Influence of Simulated Bone Quality and Cortical Bone Thickness on Implant Stability Detection Using Resonance Frequency and Damping Factor Analysis Sheng-Wei Feng, DDS, MD1/Che-Tong Lin, DDS, PhD2/Wei-Jen Chang, DDS, PhD3/ Sheng-Yang Lee, DDS, PhD2/Chiang-Hui Cheng, MD4/Haw-Ming Huang, MD, PhD5 Purpose: The aim of this study was to test whether damping factor is an adequate parameter for monitoring the status of the trabecular bone-implant interface. Materials and Methods: Implants were placed in epoxy resin with elastic moduli of 2,900, 210, and 1.4 MPa to simulate cortical bone, cancellous bone, and connective tissue, respectively. Resonance frequency and damping factor (DF) values of the tested implants were measured using vibration analysis. An impulse force was used to induce vibration within implants. The DF values of the tested implants were calculated from the obtained frequency spectrum using a half-power method. The resulting data were analyzed to test the statistical effects of the cortical height and trabecular status on the DF values of the sample implants. Results: When the simulated tissue at the implant-bone interface changed from connective tissue to bone, the detected DF value decreased markedly. In addition, the mean DF value of the tested implants increased significantly (P < .05) from 0.043 ± 0.008 when the elastic modulus of the surrounding resins was 2,900 MPa to 0.114 ± 0.018 when the modulus was 1.4 MPa. Furthermore, when the tested implants were firmly fixed with 2 mm of simulated cortical bone, the alternation of healing tissue at the trabecular bone area could be detected by the DF method. Conclusion: DF is a sensitive measure for monitoring the status of oral implant osseointegration when implant boundary conditions are good at the cortical level but still weak at the trabecular bone area. Int J Oral Maxillofac Implants 2014;29:105–112. doi: 10.11607/jomi.3181 Key words: damping factor, ISQ, implant, osseointegration, vibration analysis
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or years, a healing period without loading was widely accepted to achieve osseointegration. However, data from clinical studies on the time-to-
1PhD
Student, School of Dentistry, College of Oral Medicine, Taipei Medical University, Taipei, Taiwan. 2Professor, School of Dentistry, College of Oral Medicine, Taipei Medical University, Taipei, Taiwan. 3Associate Professor, School of Dentistry, College of Oral Medicine, Taipei Medical University, Taipei, Taiwan. 4Researcher, Graduate Institute of Biomedical Materials and Tissue Engineering, College of Oral Medicine, Taipei Medical University, Taipei, Taiwan. 5Professor, Graduate Institute of Biomedical Materials and Tissue Engineering, College of Oral Medicine, Taipei Medical University, Taipei, Taiwan. Sheng-Wei Feng and Che-Tong Lin contributed equally to this work. Correspondence to: Dr Haw-Ming Huang, Graduate Institute of Biomedical Materials and Tissue Engineering, Taipei Medical University, 250 Wu-Hsing Street, Taipei, Taiwan. Email: [email protected] ©2014 by Quintessence Publishing Co Inc.
loading for single-tooth implants are inconclusive,1–3 and therefore, shortening the edentulous state of patients remains a challenge for a dentist. It has been reported that immediate loading of single-implant crowns has a higher failure rate when compared with conventional loading.4,5 Although immediate singleimplant loading has been correlated with higher risks, it also provides important advantages including esthetic outcomes and marginal bone preservation.6 Recent clinical and laboratory evidence has shown that mechanobiologic stimulation can promote oral implant osseointegration,7,8 and this has been used to explain the concepts of immediate and early loading. Although the biologic concepts behind immediately loaded dental implants are quite different from the standard of delayed loading, dental implant stability at the time of surgery is one of the prerequisites for therapeutic success.9 Previous studies have suggested that cortical bone thickness and the ratio of cortical to cancellous bone at the time of implant installation are extremely important for treatment success.10,11 Radiographic and computed tomography (CT) imaging studies are commonly used to assess regional bone The International Journal of Oral & Maxillofacial Implants 105
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status. However, radiographic imaging has a limited resolution for assessing osseointegration.12 Although CT images can provide structural information about the jaw bones,13,14 this imaging modality is not appropriate for long-term follow-up. To overcome these disadvantages, vibration analysis using resonance frequency (RF) as a parameter was developed for noninvasive evaluation of bone healing around dental implants.15,16 However, high RF and implant stability quotient (ISQ) values at the initial stage do not guarantee a 100% success rate for implants. Furthermore, those values do not provide enough information regarding survival or failure of dental implants.12 Glauser et al17 investigated implants that had been subjected to immediate occlusal loading using resonance frequency analysis (RFA) and found that 11% of the implants with high ISQ values at placement failed during the first year of loading. This is because when immediately or early loaded implants are used, trabecular bone becomes more important during the healing period because of its high physiologic remodeling capacity.11 Although RFA is an excellent tool for assessing the primary stability of the cortical bone region, it provides little information about trabecular bone status at the bone-implant interface. Damping is an effect that reduces the amplitude of vibrations in an oscillatory system. For nondestructive tests, damping is considered an important parameter to check the viscoelastic behavior of composite materials by measuring energy loss. This loss of energy is known as the damping capacity.18 In engineering, the damping effect can be expressed as the damping factor (DF), a dimensionless measure describing how oscillations of a structure decay after a disturbance. It is defined as the fraction of strain energy lost in one full cycle of deformation.19 Recent studies have demonstrated that DF can be used as a noninvasive tool for monitoring changes of bone properties20,21 and to discriminate between varying degrees of osteoporosis and bone fracture.22 For detecting implant stability, the RF of the implant is strongly related to the surrounding cortical bone and exposed length of the implant.10,16 In contrast, the DF of the implant system is due to the soft tissue and immature bone structure where the implant makes direct contact. Therefore, monitoring the DF of an implant during the healing process can provide alternative information about the health of the trabecular bone area. However, studies regarding the application of DF in implant dentistry have largely been ignored. In 2010, Hayashi and colleagues23 developed a new implant stability detection device that incorporates DF as a parameter. They found that the device can assess the health of surrounding tissue around the implant site. However, in their in vitro study, the most impor-
tant tissue for implant stability, cortical bone, was not simulated. Accordingly, the aim of this study was to test whether DF can provide alternative information on stability when an implant’s boundary conditions are good at the cortical bone level but still weak at the trabecular bone. The hypothesis of this study was that the DF of an implant is highly dependent on the bone-implant interface at the trabecular bone.
MATERIALS AND METHODS In Vitro Model Setup
Traditional modal analysis and dental RFA were employed to assess the damping factor and frequency response of dental implants in a number of simulated bony conditions. The fixture bodies of the test implants (Brånemark, Nobel Biocare) were 3.75 mm in diameter and 10 mm in length, with a 4-mm healing abutment. To simulate the boundary effect of alveolar bone, the test implants were embedded in resin material set in a plastic container (30 × 15 × 20 mm). Three kinds of epoxy resin (Vishay) were used, with elastic moduli of 2,900 MPa (PL-1) to simulate cortical bone, 210 MPa (PL-2) to simulate cancellous bone, and 1.4 MPa (PL-3) to simulate connective tissue as previously reported.24,25 The elastic modulus values were obtained from the manufacturer’s instructions. The epoxy resins were prepared according to the manufacturer’s instructions. Briefly, before pouring the resin into the plastic containers, the epoxy resin was mixed with a hardener. The temperature increase caused by the exothermic reaction was continuously monitored with a thermometer during the stirring process. The epoxy resin then becomes a uniform mixture and is ready to use when the mixture reaches an adequate temperature.
Stability Detection
During detection, the test samples were fixed in a clamping stand with a torque of 6 kg-cm (Fig 1). For traditional modal analysis, the implant samples were subjected to vibration using a transient force produced by an impulse-force hammer (GK291C80; PCB Piezotronics). The vibration signal of each implant was detected using a noncontacting microphone (FM-10B, 20 kHz sensitivity, FC Electronics). The acoustic signals were then transferred to a computer equipped with a two-channel analog-to-digital (A/D) interface card (AD102 A, Prowave Engineering). Fast Fourier transform (FFT) software (SD200N, Signal Doctor, Prowave Engineering) was used to translate the response signal spectrum from a time domain (Fig 2a) to a frequency domain (Fig 2b). The specific resonance frequency (Fn) of the test implant was determined from the peak value of the vibration amplitude.
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Feng et al
Fig 1 Schematic diagram of the implant models and the experimental instruments.
Interface card Hammer
Sensor 2–8 mm
PC with FFT software
Cortical area Trabecular area
20 mm
Clamping stand
Amax Amplitude
Amplitude
Figs 2a and 2b FFT software translated the response signal spectrum from a (a) time domain into a (b) frequency domain. Damping factor (ζ) was calculated by the half-power method. Fn is the resonance frequency; Fa and Fb are the frequencies at 0.707 times the maximum amplitude of the resonance frequency.
Fa Fn Fb
Vibration time a
In this study, the damping factor (ζ) represented a ratio as calculated by the half-power method.26 As shown in Fig 2b, the damping factor (ζ) can be obtained from the following formula23: ζ = Fb – Fa 2Fn where Fn is the resonance frequency (Hz) and Fa and Fb are the frequencies at 0.707 times the maximum amplitude of the resonance frequency. For RFA, the healing abutment of the implant was removed and replaced by an L-shaped transducer (Brånemark type F1 L5), which was directly screwed into the implant. The transducer was kept in the same direction to standardize the experimental procedures. The ISQ values of the tested implants were obtained by an Osstell apparatus (Integration Diagnostics).
Experimental Procedures
To validate the apparatus in this study, RF, DF, and ISQ values of the tested PL-1 resin-embedded implants were measured immediately after the implants had been placed in the resin and every 30 minutes until 240 minutes after placement. In addition, to simulate differing bone qualities, the three values of the tested implants embedded in 20 mm PL-1, PL-2, and PL-3 resin were detected after the resins had completely polymerized overnight.
0.707 Amax
b
Frequency
To test the effects of trabecular bone status on DF, implant models with the same cortical bone thickness and different trabecular bone qualities were created. Briefly, the implant samples were pre-fixed with 2 mm PL-1 resin at the implant neck area. After complete polymerization of the PL-1, the remaining 18 mm space of the plastic container was filled with PL-1 to simulate cortical bone, PL-2 to simulate cancellous bone, and PL-3 to simulate connective tissue. The resin was allowed to set for 24 hours. Then, the RF, DF, and ISQ values of the tested implants were detected as mentioned above. Additionally, to evaluate the influence of cortical bone thickness on the detected DF values, the cortical bone thickness of the sample implant was changed from 2 mm to 8 mm in increments of 2 mm.
Statistical Analysis
Each measurement was repeated three times to verify accuracy. The data presented in this study were obtained from at least three measurements. The mean and standard deviation were calculated for later comparison and discussion. The null hypothesis of this study was that damping factor would provide additional information related to the status of cortical and trabecular bone. Oneway ANOVA (SPSS, IBM) with Tukey’s HSD test was used to test the association between DF values and the conditions at the implant-bone interface for various cortical bone thicknesses and trabecular conditions. P < .05 was considered to indicate statistical significance. The International Journal of Oral & Maxillofacial Implants 107
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Feng et al
16 Resonance frequency (kHz)
100 90
ISQ
80 70 60 50
0
30
60
a
90 120 150 180 210 240 Time (min)
12 10 8 6 4 2 0
b
0
30
60
90 120 150 180 210 240 Time (min)
Figs 3a to 3c An example of the simulated healing curves plotted using (a) ISQ, (b) resonance frequency, and (c) damping factor of the tested implant in epoxy resin.
0.20
Damping factor
14
0.15 0.10 0.05 0
0
c
30
60
90 120 150 180 210 240 Time (min)
RESULTS The accuracy of the experimental equipment was evaluated with ISQ values. Figure 3 demonstrates typical results from one of the tested implants. The detected simulated healing curves in ISQ (Fig 3a) and RF (Fig 3b) are similar in waveform. When the implant was embedded in PL-1 resin for over 60 minutes, both curves displayed higher readings as the time increased. Additionally, both curves reached a plateau at 120 minutes. Figure 3c shows that a 1.7-fold increase in damping factor occurred during the first 60 minutes, after which there was a sharp decline in DF until 120 minutes, at which point the measured DF values became stable throughout the following tests. Figure 4a illustrates the ISQ values of tested implants embedded in various simulated surrounding tissues. The detected ISQ values of tested implants did not differ significantly between implants embedded in PL-1 resin (71.83 ± 4.02) and those embedded in PL-2 resin (66.17 ± 2.99). However, the ISQ value was significantly lower for implants embedded in PL-3 resin than for implants embedded in PL-1 or PL-2 resin (P < .05).
A similar trend was found in RF values. Although there was no significant difference in the RF value between implants in the PL-1 group and the PL-2 group, there was a significant difference in the RF value between the PL-1 group and the PL-3 group (P < .05) (Fig 4b). Alternations in damping factor of the tested implants surrounded by various resins are illustrated in Fig 4c. There were significant differences in DF alternation when the tested implants were surrounded by different simulated healing tissues at the trabecular bone-implant interface. The DF values of the tested implants increased significantly from 0.043 ± 0.008 to 0.114 ± 0.018 when the elastic modulus of the surrounding resins decreased from 2,900 MPa (PL-1) to 1.4 MPa (PL-3) (P < .05) (Fig 4c). To assess the effect of cortical bone on stability, the experiments were also performed by replacing the top 2 mm of resin with PL-1 to simulate cortical bone. Figures 5a and 5b show that when the simulated 2-mm cortical bone was present, the alternations in ISQ and RF readings presented in Figs 4a and 4b disappeared. However, the significant differences in DF alternation remained (Fig 5c).
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ISQ
80 60
*
40 20 0
a
PL-1 PL-2 PL-3 Embedding material
10
.20
8
*
6 4 2 0
b
PL-1 PL-2 PL-3 Embedding material
Damping factor
Resonance frequency (kHz)
100
.15
*
.10
*
.05 0
c
PL-1 PL-2 PL-3 Embedding material
Figs 4a to 4c Values of (a) ISQ, (b) resonance frequency, and (c) damping factor of the tested implants embedded in 20-mm epoxy resins with various elastic moduli. PL-1, PL-2, and PL-3 represent the epoxy resins with elastic moduli of 2,900, 210, and 1.4 MPa, respectively (n = 5, P < .05).
ISQ
80 60 40 20 0 a
PL-1 PL-2 PL-3 Embedding material
10
.20
8
Damping factor
Resonance frequency (kHz)
100
6 4 2 0
b
PL-1 PL-2 PL-3 Embedding material
*
.15 .10
*
.05 0
c
PL-1 PL-2 PL-3 Embedding material
ISQ
80 60 40 20 0 a
2 4 8 Cortical thickness (mm)
b
PL-2 PL-3
10 8 6 4 2 0
2 4 8 Cortical thickness (mm)
PL-2 PL-3
.20 Damping factor
PL-2 PL-3
100
Resonance frequency (kHz)
Figs 5a to 5c Values of (a) ISQ, (b) resonance frequency, and (c) damping factor of the tested implants embedded in 2-mm simulated cortical bone and 18-mm simulated healing tissue at the trabecular bone area.
.15 .10 .05 0
c
**
2 4 8 Cortical thickness (mm)
Figs 6a to 6c Values of (a) ISQ, (b) resonance frequency, and (c) damping factor of the tested implants embedded in various thickness of simulated cortical bone (n = 5, P < .05).
The various models of cortical bone thickness were also used to evaluate the influence of cortical bone thickness on implant DF. As shown in Figs 6a and 6b, neither the ISQ nor the RF values differed significantly when the thickness of the simulated cortical bone was changed from 2 to 8 mm. In addition, there were no significant differences in ISQ and RF values when the material in the trabecular bone area was altered from simulated connective tissue (PL-3) to simulated
trabecular bone (PL-2). However, the mean DF value of the tested implant significantly decreased as the cortical bone thickness increased. As shown in Fig 6c, when 2 mm of simulated cortical bone was present, the mean DF value of the tested implants embedded in simulated connective tissue (0.122 ± 0.014) was twofold larger than the DF value of an analogous implant embedded in simulated trabecular bone (0.06 ± 0.001) (P < .05). The International Journal of Oral & Maxillofacial Implants 109
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DISCUSSION To validate the effectiveness of the apparatus used in this study, both in vitro RF and ISQ tests were performed. As shown in Figs 3a and 3b, there was a close relationship between the data obtained using Osstell and the traditional vibration analyzer. These results indicate that the device used in this study is appropriate for vibration analysis. According to the manufacturer’s instructions, the polymerization time of the PL-1 epoxy resin was approximately 1.5 to 2 hours, depending on the thickness of the sample. This is why both curves in Figs 3a and 3b were unchanged at 60 min but then markedly increased to a plateau at 120 minutes. The polymerization of the epoxy resin can be divided into three stages: viscosity, viscoelasticity, and elasticity. The alteration in mechanical properties of the healing tissue during osseointegration is similar to the polymerization process of the resin. When the simulated tissue at the implant-bone interface changed from connective tissue to bone tissue, elastic contributions dominated the viscoelastic properties of the healing tissue. Therefore, the marked increase in RF and ISQ values during the polymerization process of the resin can be used to represent the healing process of dental implants. At this stage, elastic contributions dominate the viscoelastic properties of the resin, resulting in a marked decrease in DF (Fig 3c). Accordingly, it is reasonable to predicate that the damping effect of an implant should decrease as osseointegration progresses when this technique is used clinically. These findings confirm the results obtained by Hayashi et al,23 who also found that the viscosity coefficient value decreased with an increase in implant stability. Bischof et al reported that the ISQ values of both the immediately and delayed loaded implants were unchanged during the first 4 weeks and then increased progressively with time.27 The curves shown in Figs 3a and 3b demonstrate a similar tendency. At the initial stage of implantation, loose fibrous connective tissue and inflammatory cells were noted in the threaded implant site, and clotted blood was found at the margins of the site.28 These findings were speculated to be associated with the results of this study, where a marked increase in DF occurred before 60 minutes, which was not seen in the ISQ and RF values (Fig 3c). During this period, the epoxy resin changed from a clear fluid state to a viscous state. RF and ISQ values are parameters of sensitivity for detecting elastic materials; therefore, changes in viscosity of the resin cannot be detected. Because viscous material contributions dominate the viscoelastic properties of the healing tissue during the early healing stage, it is reasonable to suggest that DF is more sensitive than RF for monitoring the bone-implant interface during the early healing stage.
A continuing question for in vitro models is how to simulate the viscoelastic properties of human tissues. In this study, although the mechanical properties of the solidified resin were predominantly elastic, the damping factor of these resins was not zero (Fig 4c). From Fig 4, PL-1 and PL-2 samples demonstrated a significant difference in DF but not in RF. That is, the increase in DF from PL-1 to PL-3 is not associated with the decrease of their elastic modulus. In addition, although the elastic modulus of the simulated bone tissue (2.9 GPa for cortical bone) used in this study was much lower than the real tissue, the results show the sensitivity of DF as a parameter for monitoring the health status of tissues surrounding an implant (Fig 4). When the elastic modulus of the simulated healing tissue changed from 1.4 to 2,900 MPa, the ISQ and RF values increased by approximately 1.5-fold (Figs 4a and 4b); however, an almost threefold alternation can be obtained using DF as an indicator (Fig 4c). Interestingly, when 2 mm of simulated cortical bone exists, the changes in embedded material cannot be detected using ISQ and RF (Figs 5a and 5b). In contrast, it was still possible to detect changes in DF. According to vibration theory and the results of clinical studies, cortical bone at the implant-bone interface has a dominant effect on RF and ISQ values.10,26,29,30 Therefore, it is not surprising that the two parameters do not provide sufficient information regarding secondary stability when the implant has good primary stability.9,31–33 Histologically, the main tissue within the threaded implant site consists of fibrous connective tissue for the first 3 weeks after surgery. Thus, DF is a potentially useful tool for monitoring the early stages of implant osseointegration. The achievement and maintenance of optimal implant stability are prerequisites for successful osseointegration. Primary implant stability and secondary implant stability are important factors that influence the long-term survival rate of dental implants.5 Primary implant stability is gained by immediate mechanical engagement between the implant and surrounding bone. Secondary implant stability is achieved by bone regeneration and remodeling.34 It was reported that the cortical bone thickness as well as the corticalcancellous ratio are extremely important for implant stability at the time of surgery and for treatment success.10,35 However, as shown in Fig 6, ISQ and RF values are not useful for detecting changes in cortical bone thickness in patients with good primary stability. However, as shown in Fig 6c, when the thickness of simulated cortical bone was increased from 2 mm to 4 mm, the detected DF values decreased to half their original value. Damping disperses vibrational energy through the surrounding environment. For an implant, dispersion of vibrational energy occurs at the implant under the cortical bone, where energy is transferred
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to the high-viscosity soft tissue. In this regard, the percentage of tissue contact with the implant would be an important factor affecting the sensitivity of the DF measurement. A limitation of this study was that the amount of simulated connective tissue surrounding the implant in an in vivo setting was less than there would be in the in vitro model. Thus, these results only reflected the trend of changes in RF and DF values. In addition, in this in vitro study, impact force was exerted on healing abutments. Therefore, measurements using this technique should occur prior to the delivery of a denture or superstructure. Clinical studies have shown that the thickness of cortical bone is approximately 2 mm at the mandible and approximately 1.5 mm at the maxilla.10,36 In our in vitro study, the simulated cortical bone thickness was 2 mm. In this regard, damping factor is not only useful for evaluating the status of secondary stability, but is also useful for evaluating the effects of cortical bone thickness.
CONCLUSION Our results suggest that damping factor is a sensitive parameter for evaluating soft tissue status at the trabecular bone area. Furthermore, measuring the damping factor during vibration analysis might be a more precise method for evaluating implant stability, especially when implant stability is good at the neck but loose at the trabecular bone.
Acknowledgments The authors reported no conflicts of interest related to this study.
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31. Barewal RM, Oates TW, Meredith N, Cochran DL. Resonance frequency measurement of implant stability in vivo on implants with a sandblasted and acid-etched surface. Int J Oral Maxillofac Implants 2003;18:641–651. 32. Chang WJ, Lee SY, Wu CC, et al. A newly designed resonance frequency analysis device for dental implant stability detection. Dent Mater J 2007;26:665–671. 33. Sim CP, Lang NP. Factors influencing resonance frequency analysis assessed by Osstell mentor during implant tissue integration: I. Instrument positioning, bone structure, implant length. Clin Oral Implants Res 2010;21:598–604.
34. Berglundh T, Abrahamsson I, Lang NP, Lindhe J. De novo alveolar bone formation adjacent to endosseous implants. Clin Oral Implants Res 2003;14:251–262. 35. Merheb J, Van Assche N, Coucke W, Jacobs R, Naert I, Quirynen M. Relationship between cortical bone thickness or computerized tomography-derived bone density values and implant stability. Clin Oral Implants Res 2010;21:612–617. 36. Katranji A, Misch K, Wang HL. Cortical bone thickness in dentate and edentulous human cadavers. J Periodontol 2007;78:874–878.
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or years, a healing period without loading was widely accepted to achieve osseointegration. However, data from clinical studies on the time-to-
1PhD
Student, School of Dentistry, College of Oral Medicine, Taipei Medical University, Taipei, Taiwan. 2Professor, School of Dentistry, College of Oral Medicine, Taipei Medical University, Taipei, Taiwan. 3Associate Professor, School of Dentistry, College of Oral Medicine, Taipei Medical University, Taipei, Taiwan. 4Researcher, Graduate Institute of Biomedical Materials and Tissue Engineering, College of Oral Medicine, Taipei Medical University, Taipei, Taiwan. 5Professor, Graduate Institute of Biomedical Materials and Tissue Engineering, College of Oral Medicine, Taipei Medical University, Taipei, Taiwan. Sheng-Wei Feng and Che-Tong Lin contributed equally to this work. Correspondence to: Dr Haw-Ming Huang, Graduate Institute of Biomedical Materials and Tissue Engineering, Taipei Medical University, 250 Wu-Hsing Street, Taipei, Taiwan. Email: [email protected] ©2014 by Quintessence Publishing Co Inc.
loading for single-tooth implants are inconclusive,1–3 and therefore, shortening the edentulous state of patients remains a challenge for a dentist. It has been reported that immediate loading of single-implant crowns has a higher failure rate when compared with conventional loading.4,5 Although immediate singleimplant loading has been correlated with higher risks, it also provides important advantages including esthetic outcomes and marginal bone preservation.6 Recent clinical and laboratory evidence has shown that mechanobiologic stimulation can promote oral implant osseointegration,7,8 and this has been used to explain the concepts of immediate and early loading. Although the biologic concepts behind immediately loaded dental implants are quite different from the standard of delayed loading, dental implant stability at the time of surgery is one of the prerequisites for therapeutic success.9 Previous studies have suggested that cortical bone thickness and the ratio of cortical to cancellous bone at the time of implant installation are extremely important for treatment success.10,11 Radiographic and computed tomography (CT) imaging studies are commonly used to assess regional bone The International Journal of Oral & Maxillofacial Implants 105
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status. However, radiographic imaging has a limited resolution for assessing osseointegration.12 Although CT images can provide structural information about the jaw bones,13,14 this imaging modality is not appropriate for long-term follow-up. To overcome these disadvantages, vibration analysis using resonance frequency (RF) as a parameter was developed for noninvasive evaluation of bone healing around dental implants.15,16 However, high RF and implant stability quotient (ISQ) values at the initial stage do not guarantee a 100% success rate for implants. Furthermore, those values do not provide enough information regarding survival or failure of dental implants.12 Glauser et al17 investigated implants that had been subjected to immediate occlusal loading using resonance frequency analysis (RFA) and found that 11% of the implants with high ISQ values at placement failed during the first year of loading. This is because when immediately or early loaded implants are used, trabecular bone becomes more important during the healing period because of its high physiologic remodeling capacity.11 Although RFA is an excellent tool for assessing the primary stability of the cortical bone region, it provides little information about trabecular bone status at the bone-implant interface. Damping is an effect that reduces the amplitude of vibrations in an oscillatory system. For nondestructive tests, damping is considered an important parameter to check the viscoelastic behavior of composite materials by measuring energy loss. This loss of energy is known as the damping capacity.18 In engineering, the damping effect can be expressed as the damping factor (DF), a dimensionless measure describing how oscillations of a structure decay after a disturbance. It is defined as the fraction of strain energy lost in one full cycle of deformation.19 Recent studies have demonstrated that DF can be used as a noninvasive tool for monitoring changes of bone properties20,21 and to discriminate between varying degrees of osteoporosis and bone fracture.22 For detecting implant stability, the RF of the implant is strongly related to the surrounding cortical bone and exposed length of the implant.10,16 In contrast, the DF of the implant system is due to the soft tissue and immature bone structure where the implant makes direct contact. Therefore, monitoring the DF of an implant during the healing process can provide alternative information about the health of the trabecular bone area. However, studies regarding the application of DF in implant dentistry have largely been ignored. In 2010, Hayashi and colleagues23 developed a new implant stability detection device that incorporates DF as a parameter. They found that the device can assess the health of surrounding tissue around the implant site. However, in their in vitro study, the most impor-
tant tissue for implant stability, cortical bone, was not simulated. Accordingly, the aim of this study was to test whether DF can provide alternative information on stability when an implant’s boundary conditions are good at the cortical bone level but still weak at the trabecular bone. The hypothesis of this study was that the DF of an implant is highly dependent on the bone-implant interface at the trabecular bone.
MATERIALS AND METHODS In Vitro Model Setup
Traditional modal analysis and dental RFA were employed to assess the damping factor and frequency response of dental implants in a number of simulated bony conditions. The fixture bodies of the test implants (Brånemark, Nobel Biocare) were 3.75 mm in diameter and 10 mm in length, with a 4-mm healing abutment. To simulate the boundary effect of alveolar bone, the test implants were embedded in resin material set in a plastic container (30 × 15 × 20 mm). Three kinds of epoxy resin (Vishay) were used, with elastic moduli of 2,900 MPa (PL-1) to simulate cortical bone, 210 MPa (PL-2) to simulate cancellous bone, and 1.4 MPa (PL-3) to simulate connective tissue as previously reported.24,25 The elastic modulus values were obtained from the manufacturer’s instructions. The epoxy resins were prepared according to the manufacturer’s instructions. Briefly, before pouring the resin into the plastic containers, the epoxy resin was mixed with a hardener. The temperature increase caused by the exothermic reaction was continuously monitored with a thermometer during the stirring process. The epoxy resin then becomes a uniform mixture and is ready to use when the mixture reaches an adequate temperature.
Stability Detection
During detection, the test samples were fixed in a clamping stand with a torque of 6 kg-cm (Fig 1). For traditional modal analysis, the implant samples were subjected to vibration using a transient force produced by an impulse-force hammer (GK291C80; PCB Piezotronics). The vibration signal of each implant was detected using a noncontacting microphone (FM-10B, 20 kHz sensitivity, FC Electronics). The acoustic signals were then transferred to a computer equipped with a two-channel analog-to-digital (A/D) interface card (AD102 A, Prowave Engineering). Fast Fourier transform (FFT) software (SD200N, Signal Doctor, Prowave Engineering) was used to translate the response signal spectrum from a time domain (Fig 2a) to a frequency domain (Fig 2b). The specific resonance frequency (Fn) of the test implant was determined from the peak value of the vibration amplitude.
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Feng et al
Fig 1 Schematic diagram of the implant models and the experimental instruments.
Interface card Hammer
Sensor 2–8 mm
PC with FFT software
Cortical area Trabecular area
20 mm
Clamping stand
Amax Amplitude
Amplitude
Figs 2a and 2b FFT software translated the response signal spectrum from a (a) time domain into a (b) frequency domain. Damping factor (ζ) was calculated by the half-power method. Fn is the resonance frequency; Fa and Fb are the frequencies at 0.707 times the maximum amplitude of the resonance frequency.
Fa Fn Fb
Vibration time a
In this study, the damping factor (ζ) represented a ratio as calculated by the half-power method.26 As shown in Fig 2b, the damping factor (ζ) can be obtained from the following formula23: ζ = Fb – Fa 2Fn where Fn is the resonance frequency (Hz) and Fa and Fb are the frequencies at 0.707 times the maximum amplitude of the resonance frequency. For RFA, the healing abutment of the implant was removed and replaced by an L-shaped transducer (Brånemark type F1 L5), which was directly screwed into the implant. The transducer was kept in the same direction to standardize the experimental procedures. The ISQ values of the tested implants were obtained by an Osstell apparatus (Integration Diagnostics).
Experimental Procedures
To validate the apparatus in this study, RF, DF, and ISQ values of the tested PL-1 resin-embedded implants were measured immediately after the implants had been placed in the resin and every 30 minutes until 240 minutes after placement. In addition, to simulate differing bone qualities, the three values of the tested implants embedded in 20 mm PL-1, PL-2, and PL-3 resin were detected after the resins had completely polymerized overnight.
0.707 Amax
b
Frequency
To test the effects of trabecular bone status on DF, implant models with the same cortical bone thickness and different trabecular bone qualities were created. Briefly, the implant samples were pre-fixed with 2 mm PL-1 resin at the implant neck area. After complete polymerization of the PL-1, the remaining 18 mm space of the plastic container was filled with PL-1 to simulate cortical bone, PL-2 to simulate cancellous bone, and PL-3 to simulate connective tissue. The resin was allowed to set for 24 hours. Then, the RF, DF, and ISQ values of the tested implants were detected as mentioned above. Additionally, to evaluate the influence of cortical bone thickness on the detected DF values, the cortical bone thickness of the sample implant was changed from 2 mm to 8 mm in increments of 2 mm.
Statistical Analysis
Each measurement was repeated three times to verify accuracy. The data presented in this study were obtained from at least three measurements. The mean and standard deviation were calculated for later comparison and discussion. The null hypothesis of this study was that damping factor would provide additional information related to the status of cortical and trabecular bone. Oneway ANOVA (SPSS, IBM) with Tukey’s HSD test was used to test the association between DF values and the conditions at the implant-bone interface for various cortical bone thicknesses and trabecular conditions. P < .05 was considered to indicate statistical significance. The International Journal of Oral & Maxillofacial Implants 107
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Feng et al
16 Resonance frequency (kHz)
100 90
ISQ
80 70 60 50
0
30
60
a
90 120 150 180 210 240 Time (min)
12 10 8 6 4 2 0
b
0
30
60
90 120 150 180 210 240 Time (min)
Figs 3a to 3c An example of the simulated healing curves plotted using (a) ISQ, (b) resonance frequency, and (c) damping factor of the tested implant in epoxy resin.
0.20
Damping factor
14
0.15 0.10 0.05 0
0
c
30
60
90 120 150 180 210 240 Time (min)
RESULTS The accuracy of the experimental equipment was evaluated with ISQ values. Figure 3 demonstrates typical results from one of the tested implants. The detected simulated healing curves in ISQ (Fig 3a) and RF (Fig 3b) are similar in waveform. When the implant was embedded in PL-1 resin for over 60 minutes, both curves displayed higher readings as the time increased. Additionally, both curves reached a plateau at 120 minutes. Figure 3c shows that a 1.7-fold increase in damping factor occurred during the first 60 minutes, after which there was a sharp decline in DF until 120 minutes, at which point the measured DF values became stable throughout the following tests. Figure 4a illustrates the ISQ values of tested implants embedded in various simulated surrounding tissues. The detected ISQ values of tested implants did not differ significantly between implants embedded in PL-1 resin (71.83 ± 4.02) and those embedded in PL-2 resin (66.17 ± 2.99). However, the ISQ value was significantly lower for implants embedded in PL-3 resin than for implants embedded in PL-1 or PL-2 resin (P < .05).
A similar trend was found in RF values. Although there was no significant difference in the RF value between implants in the PL-1 group and the PL-2 group, there was a significant difference in the RF value between the PL-1 group and the PL-3 group (P < .05) (Fig 4b). Alternations in damping factor of the tested implants surrounded by various resins are illustrated in Fig 4c. There were significant differences in DF alternation when the tested implants were surrounded by different simulated healing tissues at the trabecular bone-implant interface. The DF values of the tested implants increased significantly from 0.043 ± 0.008 to 0.114 ± 0.018 when the elastic modulus of the surrounding resins decreased from 2,900 MPa (PL-1) to 1.4 MPa (PL-3) (P < .05) (Fig 4c). To assess the effect of cortical bone on stability, the experiments were also performed by replacing the top 2 mm of resin with PL-1 to simulate cortical bone. Figures 5a and 5b show that when the simulated 2-mm cortical bone was present, the alternations in ISQ and RF readings presented in Figs 4a and 4b disappeared. However, the significant differences in DF alternation remained (Fig 5c).
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ISQ
80 60
*
40 20 0
a
PL-1 PL-2 PL-3 Embedding material
10
.20
8
*
6 4 2 0
b
PL-1 PL-2 PL-3 Embedding material
Damping factor
Resonance frequency (kHz)
100
.15
*
.10
*
.05 0
c
PL-1 PL-2 PL-3 Embedding material
Figs 4a to 4c Values of (a) ISQ, (b) resonance frequency, and (c) damping factor of the tested implants embedded in 20-mm epoxy resins with various elastic moduli. PL-1, PL-2, and PL-3 represent the epoxy resins with elastic moduli of 2,900, 210, and 1.4 MPa, respectively (n = 5, P < .05).
ISQ
80 60 40 20 0 a
PL-1 PL-2 PL-3 Embedding material
10
.20
8
Damping factor
Resonance frequency (kHz)
100
6 4 2 0
b
PL-1 PL-2 PL-3 Embedding material
*
.15 .10
*
.05 0
c
PL-1 PL-2 PL-3 Embedding material
ISQ
80 60 40 20 0 a
2 4 8 Cortical thickness (mm)
b
PL-2 PL-3
10 8 6 4 2 0
2 4 8 Cortical thickness (mm)
PL-2 PL-3
.20 Damping factor
PL-2 PL-3
100
Resonance frequency (kHz)
Figs 5a to 5c Values of (a) ISQ, (b) resonance frequency, and (c) damping factor of the tested implants embedded in 2-mm simulated cortical bone and 18-mm simulated healing tissue at the trabecular bone area.
.15 .10 .05 0
c
**
2 4 8 Cortical thickness (mm)
Figs 6a to 6c Values of (a) ISQ, (b) resonance frequency, and (c) damping factor of the tested implants embedded in various thickness of simulated cortical bone (n = 5, P < .05).
The various models of cortical bone thickness were also used to evaluate the influence of cortical bone thickness on implant DF. As shown in Figs 6a and 6b, neither the ISQ nor the RF values differed significantly when the thickness of the simulated cortical bone was changed from 2 to 8 mm. In addition, there were no significant differences in ISQ and RF values when the material in the trabecular bone area was altered from simulated connective tissue (PL-3) to simulated
trabecular bone (PL-2). However, the mean DF value of the tested implant significantly decreased as the cortical bone thickness increased. As shown in Fig 6c, when 2 mm of simulated cortical bone was present, the mean DF value of the tested implants embedded in simulated connective tissue (0.122 ± 0.014) was twofold larger than the DF value of an analogous implant embedded in simulated trabecular bone (0.06 ± 0.001) (P < .05). The International Journal of Oral & Maxillofacial Implants 109
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DISCUSSION To validate the effectiveness of the apparatus used in this study, both in vitro RF and ISQ tests were performed. As shown in Figs 3a and 3b, there was a close relationship between the data obtained using Osstell and the traditional vibration analyzer. These results indicate that the device used in this study is appropriate for vibration analysis. According to the manufacturer’s instructions, the polymerization time of the PL-1 epoxy resin was approximately 1.5 to 2 hours, depending on the thickness of the sample. This is why both curves in Figs 3a and 3b were unchanged at 60 min but then markedly increased to a plateau at 120 minutes. The polymerization of the epoxy resin can be divided into three stages: viscosity, viscoelasticity, and elasticity. The alteration in mechanical properties of the healing tissue during osseointegration is similar to the polymerization process of the resin. When the simulated tissue at the implant-bone interface changed from connective tissue to bone tissue, elastic contributions dominated the viscoelastic properties of the healing tissue. Therefore, the marked increase in RF and ISQ values during the polymerization process of the resin can be used to represent the healing process of dental implants. At this stage, elastic contributions dominate the viscoelastic properties of the resin, resulting in a marked decrease in DF (Fig 3c). Accordingly, it is reasonable to predicate that the damping effect of an implant should decrease as osseointegration progresses when this technique is used clinically. These findings confirm the results obtained by Hayashi et al,23 who also found that the viscosity coefficient value decreased with an increase in implant stability. Bischof et al reported that the ISQ values of both the immediately and delayed loaded implants were unchanged during the first 4 weeks and then increased progressively with time.27 The curves shown in Figs 3a and 3b demonstrate a similar tendency. At the initial stage of implantation, loose fibrous connective tissue and inflammatory cells were noted in the threaded implant site, and clotted blood was found at the margins of the site.28 These findings were speculated to be associated with the results of this study, where a marked increase in DF occurred before 60 minutes, which was not seen in the ISQ and RF values (Fig 3c). During this period, the epoxy resin changed from a clear fluid state to a viscous state. RF and ISQ values are parameters of sensitivity for detecting elastic materials; therefore, changes in viscosity of the resin cannot be detected. Because viscous material contributions dominate the viscoelastic properties of the healing tissue during the early healing stage, it is reasonable to suggest that DF is more sensitive than RF for monitoring the bone-implant interface during the early healing stage.
A continuing question for in vitro models is how to simulate the viscoelastic properties of human tissues. In this study, although the mechanical properties of the solidified resin were predominantly elastic, the damping factor of these resins was not zero (Fig 4c). From Fig 4, PL-1 and PL-2 samples demonstrated a significant difference in DF but not in RF. That is, the increase in DF from PL-1 to PL-3 is not associated with the decrease of their elastic modulus. In addition, although the elastic modulus of the simulated bone tissue (2.9 GPa for cortical bone) used in this study was much lower than the real tissue, the results show the sensitivity of DF as a parameter for monitoring the health status of tissues surrounding an implant (Fig 4). When the elastic modulus of the simulated healing tissue changed from 1.4 to 2,900 MPa, the ISQ and RF values increased by approximately 1.5-fold (Figs 4a and 4b); however, an almost threefold alternation can be obtained using DF as an indicator (Fig 4c). Interestingly, when 2 mm of simulated cortical bone exists, the changes in embedded material cannot be detected using ISQ and RF (Figs 5a and 5b). In contrast, it was still possible to detect changes in DF. According to vibration theory and the results of clinical studies, cortical bone at the implant-bone interface has a dominant effect on RF and ISQ values.10,26,29,30 Therefore, it is not surprising that the two parameters do not provide sufficient information regarding secondary stability when the implant has good primary stability.9,31–33 Histologically, the main tissue within the threaded implant site consists of fibrous connective tissue for the first 3 weeks after surgery. Thus, DF is a potentially useful tool for monitoring the early stages of implant osseointegration. The achievement and maintenance of optimal implant stability are prerequisites for successful osseointegration. Primary implant stability and secondary implant stability are important factors that influence the long-term survival rate of dental implants.5 Primary implant stability is gained by immediate mechanical engagement between the implant and surrounding bone. Secondary implant stability is achieved by bone regeneration and remodeling.34 It was reported that the cortical bone thickness as well as the corticalcancellous ratio are extremely important for implant stability at the time of surgery and for treatment success.10,35 However, as shown in Fig 6, ISQ and RF values are not useful for detecting changes in cortical bone thickness in patients with good primary stability. However, as shown in Fig 6c, when the thickness of simulated cortical bone was increased from 2 mm to 4 mm, the detected DF values decreased to half their original value. Damping disperses vibrational energy through the surrounding environment. For an implant, dispersion of vibrational energy occurs at the implant under the cortical bone, where energy is transferred
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to the high-viscosity soft tissue. In this regard, the percentage of tissue contact with the implant would be an important factor affecting the sensitivity of the DF measurement. A limitation of this study was that the amount of simulated connective tissue surrounding the implant in an in vivo setting was less than there would be in the in vitro model. Thus, these results only reflected the trend of changes in RF and DF values. In addition, in this in vitro study, impact force was exerted on healing abutments. Therefore, measurements using this technique should occur prior to the delivery of a denture or superstructure. Clinical studies have shown that the thickness of cortical bone is approximately 2 mm at the mandible and approximately 1.5 mm at the maxilla.10,36 In our in vitro study, the simulated cortical bone thickness was 2 mm. In this regard, damping factor is not only useful for evaluating the status of secondary stability, but is also useful for evaluating the effects of cortical bone thickness.
CONCLUSION Our results suggest that damping factor is a sensitive parameter for evaluating soft tissue status at the trabecular bone area. Furthermore, measuring the damping factor during vibration analysis might be a more precise method for evaluating implant stability, especially when implant stability is good at the neck but loose at the trabecular bone.
Acknowledgments The authors reported no conflicts of interest related to this study.
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34. Berglundh T, Abrahamsson I, Lang NP, Lindhe J. De novo alveolar bone formation adjacent to endosseous implants. Clin Oral Implants Res 2003;14:251–262. 35. Merheb J, Van Assche N, Coucke W, Jacobs R, Naert I, Quirynen M. Relationship between cortical bone thickness or computerized tomography-derived bone density values and implant stability. Clin Oral Implants Res 2010;21:612–617. 36. Katranji A, Misch K, Wang HL. Cortical bone thickness in dentate and edentulous human cadavers. J Periodontol 2007;78:874–878.
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