Implant-supported prostheses represent a predictable and highly successful treatment modality1; however, certain conditions must be respected to achieve proper results. Implant stability during the healing phase is a major prerequisite for successful osseointegration in both conventional and immediate loading protocols.2,3 Several parameters play a major role in achieving implant primary stability mainly bone density, insertion torque (IT), implant geometry, and surgical technique.4–6
Bone density evaluation is a prerequisite when planning future implant cases. Many classifications of bone density have been suggested based on radiographic appearance,7 tactile sense during drilling,8 or computed tomography measurements using Hounsfield units (HU) values.9,10 Bone density has been shown to correlate significantly with IT values.11 In a previous study,12 we described correlation of IT values with different types of bones and in different jaw locations. It was shown that the denser the bone, the higher the IT values noted. Because IT values are known to be an indicator of implant stability,4 they can dictate future loading protocols. However, IT values determine implant mechanical primary stability that will diminish over the weeks due to accelerated bone remodeling during early healing phases that will induce a resorption phenomenon around the implants.13 Resulting implant micromotion may play a negative role on osseointegration process during early or immediate loading protocols where one of the prerequisite is to attain implant stability at insertion and throughout healing period.3
Many techniques were described to measure implant stability clinically. Percussion and radiographic evaluation of bone response over the implants were the most widely used.14 Nevertheless, these techniques lacked reliable and predictable diagnosis on periimplant bone situation unless fibrous encapsulation has occurred.14 Periotest (Medizintechnik Gulden, Modautal, Germany), a noninvasive technique based on measurements of dampening effect,15 is used to measure implant stability; however, this technique failed to ensure sensitive values.16 Meredith et al17 in 1996 described a novel technique for implant stability evaluation, the resonance frequency analysis (RFA). The most recent version of RFA is wireless, where a metal rod (a peg) is connected to the implant by means of a screw connection. The peg has a small magnet attached to its top and is excited by magnetic pulses, and the resonance frequency is expressed electromagnetically as an implant stability quotient (ISQ) with units ranging from 1 to 100. ISQ values represent the stiffness of the implant-bone interface and therefore measure implant stability. In a recent study, Trisi et al18 found, in vitro, a strong correlation between measured micromotion around implants and ISQ.
ISQ measures are influenced by many clinical and operator-related factors.19 Many authors found a positive correlation between bone density measured histologically or radiographically and ISQ values, showing a significant positive correlation between high-density bone and higher ISQ values20,21 and mainly between ISQ and thickness of the cortical plate.22,23 Jaw location is also believed to play a role in implant stability because ISQ values in the mandible were found to be higher than those in the maxilla.19 Although ISQ values correlated with IT in some articles,18,20 other studies failed to correlate with these 2 values.24 Implant geometry,24 diameter,19,25 and length19 are also believed to affect ISQ measures.
ISQ values can usually vary over time. The normally described pattern shows a decrease at 3 to 4 weeks followed by an increase at 6 to 8 weeks.25,26 These findings confirm biological variations in bone after periimplant healing process.13 Implant design and surface structure may also have an impact on the implant stability during initial healing.27
To measure the degree of osseointegration, reverse torque technique was mostly used in scientific literature because it provides a quantitative measure of osseointegration break point.14 Nevertheless, this technique is very invasive for routine clinical testing and is generally used for research purposes because it may damage the implant-bone interface.28,29 Sullivan et al30 proposed a reverse torque technique in humans while applying only 20 N.cm to test osseointegration clinically. Salvi et al31 evaluated osseointegration during abutment connection by torquing with a 30 N force in a clockwise direction.
To evaluate primary and secondary implant stabilities in different types of bones, we propose to measure ISQ values of tapered, multithreaded implants with microtextured surfaces (Tapered Screw-Vent MTX, Zimmer Dental, Inc, Carlsbad, CA) inserted into histologically preassessed bony sites using RFA (Osstell ISQ; Ostell, Integration Diagnostics AB, Gothenburg, Sweden) over a 6-week period and correlate them with recorded IT values along with clinical testing of osseointegration at the final abutment torquing at 6 weeks.
Materials and Methods
Eighteen patients seeking implant therapy for fixed prosthetic restorations were included in this study. All patients were in good health with no systemic disorders. Patients were accurately informed about the procedures and study participation, and signed informed consent forms were obtained before treatment. The protocol of the study was approved by the Ethics Committee at the Saint Joseph University (Beirut, Lebanon).
Preoperative examinations included orthopantomographs and clinical examinations of edentulous ridges and natural dentition. Patients underwent a prosthodontic evaluation for treatment planning and preparation of surgical templates. All surgeries were performed by the same surgeon, from the Oral Surgery Department, Faculty of Dental Medicine, Saint Joseph University (Beirut, Lebanon).
Patients were asked to rinse with chlorhexidine digluconate solution (0.2%) for 1 minute approximately 10 minutes before the surgery. Under localized anesthesia, a crestal incision and a full-thickness flap elevation were performed. A trephine drill, 2.8 mm in external diameter and 8.0 mm in length, was used as a pilot drill under copious saline irrigation. The bone core was retrieved, rinsed, and immediately immersed in 10% neutral buffered formalin solution and sent for histomorphometric evaluation to determine BV.12 Implant site preparation was performed according to the manufacturer's protocol for the placement of 4.1-mm or 4.7 mm-diameter implants, which included an osteocompressive surgical technique in low-density (“soft”) bone by undersizing final osteotomy. Implants were manually threaded into the osteotomies until final seating of the implant collar at bone level. At that time, the final IT value was measured using a manual torque gauge (Dial Torque Screwdriver; Tohnichi Mfg, Co, Ltd, Tokyo, Japan).12 An aluminum peg was screwed into the implant, and initial implant stability was measured using an RFA device (Ostell ISQ; Ostell, Integration Diagnostics AB). RFA values were recorded using the unit's proprietary ISQ. A transmucosal healing collar was attached to the implant, and soft tissues were approximated and sutured around it for a nonsubmerged healing protocol. ISQ recordings were performed again at 3 and 6 weeks and noted in a dedicated sheet.
Periapical radiographs, using a paralleling long-cone technique (Rinn XCP; Dentsply, York, PA), were taken at day 0 and every 3 weeks until final abutment connection. Patients were prescribed prophylactic antibiotic coverage (amoxicillin 2 g daily or in case of allergy, clindamycin 600 mg daily) for 7 days, analgesics and oral rinses of 0.12% chlorhexidine gluconate for 15 days after implant placement. Patients were recalled for suture removal 7 to 10 days after the surgery and were monitored clinically and radiographically every 3 weeks until final prosthetic reconstruction.
Evaluation of Clinical Osseointegration
To evaluate osseointegration clinically, an early torquing force was applied after a 6-week healing period, in accordance with the protocol described in the clinical study of Salvi et al.31 The healing collar was unscrewed, and a final precontoured abutment was attached to the implant and tightened to 30 N.cm of applied torque, without the use of a countertorque device, according to the manufacturer's directions to achieve final abutment seating. During this procedure, the absence of implant mobility and pain were considered prerequisites for achieving osseointegration. Implants that failed to fulfill these criteria were considered not yet osseointegrated and were allowed to heal unloaded for another 8 weeks. Implants that successfully withstood the 30 N.cm of final abutment torque were provisionally restored until delivery of the final prosthetic ceramic crown.
Descriptive and comparative analyses were performed using a dedicated software program (SPSS for windows version 17.0; SPSS, Inc, Chicago, IL). Both descriptive and comparative statistics were used, and a P value of 5% or less was considered statistically significant. One-way repeated measure analysis of variance followed by Bonferroni multiple comparison was conducted to explore significance difference in ISQ between baseline and 3 and 6 weeks after implant placement. Spearman correlation coefficient and Pearson correlation coefficient were used to investigate the relationship between BV and ISQ, IT and ISQ, ISQ values at different times, and ISQ values and implant length and diameter.
A total of 18 subjects (7 men and 11 women) ranging in age from 30 to 74 years (mean, 48.8 ± 13.8 years) were selected for participation in this study. Patients were treated with a total of 40 implants placed in maxillary and mandibular locations and subsequently restored with fixed prostheses. BV values and IT values were presented with the statistical results in a previous article.12
Mean ISQ values for the 40 implants were 76.48 ± 6.83 at baseline, 74.32 ± 6.58 at 3 weeks, and 75.37 ± 6.39 at 6 weeks. Mean ISQ decreased significantly after 3 weeks and then increased significantly after 6 weeks (P value = 0.001, partial η2 = 0.325) for all implants (Fig. 1). The relationship between ISQ values at different periods was investigated using Spearman correlation coefficient. There was a strong correlation between ISQ at baseline, at 3 weeks, and at 6 weeks (r > 0.75; n = 40; P value <0.0001).
Correlation of Bone Volume and ISQ Values Over Time
At baseline, there was a positive correlation between ISQ and BV (r = 0.366; n = 40; P = 0.02). At 3 weeks, there was a positive correlation between ISQ and BV (r = 0.465; n = 40; P = 0.003). However, no relationship was found between BV and ISQ at 6 weeks (r = 0.256; n = 40; P = 0.110).
Mean ISQ Values
By jaw location, mean ISQ values were significantly higher in mandibles than in maxillas at baseline (P < 0.0001), at week 3 (P < 0.0001), and at week 6 (P = 0.006). Mean ISQ values significantly changed over time in both maxilla (P = 0.006) and mandible (P = 0.008) (Fig. 2A). By implant diameter, 4.7-mm-diameter implants exhibited significantly higher ISQ values at 3 weeks (P = 0.031) and at 6 weeks (P = 0.005) when compared to 4.1-mm-diameter implants. No significant difference in ISQ values was noted at baseline (P = 0.159) between 4.1 mm and 4.7 mm diameter. The mean ISQ changed significantly over time with 4.1-mm-diameter implants (P = 0.004) and with 4.7-mm-diameter implants (P = 0.045) (Fig. 2B). No correlation was found between implant length and ISQ over time (P > 0.05).
Positive correlation was found between IT and ISQ at baseline (r = 0.313; n = 40; P = 0.049) (Fig. 3A), at 3 weeks (r = 0.472; n = 40; P = 0.002) (Fig. 3B), and at 6 weeks (r = 0.419; n = 40; P = 0.007) (Fig. 3C).
Thirty-two implants did not show pain or movement when final abutments were torqued at 6 weeks and were successfully restored. Eight implants showed pain during tightening, and therefore, final torquing of abutments was aborted. All of these 8 implants were successfully restored after another 8 weeks healing period.
Mean and standard deviation of BV for positively and negatively torqued implants at 6 weeks are presented in Table 1. There was a positive correlation between BV and torquing at 6 weeks (r = −0.454; n = 40; P = 0.003) (Fig. 4A).
Mean and standard deviation of IT for positively and negatively torqued implants at 6 weeks are also presented in Table 1. There was a positive correlation between IT and torque test results at 6 weeks (r = −0.528; n = 40; P < 0.001) with higher IT values associated with positively torqued implants (Fig. 4B).
Mean and standard deviation of ISQ from baseline to weeks 3 and 6 for positively and negatively torqued implants after 6 weeks are presented in Table 1. For positively torqued implants after 6 weeks, mean ISQ decreased significantly after 3 weeks and then increased significantly at 6 weeks (P = 0.005) (Fig. 5). For negatively torqued implants after 6 weeks, mean ISQ significantly decreased after 3 weeks and remained unchanged at 6 weeks (P = 0.031) (Fig. 5). Mean ISQ values at baseline, and at 3 and 6 weeks were significantly higher for positively torqued implants when compared to negatively torqued implants (P < 0.05) (Fig. 5).
Implant stability is a crucial clinical factor to consider whenever implant treatment is planned.3 Early and/or immediate loading protocols require a stable mechanical connection between dental implants and bone.3 This stability is influenced by many factors. At implant placement, primary stability is related to bone density, implant geometry, and surgical technique, whereas reduced micromotion throughout healing period, surface characteristics, and bone quality play a more important role during the secondary stability phase.32
In the present study, implant primary stability was measured at implant placement using RFA and followed up at 3 and 6 weeks to evaluate dynamic changes that may occur around dental implants during healing phases. Mean ISQ value at day 0 was 76.48, which is slightly higher than values described in other studies that ranged from 65.1 to 72.19,21,25,33 Because ISQ values are often multifactorial,19 it is always important to interpret these values according to these factors.
In the present study, BV was histologically assessed at implant placement using a bone core biopsy. When comparing ISQ at day 0 and at 3 weeks with BV values, a positive correlation was found between these 2 values, whereas no correlation was found at 6 weeks. Other studies found similar results when comparing ISQ to clinically assessed bone density or to bone mineral density; Ostman et al19 described a significant correlation between clinically assessed bone density and ISQ values, as did Aksoy et al,33 who also established a correlation between HU values and ISQ but could not establish any correlation between histologically evaluated BV and ISQ values. Huwiler et al34 also could not establish any correlation between ISQ and BV. In the present study because BV was measured at baseline, bone remodeling after surgery may have occurred, leading to a variation in actual BV values at 3 weeks and mainly at 6 weeks. This may explain the absence of correlation between BV at baseline and ISQ at 6-week interval. Future studies should consider this factor whenever comparing BV at different time points.
IT values are very important for clinical determination of primary stability levels and absence of micromovement whenever early or immediate load is applied.4 IT values are thus believed to influence ISQ measures. In the present study, IT values were recorded at implant placement and showed significant correlation with ISQ. This is in agreement with in vitro experiments performed by Trisi et al18 showing a positive significant correlation between IT and ISQ. Also, Turkyilmaz et al,11 in a clinical study, found a positive correlation between IT and ISQ values (r = 0.853; P < 0.001).
Friberg et al35 compared cutting resistance values to ISQ and found a correlation only at the neck of the implant, which suggests a possible influence of the cortical bone on ISQ values. This hypothesis was also suggested by many authors.19,22,23 Preoperatively, Miyamoto et al23 digitally measured the thickness of the cortical bone at the placement sites of 225 implants. They found a strong linear correlation between cortical bone thickness and ISQ values (r = 0.84; P < 0.0001). In the present study, mean mandibular ISQ values were significantly higher than mean maxillary values, which had also been observed in other studies.19,36 This may, in a part, be explained by bone anatomy variations between both upper and lower jaws. Mandibular bone usually presents a 1- to 3-mm cortical thickness followed by softer bone. This cortical region of the bone likely plays a major role in initial primary stability because implants may be easily stabilized in this compact tissue. Nevertheless, this limited area of stability must be observed critically because bone remodeling and resorption can cause a decrease in stability over short healing periods.
In the present study, implant diameter showed correlation with ISQ values at 3 and 6 weeks, whereas implant length did not show any. These findings are in agreement with Ostman et al,19 who reported a statistically significant correlation between ISQ and implant length and diameter; there was an increase in stability with implant diameter and a decrease in stability with implant length. However, a recent study demonstrated that implant diameter did not contribute to the variability of ISQ values over a 12-week healing period.25 Our findings suggest that implants with a larger diameter may have a better chance to engage much cortical bone, which in part plays a role in increasing ISQ measures.
When comparing ISQ values over the entire 6-week period, initial decrease at 3 weeks followed by an increase at 6 weeks was observed in a statistically significant manner. These results are in agreement with other studies of RFA measurements over healing periods.21,25,26 This dynamic behavior over 6 weeks is explained by the healing process that occurs around dental implants during early healing phases. In a histological study, Berglundh et al13 described different phases of bone healing around the implants in an animal model. The authors13 suggested that osseointegration is a dynamic process that starts with an early establishment phase characterized by bone resorption at contact points between the implant and surrounding tissues, followed by a maintenance phase characterized by new bone formation around the implant surface. It is during the establishment phase that osteoclastic activity affects initial mechanical stability leading to a decrease in corresponding ISQ values at 3 weeks. The increase of ISQ at 6 weeks can presumably be explained by new bone formation over the implant osteoconductive surface leading to biological stability by a bone-implant interlocking effect.
Whether ISQ measures can predict the degree of osseointegration is still controversial. In 2009, Abrahamsson et al37 correlated ISQ values to actual bone-to-implant contact (BIC) in implants retrieved from dogs at different time intervals. The authors concluded that the correlation between the quality of osseointegration and RFA remains unclear. In 2010, Trisi et al38 also could not correlate ISQ values with BIC on osseointegrated implants retrieved from humans. The only parameter that affected ISQ values was the number of threads in contact with compact bone.38
The present study also correlated ISQ values with implant clinical stability at abutment connection. By applying a torque of 30 N.cm in a clockwise direction, the clinical stability of implants was noted. Spinning or painful implants were considered not sufficiently osseointegrated and therefore left to heal. Sullivan et al30 considered a reverse torque of 20 N.cm as a threshold to measure osseointegration clinically. An underlying assumption in the present study was that 30 N.cm force could also be considered a proper clinical threshold to measure the quality of BIC. Eight of the 40 study implants failed this test by either spinning or inducing pain. For all of these 8 implants, ISQ values were significantly lower than positively torqued implants, at baseline, 3 weeks, and 6 weeks. ISQ values at 6 weeks also showed a continuing decrease, whereas positively torqued implants showed an increase in ISQ values at 6 weeks. This decrease can be an interesting indicator on bone-to-implant interface status. These findings can be similar to those described by Glauser et al,26 who found continuously decreasing ISQ values for failing implants over 12-month follow-up, whereas surviving implants showed an increase in these values. These findings suggest that ISQ may be an indicator of future implant behavior considering a threshold value can be determined at baseline or at follow-up periods. However, because many factors may decrease or increase ISQ, it is very difficult to determine this threshold value.
On another hand, when correlating these 8 implants with BV and IT values, it was interesting to notice that mean IT was 39 N.cm for spinning/painful implants versus 88 N.cm for positively torqued implants. Because IT values correlated with ISQ values, these findings reaffirm the importance of primary stability during the early phase of implant healing. BV values were also a predictive of negative behavior at 6 weeks because mean BV for spinning/painful implants was 28% versus 48.5% for positively torqued implants. This underscored the importance of bone environment around implants from both a biological and mechanical point of view. Indeed, higher BV allowed, over rather short healing periods, better bone apposition over implant surface whenever an optimal mechanical stability was maintained.
Measuring implant stability by means of RFA can give the surgeon an indication of clinical implant behavior over healing period. IT and BV are 2 major determinants for this stability and significantly affected ISQ values in this study. When comparing implant clinical behavior at 6 weeks with IT, BV, and ISQ, it was shown that secondary healing and the quality of bone-to-implant interface correlated with all of these parameters. Nevertheless, ISQ measurements cannot yet be standardized between different implants but rather for a same implant over an observation period. Future studies may be interesting if a reproducible ISQ threshold value can be predicted and thus used as an indicator for future loading protocols.
The authors do not have any financial interests, either directly or indirectly, in the products or information listed in this article.
The dental implants used in this experiment were donated by Zimmer Dental Inc, Carlsbad, CA. The authors thank Dr Nada El Osta for her valuable statistical advice and analysis.
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