- Email: [email protected]
Clinical study of the relationship between implant stability measurements using Periotest and Osstell mentor and bone quality assessment
Vol. 113 No. 3 March 2012
Clinical study of the relationship between implant stability measurements using Periotest and Osstell mentor and bone quality assessment Ji-Su Oh, DDS, MSD,a and Su-Gwan Kim, DDS, PhD,b Gwangju, Republic of Korea CHOSUN UNIVERSITY
Objectives. The purpose of this study was to evaluate the relationship between subjective bone quality assessments and objective implant stability values using Periotest and Osstell Mentor, which are widely used clinically, to assess the correlation between these 2 measurements. Study Design. A total of 211 dental implants (114 in the maxilla and 97 in the mandible) were placed in 162 patients (89 males and 73 females). Bone quality type was classified according to the Lekholm and Zarb classification. After implant placement, implant stability was measured using Periotest and Osstell Mentor. Implant stability was represented by the implant stability quotient (ISQ) values and periotest values (PTVs). All of the procedures were performed by 1 operator to reduce potential errors. Results. The ISQ values were higher in the mandible (72.77 ⫾ 8.77) than in the maxilla (65.72 ⫾ 8.65), whereas PTVs were lower in the mandible (⫺3.02 ⫾ 2.63) than in the maxilla (⫺0.17 ⫾ 2.82). A statistically significant correlation was found between bone quality type and both ISQ values and PTVs. A significant negative correlation was found between the ISQ values and PTVs (P ⬍ .01). Conclusion. Both measurements seem to be useful in predicting implant placement prognosis and in determining loading protocols. (Oral Surg Oral Med Oral Pathol Oral Radiol 2012;113:e35-e40)
Stability is generally defined as “a measure of the difficulty of displacing an object or system from equilibrium.”1 Implant stability could be considered as a clinical condition without mobility2 and defined as the capacity to withstand loading from axial, lateral, and rotational directions.3 Therefore, maintaining implant stability is an essential condition for the successful clinical outcome of implants.2 Primary stability is difficult to define clinically, although it has been understood to involve the lack of implant movement1 or achievement of biometric stability4 immediately after placement. Primary stability has been applied as an indicator of future osseointegration.5 The early failure of implants is caused by excessive mechanical stress and poor primary stability.6 Greater primary stability enables uninhibited healing and osseointegration because of little micromotion between implants and bone.6,7 In This study was supported by a grant of the Korea Healthcare technology R&D Project, Ministry for Health, Welfare & Family Affairs, Republic of Korea (A100244). a Assistant Professor, Department of Oral & Maxillofacial Surgery, School of Dentistry, Chosun University, Gwangju, Republic of Korea. b Professor, Department of Oral & Maxillofacial Surgery, School of Dentistry, Chosun University, Gwangju, Republic of Korea. Received for publication Jan 19, 2011; returned for revision Jun 3, 2011; accepted for publication Jul 5, 2011. © 2012 Elsevier Inc. All rights reserved. 2212-4403/$ - see front matter doi:10.1016/j.tripleo.2011.07.003
other words, the failure of an implant is a result of inflammation, bone loss, biomechanical overloading, and poor primary stability,8,9 whereas poor primary stability is considered to be the major cause of implant failure.10 In addition, primary stability is the basis for the determination of loading protocols.11 High primary stability renders immediate loading more predictable.12 In particular, in immediately loaded implants, the role of primary stability is decisive in their longterm success.13 In addition, the success of immediate or early-loading implant techniques is determined by primary implant stability and the surgeon’s ability to determine changes of stability by new bone formation and remodeling.2 Factors exerting effects on implant stability could be broadly divided into 2 categories. It has been reported that factors exerting effects on primary stability include bone quantity and quality, surgical technique, the length and diameter of the implant, and surface characteristics. The factors exerting effects on secondary stability include primary stability,14 bone remodeling, and implant surface conditions.15 Esposito et al.16 reported that surgical trauma and anatomical condition are the most important factors in primary implant loss, whereas bone quality, volume, and overload are major factors in late implant failure. Among them, poor bone quantity and quality are major risk factors in implant failures owing to ex-
e35
ORAL AND MAXILLOFACIAL SURGERY e36 Oh and Kim
cessive bone resorption and healing impairment, in comparison with the higher density of bone.17 Jaffin and Berman18 reported a 35% failure rate in type 4 bone; in their study, poor bone quantity and especially poor bone quality were the main risk factors of implant failures in cases in which the standard protocol was used. In addition, Bischof et al.19 examined the mediating effects of primary stability and reported that the diameter or length of the implant and implant deepening does not affect primary stability, but jaw type and bone type affect primary stability. Therefore, studies about correlation among various stability measurements and relationship between bone quality and implant stability may be important to evaluate the prognosis of implants and achieve effective treatment planning. In addition, the objective guideline is necessary to decide the loading protocols for immediate loading, early loading or delayed loading. Clinical studies on the relationship between bone quality and stability measurement have seldom been reported. In addition, no clinical study has compared primary stability and bone quality by applying both measurements, such as Periotest or Osstell Mentor, simultaneously. Therefore, the purpose of this study was to evaluate the correlations between 2 objective values by the Periotest and Osstell Mentor measurements, which have been clinically used primarily for the evaluation of implant stability and the relationship between these values and subjective bone quality assessments.
MATERIAL AND METHODS The study consisted of 162 patients who had implants placed at the Department of Oral and Maxillofacial Surgery of Chosun University Dental Hospital. Approval from the Institutional Review Board at Chosun University Dental Hospital, Gwangju, Korea, was obtained before onset of study. We have followed the guidelines of the Helsinki Declaration in this study. Patients with systemic diseases, such as uncontrolled diabetes mellitus, osteoporosis, liver pathology, or autoimmune disease; immunosuppressed patients; pregnant women; and those with poor oral hygiene were excluded from our study. In addition, cases involving immediate implant placement after extraction, ridge split techniques, and residual bone heights of less than 7 mm were excluded from our study and implants were limited below 5-mm diameter. The clinical evaluation of bone quality was performed according to the Lekholm and Zarb classification20 based on a radiographic assessment and the drilling resistance felt by the operator and was reported as
OOOO March 2012
Table I. The ISQ values and PTVs according to Lekholm and Zarb classification Type Type Type Type
1 2 3 4
No. of implants
ISQ
PTV
43 84 62 22
75.69 ⫾ 4.28 70.38 ⫾ 5.34 68.73 ⫾ 5.86 56.82 ⫾ 5.97
–4.79 ⫾ 2.35 ⫺2.58 ⫾ 1.87 ⫺0.53 ⫾ 1.75 3.07 ⫾ 2.59
ISQ, implant stability quotient (Osstell Mentor); PTV, periotest value (Periotest).
type 1 to type 4 immediately after implant placement. The evaluation method involved tactile sensation and was limited to 1 operator to rule out interoperator error. In addition, measurement of implant stability by Periotest and Osstell Mentor was restricted to 1 operator to minimize the intraoperator error. Immediately after implant placement, a healing abutment of 4 mm in height was installed, and the stability of the implant at the abutment connection was measured by Periotest to reduce errors associated with periotest values (PTVs), depending on the site of measurement.21 According to the manufacturer’s instructions, the handpiece of the Periotest was positioned perpendicular to the implant and PTVs were measured from the buccal and lingual directions to obtain average values. In addition, for resonance frequency analysis, Smartpeg (Integration Diagnostics AB, Göteborg, Sweden) was installed in the fixture immediately after implant placement. From both buccal and lingual directions, an analyzer probe was located closer to the Smartpeg, and the implant stability quotient (ISQ) value was obtained from the Osstell Mentor. For statistical analysis, analysis of variance and t tests were performed using the software package SPSS 12.0K (SPSS Inc., Chicago, IL, USA) and differences were considered to be significant at P less than .05.
RESULTS The subjects were 162 patients (89 males and 73 females), with ages ranging from 19 to 79 years and an average age of 55.7 years. A total of 211 implants were placed. The average diameter of the placed implants was 4.18 mm (3.8-5.0 mm), and the average length was 10.54 mm (8-13 mm). Among the 211 total implants, 114 (54%) were placed in the maxilla, and 97 (46%) were placed in the mandible. Using the Lekholm and Zarb system involving classification types 1 to 4, the ISQ value and PTV for type 1 were 75.69 (SD 4.28) and ⫺4.79 (SD 2.35), respectively. For type 2, the ISQ value was 70.38 (SD 5.34), and the PTV was ⫺2.58 (SD 1.87). In bone classified as type 3, the ISQ value was 68.73 (SD 5.86), and the PTV was ⫺0.53 (SD 1.75). Finally, in type 4 cases with the
OOOO Volume 113, Number 3
ORIGINAL ARTICLE Oh and Kim e37
Table II. The correlation between ISQ values and PTVs according to jaw type Jaw type
ISQ
t
PTV
t
Maxilla Mandible
65.72 ⫾ 8.65 72.77 ⫾ 8.77
–5.867*
–0.17 ⫾ 2.82 ⫺3.02 ⫾ 2.63
7.563*
ISQ, implant stability quotient (Osstell Mentor); PTV, periotest value (Periotest). *P ⬍ .01.
Table III. The correlation between ISQ values and PTVs Variance
ISQ
PTV
ISQ PTV
1 ⫺0.777*
1
ISQ, implant stability quotient (Osstell Mentor); PTV, periotest value (Periotest). *P ⬍ .01.
weakest bone quality, the ISQ value was 56.82 (SD 5.97), and the PTV was 3.07 (SD 2.59) (Table I). For both ISQ and PTV, regarding the relationship between bone quality according to the Lekholm and Zarb classification, type 4 showed a significant difference from types 1, 2, and 3 (P ⬍ .01). The ISQ value in the mandible was 72.77 (SD 8.77), whereas the PTV was ⫺3.02 (SD 2.63). The ISQ value in the maxilla was 65.72 (SD 8.65), whereas the PTV was ⫺0.17 (SD 2.82). For both the ISQ value and PTV, the mandible was shown to be more stable than the maxilla (P ⬍ .01) (Table II). The ISQ value in the anterior mandible was 70.21 (SD 8.53) and the PTV was ⫺2.03 (SD 2.74), whereas the ISQ value in the posterior mandible was 73.87 (SD 8.70) and the PTV was ⫺3.44 (SD 2.48). There was no statistically significant difference between anterior mandible and posterior mandible (P ⬎ .05). The ISQ value in the anterior maxilla was 65.16 (SD 7.27) and the PTV was 0.01 (SD 2.12). The ISQ value in the posterior maxilla was 66.00 (SD 9.23) and the PTV was ⫺0.28 (SD 3.01). The ISQ and the PTV between anterior maxilla and posterior maxilla were not statistically significant (P ⬎ .05). The correlation between ISQ value and PTV was ⫺0.777, which was statistically significant (Table III). Fig. 1 shows the relevant scatter plot.
DISCUSSION Many methods evaluating bone density have been introduced. Among them, histologic and morphometric measurements are the gold standard for the measurement of bone density.1 These measurements include the Hounsfield unit22 using quantitative computerized tomography or quantitative cone-beam computerized to-
Fig. 1. Scatter plot of the Periotest values (PTVs) and ISQ values.
mography, dual energy X-ray absorptiometry,23 and magnetic resonance imaging24; however, such methods are limited in that they cannot be applied to all implants clinically. In 1985, Lekholm and Zarb suggested a method to evaluate bone quality based on panoramic radiographs,20 and this classification has been used worldwide because it is easy to use and does not involve a huge investment.1 Methods that can evaluate the clinical stability of implants, involve quantitative assessments that are noninvasive, do not damage the implant-bone interface, and objectively measure stability include Periotest (Siemens AG, Bensheim, Germany) and resonance frequency analysis.2 Periotest is an electronic instrument developed to quantitatively measure the damping characteristic of the periodontal ligament of teeth and to evaluate their mobility.25 It comprises a handpiece containing a metal slug that is accelerated toward a tooth. Using an electromagnetic accelerator, the tapping rod strikes 16 times in 4 seconds. The results are represented as Periotest values (PTVs), from ⫺8 (lowest mobility) to ⫹50 (highest mobility). Recently, this method has been used to assess the stability of implants26; however, this method has limitations in that it has a narrow range of values, from approximately ⫺5 to ⫹5 for measuring implant mobility and the sensitivity of this method is not sufficient.15,27 In addition, this method has been reported to be affected by a variety of factors, such as the striking position, the location of implants, and handpiece angulation.28 Therefore, although nega-
ORAL AND MAXILLOFACIAL SURGERY e38 Oh and Kim
tive PTVs imply the stability of an implant and high and positive PTVs imply the loss of stability, they cannot be documented as prognostic values.27 The Osstell Mentor (Integration Diagnostics AB, Göteborg, Sweden) is the most recently developed method of resonance frequency analysis and consists of a wireless frequency response analyzer and the metal rod Smartpeg connected to the implants. The Smartpeg contains a magnet that senses magnetic pulses generated by the frequency response analyzer. The consequent vibration results are shown as the ISQ electromagnetically. The values range from 1 (lowest stability) to 100 (highest stability).2 In studies on the prognostic value of Periotest and Osstell, the cutoff value for Periotest was ⫺2, with an 84% sensitivity and a 39% specificity.29 For Osstell, the cutoff ISQ value was 47, with sensitivity of 100% and specificity of 97%.30 Presently, resonance frequency analysis has been used more extensively for the evaluation of implant stability in clinical studies.27 Therefore, our study was performed using the Lekholm and Zarb bone quality classification, which has been widely used clinically as well as Periotest and Osstell Mentor. The high resonance frequency analysis values show both the success of the implants and the low risk of failure, whereas low or decreasing resonance frequency analysis values suggest the failure of implants and increased risks. Nevertheless, the accuracy of resonance frequency analysis threshold values for the success and failure of implants has not been elucidated.2 Glauser et al.31 reported in an immediate loading study that the ISQ value was 52 in a future failure group. On the other hand, in a future success group, the ISQ value was 68, and the probability of failure of ISQ values between 49 and 58 was 18.2%. Östman et al.32,33 reported that in immediate loading in the totally edentulous maxilla and the posterior mandible, failure rates were low when the ISQ value was greater than 60. In addition, it has been reported that ISQ values higher than 65 are associated with good responses to immediate loading, whereas low ISQ values suggest overloads or failures. In studies assessing the association of RFA and Periotest, Zix et al.34 studied the correlation between the 2 measurement methods and reported that the Osstell instrument was more precise than Periotest. In addition, in vitro studies have reported that the 2 measurement methods show a significant linear association.35,36 In our study, a similar ⫺0.777 inverse correlation was observed.
OOOO March 2012
It has been reported that PTVs are inversely correlated with bone density.28 On the other hand, Truhlar et al.26,37 evaluated the association between bone density and PTVs according to the Lekholm and Zarb classification and showed that type 1 had the lowest PTVs, although the linear correlation between PTV and the degree of bone density was not detected. In our study, regarding the association between the Lekholm and Zarb classification and PTVs, an inverse correlation was observed. In comparison with types 1, 2, and 3, PTVs for type 4 were found to be significantly higher. Degidi et al.38 reported that bone quality does not appear to be important in obtaining high ISQ values, and it has also been reported in clinical studies that the association between bone quality and ISQ values is low.39 In addition, Barewal et al.40 examined the correlation between RFA and the Lekholm and Zarb classification and reported that a difference was observed only between bone types 1 and 4. In contrast, Östman et al.3 reported that bone quality was significantly correlated to the resonance frequency analysis values. Huang et al.41 reported that when the bone quality around implants was decreased, the calculated frequency was also decreased. In addition, Friberg et al.42 measured the cutting torque and RFA values during implant placement and reported that bone quality was correlated with implant stability. It has been reported that this is because the cortical bone is 10 to 20 times stiffer than the trabecular bone.3 In our study, the ISQ value for type 1 was 75.69 (SD 4.28), whereas the ISQ value for type 4 was 56.82 (SD 5.97). As bone quality was decreased, the ISQ values decreased and types 1, 2, and 3 showed significant differences from type 4. This study was conducted to provide useful information by suggesting the approximate values associated with bone quality measurement methods that have been widely applied clinically, although they have not been the most accurate methods in assessing primary stability. This is a clinical study evaluating the correlation between the 2 primary stability measurements and bone quality, and, thus, it was difficult to control all possible factors affecting the measurement values as an in vitro study. Therefore, for the establishment of an accurate threshold or guidelines for the clinical use of Periotest and Osstell Mentor, more longitudinal analyses and clinical studies are needed. REFERENCES 1. Molly L. Bone density and primary stability in implant therapy. Clin Oral Implants Res 2006;17:124-35.
OOOO Volume 113, Number 3 2. Sennerby L, Meredith N. Implant stability measurements using resonance frequency analysis: biological and biomechanical aspects and clinical implications. Periodontol 2000 2008;47:51-66. 3. Östman PO, Hellman M, Wendelhag I, Sennerby L. Resonance frequency analysis measurements of implants at placement surgery. Int J Prosthodont 2006;19:77-83. 4. Rabel A, Kh¨ler SG, Schmidt-Westhausen AM. Clinical study on the primary stability of two dental implant systems with resonance frequency analysis. Clin Oral Investig 2007;11:257-65. 5. Friberg B, Sennerby L, Linden B, Gröndahl K, Lekholm U. Stability measurements of one-stage Brånemark implants during healing in mandibles. A clinical resonance frequency analysis study. Int J Oral Maxillofac Surg 1999;28:266-72. 6. Friberg B, Jemt T, Lekholm U. Early failures in 4,641 consecutively placed Brånemark dental implants: a study from stage 1 surgery to the connection of completed prostheses. Int J Oral Maxillofac Implants 1991;6:142-6. 7. Ivanoff CJ, Sennerby L, Lekholm U. Influence of mono and bicortical anchorage on the integration of titanium implants. A study in the rabbit tibia. Int J Oral Maxillofac Surg 1996;25:229-35. 8. Javed F, Romanos GE. Impact of diabetes mellitus and glycemic control on the osseointegration of dental implants: a systematic literature review. J Periodontol 2009;80:1719-30. 9. Javed F, Almas K. Osseointegration of dental implants in patients undergoing bisphosphonate treatment. A literature review. J Periodontol 2010;81:479-84. 10. Romanos GE. Surgical and prosthetic concepts for predictable immediate loading of oral implants. J Calif Dent Assoc 2004;32:991-1001. 11. Seong WJ, Holte JE, Holtan JR, Olin PS, Hodges JS, Ko CC. Initial stability measurement of dental implants placed in different anatomical regions of fresh human cadaver jawbone. J Prosthet Dent 2008;99:425-34. 12. Glauser R, Rée A, Lundgren A, Gottlow J, Hämmerle CH, Schärer P. Immediate occlusal loading of Brånemark implants applied in various jawbone regions: a prospective, 1-year clinical study. Clin Oral Implants Res 2001;3:204-13. 13. Romanos GE. Bone quality and the immediate loading of implants-critical aspects based on literature, research, and clinical experience. Implant Dent 2009;18:203-9. 14. Davies JE. Mechanisms of endosseous integration. Int J Prosthodont 1998;11:391-401. 15. Atsumi M, Park SH, Wang HL. Methods used to assess implant stability: current status. Int J Oral Maxillofac Implants 2007; 22:743-54. 16. Esposito M, Hirsch JM, Lekholm U, Thomsen P. Biological factors contributing to failures of osseointegrated oral implants. (I). Success criteria and epidermiology. Eur J Oral Sci 1998; 106:527-51. 17. Herrmann I, Lekholm U, Holm S, Kultje C. Evaluation of patient and implant characteristics as potential prognostic factors for oral implant failures. Int J Oral Maxillofac Implants 2005;20:220-30. 18. Jaffin RA, Berman CL. The excessive loss of Branemark fixtures in type IV bone: a 5-year analysis. J Periodontol 1991;62:2-4. 19. Bischof M, Nedir R, Szmukler-Moncler S, Bernard JP, Samson J. Implant stability measurement of delayed and immediately loaded implants during healing. Clin Oral Implants Res 2004;15:529-39. 20. Lekholm U, Zarb GA. Patient selection and preparation. In: Brånemark PI, Zarb GA, Albrektson T, editors. Tissue-integrated prostheses: osseointegration in clinical dentistry. Chicago: Quintessence; 1985. p. 199-209.
ORIGINAL ARTICLE Oh and Kim e39 21. Van Steenberghe D, Tricio J, Naert I, Nys M. Damping characteristics of bone-to-implant interfaces. A clinical study with the Periotest device. Clin Oral Implants Res 1995;6:31-9. 22. Aranyarachkul P, Caruso J, Gantes B, Schulz E, Riggs M, Dus I, et al. Bone density assessments of dental implant sites: 2. Quantitative cone-beam computerized tomography. Int J Oral Maxillofac Implants 2005;20:416-24. 23. Denissen H, Eijsink-Smeets R, van Lingen A, van Waas R. Assessing mineral density in small trephined jawbone biopsy specimens. Clin Oral Implants Res 1999;10:320-5. 24. Gray CF, Redpath TW, Smith FW. Pre-surgical dental implant assessment by magnetic resonance imaging. J Oral Implantol 1996;22:147-53. 25. Schulte W, Lukas D. Periotest to monitor osseointegration and to check the occlusion in oral implantology. J Oral Implantol 1993;19:23-32. 26. Truhlar RS, Lauciello F, Morris HF, Ochi S. The influence of bone quality on Periotest values of endosseous dental implants at stage II surgery. J Oral Maxillofac Surg 1997;55:55-61. 27. Aparicio C, Lang NP, Rangert B. Validity and clinical significance of biomechanical testing of implant/bone interface. Clin Oral Implants Res 2006;17:2-7. 28. Tricio J, van Steenberghe D, Rosenberg D, Duchateau L. Implant stability related to insertion torque force and bone density: an in vitro study. J Prosthet Dent 1995;74:608-12. 29. Noguerol B, Muñoz R, Mesa F, de Dios Luna J, O’Valle F. Early implant failure. Prognostic capacity of Periotest: retrospective study of a large sample. Clin Oral Implants Res 2006;17:459-64. 30. Nedir R, Bischof M, Szmukler-Moncler S, Bernard JP, Samson J. Predicting osseointegration by means of implant primary stability. Clin Oral Implants Res 2004;15:520-8. 31. Glauser R, Sennerby L, Meredith N, Rée A, Lundgren A, Gottlow J, et al. Resonance frequency analysis of implants subjected to immediate or early functional occlusal loading. Successful vs. failing implants. Clin Oral Implants Res 2004;15:428-34. 32. Östman PO, Hellman M, Sennerby L. Direct implant loading in the edentulous maxilla using a bone density adapted surgical protocol and primary implant stability criteria for inclusion. Clin Implant Dent Relat Res 2005;7:60-9. 33. Östman PO, Hellman M, Sennerby L. Occlusal loading of implants in the partially edentate mandible: a prospective 1-year radiographic and 4-year clinical study. Int J Oral Maxillofac Implants 2008;23:315-22. 34. Zix J, Hug S, Kessler-Liechti G, Mericske-Stern R. Measurement of dental implant stability by resonance frequency analysis and damping capacity assessment: comparison of both techniques in a clinical trial. Int J Oral Maxillofac Implants 2008;23:525-30. 35. Lachmann S, Jäger B, Axmann D, Gomez-Roman G, Groten M, Weber H. Resonance frequency analysis and damping capacity assessment. Part I: An in vitro study on measurement reliability and a method of comparison in the determination of primary dental implant stability. Clin Oral Implants Res 2006;17:75-9. 36. Lachmann S, Laval JY, Jäger B, Axmann D, Gomez-Roman G, Groten M, et al. Resonance frequency analysis and damping capacity assessment. Part 2: Peri-implant bone loss follow-up. An in vitro study with the Periotest and Osstell instruments. Clin Oral Implants Res 2006;17:80-4. 37. Truhlar RS, Morris HF, Ochi S. Stability of the bone-implant complex. Results of longitudinal testing to 60 months with the Periotest device on endosseous dental implants. Ann Periodontol 2000;5:42-55. 38. Degidi M, Daprile G, Piattelli A, Carinci F. Evaluation of factors influencing resonance frequency analysis values, at insertion surgery, of implants placed in sinus-augmented and nongrafted sites. Clin Implant Dent Relat Res 2007;9:144-9.
ORAL AND MAXILLOFACIAL SURGERY e40 Oh and Kim 39. Zix J, Kessler-Liechti G, Mericske-Stern R. Stability measurement of 1-stage implants in the maxilla by means of resonance frequency analysis: a pilot study. Int J Oral Maxillofac Implants 2005;5:747-52. 40. 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;18:641-51. 41. Huang HM, Lee SY, Yeh CY, Lin CT. Resonance frequency assessment of dental implant stability with various bone qualities: a numerical approach. Clin Oral Implants Res 2000;13:65-74. 42. Friberg B, Sennerby L, Roos J, Lekholm U. Identification of bone quality in conjunction with insertion of titanium implants.
OOOO March 2012 A pilot study in jaw autopsy specimens. Clin Oral Implants Res 1995;6:213-9.
Reprint requests: Su-Gwan Kim, DDS, PhD Department of Oral and Maxillofacial Surgery School of Dentistry Chosun University 375, SeoSukDong, DongGu GwangJu City, South Korea 501-759 [email protected]
Clinical study of the relationship between implant stability measurements using Periotest and Osstell mentor and bone quality assessment Ji-Su Oh, DDS, MSD,a and Su-Gwan Kim, DDS, PhD,b Gwangju, Republic of Korea CHOSUN UNIVERSITY
Objectives. The purpose of this study was to evaluate the relationship between subjective bone quality assessments and objective implant stability values using Periotest and Osstell Mentor, which are widely used clinically, to assess the correlation between these 2 measurements. Study Design. A total of 211 dental implants (114 in the maxilla and 97 in the mandible) were placed in 162 patients (89 males and 73 females). Bone quality type was classified according to the Lekholm and Zarb classification. After implant placement, implant stability was measured using Periotest and Osstell Mentor. Implant stability was represented by the implant stability quotient (ISQ) values and periotest values (PTVs). All of the procedures were performed by 1 operator to reduce potential errors. Results. The ISQ values were higher in the mandible (72.77 ⫾ 8.77) than in the maxilla (65.72 ⫾ 8.65), whereas PTVs were lower in the mandible (⫺3.02 ⫾ 2.63) than in the maxilla (⫺0.17 ⫾ 2.82). A statistically significant correlation was found between bone quality type and both ISQ values and PTVs. A significant negative correlation was found between the ISQ values and PTVs (P ⬍ .01). Conclusion. Both measurements seem to be useful in predicting implant placement prognosis and in determining loading protocols. (Oral Surg Oral Med Oral Pathol Oral Radiol 2012;113:e35-e40)
Stability is generally defined as “a measure of the difficulty of displacing an object or system from equilibrium.”1 Implant stability could be considered as a clinical condition without mobility2 and defined as the capacity to withstand loading from axial, lateral, and rotational directions.3 Therefore, maintaining implant stability is an essential condition for the successful clinical outcome of implants.2 Primary stability is difficult to define clinically, although it has been understood to involve the lack of implant movement1 or achievement of biometric stability4 immediately after placement. Primary stability has been applied as an indicator of future osseointegration.5 The early failure of implants is caused by excessive mechanical stress and poor primary stability.6 Greater primary stability enables uninhibited healing and osseointegration because of little micromotion between implants and bone.6,7 In This study was supported by a grant of the Korea Healthcare technology R&D Project, Ministry for Health, Welfare & Family Affairs, Republic of Korea (A100244). a Assistant Professor, Department of Oral & Maxillofacial Surgery, School of Dentistry, Chosun University, Gwangju, Republic of Korea. b Professor, Department of Oral & Maxillofacial Surgery, School of Dentistry, Chosun University, Gwangju, Republic of Korea. Received for publication Jan 19, 2011; returned for revision Jun 3, 2011; accepted for publication Jul 5, 2011. © 2012 Elsevier Inc. All rights reserved. 2212-4403/$ - see front matter doi:10.1016/j.tripleo.2011.07.003
other words, the failure of an implant is a result of inflammation, bone loss, biomechanical overloading, and poor primary stability,8,9 whereas poor primary stability is considered to be the major cause of implant failure.10 In addition, primary stability is the basis for the determination of loading protocols.11 High primary stability renders immediate loading more predictable.12 In particular, in immediately loaded implants, the role of primary stability is decisive in their longterm success.13 In addition, the success of immediate or early-loading implant techniques is determined by primary implant stability and the surgeon’s ability to determine changes of stability by new bone formation and remodeling.2 Factors exerting effects on implant stability could be broadly divided into 2 categories. It has been reported that factors exerting effects on primary stability include bone quantity and quality, surgical technique, the length and diameter of the implant, and surface characteristics. The factors exerting effects on secondary stability include primary stability,14 bone remodeling, and implant surface conditions.15 Esposito et al.16 reported that surgical trauma and anatomical condition are the most important factors in primary implant loss, whereas bone quality, volume, and overload are major factors in late implant failure. Among them, poor bone quantity and quality are major risk factors in implant failures owing to ex-
e35
ORAL AND MAXILLOFACIAL SURGERY e36 Oh and Kim
cessive bone resorption and healing impairment, in comparison with the higher density of bone.17 Jaffin and Berman18 reported a 35% failure rate in type 4 bone; in their study, poor bone quantity and especially poor bone quality were the main risk factors of implant failures in cases in which the standard protocol was used. In addition, Bischof et al.19 examined the mediating effects of primary stability and reported that the diameter or length of the implant and implant deepening does not affect primary stability, but jaw type and bone type affect primary stability. Therefore, studies about correlation among various stability measurements and relationship between bone quality and implant stability may be important to evaluate the prognosis of implants and achieve effective treatment planning. In addition, the objective guideline is necessary to decide the loading protocols for immediate loading, early loading or delayed loading. Clinical studies on the relationship between bone quality and stability measurement have seldom been reported. In addition, no clinical study has compared primary stability and bone quality by applying both measurements, such as Periotest or Osstell Mentor, simultaneously. Therefore, the purpose of this study was to evaluate the correlations between 2 objective values by the Periotest and Osstell Mentor measurements, which have been clinically used primarily for the evaluation of implant stability and the relationship between these values and subjective bone quality assessments.
MATERIAL AND METHODS The study consisted of 162 patients who had implants placed at the Department of Oral and Maxillofacial Surgery of Chosun University Dental Hospital. Approval from the Institutional Review Board at Chosun University Dental Hospital, Gwangju, Korea, was obtained before onset of study. We have followed the guidelines of the Helsinki Declaration in this study. Patients with systemic diseases, such as uncontrolled diabetes mellitus, osteoporosis, liver pathology, or autoimmune disease; immunosuppressed patients; pregnant women; and those with poor oral hygiene were excluded from our study. In addition, cases involving immediate implant placement after extraction, ridge split techniques, and residual bone heights of less than 7 mm were excluded from our study and implants were limited below 5-mm diameter. The clinical evaluation of bone quality was performed according to the Lekholm and Zarb classification20 based on a radiographic assessment and the drilling resistance felt by the operator and was reported as
OOOO March 2012
Table I. The ISQ values and PTVs according to Lekholm and Zarb classification Type Type Type Type
1 2 3 4
No. of implants
ISQ
PTV
43 84 62 22
75.69 ⫾ 4.28 70.38 ⫾ 5.34 68.73 ⫾ 5.86 56.82 ⫾ 5.97
–4.79 ⫾ 2.35 ⫺2.58 ⫾ 1.87 ⫺0.53 ⫾ 1.75 3.07 ⫾ 2.59
ISQ, implant stability quotient (Osstell Mentor); PTV, periotest value (Periotest).
type 1 to type 4 immediately after implant placement. The evaluation method involved tactile sensation and was limited to 1 operator to rule out interoperator error. In addition, measurement of implant stability by Periotest and Osstell Mentor was restricted to 1 operator to minimize the intraoperator error. Immediately after implant placement, a healing abutment of 4 mm in height was installed, and the stability of the implant at the abutment connection was measured by Periotest to reduce errors associated with periotest values (PTVs), depending on the site of measurement.21 According to the manufacturer’s instructions, the handpiece of the Periotest was positioned perpendicular to the implant and PTVs were measured from the buccal and lingual directions to obtain average values. In addition, for resonance frequency analysis, Smartpeg (Integration Diagnostics AB, Göteborg, Sweden) was installed in the fixture immediately after implant placement. From both buccal and lingual directions, an analyzer probe was located closer to the Smartpeg, and the implant stability quotient (ISQ) value was obtained from the Osstell Mentor. For statistical analysis, analysis of variance and t tests were performed using the software package SPSS 12.0K (SPSS Inc., Chicago, IL, USA) and differences were considered to be significant at P less than .05.
RESULTS The subjects were 162 patients (89 males and 73 females), with ages ranging from 19 to 79 years and an average age of 55.7 years. A total of 211 implants were placed. The average diameter of the placed implants was 4.18 mm (3.8-5.0 mm), and the average length was 10.54 mm (8-13 mm). Among the 211 total implants, 114 (54%) were placed in the maxilla, and 97 (46%) were placed in the mandible. Using the Lekholm and Zarb system involving classification types 1 to 4, the ISQ value and PTV for type 1 were 75.69 (SD 4.28) and ⫺4.79 (SD 2.35), respectively. For type 2, the ISQ value was 70.38 (SD 5.34), and the PTV was ⫺2.58 (SD 1.87). In bone classified as type 3, the ISQ value was 68.73 (SD 5.86), and the PTV was ⫺0.53 (SD 1.75). Finally, in type 4 cases with the
OOOO Volume 113, Number 3
ORIGINAL ARTICLE Oh and Kim e37
Table II. The correlation between ISQ values and PTVs according to jaw type Jaw type
ISQ
t
PTV
t
Maxilla Mandible
65.72 ⫾ 8.65 72.77 ⫾ 8.77
–5.867*
–0.17 ⫾ 2.82 ⫺3.02 ⫾ 2.63
7.563*
ISQ, implant stability quotient (Osstell Mentor); PTV, periotest value (Periotest). *P ⬍ .01.
Table III. The correlation between ISQ values and PTVs Variance
ISQ
PTV
ISQ PTV
1 ⫺0.777*
1
ISQ, implant stability quotient (Osstell Mentor); PTV, periotest value (Periotest). *P ⬍ .01.
weakest bone quality, the ISQ value was 56.82 (SD 5.97), and the PTV was 3.07 (SD 2.59) (Table I). For both ISQ and PTV, regarding the relationship between bone quality according to the Lekholm and Zarb classification, type 4 showed a significant difference from types 1, 2, and 3 (P ⬍ .01). The ISQ value in the mandible was 72.77 (SD 8.77), whereas the PTV was ⫺3.02 (SD 2.63). The ISQ value in the maxilla was 65.72 (SD 8.65), whereas the PTV was ⫺0.17 (SD 2.82). For both the ISQ value and PTV, the mandible was shown to be more stable than the maxilla (P ⬍ .01) (Table II). The ISQ value in the anterior mandible was 70.21 (SD 8.53) and the PTV was ⫺2.03 (SD 2.74), whereas the ISQ value in the posterior mandible was 73.87 (SD 8.70) and the PTV was ⫺3.44 (SD 2.48). There was no statistically significant difference between anterior mandible and posterior mandible (P ⬎ .05). The ISQ value in the anterior maxilla was 65.16 (SD 7.27) and the PTV was 0.01 (SD 2.12). The ISQ value in the posterior maxilla was 66.00 (SD 9.23) and the PTV was ⫺0.28 (SD 3.01). The ISQ and the PTV between anterior maxilla and posterior maxilla were not statistically significant (P ⬎ .05). The correlation between ISQ value and PTV was ⫺0.777, which was statistically significant (Table III). Fig. 1 shows the relevant scatter plot.
DISCUSSION Many methods evaluating bone density have been introduced. Among them, histologic and morphometric measurements are the gold standard for the measurement of bone density.1 These measurements include the Hounsfield unit22 using quantitative computerized tomography or quantitative cone-beam computerized to-
Fig. 1. Scatter plot of the Periotest values (PTVs) and ISQ values.
mography, dual energy X-ray absorptiometry,23 and magnetic resonance imaging24; however, such methods are limited in that they cannot be applied to all implants clinically. In 1985, Lekholm and Zarb suggested a method to evaluate bone quality based on panoramic radiographs,20 and this classification has been used worldwide because it is easy to use and does not involve a huge investment.1 Methods that can evaluate the clinical stability of implants, involve quantitative assessments that are noninvasive, do not damage the implant-bone interface, and objectively measure stability include Periotest (Siemens AG, Bensheim, Germany) and resonance frequency analysis.2 Periotest is an electronic instrument developed to quantitatively measure the damping characteristic of the periodontal ligament of teeth and to evaluate their mobility.25 It comprises a handpiece containing a metal slug that is accelerated toward a tooth. Using an electromagnetic accelerator, the tapping rod strikes 16 times in 4 seconds. The results are represented as Periotest values (PTVs), from ⫺8 (lowest mobility) to ⫹50 (highest mobility). Recently, this method has been used to assess the stability of implants26; however, this method has limitations in that it has a narrow range of values, from approximately ⫺5 to ⫹5 for measuring implant mobility and the sensitivity of this method is not sufficient.15,27 In addition, this method has been reported to be affected by a variety of factors, such as the striking position, the location of implants, and handpiece angulation.28 Therefore, although nega-
ORAL AND MAXILLOFACIAL SURGERY e38 Oh and Kim
tive PTVs imply the stability of an implant and high and positive PTVs imply the loss of stability, they cannot be documented as prognostic values.27 The Osstell Mentor (Integration Diagnostics AB, Göteborg, Sweden) is the most recently developed method of resonance frequency analysis and consists of a wireless frequency response analyzer and the metal rod Smartpeg connected to the implants. The Smartpeg contains a magnet that senses magnetic pulses generated by the frequency response analyzer. The consequent vibration results are shown as the ISQ electromagnetically. The values range from 1 (lowest stability) to 100 (highest stability).2 In studies on the prognostic value of Periotest and Osstell, the cutoff value for Periotest was ⫺2, with an 84% sensitivity and a 39% specificity.29 For Osstell, the cutoff ISQ value was 47, with sensitivity of 100% and specificity of 97%.30 Presently, resonance frequency analysis has been used more extensively for the evaluation of implant stability in clinical studies.27 Therefore, our study was performed using the Lekholm and Zarb bone quality classification, which has been widely used clinically as well as Periotest and Osstell Mentor. The high resonance frequency analysis values show both the success of the implants and the low risk of failure, whereas low or decreasing resonance frequency analysis values suggest the failure of implants and increased risks. Nevertheless, the accuracy of resonance frequency analysis threshold values for the success and failure of implants has not been elucidated.2 Glauser et al.31 reported in an immediate loading study that the ISQ value was 52 in a future failure group. On the other hand, in a future success group, the ISQ value was 68, and the probability of failure of ISQ values between 49 and 58 was 18.2%. Östman et al.32,33 reported that in immediate loading in the totally edentulous maxilla and the posterior mandible, failure rates were low when the ISQ value was greater than 60. In addition, it has been reported that ISQ values higher than 65 are associated with good responses to immediate loading, whereas low ISQ values suggest overloads or failures. In studies assessing the association of RFA and Periotest, Zix et al.34 studied the correlation between the 2 measurement methods and reported that the Osstell instrument was more precise than Periotest. In addition, in vitro studies have reported that the 2 measurement methods show a significant linear association.35,36 In our study, a similar ⫺0.777 inverse correlation was observed.
OOOO March 2012
It has been reported that PTVs are inversely correlated with bone density.28 On the other hand, Truhlar et al.26,37 evaluated the association between bone density and PTVs according to the Lekholm and Zarb classification and showed that type 1 had the lowest PTVs, although the linear correlation between PTV and the degree of bone density was not detected. In our study, regarding the association between the Lekholm and Zarb classification and PTVs, an inverse correlation was observed. In comparison with types 1, 2, and 3, PTVs for type 4 were found to be significantly higher. Degidi et al.38 reported that bone quality does not appear to be important in obtaining high ISQ values, and it has also been reported in clinical studies that the association between bone quality and ISQ values is low.39 In addition, Barewal et al.40 examined the correlation between RFA and the Lekholm and Zarb classification and reported that a difference was observed only between bone types 1 and 4. In contrast, Östman et al.3 reported that bone quality was significantly correlated to the resonance frequency analysis values. Huang et al.41 reported that when the bone quality around implants was decreased, the calculated frequency was also decreased. In addition, Friberg et al.42 measured the cutting torque and RFA values during implant placement and reported that bone quality was correlated with implant stability. It has been reported that this is because the cortical bone is 10 to 20 times stiffer than the trabecular bone.3 In our study, the ISQ value for type 1 was 75.69 (SD 4.28), whereas the ISQ value for type 4 was 56.82 (SD 5.97). As bone quality was decreased, the ISQ values decreased and types 1, 2, and 3 showed significant differences from type 4. This study was conducted to provide useful information by suggesting the approximate values associated with bone quality measurement methods that have been widely applied clinically, although they have not been the most accurate methods in assessing primary stability. This is a clinical study evaluating the correlation between the 2 primary stability measurements and bone quality, and, thus, it was difficult to control all possible factors affecting the measurement values as an in vitro study. Therefore, for the establishment of an accurate threshold or guidelines for the clinical use of Periotest and Osstell Mentor, more longitudinal analyses and clinical studies are needed. REFERENCES 1. Molly L. Bone density and primary stability in implant therapy. Clin Oral Implants Res 2006;17:124-35.
OOOO Volume 113, Number 3 2. Sennerby L, Meredith N. Implant stability measurements using resonance frequency analysis: biological and biomechanical aspects and clinical implications. Periodontol 2000 2008;47:51-66. 3. Östman PO, Hellman M, Wendelhag I, Sennerby L. Resonance frequency analysis measurements of implants at placement surgery. Int J Prosthodont 2006;19:77-83. 4. Rabel A, Kh¨ler SG, Schmidt-Westhausen AM. Clinical study on the primary stability of two dental implant systems with resonance frequency analysis. Clin Oral Investig 2007;11:257-65. 5. Friberg B, Sennerby L, Linden B, Gröndahl K, Lekholm U. Stability measurements of one-stage Brånemark implants during healing in mandibles. A clinical resonance frequency analysis study. Int J Oral Maxillofac Surg 1999;28:266-72. 6. Friberg B, Jemt T, Lekholm U. Early failures in 4,641 consecutively placed Brånemark dental implants: a study from stage 1 surgery to the connection of completed prostheses. Int J Oral Maxillofac Implants 1991;6:142-6. 7. Ivanoff CJ, Sennerby L, Lekholm U. Influence of mono and bicortical anchorage on the integration of titanium implants. A study in the rabbit tibia. Int J Oral Maxillofac Surg 1996;25:229-35. 8. Javed F, Romanos GE. Impact of diabetes mellitus and glycemic control on the osseointegration of dental implants: a systematic literature review. J Periodontol 2009;80:1719-30. 9. Javed F, Almas K. Osseointegration of dental implants in patients undergoing bisphosphonate treatment. A literature review. J Periodontol 2010;81:479-84. 10. Romanos GE. Surgical and prosthetic concepts for predictable immediate loading of oral implants. J Calif Dent Assoc 2004;32:991-1001. 11. Seong WJ, Holte JE, Holtan JR, Olin PS, Hodges JS, Ko CC. Initial stability measurement of dental implants placed in different anatomical regions of fresh human cadaver jawbone. J Prosthet Dent 2008;99:425-34. 12. Glauser R, Rée A, Lundgren A, Gottlow J, Hämmerle CH, Schärer P. Immediate occlusal loading of Brånemark implants applied in various jawbone regions: a prospective, 1-year clinical study. Clin Oral Implants Res 2001;3:204-13. 13. Romanos GE. Bone quality and the immediate loading of implants-critical aspects based on literature, research, and clinical experience. Implant Dent 2009;18:203-9. 14. Davies JE. Mechanisms of endosseous integration. Int J Prosthodont 1998;11:391-401. 15. Atsumi M, Park SH, Wang HL. Methods used to assess implant stability: current status. Int J Oral Maxillofac Implants 2007; 22:743-54. 16. Esposito M, Hirsch JM, Lekholm U, Thomsen P. Biological factors contributing to failures of osseointegrated oral implants. (I). Success criteria and epidermiology. Eur J Oral Sci 1998; 106:527-51. 17. Herrmann I, Lekholm U, Holm S, Kultje C. Evaluation of patient and implant characteristics as potential prognostic factors for oral implant failures. Int J Oral Maxillofac Implants 2005;20:220-30. 18. Jaffin RA, Berman CL. The excessive loss of Branemark fixtures in type IV bone: a 5-year analysis. J Periodontol 1991;62:2-4. 19. Bischof M, Nedir R, Szmukler-Moncler S, Bernard JP, Samson J. Implant stability measurement of delayed and immediately loaded implants during healing. Clin Oral Implants Res 2004;15:529-39. 20. Lekholm U, Zarb GA. Patient selection and preparation. In: Brånemark PI, Zarb GA, Albrektson T, editors. Tissue-integrated prostheses: osseointegration in clinical dentistry. Chicago: Quintessence; 1985. p. 199-209.
ORIGINAL ARTICLE Oh and Kim e39 21. Van Steenberghe D, Tricio J, Naert I, Nys M. Damping characteristics of bone-to-implant interfaces. A clinical study with the Periotest device. Clin Oral Implants Res 1995;6:31-9. 22. Aranyarachkul P, Caruso J, Gantes B, Schulz E, Riggs M, Dus I, et al. Bone density assessments of dental implant sites: 2. Quantitative cone-beam computerized tomography. Int J Oral Maxillofac Implants 2005;20:416-24. 23. Denissen H, Eijsink-Smeets R, van Lingen A, van Waas R. Assessing mineral density in small trephined jawbone biopsy specimens. Clin Oral Implants Res 1999;10:320-5. 24. Gray CF, Redpath TW, Smith FW. Pre-surgical dental implant assessment by magnetic resonance imaging. J Oral Implantol 1996;22:147-53. 25. Schulte W, Lukas D. Periotest to monitor osseointegration and to check the occlusion in oral implantology. J Oral Implantol 1993;19:23-32. 26. Truhlar RS, Lauciello F, Morris HF, Ochi S. The influence of bone quality on Periotest values of endosseous dental implants at stage II surgery. J Oral Maxillofac Surg 1997;55:55-61. 27. Aparicio C, Lang NP, Rangert B. Validity and clinical significance of biomechanical testing of implant/bone interface. Clin Oral Implants Res 2006;17:2-7. 28. Tricio J, van Steenberghe D, Rosenberg D, Duchateau L. Implant stability related to insertion torque force and bone density: an in vitro study. J Prosthet Dent 1995;74:608-12. 29. Noguerol B, Muñoz R, Mesa F, de Dios Luna J, O’Valle F. Early implant failure. Prognostic capacity of Periotest: retrospective study of a large sample. Clin Oral Implants Res 2006;17:459-64. 30. Nedir R, Bischof M, Szmukler-Moncler S, Bernard JP, Samson J. Predicting osseointegration by means of implant primary stability. Clin Oral Implants Res 2004;15:520-8. 31. Glauser R, Sennerby L, Meredith N, Rée A, Lundgren A, Gottlow J, et al. Resonance frequency analysis of implants subjected to immediate or early functional occlusal loading. Successful vs. failing implants. Clin Oral Implants Res 2004;15:428-34. 32. Östman PO, Hellman M, Sennerby L. Direct implant loading in the edentulous maxilla using a bone density adapted surgical protocol and primary implant stability criteria for inclusion. Clin Implant Dent Relat Res 2005;7:60-9. 33. Östman PO, Hellman M, Sennerby L. Occlusal loading of implants in the partially edentate mandible: a prospective 1-year radiographic and 4-year clinical study. Int J Oral Maxillofac Implants 2008;23:315-22. 34. Zix J, Hug S, Kessler-Liechti G, Mericske-Stern R. Measurement of dental implant stability by resonance frequency analysis and damping capacity assessment: comparison of both techniques in a clinical trial. Int J Oral Maxillofac Implants 2008;23:525-30. 35. Lachmann S, Jäger B, Axmann D, Gomez-Roman G, Groten M, Weber H. Resonance frequency analysis and damping capacity assessment. Part I: An in vitro study on measurement reliability and a method of comparison in the determination of primary dental implant stability. Clin Oral Implants Res 2006;17:75-9. 36. Lachmann S, Laval JY, Jäger B, Axmann D, Gomez-Roman G, Groten M, et al. Resonance frequency analysis and damping capacity assessment. Part 2: Peri-implant bone loss follow-up. An in vitro study with the Periotest and Osstell instruments. Clin Oral Implants Res 2006;17:80-4. 37. Truhlar RS, Morris HF, Ochi S. Stability of the bone-implant complex. Results of longitudinal testing to 60 months with the Periotest device on endosseous dental implants. Ann Periodontol 2000;5:42-55. 38. Degidi M, Daprile G, Piattelli A, Carinci F. Evaluation of factors influencing resonance frequency analysis values, at insertion surgery, of implants placed in sinus-augmented and nongrafted sites. Clin Implant Dent Relat Res 2007;9:144-9.
ORAL AND MAXILLOFACIAL SURGERY e40 Oh and Kim 39. Zix J, Kessler-Liechti G, Mericske-Stern R. Stability measurement of 1-stage implants in the maxilla by means of resonance frequency analysis: a pilot study. Int J Oral Maxillofac Implants 2005;5:747-52. 40. 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;18:641-51. 41. Huang HM, Lee SY, Yeh CY, Lin CT. Resonance frequency assessment of dental implant stability with various bone qualities: a numerical approach. Clin Oral Implants Res 2000;13:65-74. 42. Friberg B, Sennerby L, Roos J, Lekholm U. Identification of bone quality in conjunction with insertion of titanium implants.
OOOO March 2012 A pilot study in jaw autopsy specimens. Clin Oral Implants Res 1995;6:213-9.
Reprint requests: Su-Gwan Kim, DDS, PhD Department of Oral and Maxillofacial Surgery School of Dentistry Chosun University 375, SeoSukDong, DongGu GwangJu City, South Korea 501-759 [email protected]