detached, and the Schneiderian membrane was gently elevated with the aid of special curettes (Hu-Friedy, Chicago, IL, USA). Small and large particles of Bio-Oss were inserted into the respective sinus cavities and a resorbable collagen membrane (Bio-Gide; Geistlich Pharma AG) was applied to cover the entire obturated lateral window, as per the protocol established by Wallace and Froum.

After surgery, all patients received postoperative instructions for good oral hygiene control and were prescribed oral antibiotics (amoxicillin, 500 mg three times a day for a week) and an oral anti-inflammatory (nimesulide, 100 mg twice a day for 5 days). They were also advised to rinse their mouth with chlorhexidine (0.2%) for 14 days. The sutures were removed 7 days after the surgical procedure, and the area was not subjected to any direct loading during the entire bone regeneration phase. All patients were checked every month to verify the healing process. Any alteration during the postoperative follow-up was recorded.

Implant installation

Eight months after the sinus floor augmentation procedure, dental implants were installed in both maxillary sinuses. Under local anaesthesia (mepivacaine 2% and epinephrine 1:100,000; DFL), a full thickness flap was raised to expose the alveolar bone, and the receptor area was prepared according to the manufacturer’s protocol (Conexão Sistemas de Prótese Ltda, Aruja, Sao Paulo, Brazil). Twenty-five double acid-etched, commercially available implants (MasterPorous; Conexão Sistemas de Prótese Ltda) with an external tapered connection were placed by the same experienced surgeon.

Thirteen implants were placed in the maxillary sinus filled with small particles of Bio-Oss and 12 implants were placed in the sinus filled with large particles of Bio-Oss. All implants had the same diameter (3.75 mm), and the implant length ranged from 8.5 mm to 13.0 mm. Immediately after implant placement (T0), the insertion torque of each implant was recorded using a torque controller (Conexão Sistemas de Prótese Ltda) and the implant stability was recorded using a RFA device. Subsequently, healing caps were installed and the flaps were repositioned and sutured. Patients received oral hygiene instructions and postoperative medication (amoxicillin, 500 mg three times a day for a week; nimesulide, 100 mg twice a day for 5 days; sodium dipyrone 500 mg four times a day for 3 days, in the case of pain). Six months after implant placement (T1), transepithelial healing abutments were installed and the implant stability was again recorded, as described below.

Follow-up control

Patients were evaluated immediately after implant installation (T0) and at 6 months after implant placement (T1). Implant survival was defined according to Buser et al., and the following parameters were recorded: (1) absence of pain in the receptor area, (2) absence of peri-implant suppuration or infection, (3) lack of implant mobility, (4) absence of sulcus bleeding, and (5) lack of peri-implant radiolucency.

Implant stability quotient (ISQ)

The implant stability coefficient, i.e. RFA, was measured with a RFA device (Osstell; Integration Diagnostics, Gothenburg, Sweden). SmartPegs were used to measure the implant stability at T0 and T1. The RFA device determines the resonance frequency of a peg, which can be attached to the implant with the aid of a cylindrical holder. The Osstell apparatus makes contact-free measurements over a range of frequencies by exciting the SmartPeg, which starts to vibrate when the highest and lowest resonance frequencies occur. The measurements were performed in the mesiodistal, distomesial, buccal-lingual, and lingual-buccal regions and the mean values were used, as described previously. The ISQ value, displayed on the screen of the analyzer, ranges between 1 and 100; a high ISQ value indicates great stability and a low value indicates a reduced integration between the implant and the surrounding bone. The average values obtained were recorded in a spreadsheet. If unstable osseointegration is present, the vibrations will be high and a low ISQ value will be measured. All ISQ measurements were performed in a standardized manner by one experienced, blinded, and calibrated examiner, who was masked to the treatment protocol.

Radiographic examination

To evaluate the effect of bone tissue and implant length on stability at T0 and T1, the length of each implant (in millimetres) fixed in the grafted area (intrasinus bone graft) and fixed in the pristine alveolar bone (non-grafted sites) was measured. For this evaluation, panoramic radiographs were taken after implant placement. Digital radiographs were imported into image analysis software (UTHSCSA ImageTool version 3.0) and measurements were performed in a standardized manner by one blinded and calibrated examiner, who was masked to the original treatment protocol. For software calibration, the known sizes of the implants were used to correct image distortion. Errors in the radiographic measurements were evaluated per patient by means of duplicate recordings of one randomly selected implant. After image acquisition, one randomly selected implant was measured twice and the mean and standard deviation measurement recorded in a spreadsheet. The measurements were repeated for all patients with a 1-day interval between analyses. The highest level of the pristine bone and the length of the implant that lay in the bone were then calculated. The length values (%) of each implant in contact with the pristine bone and in contact with the intrasinus bone graft were correlated with the ISQ values obtained, in order to determine the role of bone conditions in the primary and biological stability of the implants. The ISQ values at the two time points evaluated were also correlated with the implant length (in millimetres) in order to determine whether its size is capable of interfering in the primary and biological stability of the implants.

Statistical analysis

GraphPad Prism version 6.0 software (GraphPad Software, Inc., La Jolla, CA, USA) was used for the statistical analysis and visualization of data. All data were expressed as the mean ± the standard error of the mean (SEM). The intra-examiner reproducibility with consideration to the ISQ and radiographic measurements was assessed at baseline. The analyses were repeated for five patients with a 1-h interval between examinations, and the data were submitted to the Pearson correlation test. After testing for a normal distribution (Kolmogorov–Smirnov test), differences were analyzed by Student t -test for the insertion torque, ISQ values, and radiographic measurements. In addition, correlations between the ISQ and insertion torque values, between the percentage of implant length installed in pristine bone and ISQ values, and between the implant length (in millimetres) and ISQ values at T0 and T1 were investigated for the two groups using Pearson’s rank correlation coefficient. A further non-parametric model (linear regression) was used to explore the association between ISQ values and any single variable of interest. Differences were considered significant at P < 0.05.


Patient characteristics

Maxillary sinus floor augmentation was performed bilaterally in 10 participants. One side, selected randomly, was filled with small particles of Bio-Oss and the contralateral side was filled with large particles. Implants were placed after a minimum period of 8 months. After the procedure, during the 240-day healing time, the patients did not wear any provisional removable partial denture or fixed prosthesis. After this healing time, 25 implants were placed; 12 were installed in the maxillary sinus filled with large particles and the other 13 in the contralateral side. None of the implants inserted was lost during the postoperative period. Peri-implant infection, implant mobility, sulcus bleeding, and peri-implant radiolucency were not observed in any of the patients included in this study. No perforations of the maxillary sinus membrane were noted.

Primary implant stability

The insertion torque of each implant was recorded using a torque controller immediately after implant placement. All implants installed in the maxillary sinus presented high insertion torque values, suggesting that all implants had great primary stability. Comparing the insertion torque at T0 between sites with small particles and large particles of DBBM, no statistically significant difference was found ( P > 0.05): small particles 37.92 ± 12.33 N·cm and large particles 35.0 ± 9.77 N·cm ( Fig. 1 ). The correlation between ISQ values and primary implant stability (insertion torque values) was not significant for small particles ( P = 0.09) or large particles ( P = 0.45) ( Fig. 2 ).

Fig. 1
Insertion torque values (N cm) obtained for small and large particle sizes of Bio-Oss immediately after implant placement; no statistical difference was found between the sizes ( P > 0.05).

Fig. 2
Correlation between the implant stability quotient (ISQ) and insertion torque values (N cm) at T0. The correlation was assessed using Pearson’s correlation coefficient. No statistically positive correlation was found between the ISQ and the insertion torque values for either small particle sizes ( P = 0.09) or large particle sizes of deproteinized bovine bone mineral ( P = 0.45).

ISQ analysis

The intra-examiner reproducibility for the ISQ analysis was r = 0.937. RFA was performed at T0 (immediately after implant placement) and at T1 (6 months after implant placement) for each group. All implants installed in both groups (small and large particles) demonstrated high RFA values at T0 and T1. No statistically significant difference was found between small particles at T0 (62.9 ± 6.8) and T1 (63.5 ± 5.4) and large particles at T0 (59.7 ± 7.6) and T1 (62.1 ± 7.4) ( Fig. 3 ).

Dec 15, 2017 | Posted by in Oral and Maxillofacial Surgery | Comments Off on Implant stability after sinus floor augmentation with deproteinized bovine bone mineral particles of different sizes: a prospective, randomized and controlled split-mouth clinical trial

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