Abstract
Objective
The objective of this research was to evaluate implant stability following sinus lift with two grafting materials, and to compare it with the results obtained for the implants placed in a pristine posterior maxilla.
Materials and methods
The study included 44 healthy patients with an existing indication for sinus lift procedure (test group). 46 implants were placed following sinus lift with a pure-phase beta-tricalcium phosphate, while 39 implants were placed following augmentation with 60% hydroxyapatite with 40% beta-tricalcium phosphate material. The control group consisted of 48 healthy patients who were treated with 85 implants but without bone augmentation in posterior maxilla. Astra Tech OsseoSpeed implants were placed in all subjects. Resonance frequency analysis was used in both groups for determining implant stability 4 months after insertion. A mean implant stability quotient (ISQ) was calculated on the basis of 3 measurements.
Results
No statistical difference was observed in ISQ values of implants placed with and without augmentation procedure (p=0,789). Statistically significant difference was not found when ISQ values of implants placed following particular grafting material were compared with ISQ values of corresponding implants in a pristine bone (p=0.697 and p=0.402).
Conclusions
This study demonstrated that the implant stability is comparable among implants placed in the posterior maxilla regardless of sinus lift and grafting procedure. Implants placed in the grafted posterior maxilla can be predictably loaded as the implants placed in a non-grafted, pristine maxilla.
Key words: Dental Implants, Sinus Floor Augmentation, Resonance Frequency Analysis, Beta-tricalcium Phosphate, Hydroxyapatite
Introduction
The posterior maxilla is often associated with different challenges to the implant dentist. In order to adequately restore posterior maxilla with dental implants, a sufficient bone volume in the maxillary ridge is required. However, certain anatomic limitations can be encountered and these include increased pneumatization of the maxillary sinus, thin lateral and occlusal bone, flat palatal vault, and proximity of the sinus to crestal bone (1). In patients with insufficient bone volume of the posterior maxilla, elevation of the sinus floor is indicated to allow for implant restorations. Since it was originally described by Tatum in the mid 1970s, maxillary sinus floor elevation has been extensively investigated with respect to different grafting materials, and comparison between similar approaches (2-4).
The most widely used treatment modalities include the two-step lateral antrostomy, the one-step lateral antrostomy, and the osteotome technique with crestal approach. The two-step lateral antrostomy is indicated when the residual bone height is less than 4 mm. The one-step lateral antrostomy is used for the residual bone height of 4 to 6 mm, and the less invasive osteotome technique is recommended when more than 6 mm of residual bone height is present (5, 6).
Although the patient's own bone is considered the best grafting material for sinus augmentation, various alternatives have been proposed to simplify the grafting procedure including demineralized freeze-dried bone, hydroxyapatite (HA), beta-tricalcium phosphate (ß-TCP), inorganic deproteinized bovine bone and combination of these and others (7, 8). In a systematic review, Del Fabbro et al. determined the survival rate of implants placed in the grafted maxillary sinus, and the effects of grafting materials. Implant survival rate was 87.70% with autogenous grafts, 94.88% when combining autogenous bone with different bone substitutes and 95.98% with bone substitutes alone. Therefore, bone-substitute grafts were shown to be as effective as autogenous bone when used alone or in combination with autogenous bone (9).
Implant stability and successful osseointegration are prerequisites for implant survival. Thus, continuous monitoring in a reproducible and objective manner is crucial in determining the implant stability. Various non-invasive methods are available today for this purpose: radiographs, reverse torque, cutting torque resistance, modal analysis, and resonance frequency analysis (RFA). When different measurements were compared, a significant correlation was found between cutting torque or insertion torque and RFA (10, 11).
Huang et al. evaluated natural frequency to assess implant-bone interface. Natural frequency is a physical characteristic of a structure, which is closely related to its boundary conditions. They concluded that the boundary status of an implant can be monitored by detecting its natural frequency (12). In another study, the same researchers found RFA as a reliable and accurate method for early assessment of osseointegration process. These measurements cannot only be used as an indicator for primary stability, but can also be useful regarding the secondary implant stability (13). Study on RFA of one-stage dental implant stability during the osseointegration period revealed the weakest stability at 3-6 weeks in one-stage non-loaded implants. Values obtained with RFA can be therefore valuable in determining different healing phases and the stability of dental implants. Those results support the need for a clinical device to evaluate implant stability prior to loading (14).
The objective of this research was to evaluate implant stability following sinus lift with two grafting materials, and to compare it with the implants placed in a pristine posterior maxilla.
Materials and methods
This parallel study included 44 healthy subjects with an existing indication for unilateral or bilateral sinus lift procedure (test group), and 48 healthy patients who were treated with 85 implants but without bone augmentation in maxilla (control group). The study was only randomized in a test group where 46 implants were placed following sinus lift with pure-phase ß-TCP, while 39 implants were placed following augmentation with HA/ß-TCP material. The inclusion criteria for test groups were: age> 18 years, interrupted or shortened dental arch in the lateral part of the upper jaw, the amount of residual bone ridge <5mm and a good oral hygiene. The exclusion criteria were: systemic contraindications for augmentation procedures (pregnancy, poor general condition, untreated diabetes, glucocorticoids and bisphosphonates medication, and advanced osteoporosis), radiation of maxillofacial region, smoking > 10 cigarettes per day, poor oral hygiene, and infections or tumors of the maxillary area.
One hour prior to surgery patients took oral antibiotics (1g amoxicillin or 600mg clindamycin if allergic to penicillin). After rinsing with 0.20% chlorhexidine and administration of local anesthesia, a crestal incision with vertical releasing incisions were performed to raise a full thickness flap and to expose a buccal bone wall of the maxillary sinus. Bone wall was carefully fenestrated with copious saline cooling. Preoperative residual bone height varied from 0.6 to 5.7 mm. After lifting the Schneiderian membrane from the sinus floor, depending on the randomization, a pure-phase ß-TCP bone grafting material (Bioresorb, Sybron Implant Solutions, Orange, USA) or a 60% HA with 40% ß-TCP material (Maxresorb, Botiss, Berlin, Germany) was applied after previous rehydration with 1-5 mL of sterile saline. Buccal window was covered with rehydrated collagen membrane (Jason membrane, Botiss, Berlin, Germany). A full thickness flap was adapted and the wound was sutured. Control cone-beam computed tomography (CBCT) scan was recorded to exclude dislocation of the bone grafting material. Following 5 days after the surgery, patients took 2x1000mg amoxicillin or 3x300mg clindamycin if allergic to penicillin. Sutures were removed 7-10 days after the surgery. After the healing phase of 6 months, a CBCT scan was repeated to determine the position, length and width of the planned implant.
In both groups, Astra Tech OsseoSpeed implants (Astra Tech AB, Mölndal, Sweden) were placed using the same drilling protocol, with regard to bone quality and in accordance with the manufacturer’s recommendations. Insertion torque was recorded in a scale from “poor” to “excellent” in both groups. Standard loading protocol, without immediate loading or differences among groups, included loading 4 months after implant placement. No implant loss was observed during the study period. Seven sinus membrane perforations occurred, but they were immediately treated and did not influence the further protocol.
RFA method (Osstell ISQ, Osstell, Gothenburg, Sweden) was used for determining implant stability in both groups. After mapping of resonance frequencies, this method provided a measurement scale of 1-100 ISQ values (implant stability quotient). For each implant, a mean ISQ value was calculated on the basis of 3 ISQ measurements recorded from different directions. To precisely compare mean ISQ values, each implant in the test group was paired with the implant of the same length and diameter in the control group. RFA examinations were performed in both groups 4 months after implant placement by one and the same experienced dental examiner.
The patients within the test group were randomly chosen to avoid selection bias and to ensure normal distribution of the sampled variables. This study was approved by the Ethics Committee of the School of Dental Medicine, and it was conducted in accordance with the ethical principles of the Helsinki Declaration. All participants were informed about the nature of the study and gave their written consent prior to clinical protocol.
Data were analyzed with statistical software package SPSS v.21.0 (SPSS Inc., Chicago, IL, USA). Normal distribution of the values was evaluated using the Kolmogorov-Smirnov test. Wilcoxon signed ranks test was used to evaluate ISQ values of implants placed with and without augmentation procedure. The statistical significance was set at p<0.05.
Results
Out of 85 implants paired in both groups, most of them were 4.0 mm in diameter (76.5%) and 11 mm in length (48.2%) (Tables 1 and 2). Wilcoxon signed ranks test revealed no statistical difference in ISQ values of implants placed with and without augmentation procedure (p=0.789) (Table 3). Statistically significant difference was not found when ISQ values of implants placed following particular grafting material were compared with ISQ values of corresponding implants in a pristine bone. ISQ values of implants placed following ß-TCP were lower than in controls, but without significance (p=0.697) (Table 4). Implants placed following HA/ß-TCP showed higher ISQ values, but statistical significance was not observed (p=0.402) (Table 5).
Table 1. Distribution of implant diameter in both groups.
| Diameter Mm |
ß-TCP | HA/ß-TCP | Pristine bone |
|---|---|---|---|
| 3.5 |
1 |
1 |
2 |
| 4.0 |
33 |
32 |
65 |
| 4.5 |
2 |
0 |
2 |
| 5.0 |
10 |
6 |
16 |
| 46 | 39 | 85 |
Table 2. Distribution of implant length in both groups.
| Length Mm |
ß-TCP | HA/ß-TCP | Pristine bone |
|---|---|---|---|
| 8 |
4 |
0 |
4 |
| 9 |
19 |
7 |
26 |
| 11 |
22 |
19 |
41 |
| 13 |
1 |
13 |
14 |
| 46 | 39 | 85 |
Table 3. Comparison of ISQ values of implants placed in augmented and pristine maxilla.
| N | Mean | SD | Minimum | Maximum | p | |
|---|---|---|---|---|---|---|
| ISQ augmented bone |
85 |
78.9 |
6.3 |
60.0 |
90.0 |
0.789 |
| ISQ pristine bone | 85 | 78.7 | 6.1 | 59.6 | 90.0 |
Wilcoxon signed ranks test, SD=standard deviation, p=statistical significance.
Table 4. ISQ values of implants placed in sinus augmented with ß-TCP.
| N | Mean | SD | Minimum | Maximum | p | |
|---|---|---|---|---|---|---|
| ISQ ß-TCP |
46 |
78.3 |
5.9 |
61.0 |
87.0 |
0.697 |
| ISQ pristine bone | 46 | 78.9 | 5.7 | 65.6 | 90.0 |
Wilcoxon signed ranks test, SD=standard deviation, p=statistical significance.
Table 5. ISQ values of implants placed in sinus augmented with HA/ß-TCP.
| N | Mean | SD | Minimum | Maximum | p | |
|---|---|---|---|---|---|---|
| ISQ HA/ß-TCP |
39 |
79.8 |
6.8 |
60.0 |
90.0 |
0.402 |
| ISQ pristine bone | 39 | 78.4 | 6.6 | 59.6 | 88.3 |
Wilcoxon signed ranks test, SD=standard deviation, p=statistical significance.
Discussion
RFA revealed no difference in implant stability with regard to grafting procedure or grafting material used. The mean values of stability of implants that were inserted in the posterior maxilla with or without augmentation procedure were 78.9±6.3 and 78.7±6.1, respectively. According to the scientific literature, ISQ values above 70 indicate high implant stability and successful osseointegration of inserted implant. Adequate implant stability value is the main prerequisite for immediate and early loading protocol (15, 16).
Various clinical factors that could influence resonance frequency values were assessed in a study by Degidi et al. A statistically significant positive correlation was observed between ISQ values and implant diameter and length (17). For that reason, we only analyzed implants of the same diameter and length between test and control sites to obtain comparable ISQ values. Implants mostly used in the present study were 4.0 mm in diameter and 11 mm in length.
Ersanli et al. emphasized that ISQ level should also be calibrated for each implant system separately, since it is difficult to define a general standardized range of ISQ values for successful implant integration for various implant systems (14). Stability measurements obtained with the present study, consequently, can only be applied to Astra Tech OsseoSpeed implants. Statistical analysis of measurements revealed no difference in overall ISQ values of implants that were inserted in posterior maxilla with or without augmentation procedure (p=0.789). Similar results were found with Astra Tech TiOblast implants that were inserted in grafted and non-grafted maxillary bone, and demonstrated similar stability during the early phase of osseointegration (18).
A literature review on biomaterials in sinus augmentation procedures evidenced that initial osseointegration of dental implants seems to be independent of the biomaterial used in grafting procedure (19). In the present study, we used two different grafting materials (ß-TCP and HA/ß-TCP) that were previously shown to be reliable substitutes for sinus augmentation. Suba et al. compared the effects of ß-TCP and of autogenous bone graft using histomorphometry. The results showed that, 6 months after insertion of the grafts, the augmented sinus floor bone was strong and suitable for dental implant placement, regardless of whether alloplastic or autogenous graft had been applied (20). Similar findings were observed by Zijderveld et al. on the basis of the clinical and histologic formation ability of ß-TCP and autogenous chin bone (21). Also, HA and ß-TCP were separately compared when used for sinus augmentation procedures. It was demonstrated that a new bone formation was more pronounced in the HA group with less residual graft particle areas. Although both materials showed successful osteoconductivity and biocompatibility for the sinus floor elevation, HA appeared to be more efficient in osteoconduction when compared with ß-TCP (22). Despite these differences, our ISQ values were shown not to be influenced by a particular grafting material, because no significance was observed in comparison to ISQ values of corresponding implants in non-augmented sites.
No difference that we observed at the time of implant placement can probably be expected in a long-term follow-up. Degidi et al. evaluated the evolution of ISQ values at 6 and 12 months from the implant insertion in sinus grafted and non-grafted sites. Using this method, it was found that sites treated with sinus lift can offer good long-term stability (23). In a similar 12-month clinical study, no statistically significant difference was found in ISQ values of implants placed in sinus-grafted and non-grafted sites after the surgery as well as at 6 and 12 months (24).
Our results also indicate that implants inserted in a grafted sinus, regardless of the substitute material, can be predictably loaded as the implants inserted in a pristine, non-grafted maxilla. Previous studies concluded that the prognosis of implants inserted in augmented sinuses and fixed restoration supported by this implants seemed not to be influenced by factors such as graft material, type of restoration, residual bone height and time of implant placement (25). RFA measurements are therefore highly recommended, especially if a clinician is considering immediate or early implant loading.
Conclusion
The results observed in this study clearly demonstrated that the examined implant stability is comparable among implants placed in the posterior maxilla regardless of sinus lift or grafting procedure. In conclusion, the implants placed in the grafted maxilla following sinus lift can be predictably loaded as the implants placed in a non-grafted, pristine maxilla. RFA can serve as a valuable clinical method for determining implant stability of the dental implant.
Acknowledgements
This paper was supported by the Ministry of Science, Education and Sport of the Republic of Croatia Grant No. 065-0650444-0415 (chief investigator Darije Plančak, project “Systemic aspects in the etiology of periodontal diseases”).
Footnotes
The authors deny any conflicts of interest.
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