Kei Isoda Y asunori Ayukawa Y oshihiro Tsukiyama Motofumi Sogo Y asuyuki Matsushita Kiyoshi Koyano

Relationship between the bone density estimated by cone-beam computed tomography and the primary stability of dental implants

Authors afliations: Kei Isoda, Y asunori Ayukawa, Yoshihiro Tsukiyama, Y asuyuki Matsushita, Kiyoshi Koyano, Section of Implant and Rehabilitative Dentistry, Division of Oral Rehabilitation, Faculty of Dental Science, Kyushu University, Fukuoka, Japan Motofumi Sogo, Department of Prosthodontics and Oral Rehabilitation, Osaka University Graduate School of Dentistry, Osaka, Japan Corresponding author: Kei Isoda, DDS, PhD Section of Implant and Rehabilitative Dentistry Division of Oral Rehabilitation Faculty of Dental Science Kyushu University 3-1-1 Maidashi Higashi-ku Fukuoka 812-8582 Japan Tel.: 81 92 642 6441 Fax: 81 92 642 6380 e-mail: k-isoda @dent.kyushu-u.ac.jp

Key words: bone density, cone-beam computed tomography, dental implants, insertion torque,

primary stability, resonance frequency analysis

Abstract Objectives: The aims of this study were to objectively assess bone quality with density values obtained by cone-beam computed tomography (CBCT) and to determine the correlations between bone density and primary stability of dental implants. Material and methods: Eighteen Straumann implants were inserted into 18 fresh femoral heads of swine. The bone densities of implant recipient sites were preoperatively determined by the density value using CBCT. The maximum insertion torque value of each implant was recorded using a digital torque meter. Resonance frequency, which represented a quantitative unit called the implant stability quotient (ISQ), was measured using an Osstell Mentor immediately after the implant placement. Spearmans correlation coefcient was calculated to evaluate the correlations among density values, insertion torques, and ISQs at implant placement. Results: The density values ranged from 98 to 902. The mean density value, insertion torque, and ISQ were 591 226, 13.4 5.2 Ncm, and 67.1 8.1, respectively. Statistically signicant correlations were found between the density values and insertion torque (rs 0.796, Po0.001), density values and ISQ (rs 0.529, P 0.024), and insertion torque and ISQ (rs 0.758, Po0.001). Conclusions: The bone quality evaluated by specic CBCT showed a high correlation with the primary stability of the implants. Hence, preoperative density value estimations by CBCT may allow clinicians to predict implant stability. Whether the density values obtained by the CBCT device used in the present study could be applied to other devices requires further elucidation.
s

Date: Accepted 14 March 2011

To cite this article: Isoda K, Ayukawa Y, Tsukiyama Y, Sogo M, Matsushita Y, Koyano K. Relationship between the bone density estimated by cone-beam computed tomography and the primary stability of dental implants. Clin. Oral Impl. Res. 23, 2012; 832836. doi: 10.1111/j.1600-0501.2011.02203.x

The successful treatment of dental implants is considered to be inuenced by both the quality and the quantity of available bone for implant placement. Studies have shown higher failure rates for implants placed in bone of poor quality and quantity (Jafn & Berman 1991; Herrmann et al. 2005). Hence, a precise evaluation of bone structure is essential before implant placement. Several bone classication systems have been proposed for assessing bone quality. In 1985, Lekholm and Zarb used radiographs to subjectively classify bone density into four types based on the amount of cortical and trabecular bone. This classication system has been utilized worldwide because it is easy to use without considerable investment. Misch (2008) used computed tomography (CT) to objectively classify bone density into 5 types based on Hounseld units (HU) (Hounseld 1980). This method allows for a precise and objective assessment of bone quality.

CT has been an established method to evaluate bone images before implant placement (Schwarz et al. 1987a, 1987b). It has also been used for the objective quantication of direct density measurements of bone, expressed in HU. Recently, cone-beam CT (CBCT) was exploited in machines specically designed for head and neck imaging (Hatcher et al. 2003). The overall advantages of CBCT are its high resolution (Kobayashi et al. 2004; Loubele et al. 2006; Pinsky et al. 2006; Loubele et al. 2007), potentially lower radiation dose, and reduced costs compared with CT. Although the radiation dose by CBCT depends on the exposure conditions and scan volume, it is usually lower than that by multislice CT (Okano & Jaideep 2010). However, there are several disadvantages of CBCT, including scattered radiation, the limited dynamic range of the X-ray area detectors, and density values without a linear correlation to bone density. Therefore, a method of objectively assessing bone quality has not yet been established.
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In patients with extremely low bone density, the primary stability of the implant immediately after placement is usually low. Osseointegration may not be established during the healing period (Friberg et al. 1991). A prospective clinical study regarding long-term survival rates for both mobile and immobile implants at placement was conducted (Orenstein et al. 2000). They reported that the 3-year survival rate was signicantly lower for mobile implants than that for immobile ones (Po0.001). Accordingly, the ability to predict primary implant stability and bone quality during the presurgical assessment of the implant placement site may represent an implant treatment protocol with higher predictability. A number of devices and techniques have been developed to assess implant stability, including cutting torque resistance analysis, the reverse torque test, the insertion torque test, the mobility measurement test, and resonance frequency (RF) analysis. Implant stability can be evaluated objectively, noninvasively, and easily by the insertion torque test and RF analysis. The insertion torque measurement technique, which records the torque during implant placement, provides information on the local bone quality. For the RF analysis technique, the implant stability is estis mated using an Osstell Mentor (Integration Diagnostics, Go teborg, Sweden) and SmartPeg. A number of studies have shown the relationship between bone density based on CT and primary implant stability (Ikumi & Tsutsumi 2005; Turkyilmaz et al. 2006; Horwitz et al. 2007; Turkyilmaz et al. 2007; Turkyilmaz et al. 2009). However, there are few studies about the relationship between bone density estimated by CBCT and primary implant stability. The purposes of this study were to evaluate (1) the variations in bone quality in implant recipient sites using density value recordings with CBCT, (2) insertion torque during implant placement, and (3) RF analysis immediately after implant placement and to explore possible correlations among these three parameters.

Fig. 1. Specimens (a) before preparing implant socket; (b) after preparing the implant socket.

Fig. 2. Cross-sectional cone-beam computed tomography image of the femoral head.

Straumann AG, Basel, Switzerland) with a diameter of 4.1 mm and an intrabony length of 10 mm were used.
Surgical procedure

Materials and methods

Specimens and implants

A total of 18 fresh femoral heads of swine were included in this study. After the removal of adjacent soft tissue, the surfaces of the bone blocks were attened using a carbide bur (Fig. 1). The thickness of each block was veried using precision calipers and maintained at more than 10 mm. The specimens were then examined macroscopically; a wide variety of bone types were included. Eighteen titanium screw-type implants with a large-grid sandblasted and acids etched surface (Straumann Standard Implant ,
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All implant sockets were prepared according to the manufacturers instructions using a surgical s micromotor (Implanteo , Anthogyr, Sallanches, France). Briey, a 2.2-mm pilot drill was used rst, followed by 2.8- and 3.5-mm twist drills and a 4.1-mm tap for preparation.
Radiological evaluation

The bone density of the implant recipient sites, which was expressed in density values, was preoperatively estimated using CBCT data. The density value of the CBCT device used in the present study was already conrmed in the previous study to coincide with that of helical CT (Sogo 2009). The average density values of the surrounding bone to a distance of 1 mm from the surfaces of the implant sockets were measured using specially modied software (LANDmarker Ver5, iLAND Solutions Inc., Osaka, Japan) (Fig. 3).

Radiological evaluation was performed by one s observer. CBCT scanning (GXCB-500 , Gendex, Des Plaines, IL, USA) of the specimens, which were placed in containers of water, was performed under the following conditions: 120 kV, 5 mA, a voxel size of 0.2 mm, and a scan volume 8.5 cm in diameter and 8.5 cm in height (Fig. 2).

Implant placement and insertion torque measurements

All implants were inserted by one operator. During the implant placement, the maximum insertion torque value of each implant was measured using a digital torquemeter (STC400CN, Tohnichi, Tokyo, Japan).

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Isoda et al Relationship between bone density and implant stability

Fig. 3. Average density values of the surrounding bone to a distance of 1 mm from the surfaces of the implant sockets were measured.

Fig. 4. Resonance frequency analysis measurement.

RF measurements

Immediately after the implant placement, RF s measurements were performed using the Osstell Mentor (Integration Diagnostics, Go teborg, Sweden). The SmartPegs were mounted on the implants and tightened by hand with a screw. The RF value was measured four times in four directions (every 901) for each implant (Fig. 4). RF values were represented by a quantitative unit called the implant stability quotient (ISQ) on a scale from 1 to 100. The results were expressed in ISQ and averaged for each implant.
Statistics

The statistical analyses were performed using SPSS Statistics 17.0J software (SPSS Inc., Tokyo, Japan). Spearmans correlation coefcient (rs) was calculated to evaluate the correlations among density values, insertion torques, and ISQ at implant placement. A value of Po0.05 was considered to be statistically signicant.
Fig. 5. Scatter plots of density value vs. insertion torque (a), density value vs. implant stability quotient (ISQ) (b), and insertion torque vs. ISQ (c).

Results
The density value ranged from 98 to 902. The mean density value, insertion torque, and ISQ of all implants were 591 226, 13.4 5.2 Ncm, and 67.1 8.1, respectively. Statistically significant correlations were found between bone density and insertion torque (rs 0.796, Po0.001), bone density and ISQ (rs 0.529, P 0.024), and insertion torque and ISQ (rs 0.758, Po0.001) (Fig. 5).

Discussion
Preoperative evaluation of bone quality is essential for the clinician to establish a treatment plan for implant restoration. Accurate information on bone density will help the dentist to identify suitable implant sites and determine implant design and surgical procedures. The femoral heads of swine used in this study were good representations of an actual clinical

situation regarding variances in bone density and volume. Several studies have reported the relation between bone density recordings of actual patients (Turkyilmaz & McGlumphy 2008; Song et al. 2009) or dry bones (Roze et al. 2009; Turkyilmaz et al. 2009) and primary implant stability. However, clinical studies in actual patients could not perform a unied surgical procedure with a single type of implant design. Because the dry bone used in the previous study was not fresh, the bone density values might be lower than those of actual patients (Turkyilmaz et al. 2009). Thus, experimental studies have extensively used femoral heads as the experimental model in which to insert implants (Kim et al. 2006; Siebers et al. 2007; Cehreli et al. 2009). Regarding the condition of bone, femoral heads in this study were relatively similar to actual patients because they were fresh compared with the dry bone. In the present study, the implant socket created by the tap drill was identical to that of the

implant dimensions, according to the manufacturers instructions. Hence, it was considered that the implant did not condense surrounding bone during insertion. Under this condition, preoperatively determined implant recipient sites using CBCT precisely reected the actual sites after insertion. When helical CT is used, bone density can be obtained in HU. For CBCT, however, there is no standard unit such as HU because no calibration has been conducted as yet. In this study, therefore, bone density obtained by CBCT was expressed in density values. The density values obtained by the CBCT device were conrmed to correspond reasonably with those estimated using helical CT (Activiont, Toshiba Co., Tokyo, Japan) and a monochromatic X-ray at the large synchrotron radiation facility (SPring-8, Hyogo, Japan) using a phantom made of diluted s water-soluble contrast medium (Iopamiron , Bayer Schering Pharma AG, Berlin, Germany)
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(Sogo 2009). Several studies also reported a highlevel correlation between the density values of CBCT and HU of multi-slice CT (Aranyarachkul et al. 2005; Naitoh et al. 2009; Nomura et al. 2010). The bone density might be estimated by the density values obtained by these specic CBCT devices. However, it should be noted that the density values in the present study should not be applied to other CBCT devices until further conrmatory studies are conducted. Numerous studies have reported that structures outside the scan volume affected the density values of hard and soft tissue structures within the scan volume in limited-volume CBCT (Ohnesorge et al. 2000; Katsumata et al. 2007). However, an in vitro study observed fewer effects in CBCT scans of larger (more than 10 cm) volumes (Katsumata et al. 2009). In this study, we considered that the density value of the specimen was less affected because the object was smaller than the scan volume. However, during CT acquisition of patients, there are various structures outside the scan volume affecting the density value. Hence, whether the density values obtained by the CBCT device used in the present study could be applied to other situations requires further elucidation. The previous study examined 32 helical CT scans of patients, and the recorded mean bone density value ranged from 77 to 1421 (Norton & Gamble 2001). The bone density values from 20 patients evaluated by CBCT reportedly ranged from 238 to 777 (Song et al. 2009). However, the bone density values in their study were not calibrated by standard values. In addition, the bone density values of three human mandibles (dry bone) varied between 267 and 553 HU, with a mean of 113 HU (Turkyilmaz et al. 2009). The density values recorded in the present study were similar to those of the bone density values in these reports, and can be considered to correspond to HU evaluated by helical CT.

In the present study, signicant correlations were observed between density value and insertion torque, density value and ISQ, and insertion torque and ISQ, with correlation coefcients of 0.796, 0.529, and 0.758, respectively. These ndings suggest a high correlation between the density values obtained by CBCT and primary implant stability. Previous studies also reported signicant correlations between bone density and implant stability. Twenty-four implants were placed into the anterior and posterior regions of three human cadaver mandibles, demonstrating statistically signicant correlations between the bone density values obtained by helical CT and insertion torque, bone density and ISQ, and insertion torque and ISQ (Turkyilmaz et al. 2009). The study by Akca et al. (2006) revealed signicant correlations between bone morphology and insertion torque for 12 implants placed into the edentulous maxilla and mandible of a human cadaver. A clinical study by Song et al. (2009) evaluated 61 implants placed in 20 patients and showed that the bone density obtained by CBCT showed a strong correlation with ISQ. Turkyilmaz et al. (2007) also found similar ndings with 142 implants. According to the study by Ikumi and Tsutsumi (2005), there was a strong correlation between bone density obtained by CT and cutting torque values. On the other hand, several studies have demonstrated no correlations between bone density and implant stability. Twenty-two implants were inserted into the maxillae and mandibles of human cadavers, and no correlations were found between ISQ and histomorphometric parameters of trabecular bone analyzed by micro-CT (Roze et al. 2009). A previous study by Huwiler et al. (2007) reported similar ndings in 13 patients. Unfortunately, only trabecular, not cortical, bone density was evaluated in these studies. These results suggest that preoperative evaluation of bone density should include cortical bone. In most of these

studies, either helical CT or micro-CT was used to evaluate bone density. Considering the recent broadening of the distribution of CBCT to clinics, it was required, as mentioned previously, to observe the correlation between bone density obtained by CBCT and primary implant stability. There are limitations in this study. First, the bone quality of the femoral heads of swine does not necessarily correspond completely with that of the vital jawbone of an actual patient. Second, it should be elucidated whether the density values obtained by the CBCT device used in the present study could be applied to other devices. Third, the present study utilized a unied surgical procedure with a single type of implant design. Further studies are required to determine the effects of surgical techniques and implant design, especially the tapered implant system and the condensing-osteotome technique, on primary implant stability. Within these limitations, the present study has shown that the CBCT examination before implant surgery can be helpful for evaluating bone density and predicting the primary stability of the implant.

Acknowledgements:

Special thanks are due to Dr Toru Chikui, Department of Oral and Maxillofacial Radiology, Faculty of Dental Science, Kyushu University, for providing the suggestion for this study. The authors also sincerely thank Dr Tetsuaki Watanabe, Watanabe Dental Ofce, Fukuoka, Japan, for providing access to the CBCT device. Additionally, the authors thank Dr Daisuke Kondo, Division of Oral Rehabilitation, Faculty of Dental Science, Kyushu University, for assistance with this experiment. Finally, thanks are due to Straumann Japan (Tokyo, Japan) for providing implants.

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