The Influence of Tactile Perception on Classification of Bone Tissue at Dental Implant Insertion Gláucia Kelly Silva Barbosa Linck, DDS;* Geovane Miranda Ferreira, DDS;* Rubelisa Cândido Gomes De Oliveira, DDS, PhD;* Christina Lindh, DDS, PhD;† Cláudio Rodrigues Leles, DDS, PhD;‡ Rejane Faria Ribeiro-Rotta, DDS, PhD‡
ABSTRACT Background: Various ways of using the Lekholm and Zarb (L&Z) classification have added to the lack of scientific evidence of the effectiveness of this clinical method in the evaluation of implant treatment. Purpose: The study aims to assess subjective jawbone classifications in patients referred for implant treatment, using L&Z classification with and without surgeon’s hand perception at implant insertion. The association between bone type classifications and quantitative parameters of primary implant stability was also assessed. Materials and Methods: One hundred thirty-five implants were inserted using conventional loading protocol. Three surgeons classified bone quality at implant sites using two methods: one based on periapical and panoramic images (modified L&Z) and one based on the same images associated with the surgeon’s tactile perception during drilling (original L&Z). Peak insertion torque and implant stability quotient (ISQ) were recorded. Results: The modified and original L&Z were strongly correlated (rho = 0.79; p < .001); Wilcoxon signed-rank test showed no significant difference in the distribution of bone type classification between pairs using the two methods (p = .538). Spearman correlation tested the association between primary stability parameters and bone type classifications (−0.34 to −0.57 [p < .001]). Conclusions: Tactile surgical perception has a minor influence on rating of subjective bone type for dental implant treatment using the L&Z classification. KEY WORDS: bone classification, bone type, dental implant
INTRODUCTION
bone tissue characteristics at the implant site, implant design, and surgical protocol.1,2 Over time, as remodeling of the surrounding bone takes place, implant stability increases as a result of osseointegration processes that occur following the formation of new bone adjacent to the implant.3,4 A number of devices and techniques have been developed to assess primary stability during implant insertion. The peak insertion torque (PIT) measurement is one of the most commonly used perioperative methods for quantifying the torsional strength of the bone–implant contact.5,6 Implant stability can also be measured and monitored over the healing period by resonance frequency analyses (RFAs), a noninvasive clinical technique that promotes vibration of the implant and, at the same time, analyzes implant motion
Implant stability immediately after implant insertion (primary stability) is a critical requirement for the achievement and maintenance of osseointegration. It has been reported that primary stability is affected by *Postgrad students, School of Dentistry, Federal University of Goias, Goiania, Goias, Brazil; †Professor, Faculty of Odontology, Malmö University, Malmö, Sweden; ‡Associate Professor, School of Dentistry, Federal University of Goias, Goiania, Goias, Brazil Corresponding Author: Professor Rejane Faria Ribeiro-Rotta, School of Dentistry, Federal University of Goiás, Rua C-235, N. 1323, Apto. 1501, Nova Suíça, Goiânia – GO CEP: 74280-130, Brazil; e-mail: [email protected] Conflict of interest: The authors report no conflict of interest. © 2015 Wiley Periodicals, Inc. DOI 10.1111/cid.12341
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and provides a numerical value named the implant stability quotient (ISQ), measured on a scale from 1 to 100.4,7 Both PIT and RFA measures have been used by clinicians as predictive parameters to establish the optimal healing period prior to implant loading.4,8–16 The bone type classification proposed by Lekholm and Zarb12 is one of the most frequently used classifications in dental implant planning.6 This classification12 is related to jawbone shape and quality, and used before as well as during implant insertion. The four types of bone quality were described as a ratio of amount and homogeneity of cortical bone and density of trabecular component. There is not enough scientific evidence, however, whether bone quality or quantity affects primary stability and treatment outcome.9,10,17 The validity and efficacy of the Lekholm & Zarb (L&Z) classification have been evaluated, suggesting a close relationship with micro-computed tomography (micro-CT) and histomorphometric bone parameters,18–20 and bone mineral density.21 In addition, it is unclear whether there are differences between the subjective jawbone classification when performed with conventional radiographs and when it is established in accordance with the original description of Lekholm and Zarb,12 which includes surgeon’s tactile perception during drilling. Many studies used the L&Z classification based only on preoperative evaluation with panoramic and periapical radiographs,2,16,22 while other studies were based on tomographic images23,24 and just a few used tactile perception for bone rating.20,25 These various ways of using the L&Z classification have added to the lack of scientific evidence of the effectiveness of this clinical method in pre- and perioperative evaluation of implant treatment. Thus, the aim of this study was to assess subjective jawbone classifications in a sample of patients referred for implant treatment using the L&Z classification, with and without surgeon’s hand perception during implant insertion. In addition, the association between bone type classifications and quantitative parameters of primary implant stability was assessed.
MATERIALS AND METHODS This was a clinical observational study previously approved by the Ethical Committee of the Federal University of Goias and National Ethics Committee (Brazil),
protocols numbers 114/07 and 418/2008. All subjects gave consent prior to the start of the study. Patients and Sample Partially edentulous subjects who were referred for implant treatment were submitted to clinical and radiographic evaluation. Only those with good general health conditions were included in the sample. Smokers and individuals with a history of diabetes or any other systemic disease that might impact healing process/ osseointegration were excluded from the sample. After intraoral physical examination and analysis of dental casts, those subjects with limited bone height and width at the potential implant sites and complex rehabilitation needs were also excluded. The study sample included only potential implant sites presenting with sufficient bone for the insertion of an implant of at least 3.75 × 9.0 mm assessed in the radiographic evaluation. The justification for the mentioned inclusion criteria is that this study was part of a wider investigation, which intended to evaluate longitudinally other variables related to bone quality. So, there was a need to standardize, as much as possible, the type of implant and prostheses. Radiographic Protocol Periapical and panoramic radiographs were obtained from all selected patients. The periapical radiographs were taken using Heliodent Dentotime dental x-ray equipment (Siemens, Benshein, Germany), with the following technical parameters: bisector technique, 70 kVp, 10 mA, 2.0 mm aluminum filter, rectangular collimation (3 cm × 4 cm), focus-aperture distance of 21 cm. E-speed dental film (Kodak Ektaspeed, Eastman Kodak Co., Rochester, NY, USA) was exposed for between 0.25 second and 0.4 second. The films were automatically processed (Peri-pro; Air Maintenance Techniques, Melville, NY, USA) with a 6-minute cycle at 27°C. Panoramic radiographs were obtained with the X Mind Tome Ceph unit (Soredex, Helsinki, Finland), operating from 70 kV to 73 kV/5 to 8 mAs. T-Mat 15 × 30 cm (Kodak, São Paulo, Brazil) films were also automatically processed (A/T2000 XR, Air Maintenance Techniques) with a 5.5-minute cycle at 82°F. Classification of Bone Tissue The subjective assessments of bone characteristics before and during surgery were performed by three
Tactile Perception on Bone Type Classification
trained and calibrated surgeons. Two methods for subjective bone classification were used: one based only on radiographs (modified L&Z) and the other based on radiographs associated with the surgeon’s tactile perception during drilling at implant insertion (original L&Z).12 The modified L&Z method consisted on placing panoramic and periapical radiographs on a standard viewbox (Apollo Portable Light Box Model LB 100 15W, Ronkonkoma, NY, USA) with a mask to block excessive light from the surroundings for radiographic interpretation. Image interpretation was performed by each surgeon at ambient light levels minutes before each operation. The surgeons received a calibration card with the schematic design and description of the L&Z classification,12 which served as a reference during each reading. The original description of L&Z classification consisted of the following: type 1 – almost the entire jaw is comprised of homogenous compact bone; type 2 – a thick layer of compact bone surrounds a core of dense trabecular bone; type 3 – a thin layer of cortical bone surrounds a core of dense trabecular bone of favorable strength; and type 4 – a thin layer of cortical bone surrounds a core of low density trabecular bone.12 The surgeons registered their subjective rate of each potential implant site on a ranking card. During surgery, taking into account the previous known bone type classification, the surgeon rerated it while also considering the tactile perception of bone drilling at the implant site. This method was based on the original report of the classification proposed by Lekholm and Zarb (original L&Z). Each calibrated surgeon rated the implant sites on which they operated, as tactile perception cannot be performed more than once at each bone site. Surgical Procedures and Primary Stability Measures (PIT and RFA) The surgical procedure was performed under local anesthesia, with crestal incision and a mucoperiosteal flap. The tactile perception of bone drilling was assessed during the penetration of the first bur while creating the initial drill hole. Instead of using a spherical drill for marking the implant location as the first drill, a 2.7 × 15 mm trephine bur, especially designed for this study (Neodent, Curitiba, Brazil), was used. The purpose of using the trephine was to obtain biopsies,
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which were used to evaluate other variables related to bone quality, part of other publications. External hexagon implants (Titamax TI, Neodent) were placed under sterile saline irrigation using a surgical micromotor (BLM 600 Plus, Driller, São Paulo, Brazil). For PIT measurement, the initial torque was set at 15 Ncm in the motor, and this value was gradually increased at consecutive 5 Ncm intervals until the motor rotation was automatically interrupted. The PIT measure was recorded when the rotation of the implant stopped due to friction with the peri-implant bone tissue and reached its final position. These values ranged from 15 to 55 Ncm. In cases in which the final anchorage required a torque higher than 55 Ncm, PIT was achieved using a manual wrench (Neodent) and recorded accordingly. RFA was measured immediately after implant insertion and during the uncovering procedure using a wireless device (Osstell™ Mentor, Osstell AB – Integration Diagnostics AB, Gothenburg, Sweden), and a transductor (Smartpeg, Integration Diagnostics AB) was attached to the implant. The probe of the wireless device was held close to the transductor in three different directions (bucco-lingual, lingual-buccal and mesio-distal) during the pulsing time. Resonance frequency values were automatically converted into ISQ values, which were also automatically displayed by the device. ISQ values range from 1 to 100, and the higher the measure, the more stable the implant. After the osseointegration period (4 to 6 months), RFA was performed again (uncovering ISQ). Statistical Analysis The agreement in bone type classification assessed using the two methods was measured using weighted kappa statistics, as the data came from an ordered scale (bone types 1–4), to reflect the degree of disagreement assigning greater emphasis to large differences between ratings than to small differences. Quadratic weighting was used due to the assumption that the differences between categories were not evenly balanced along the whole scale. Descriptive analysis, Wilcoxon signed-rank test, Kruskal–Wallis test and Spearman’s correlation were used for data analysis using the IBM-SPSS 20.0 software (IBM Corporation, Armonk, NY, USA). Statistical significance was set at p < .05 and was used for data analysis.
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TABLE 1 Characteristics of Implants (n = 135) n (%)
Number of implants per patient
Implant length (mm)
Implant diameter (mm)
1 2 3 or + 9 11 13 15 3.75 4.0 4.5 5.0
12 (23.0) 17 (32.6) 23 (44.3) 39 (28.8) 54 (40.0) 41 (30.4) 1 (0.8) 55 (40.7) 58 (42.9) 1 (0.7) 21 (15.5)
RESULTS A total of 135 dental implants were inserted in 52 patients. The majority of patients were female (61.5%), with mean age 42 years (SD = 10.3). The number of implants per patient and the distribution of implants according to length and diameter are described in Table 1. The majority of implants was inserted in the posterior mandible (57.0%) and maxilla (28.9%). Figure 1 shows the distribution of the implant sites classified according to the modified and original L&Z methods. The two methods were strongly correlated
Figure 1 Frequency distribution of bone sites according to original and modified L&Z methods for bone type classification of implant sites. L&Z = Lekholm and Zarb.
(rho = 0.79; p < .001) and the Wilcoxon signed-rank test showed that there was no significant difference in the distribution of bone type classification between pairs using the two methods (p = .538). Percent agreement was 73.3% and weighted kappa (quadratic weight) showed good agreement between the modified and original L&Z methods (kappa = 0.78; 95% CI = 0.71– 0.86). The majority of bone sites evaluated were classified as types 2 and 3 (Table 2). Higher values of PIT, ISQ at insertion, and uncovering were observed when the bone was classified as type I. These values decreased steadily as the bone type classification increased from type 1 to 4, independently of the bone classification method (Figure 2). All betweengroup comparisons revealed significant differences among bone type groups (p < .001). Spearman correlation tests for the association between primary stability parameters and bone type classifications ranged from −0.34 to −0.57 (p < .001). DISCUSSION Bone classification according to Lekholm and Zarb is commonly used in routine dental implant practice, but has only recently been validated using different techniques, including bone mineral density,21 histomorphometry,19 and microtomography.20 Our study showed that the L&Z method is an acceptable rating procedure for the assessment of bone tissue characteristics, irrespective of whether tactile perception during bone drilling is considered, as was included in the original proposal. Bone types 2 and 3 were the most prevalent in this study sample, corresponding to approximately twothirds of the implant sites. These bone types have been associated with successful treatment outcome, possibly due to their higher microarchitectural complexity, and have a cortical thickness and trabecular density suitable for implant reconstruction.17,20 Bone type 1 was the least prevalent, corresponding to wide cortical bone surrounding denser trabecular bone. Bone type 4, described as thin cortical bone surrounding sparse trabecular bone, was observed in approximately 20% of patients. A number of studies indicated that the failure rate is greater in type 4 bone.3,26 Clinicians generally observe limited bone resistance while drilling in this area.9,10 Nevertheless, different bone types can be found in the anterior and posterior sites of the maxilla and mandible, and a site-specific bone tissue evaluation during implant
Tactile Perception on Bone Type Classification
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TABLE 2 Cross-Tabulation of the Distribution of Bone Type Classifications of Implant Sites Using the Original and Modified L&Z Methods Original L&Z Modified L&Z
1 2 3 4 Total (%)
1
2
3
4
Total (%)
5 5 1 0 11 (8.1)
0 30 11 0 41 (30.4)
1 7 41 3 52 (38.5)
0 0 8 23 31 (23.0)
6 (4.4) 42 (31.1) 61 (45.2) 26 (19.3) 135
Weighted kappa = 0.784. L&Z = Lekholm and Zarb.
planning should be performed to determine the length of the healing period needed for osseointegration.24 Bone quality may influence the primary stability of dental implants, and is thought to play a significant role in early implant treatment failure.10,27 The low and moderate correlations between subjective classifications and PIT and ISQ values at insertion and uncovering can be explained by differences between the parameters used by each of the methods. Bone types 1, 2, 3, and 4 are a subjective measure of the ratio between cortical and trabecular bone, in which trabecular bone tissue varies in structure and the cortical layer surrounding trabecular bone varies in thickness. Some authors have highlighted the importance of the cortical bone for achieving an acceptable level of implant lock, which can lead to
differences in torque values and resonance frequency.28,29 As a subjective classification, L&Z classification has limitations. Its criteria to classify bone quality into the four types (1–4) include three-dimensional aspects and the methods recommended to collect bone information are two-dimensional (conventional radiographs) or subjective (tactil perception). As there is a wide-range bone densities in each type, the classification cannot give precise details of bone quality, especially those with minor nuances between them, as types 2 and 3. Also, still there is a lack of scientific evidence whether bone characteristics, specially bone quality and quantity, affect primary implant stability and treatment outcome. If there is no generally accepted definition of bone tissue characteristics and the methods used for
Figure 2 Implant stability measurements (means and 95% confidence intervals) in the different jawbone types using the original (left) and modified (right) L&Z methods. Between-group comparison (Kruskal–Wallis test) showed significant differences among bone type groups (p < .001). Spearman correlation tests for the association between primary stability parameters and bone type classifications were all p < .001 (correlation coefficients ranged from −0.34 to −0.57). ISQ = implant stability quotient; L&Z = Lekholm and Zarb; PIT = peak insertion torque.
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classification differ as well as measurement units, results from different studies are difficult to compare and so cannot be trusted.30,31 Besides bone characteristics, the combined effect of several variables related to type of implant and surgical technique may also contribute to the variations in ISQ and PIT among studies.32 The 135 bone sites evaluated provided mean PIT and ISQ values at insertions and uncovering similar to the results of other studies.33,34 These values were within the range considered successful for early and immediate assessment of implants: PIT greater than 30 Ncm and ISQ between 57 and 82.35 PIT and ISQ values (at insertion and uncovering) showed similar and regular variations from bone type 1 to type 4, whether or not surgeon’s perception during drilling was included. The increase in ISQ values over time (from insertion to uncovering stage) suggests osseointegration progresses in a similar way for the different bone types,32,34 and is not affected by changes in marginal bone level during the first year of loading.36 Nevertheless, studies have shown that insertion torque could be a good indicator of primary implant stability, whereas ISQ measurements have some limitations and should not be used alone.20,32 The results showed good agreement between methods (weighted kappa = 0.78). However, the kappa coefficient does not itself indicate whether any disagreement is due to random differences (i.e., those due to chance) or systematic differences (i.e., those due to a consistent pattern) between the clinicians’ ratings, and the data should be examined accordingly.37 When disagreements between the two methods occurred (Table 2), they seemed to be randomly distributed, with no tendency for underestimated or overestimated scores in bone classification using the modified L&Z method. Thus, overall bias due to the extent to which the methods disagree regarding the proportion of positive (or negative) cases was correspondingly low. In addition, most disagreements were of only a single category in the ordinal bone classification scale using the modified method (negative difference in 15 cases and positive difference in 19 cases). In only two cases was there a 2-point difference in score on the classification scale (one positive and one negative). Another limitation of kappa statistics is that it is affected by the prevalence of the finding under observation.38 The low number of cases classified as bone type 1 compared with the other bone types, irrespective of the
assessment method, may subject kappa statistics to a prevalence bias. However, we cannot assume that this frequency distribution represents the true prevalence of jawbone types. Rather, it indicates whether a specific bone type is either very common or very rare (also considering that different bone types are more or less likely to occur in certain regions of the maxilla and mandible), and this will predispose clinicians to assign or not assign a bone type score, so that this prevalence provides only an indirect indication of true prevalence, mediated by the clinicians’ diagnostic behavior.37 An important assumption underlying the use of the kappa coefficient is that it requires the patients or subjects to be independent, and that errors associated with clinicians’ ratings are independent. In the case of subjective jawbone-type evaluation, agreement on the underlying attribute is contaminated by the knowledge of the location of the implant bone site, and the magnitude of kappa is likely to be inflated and should be interpreted cautiously.39 In summary, the results of this study support the use of the L&Z method in daily practice in a different way than was originally proposed, in particular without a surgeon’s hand perception at implant insertion.6,31 Although tactile perception has a minor influence on preoperative bone assessment, hand-felt perception should not be excluded as providing additional information for overall dental implant planning and potential outcomes. As a perioperative procedure, surgical tactile perception brings out unique and relevant information that may only be obtained in this treatment step. ACKNOWLEDGMENTS This study was supported by a grant from the FAPEG (Fundação de Amparo à Pesquisa do Estado de Goiás, Brazil) and ILAPEO (Instituto Latino Americano de Pesquisa e Ensino Odontológico, Curitiba, Brazil). REFERENCES 1. O’Sullivan D, Sennerby L, Meredith N. Measurements comparing the initial stability of five designs of dental implants: a human cadaver study. Clin Implant Dent Relat Res 2000; 2:85–92. 2. Molly L. Bone density and primary stability in implant therapy. Clin Oral Implants Res 2006; 17(Suppl 2):124–135. 3. 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; 6:142–146.
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4. Meredith N. Assessment of implant stability as a prognostic determinant. Int J Prosthodont 1998; 11:491–501. 5. Cehreli MC, Karasoy D, Akca K, Eckert SE. Meta-analysis of methods used to assess implant stability. Int J Oral Maxillofac Implants 2009; 24:1015–1032. 6. Ribeiro-Rotta RF, Pereira AC, Oliveira GH, Freire MC, Leles CR, Lindh C. An exploratory survey of diagnostic methods for bone quality assessment used by Brazilian dental implant specialists. J Oral Rehabil 2010; 37:698–703. 7. Meredith N, Alleyne D, Cawley P. Quantitative determination of the stability of the implant-tissue interface using resonance frequency analysis. Clin Oral Implants Res 1996; 7:261–267. 8. Johansson P, Strid KG. Assessment of bone quality from cutting resistance during implant surgery. Int J Oral Maxillofac Implants 1994; 9:279–288. 9. Friberg B, Sennerby L, Roos J, Johansson P, Strid CG, Lekholm U. Evaluation of bone density using cutting resistance measurements and microradiography: an in vitro study in pig ribs. Clin Oral Implants Res 1995; 6:164–171. 10. Friberg B, Sennerby L, Roos J, Johansson P, Strid CG, Lekholm U. Identification of bone quality in conjunction with insertion of titanium implants: a pilot study in jaw autopsy specimens. Clin Oral Implants Res 1995; 6:213–219. 11. Akça K, Chang TL, Tekdemir I, Fanuscu MI. Biomechanical aspects of initial intraosseous stability and implant design: a quantitative micro-morphometric analysis. Clin Oral Implants Res 2006; 17:465–472. 12. Lekholm U, Zarb GA. Patient selection and preparation. In: Brånemark P-I, Zarb GA, Albrektsson T, eds. Tissue integrated prostheses: osseointegration in clinical dentistry. Chicago: Quintessence, 1985:199–209. 13. Misch CE. Density of bone – Effect on treatment plans, surgical approach, and progressive loading. Int J Oral Implantol 1990; 6:23–31. 14. Trisi P, Rao W. Bone classification: clinicalhistomorphometric comparison. Clin Oral Implants Res 1999; 10:1–7. 15. Lindh C, Nilsson M, Klinge B, Petersson A. Quantitative computed tomography of trabecular bone in the mandible. Dentomaxillofac Radiol 1996; 25:146–150. 16. Lindh C, Petersson A, Rohlin M. Assessment of the trabecular pattern before endosseous implant treatment: diagnostic outcome of periapical radiography in the mandible. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1996; 82:335– 343. 17. Thrular RS, Orenstein IH, Morris HF, Ochi S. Distribution of bone quality in patients receiving endosseous dental implants. J Oral Maxillofac Surg 1997; 55:38–45. 18. De Oliveira RC, Leles CR, Lindh C, Ribeiro-Rotta RF. Bone tissue microarchitectural characteristics at dental implant sites. Part 1: identification of clinical-related parameters. Clin Oral Implants Res 2012; 23:981–986.
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19. Pereira AC, Souza PP, Souza JA, Silva TA, Batista AC, Ribeiro-Rotta RF. Histomorphometrical and molecular evaluation of endosseous dental implants sites in humans: correlation with clinical and radiographic aspects. Clin Oral Implants Res 2013; 24:414–421. 20. Ribeiro-Rotta RF, De Oliveira RC, Dias DR, Lindh C, Leles CR. Bone tissue microarchitectural characteristics at dental implant sites part 2: correlation with bone classification and primary stability. Clin Oral Implants Res 2014; 25:47–53. 21. Bergkvist G, Koh KJ, Sahlholm S, Klintström E, Lindh C. Bone density at implant sites and its relationship to assessment of bone quality and treatment outcome. Int J Oral Maxillofac Implants 2010; 25:321–328. 22. Johansson B, Bäck T, Hirsch JM. Cutting torque measurements in conjunction with implant placement in grafted and nongrafted maxillas as an objective evaluation of bone density: a possible method for identifying early implant failures? Clin Implant Dent Relat Res 2004; 6:9–15. 23. Norton MR, Gamble C. Bone classification: an objective scale of bone density using computerized tomography scan. Clin Oral Implants Res 2001; 12:79–84. 24. De Oliveira RC, Leles CR, Normanha LM, Lindh C, Ribeiro-Rotta RF. Assessments of trabecular bone density at implant sites on CT images. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008; 105:231–238. 25. Alsaadi G, Quirynen M, Michiels K, Jacobs R, Van Steenberghe D. A biomechanical assessment of the relation between the oral implant stability at insertion and subjective bone quality assessment. J Clin Periodontol 2007; 34:359–366. 26. Jaffin RA, Berman CL. The excessive loss of Brånemark fixtures in type IV bone: a 5-year analysis. J Periodontol 1991; 62:2–4. 27. Nedir R, Bschof M, Szmukler-Moncler S, Bernard J-P, Samson J. Predicting osseointegration by means of implant primary stability. Clin Oral Implants Res 2004; 15:520–528. 28. Sennerby L, Thomsen P, Ericson LE. A morphometric and biomechanic comparison of titanium implants inserted in rabbit cortical and cancellous bone. Int J Oral Maxillofac Implants 1992; 7:62–71. 29. Tözüm TF, Turkyilmaz I, Yamalik N, Karabulut E, Eratalay K. Analysis of the potential association of implant stability, laboratory, and image based measures used to assess osteotomy sites: early versus delayed loading. J Periodontol 2007; 78:1675–1682. 30. Ribeiro-Rotta RF, Lindh C, Pereira AC, Rohlin M. Ambiguity in bone tissue characteristics as presented in studies on dental implant planning and placement: a systematic review. Clin Oral Implants Res 2011; 22:789–801. 31. Ribeiro-Rotta RF, Lindh C, Rohlin M. Efficacy of clinical methods to assess jawbone tissue prior to and during
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endosseous dental implant placement: a systemic literature review. Int J Oral Maxillofac Implants 2007; 22:289–300. 32. Rabel A, Kohler SG, Schmidt-Westhausen AM. Clinical study on the primary stability of two dental implant systems with resonance frequency analysis. Clin Oral Investig 2007; 11:257–265. 33. Turkyilmaz I, Tözüm TF, Tumer C, Ozbek EN. Assessment of correlation between computerized tomography values of the bone, and final torque and resonance frequency values at dental implant placement. J Oral Rehabil 2006; 33:881–888. 34. Aksoy U, Eratalay K, Tozum TF. The possible association among bone density values, resonance frequency measurements, tactile sense, and histomorphometric evaluations of dental implant osteotomy sites: a preliminary study. Implant Dent 2009; 18:316–325.
35. Al-Nawas B, Wagner W, Grötz KA. Insertion torque and resonance frequency analysis of dental implant systems in an animal model with loaded implants. Int J Oral Maxillofac Implants 2006; 21:726–732. 36. Dias DR, Leles CR, Lindh C, Ribeiro-Rotta RF. The effect of marginal bone level changes on the stability of dental implants in a short-term evaluation. Clin Oral Implants Res 2014; doi: 10.1111/clr.12426; [Epub ahead of print]. 37. Sim J, Wright CC. The kappa statistic in reliability studies: use, interpretation, and sample size requirements. Phys Ther 2005; 85:257–268. 38. Viera AJ, Garrett JM. Understanding interobserver agreement: the kappa statistic. Fam Med 2005; 37:360–363. 39. Thompson WD, Walter SD. A reappraisal of the kappa coefficient. J Clin Epidemiol 1988; 41:949–958.
ABSTRACT Background: Various ways of using the Lekholm and Zarb (L&Z) classification have added to the lack of scientific evidence of the effectiveness of this clinical method in the evaluation of implant treatment. Purpose: The study aims to assess subjective jawbone classifications in patients referred for implant treatment, using L&Z classification with and without surgeon’s hand perception at implant insertion. The association between bone type classifications and quantitative parameters of primary implant stability was also assessed. Materials and Methods: One hundred thirty-five implants were inserted using conventional loading protocol. Three surgeons classified bone quality at implant sites using two methods: one based on periapical and panoramic images (modified L&Z) and one based on the same images associated with the surgeon’s tactile perception during drilling (original L&Z). Peak insertion torque and implant stability quotient (ISQ) were recorded. Results: The modified and original L&Z were strongly correlated (rho = 0.79; p < .001); Wilcoxon signed-rank test showed no significant difference in the distribution of bone type classification between pairs using the two methods (p = .538). Spearman correlation tested the association between primary stability parameters and bone type classifications (−0.34 to −0.57 [p < .001]). Conclusions: Tactile surgical perception has a minor influence on rating of subjective bone type for dental implant treatment using the L&Z classification. KEY WORDS: bone classification, bone type, dental implant
INTRODUCTION
bone tissue characteristics at the implant site, implant design, and surgical protocol.1,2 Over time, as remodeling of the surrounding bone takes place, implant stability increases as a result of osseointegration processes that occur following the formation of new bone adjacent to the implant.3,4 A number of devices and techniques have been developed to assess primary stability during implant insertion. The peak insertion torque (PIT) measurement is one of the most commonly used perioperative methods for quantifying the torsional strength of the bone–implant contact.5,6 Implant stability can also be measured and monitored over the healing period by resonance frequency analyses (RFAs), a noninvasive clinical technique that promotes vibration of the implant and, at the same time, analyzes implant motion
Implant stability immediately after implant insertion (primary stability) is a critical requirement for the achievement and maintenance of osseointegration. It has been reported that primary stability is affected by *Postgrad students, School of Dentistry, Federal University of Goias, Goiania, Goias, Brazil; †Professor, Faculty of Odontology, Malmö University, Malmö, Sweden; ‡Associate Professor, School of Dentistry, Federal University of Goias, Goiania, Goias, Brazil Corresponding Author: Professor Rejane Faria Ribeiro-Rotta, School of Dentistry, Federal University of Goiás, Rua C-235, N. 1323, Apto. 1501, Nova Suíça, Goiânia – GO CEP: 74280-130, Brazil; e-mail: [email protected] Conflict of interest: The authors report no conflict of interest. © 2015 Wiley Periodicals, Inc. DOI 10.1111/cid.12341
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and provides a numerical value named the implant stability quotient (ISQ), measured on a scale from 1 to 100.4,7 Both PIT and RFA measures have been used by clinicians as predictive parameters to establish the optimal healing period prior to implant loading.4,8–16 The bone type classification proposed by Lekholm and Zarb12 is one of the most frequently used classifications in dental implant planning.6 This classification12 is related to jawbone shape and quality, and used before as well as during implant insertion. The four types of bone quality were described as a ratio of amount and homogeneity of cortical bone and density of trabecular component. There is not enough scientific evidence, however, whether bone quality or quantity affects primary stability and treatment outcome.9,10,17 The validity and efficacy of the Lekholm & Zarb (L&Z) classification have been evaluated, suggesting a close relationship with micro-computed tomography (micro-CT) and histomorphometric bone parameters,18–20 and bone mineral density.21 In addition, it is unclear whether there are differences between the subjective jawbone classification when performed with conventional radiographs and when it is established in accordance with the original description of Lekholm and Zarb,12 which includes surgeon’s tactile perception during drilling. Many studies used the L&Z classification based only on preoperative evaluation with panoramic and periapical radiographs,2,16,22 while other studies were based on tomographic images23,24 and just a few used tactile perception for bone rating.20,25 These various ways of using the L&Z classification have added to the lack of scientific evidence of the effectiveness of this clinical method in pre- and perioperative evaluation of implant treatment. Thus, the aim of this study was to assess subjective jawbone classifications in a sample of patients referred for implant treatment using the L&Z classification, with and without surgeon’s hand perception during implant insertion. In addition, the association between bone type classifications and quantitative parameters of primary implant stability was assessed.
MATERIALS AND METHODS This was a clinical observational study previously approved by the Ethical Committee of the Federal University of Goias and National Ethics Committee (Brazil),
protocols numbers 114/07 and 418/2008. All subjects gave consent prior to the start of the study. Patients and Sample Partially edentulous subjects who were referred for implant treatment were submitted to clinical and radiographic evaluation. Only those with good general health conditions were included in the sample. Smokers and individuals with a history of diabetes or any other systemic disease that might impact healing process/ osseointegration were excluded from the sample. After intraoral physical examination and analysis of dental casts, those subjects with limited bone height and width at the potential implant sites and complex rehabilitation needs were also excluded. The study sample included only potential implant sites presenting with sufficient bone for the insertion of an implant of at least 3.75 × 9.0 mm assessed in the radiographic evaluation. The justification for the mentioned inclusion criteria is that this study was part of a wider investigation, which intended to evaluate longitudinally other variables related to bone quality. So, there was a need to standardize, as much as possible, the type of implant and prostheses. Radiographic Protocol Periapical and panoramic radiographs were obtained from all selected patients. The periapical radiographs were taken using Heliodent Dentotime dental x-ray equipment (Siemens, Benshein, Germany), with the following technical parameters: bisector technique, 70 kVp, 10 mA, 2.0 mm aluminum filter, rectangular collimation (3 cm × 4 cm), focus-aperture distance of 21 cm. E-speed dental film (Kodak Ektaspeed, Eastman Kodak Co., Rochester, NY, USA) was exposed for between 0.25 second and 0.4 second. The films were automatically processed (Peri-pro; Air Maintenance Techniques, Melville, NY, USA) with a 6-minute cycle at 27°C. Panoramic radiographs were obtained with the X Mind Tome Ceph unit (Soredex, Helsinki, Finland), operating from 70 kV to 73 kV/5 to 8 mAs. T-Mat 15 × 30 cm (Kodak, São Paulo, Brazil) films were also automatically processed (A/T2000 XR, Air Maintenance Techniques) with a 5.5-minute cycle at 82°F. Classification of Bone Tissue The subjective assessments of bone characteristics before and during surgery were performed by three
Tactile Perception on Bone Type Classification
trained and calibrated surgeons. Two methods for subjective bone classification were used: one based only on radiographs (modified L&Z) and the other based on radiographs associated with the surgeon’s tactile perception during drilling at implant insertion (original L&Z).12 The modified L&Z method consisted on placing panoramic and periapical radiographs on a standard viewbox (Apollo Portable Light Box Model LB 100 15W, Ronkonkoma, NY, USA) with a mask to block excessive light from the surroundings for radiographic interpretation. Image interpretation was performed by each surgeon at ambient light levels minutes before each operation. The surgeons received a calibration card with the schematic design and description of the L&Z classification,12 which served as a reference during each reading. The original description of L&Z classification consisted of the following: type 1 – almost the entire jaw is comprised of homogenous compact bone; type 2 – a thick layer of compact bone surrounds a core of dense trabecular bone; type 3 – a thin layer of cortical bone surrounds a core of dense trabecular bone of favorable strength; and type 4 – a thin layer of cortical bone surrounds a core of low density trabecular bone.12 The surgeons registered their subjective rate of each potential implant site on a ranking card. During surgery, taking into account the previous known bone type classification, the surgeon rerated it while also considering the tactile perception of bone drilling at the implant site. This method was based on the original report of the classification proposed by Lekholm and Zarb (original L&Z). Each calibrated surgeon rated the implant sites on which they operated, as tactile perception cannot be performed more than once at each bone site. Surgical Procedures and Primary Stability Measures (PIT and RFA) The surgical procedure was performed under local anesthesia, with crestal incision and a mucoperiosteal flap. The tactile perception of bone drilling was assessed during the penetration of the first bur while creating the initial drill hole. Instead of using a spherical drill for marking the implant location as the first drill, a 2.7 × 15 mm trephine bur, especially designed for this study (Neodent, Curitiba, Brazil), was used. The purpose of using the trephine was to obtain biopsies,
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which were used to evaluate other variables related to bone quality, part of other publications. External hexagon implants (Titamax TI, Neodent) were placed under sterile saline irrigation using a surgical micromotor (BLM 600 Plus, Driller, São Paulo, Brazil). For PIT measurement, the initial torque was set at 15 Ncm in the motor, and this value was gradually increased at consecutive 5 Ncm intervals until the motor rotation was automatically interrupted. The PIT measure was recorded when the rotation of the implant stopped due to friction with the peri-implant bone tissue and reached its final position. These values ranged from 15 to 55 Ncm. In cases in which the final anchorage required a torque higher than 55 Ncm, PIT was achieved using a manual wrench (Neodent) and recorded accordingly. RFA was measured immediately after implant insertion and during the uncovering procedure using a wireless device (Osstell™ Mentor, Osstell AB – Integration Diagnostics AB, Gothenburg, Sweden), and a transductor (Smartpeg, Integration Diagnostics AB) was attached to the implant. The probe of the wireless device was held close to the transductor in three different directions (bucco-lingual, lingual-buccal and mesio-distal) during the pulsing time. Resonance frequency values were automatically converted into ISQ values, which were also automatically displayed by the device. ISQ values range from 1 to 100, and the higher the measure, the more stable the implant. After the osseointegration period (4 to 6 months), RFA was performed again (uncovering ISQ). Statistical Analysis The agreement in bone type classification assessed using the two methods was measured using weighted kappa statistics, as the data came from an ordered scale (bone types 1–4), to reflect the degree of disagreement assigning greater emphasis to large differences between ratings than to small differences. Quadratic weighting was used due to the assumption that the differences between categories were not evenly balanced along the whole scale. Descriptive analysis, Wilcoxon signed-rank test, Kruskal–Wallis test and Spearman’s correlation were used for data analysis using the IBM-SPSS 20.0 software (IBM Corporation, Armonk, NY, USA). Statistical significance was set at p < .05 and was used for data analysis.
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TABLE 1 Characteristics of Implants (n = 135) n (%)
Number of implants per patient
Implant length (mm)
Implant diameter (mm)
1 2 3 or + 9 11 13 15 3.75 4.0 4.5 5.0
12 (23.0) 17 (32.6) 23 (44.3) 39 (28.8) 54 (40.0) 41 (30.4) 1 (0.8) 55 (40.7) 58 (42.9) 1 (0.7) 21 (15.5)
RESULTS A total of 135 dental implants were inserted in 52 patients. The majority of patients were female (61.5%), with mean age 42 years (SD = 10.3). The number of implants per patient and the distribution of implants according to length and diameter are described in Table 1. The majority of implants was inserted in the posterior mandible (57.0%) and maxilla (28.9%). Figure 1 shows the distribution of the implant sites classified according to the modified and original L&Z methods. The two methods were strongly correlated
Figure 1 Frequency distribution of bone sites according to original and modified L&Z methods for bone type classification of implant sites. L&Z = Lekholm and Zarb.
(rho = 0.79; p < .001) and the Wilcoxon signed-rank test showed that there was no significant difference in the distribution of bone type classification between pairs using the two methods (p = .538). Percent agreement was 73.3% and weighted kappa (quadratic weight) showed good agreement between the modified and original L&Z methods (kappa = 0.78; 95% CI = 0.71– 0.86). The majority of bone sites evaluated were classified as types 2 and 3 (Table 2). Higher values of PIT, ISQ at insertion, and uncovering were observed when the bone was classified as type I. These values decreased steadily as the bone type classification increased from type 1 to 4, independently of the bone classification method (Figure 2). All betweengroup comparisons revealed significant differences among bone type groups (p < .001). Spearman correlation tests for the association between primary stability parameters and bone type classifications ranged from −0.34 to −0.57 (p < .001). DISCUSSION Bone classification according to Lekholm and Zarb is commonly used in routine dental implant practice, but has only recently been validated using different techniques, including bone mineral density,21 histomorphometry,19 and microtomography.20 Our study showed that the L&Z method is an acceptable rating procedure for the assessment of bone tissue characteristics, irrespective of whether tactile perception during bone drilling is considered, as was included in the original proposal. Bone types 2 and 3 were the most prevalent in this study sample, corresponding to approximately twothirds of the implant sites. These bone types have been associated with successful treatment outcome, possibly due to their higher microarchitectural complexity, and have a cortical thickness and trabecular density suitable for implant reconstruction.17,20 Bone type 1 was the least prevalent, corresponding to wide cortical bone surrounding denser trabecular bone. Bone type 4, described as thin cortical bone surrounding sparse trabecular bone, was observed in approximately 20% of patients. A number of studies indicated that the failure rate is greater in type 4 bone.3,26 Clinicians generally observe limited bone resistance while drilling in this area.9,10 Nevertheless, different bone types can be found in the anterior and posterior sites of the maxilla and mandible, and a site-specific bone tissue evaluation during implant
Tactile Perception on Bone Type Classification
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TABLE 2 Cross-Tabulation of the Distribution of Bone Type Classifications of Implant Sites Using the Original and Modified L&Z Methods Original L&Z Modified L&Z
1 2 3 4 Total (%)
1
2
3
4
Total (%)
5 5 1 0 11 (8.1)
0 30 11 0 41 (30.4)
1 7 41 3 52 (38.5)
0 0 8 23 31 (23.0)
6 (4.4) 42 (31.1) 61 (45.2) 26 (19.3) 135
Weighted kappa = 0.784. L&Z = Lekholm and Zarb.
planning should be performed to determine the length of the healing period needed for osseointegration.24 Bone quality may influence the primary stability of dental implants, and is thought to play a significant role in early implant treatment failure.10,27 The low and moderate correlations between subjective classifications and PIT and ISQ values at insertion and uncovering can be explained by differences between the parameters used by each of the methods. Bone types 1, 2, 3, and 4 are a subjective measure of the ratio between cortical and trabecular bone, in which trabecular bone tissue varies in structure and the cortical layer surrounding trabecular bone varies in thickness. Some authors have highlighted the importance of the cortical bone for achieving an acceptable level of implant lock, which can lead to
differences in torque values and resonance frequency.28,29 As a subjective classification, L&Z classification has limitations. Its criteria to classify bone quality into the four types (1–4) include three-dimensional aspects and the methods recommended to collect bone information are two-dimensional (conventional radiographs) or subjective (tactil perception). As there is a wide-range bone densities in each type, the classification cannot give precise details of bone quality, especially those with minor nuances between them, as types 2 and 3. Also, still there is a lack of scientific evidence whether bone characteristics, specially bone quality and quantity, affect primary implant stability and treatment outcome. If there is no generally accepted definition of bone tissue characteristics and the methods used for
Figure 2 Implant stability measurements (means and 95% confidence intervals) in the different jawbone types using the original (left) and modified (right) L&Z methods. Between-group comparison (Kruskal–Wallis test) showed significant differences among bone type groups (p < .001). Spearman correlation tests for the association between primary stability parameters and bone type classifications were all p < .001 (correlation coefficients ranged from −0.34 to −0.57). ISQ = implant stability quotient; L&Z = Lekholm and Zarb; PIT = peak insertion torque.
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classification differ as well as measurement units, results from different studies are difficult to compare and so cannot be trusted.30,31 Besides bone characteristics, the combined effect of several variables related to type of implant and surgical technique may also contribute to the variations in ISQ and PIT among studies.32 The 135 bone sites evaluated provided mean PIT and ISQ values at insertions and uncovering similar to the results of other studies.33,34 These values were within the range considered successful for early and immediate assessment of implants: PIT greater than 30 Ncm and ISQ between 57 and 82.35 PIT and ISQ values (at insertion and uncovering) showed similar and regular variations from bone type 1 to type 4, whether or not surgeon’s perception during drilling was included. The increase in ISQ values over time (from insertion to uncovering stage) suggests osseointegration progresses in a similar way for the different bone types,32,34 and is not affected by changes in marginal bone level during the first year of loading.36 Nevertheless, studies have shown that insertion torque could be a good indicator of primary implant stability, whereas ISQ measurements have some limitations and should not be used alone.20,32 The results showed good agreement between methods (weighted kappa = 0.78). However, the kappa coefficient does not itself indicate whether any disagreement is due to random differences (i.e., those due to chance) or systematic differences (i.e., those due to a consistent pattern) between the clinicians’ ratings, and the data should be examined accordingly.37 When disagreements between the two methods occurred (Table 2), they seemed to be randomly distributed, with no tendency for underestimated or overestimated scores in bone classification using the modified L&Z method. Thus, overall bias due to the extent to which the methods disagree regarding the proportion of positive (or negative) cases was correspondingly low. In addition, most disagreements were of only a single category in the ordinal bone classification scale using the modified method (negative difference in 15 cases and positive difference in 19 cases). In only two cases was there a 2-point difference in score on the classification scale (one positive and one negative). Another limitation of kappa statistics is that it is affected by the prevalence of the finding under observation.38 The low number of cases classified as bone type 1 compared with the other bone types, irrespective of the
assessment method, may subject kappa statistics to a prevalence bias. However, we cannot assume that this frequency distribution represents the true prevalence of jawbone types. Rather, it indicates whether a specific bone type is either very common or very rare (also considering that different bone types are more or less likely to occur in certain regions of the maxilla and mandible), and this will predispose clinicians to assign or not assign a bone type score, so that this prevalence provides only an indirect indication of true prevalence, mediated by the clinicians’ diagnostic behavior.37 An important assumption underlying the use of the kappa coefficient is that it requires the patients or subjects to be independent, and that errors associated with clinicians’ ratings are independent. In the case of subjective jawbone-type evaluation, agreement on the underlying attribute is contaminated by the knowledge of the location of the implant bone site, and the magnitude of kappa is likely to be inflated and should be interpreted cautiously.39 In summary, the results of this study support the use of the L&Z method in daily practice in a different way than was originally proposed, in particular without a surgeon’s hand perception at implant insertion.6,31 Although tactile perception has a minor influence on preoperative bone assessment, hand-felt perception should not be excluded as providing additional information for overall dental implant planning and potential outcomes. As a perioperative procedure, surgical tactile perception brings out unique and relevant information that may only be obtained in this treatment step. ACKNOWLEDGMENTS This study was supported by a grant from the FAPEG (Fundação de Amparo à Pesquisa do Estado de Goiás, Brazil) and ILAPEO (Instituto Latino Americano de Pesquisa e Ensino Odontológico, Curitiba, Brazil). REFERENCES 1. O’Sullivan D, Sennerby L, Meredith N. Measurements comparing the initial stability of five designs of dental implants: a human cadaver study. Clin Implant Dent Relat Res 2000; 2:85–92. 2. Molly L. Bone density and primary stability in implant therapy. Clin Oral Implants Res 2006; 17(Suppl 2):124–135. 3. 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; 6:142–146.
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endosseous dental implant placement: a systemic literature review. Int J Oral Maxillofac Implants 2007; 22:289–300. 32. Rabel A, Kohler SG, Schmidt-Westhausen AM. Clinical study on the primary stability of two dental implant systems with resonance frequency analysis. Clin Oral Investig 2007; 11:257–265. 33. Turkyilmaz I, Tözüm TF, Tumer C, Ozbek EN. Assessment of correlation between computerized tomography values of the bone, and final torque and resonance frequency values at dental implant placement. J Oral Rehabil 2006; 33:881–888. 34. Aksoy U, Eratalay K, Tozum TF. The possible association among bone density values, resonance frequency measurements, tactile sense, and histomorphometric evaluations of dental implant osteotomy sites: a preliminary study. Implant Dent 2009; 18:316–325.
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