Does intraoperative bone density testing correlate with parameters of primary implant stability? A pilot study in minipigs

Abstract Objectives Bone density, surgical protocol, and implant design are the major determinants of primary stability. The goal of this animal trial was to investigate potential correlations of intraoperative bone density testing with clinical and histologic parameters of primary implant stability. Material and methods Following extractions of all mandibular premolars and subsequent healing, four implants each were placed in a total of four minipigs. Bone density was determined by applying intraoperative compressive tests using a device named BoneProbe whereas measurements of implant insertion torque and resonance frequency analysis were used for evaluating implant stability. Bone mineral density (BMD) and bone to implant contact were quantified after harvesting mandibular block sections. Spearman rank correlation tests were performed for evaluating correlations (α = .05). Results Due to variation in clinical measurements, only weak correlations could be identified. A positive correlation was found between the parameters bone to implant contact and BMD (Spearman's rho .53; p = .05) whereas an inverse correlation was observed between BMD and implant stability (Spearman's rho −.61; p = .03). Both BoneProbe measurements in the cortical and trabecular area positively correlated with implant insertion torque (Spearman's rho 0.60; p = .02). A slightly stronger correlation was observed between the average of both BoneProbe measurements and implant insertion torque (Spearman's rho.66; p = .01). Conclusions While establishing exact relationships among parameters of implant stability and the measurement techniques applied would require greater sample size, intraoperative compressive testing of bone might, despite the weak correlations seen here, be a useful tool for predicting primary implant stability.

All these measurements have in common that they are applied in a retrospective fashion, that is, the implant has already been installed, and alterations in the surgical protocol are no longer possible.
Although high levels of insertion torque have been recommended for immediate loading protocols due to lower micromotion at the implant bone interface (Trisi, Todisco, Consolo, & Travaglini, 2011), potentially negative effects resulting from the associated bone damage and microfractures leading to implant stability loss at compression sites (Wilson et al., 2016) and bone resorption (Cha et al., 2015) have been discussed. In this context, it has been shown that also trabecular bone may contribute to primary implant stability (Dorogoy, Rittel, Shemtov-Yona, & Korabi, 2017) whereas cortical bone may resorb if implants cause too much strain during insertion (Eom et al., 2016). It could be shown in a clinical study that overstressing cortical bone by inserting a tapered implant can result in greater likelihood of failure (Menicucci et al., 2012). Similarly, Duyck and coworkers showed that lower levels of insertion torque applied on dental implants led to pronounced bone neoformation (Duyck et al., 2015).
Based on a materials law describing the mechanical properties of both cortical and trabecular bone and following Finite Element Simulations, compressive tests of alveolar bone surrounding an implant osteotomy seemed to be suitable for objectively determining bone density (Winter, Krafft, Steinmann, & Karl, 2011). A device named BoneProbe and consisting of a gradually expandable segmented metal cylinder, which could be inserted into an implant osteotomy, was designed and tested in vitro (Krafft, Winter, Wichmann, & Karl, 2012). In principal, the BoneProbe correlates a certain level of sensor expansion with the force needed to reach this level of expansion. Further studies showed that even small changes in bone density induced, for example, by osteotomes could be detected in vitro (Krafft, Graef, Winter, Wichmann, & Karl, 2013), and BoneProbe measurements correlated well with early implant healing in an extraoral animal model . The latest version of the BoneProbe was designed as an addition to a surgical motor in the form of a modified contra angle handpiece, where the motor could be used for measuring the torque required for a certain level of expansion. Reasonable reliability of this device could be proven in a human cadaver study (Karl, Buder, Krafft, & Grobecker-Karl, 2019).
The primary goal of this animal experiment was to obtain preliminary BoneProbe values for an intraoral animal model. As a secondary endpoint, intraoperative compressive bone density testing of native alveolar bone was to be correlated with measurements of implant insertion torque and implant stability as well as with bone mineral density (BMD) and bone to implant contact (BIC) as determined by microradiographs and histomorphometry.

| Surgical interventions
The first intervention included the bilateral extraction of all mandibular premolars. Alveolar bone was reduced vertically, bone contours were rounded, and periosteal incisions were made in order to achieve primary closure of the soft tissue. After a healing period of 12 weeks, midcrestal incisions were made and mucoperiosteal flaps spanning the complete edentulous area on both sides of the mandible were carefully reflected. A total of four study sites were subsequently available in each animal. Implant site preparation Osstell mentor device and implant-specific SmartPeg abutments (RFA, Osstell AB, Gothenburg, Sweden). All of these measurements were carried out by one single experienced surgeon. As the animals were sacrificed following implant insertion, the wounds were not closed.

| Histomorphometric and mircoradiographic analysis
All bone specimens were fixed in 10% neutral-buffered formalin for 48 hr and reduced to rectangular blocks containing the study sites using a diamond band saw (EXAKT 300, EXAKT Advanced Technologies GmbH, Norderstedt, Germany). Subsequently, the specimens were dehydrated in alcohol solutions of increasing concentrations, clarified in xylene and embedded in polymethylmethacrylate (Technovit 9100, Heraeus Kulzer, Hanau, Germany). One buccolingual section parallel to the long axis of the implant was obtained per specimen by a cutting and grinding technique (Donath & Breuner, 1982). With the sections reduced to a thickness of 120 μm, microra- F I G U R E 1 Creation of a 2.8-mm osteotomy in a healed alveolar ridge (a) was followed by BoneProbe measurements depicted here with the sensing element of the BoneProbe inserted into the drill hole and gradually expanded recording the required torque as a measure of bone density (b). As a final step, a bone level implant was inserted while actively measuring the torque required (c)

| Statistical analysis
In addition to compressive bone density testing in the cervical and apical part of an implant osteotomy (BP cortical and BP trabecular), the parameters determined were maximum implant insertion torque, primary implant stability, BMD, and BIC. Spearman rank correlation tests were used for describing potential correlations between different parameters. The level of significance was set at α = .05 for all statistical operations conducted.

| RESULTS
All surgical interventions could be completed successfully, and healing following tooth extractions was uneventful. Due to insufficient vertical bone volume above the mandibular canal in two study sites, only a total of 14 implants instead of the envisaged 16 implants could be placed.
The mean values and standard deviations for all measurements conducted are given in Table 1 The only significant correlations among clinical measurements were found between compressive testing and implant insertion torque. This seems to be in line with previous studies in this field (Degidi F I G U R E 2 Typical microradiograph (a) and histologic section following toluidine blue staining (b) used for determining bone mineral density and bone to implant contact Results of clinical, microradiographic, and histomorphometric measurements performed  and cortical thickness having an impact on primary stability but were not totally linearly correlated with insertion torque and stability measurements (Huang et al., 2011). Similarly, an increase in bone density or the presence of a cortical layer led to higher primary stability in an in vitro study, but the interrelationships among the measurements made remained unclear (Wang et al., 2015).
The benefit of intraoperative compressive testing of bone could be the possibility of adapting the surgical protocol (Sierra-Rebolledo et al., 2016) in order not to overstress cortical bone (Duyck et al., 2015) trying to avoid bone damage leading to bone resorption (Eom et al., 2016;Menicucci et al., 2012). Another advantage of the BoneProbe besides being independent from a specific implant system might be that it allows for assessing cortical and trabecular bone separately, which takes into account that also trabecular bone may also contribute to primary implant stability (Dorogoy et al., 2017