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Applicability of strain measurements on a contra angle handpiece for the determination of alveolar bone quality during dental implant surgery
Journal of Cranio-Maxillo-Facial Surgery 40 (2012) e144ee149
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Applicability of strain measurements on a contra angle handpiece for the determination of alveolar bone quality during dental implant surgery Tim Krafft, Werner Winter, Manfred Wichmann, Matthias Karl* Department of Prosthodontics (Head: Prof. Dr. M. Wichmann), School of Dental Medicine, University of Erlangen-Nuremberg, 91054 Erlangen, Germany
a r t i c l e i n f o
a b s t r a c t
Article history: Paper received 10 April 2011 Accepted 30 July 2011
Alveolar bone quality is considered to be an important prognostic factor in dental implant stability. Although numerous methods have been described, no technique allows for reliable diagnostics. The purpose of this study was to determine if strain measurements on the shaft of a contra angle handpiece during implant bed preparation could be used for the determination of bone quality. Experiments in polyurethane foam and human cadaver bone were conducted to investigate whether strain measurements could be correlated with other diagnostic parameters, such as the surgeon’s tactile sensation during drilling, implant insertion torque, implant stability, elastic modulus of bone and bone quality as assessed radiographically. Tests were also performed to determine if strain measurements could be used to distinguish various types of bone. As axial feed and contact pressure during the drilling process could not be standardized under simulated clinical conditions, substantial deviations in the time needed to complete the drilling occurred. Under controlled circumstances using polyurethane foam, this problem could be addressed by a normalization procedure, but great variations occurred in human cadaver bone. As bone quality could not be reliably determined, especially when a cortical layer was present, strain measurements on a contra angle handpiece appears to be inappropriate for this purpose. Ó 2011 European Association for Cranio-Maxillo-Facial Surgery.
Keywords: Bone density Dental implant stability Mechanical testing Strain gauge Implant bed preparation
1. Introduction The quality of alveolar bone has been shown to affect treatment planning, the surgical and loading protocol applied as well as the long term success of dental implants (Brunski, 1988; Norton and Gamble, 2001). For treatment planning purposes, preoperative assessment methods based on radiographic examinations as well as specific classification systems have been described (Vercellotti and Vercellotti, 2009). Based on the partially contradictory results presented in the literature, it appears that these techniques do have specific limitations in the field of implant dentistry. The widely applied classification system for alveolar bone quality introduced by Lekholm and Zarb allows for a clinically relevant classification of alveolar bone in four categories ranging from solid, mainly cortical bone to soft trabecular bone providing limited primary stability for dental implants (Lekholm and Zarb, 1985). This classification system in its original form is based on the surgeon’s tactile sensation during implant site preparation using varying sets of drills (Trisi and Rao, 1999; Alsaadi et al., 2007). It has been shown that with this technique differentiating between * Corresponding author. Zahnklinik 2, Department of Prosthodontics, Glueckstrasse 11, 91054 Erlangen, Germany. Tel.: þ49 91318535802; fax: þ49 9131 8536781. E-mail address: [email protected] (M. Karl).
the two extreme classes described above is possible, but differentiating between the two intermediate classes as well as between neighboring classes is not possible (Trisi and Rao, 1999; Shapurian et al., 2006). Given the variability in design and surgical protocol of the different implant systems available, it appears that an objective classification cannot be established using subjective hand feelings. Implant related measurement techniques allowing for assumptions to be made about the underlying bone quality have also been introduced. Besides implant insertion torque measurements (Friberg et al., 1999a; Beer et al., 2003; Johansson et al., 2004), evaluating the primary stability of dental implants by means of resonance frequency and damping capacity assessments are being used (Schulte et al., 1992; Tricio et al., 1995; Meredith, 1998; Nkenke et al., 2003; Turkyilmaz et al., 2006). With varying correlations of the resulting measurement values with other factors related to bone architecture and the differences in the implant systems available, it appears to be impossible to establish a valid classification system based on these approaches. Based on the clinical observation that the pressure exerted on the contra angle handpiece during implant bed preparation depends on the drilling resistance experienced by the surgeon, it was the aim of this investigation to determine whether strain gauge measurements on the shaft of the contra angle handpiece could be used for setting up an objective classification system for alveolar bone.
1010-5182/$ e see front matter Ó 2011 European Association for Cranio-Maxillo-Facial Surgery. doi:10.1016/j.jcms.2011.07.013
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2. Materials and methods
2.3. Testing in human cadaver bone
2.1. Modification of a contra angle handpiece for strain measurements during implant bed preparation
Segments of embalmed human mandibles and maxillas were obtained from the Institute of Anatomy, University of ErlangenNuremberg and subject to cone beam computed tomography
A unidirectional strain gauge (LY11-0.6/120; 120 U reference resistance; Hottinger Baldwin Messtechnik GmbH, Darmstadt, Germany) was attached to a contra angle handpiece (E20RI, NSK Europe, Eschborn, Germany; gear ratio 20:1) with the sensing element being oriented in the anterioreposterior direction (Fig. 1). A measurement amplifier (Spider 8Ò; Hottinger Baldwin) and analyzing software (BEAM for Spider 8Ò; AMS Gesellschaft für Angewandte Mess-und Systemtechnik GmbH, Flöha, Germany) allowed recording of the strains occurring in the contra angle handpiece during drilling.
Testing in polyurethane foam materials Commercially available polyurethane foam blocks (Sawbones Europe AB, Malmö, Sweden) differing in structure and density (given in pound per cubic foot; pcf) were used as bone surrogate material for preliminary testing (Gibson, 1985): Blocks with a solid, homogeneous structure (Solid Rigid Polyurethane Foam 10 pcf, 20 pcf, 30 pcf, 40 pcf) Blocks with a cellular structure (Cellular Rigid Polyurethane Foam 10 pcf, 20 pcf) Blocks with a simulated cortical layer (Solid Rigid Polyurethane Foam 10 pcf, 20 pcf laminated with one sheet of Solid Rigid Polyurethane Foam 40 pcf; Cellular Rigid Polyurethane Foam 10 pcf, 20 pcf laminated with one sheet of Solid Rigid Polyurethane Foam 40 pcf) Ten sockets 3.5 mm in diameter and 11 mm in length were prepared for the placement of screw-shaped cylindrical implants with a diameter of 4.1 mm and 10 mm length (Straumann Standard Implant; Institut Straumann AG, Basel, Switzerland) in each of the materials. The implant positions were marked with a round burr and a set of twist drills 2.2 mm, 2.8 mm and 3.5 mm in diameter was used in combination with a surgical motor (KaVo INTRAsurg 1000; KaVo Dental GmbH, Biberach, Germany) to create standardized implant beds. For drilling with the 2.8 mm twist drill, the strain gauge equipped contra angle handpiece was used and the strains occurring at the contra angle handpiece during drilling were recorded (Fig. 2). Mean values for the time required to complete the 2.8 mm drilling were calculated for each material and measurements showing deviations from the mean value greater than 0.9 s were excluded from analysis. For valid measurements, strain readings over time were approximated using a polynomial of 5th degree and the integral value was taken for analysis. Implants were installed using the surgical motor (KaVo INTRAsurg 1000) which also allowed for measuring the maximum torque needed to seat the implants. Primary implant stability was determined by means of damping capacity assessment (Periotest, Medizintechnik Gulden, Modautal, Germany) and resonance frequency measurements (Osstell mentor, Osstell AB, Gothenburg, Sweden). Ten standardized cylinders 6 mm in diameter and 10 mm in length were harvested from each material using trephine burrs (Meisinger Bone Management, Meisinger, Neuss, Germany). The elastic moduli of the cylinders were determined by compressive testing in a universal testing machine (Inspekt mini 3kN; Hegewald & Peschke, Nossen, Germany) at a crosshead speed of 1 mm/min until 1 mm compression was reached.
Fig. 1. Total view of the modified contra angle handpiece used for strain measurements during dental implant surgery. The strain gauge is positioned with the sensing element in the anterioreposterior direction and in conjunction with a measurement amplifier allows for strain measurements during implant bed preparation.
Fig. 2. Following the creation of an initial 2.2 mm osteotomy, a 2.8 mm twist drill in combination with the strain gauged contra angle handpiece was used to further prepare the implant site while the strains occurring were measured.
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(CBCT) scans (3D Accuitomo, J. Morita Europe GmbH, Dietzenbach, Germany). A total of 110 sites were identified radiographically to be suitable for implant placement and were classified according to their location in the oral cavity (maxilla/mandible; anterior/ posterior). During implant bed preparation with the 2.2 mm twist drill, the surgeon subjectively rated bone quality according to the Lekholm and Zarb classification system (Lekholm and Zarb, 1985). Strain readings over time occurring at the contra angle handpiece during drilling with the 2.8 mm twist drill were approximated using a polynomial of 5th degree and the integral value was taken for analysis. As no reference values could be established, all measurements were used for analysis. Additionally, maximum values for implant insertion torque (KaVo INTRAsurg 1000) were recorded and primary implant stability was determined by means of resonance frequency measurements (Osstell mentor). Whenever possible, bone cylinders 6 mm in diameter and 10 mm in length were harvested from the vicinity of the implant sites and subject to compressive testing in a universal testing machine (Inspekt mini 3kN) at a crosshead speed of 1 mm/min until 1 mm compression was reached. Based on a second CBCT scan (3D Accuitomo) following removal of the implants, the thickness of cortical bone at the implant sites was measured and the density of trabecular bone was subjectively classified based on the surgeon’s experience as low (1), medium (2) or high (3) according to the classification system proposed by Vercellotti and Vercellotti (2009).
2.4. Statistical analysis of measurement values obtained from polyurethane foam materials As a box test of homogeneity of covariances revealed significant differences among groups (p ¼ 0.000), statistical analysis (SPSS 14.0 for Windows, SPSS Inc, Chicago, Ill.) of the measurement values obtained was done by multivariate analysis of variance (MANOVA) with Pillai’s trace, which is robust to heterogeneous variances (Olson, 1974; Olson, 1976). The level of significance was set at a ¼ 0.05. Pairwise comparisons between groups were conducted applying Bonferroni correction for multiple comparisons. In addition, Pearson correlation coefficients were calculated for all combinations of parameters.
2.5. Statistical analysis of measurement values obtained from human cadaver bone Pearson productemoment correlation coefficients were calculated for all combinations of parameters (level of significance a ¼ 0.05). Multivariate analysis of variance (MANOVA) did not indicate any significant influence of the fixed factors dental status and position (anterior, posterior) on measurement results. For that reason, all implant sites were classified according to the jaw type (maxilla, mandible). For comparing the different implant sites two sample t-tests were conducted for all parameters with the level of significance set at a ¼ 0.05. 3. Results 3.1. Testing in polyurethane foam materials The mean values and standard deviations for all parameters obtained are given in Table 1. Significant correlations between all parameters were found based on Pearson correlation coefficients (Table 2). Global multivariate analysis of variance (MANOVA) with Pillai’s trace revealed a significant influence of the different polyurethane foam materials on all measurement results (p ¼ 0.000). Pairwise comparisons based on the strain values determined (Table 3), showed that it was not possible to distinguish polyurethane foam blocks differing in density and structure when a cortical layer was present (p ¼ 0.319; p ¼ 1.000). Differentiating materials showing the same density but different structure (Cellular vs. Solid) was not possible (p ¼ 1.000). The only material which could consistently be identified was Solid 40 where significant differences in strain values were found for all comparisons (p ¼ 0.000; p ¼ 0.001). All other comparisons were inconsistent. 3.2. Testing in human cadaver bone The mean values and standard deviations for all parameters obtained are given in Table 4. In contrast to testing in polyurethane foam, only three significant correlations of the strain gauge signals with other parameters (Drilling resistance 0.33; Implant insertion torque 0.16; Resonance frequency analysis 0.29) could be established (Table 5). With the exception of the parameters elastic
Table 1 Mean values and standard deviations for all parameters determined in different polyurethane foam materials.
Cellular 10 Cellular 20 Solid 10 Solid 20 Solid 30 Solid 40 Cellular 10 & Solid 40 Cellular 20 & Solid 40 Solid 10 & Solid 40 Solid 20 & Solid 40
Strain gauge signal [mm/m]
Insertion torque [N cm]
Osstell [ISQ]
Periotest [PTV]
Elastic modulus [MPa]
210.28 373.58 104.50 293.20 771.22 2870.20 1392.80 1119.00 1617.00 1803.33
1.79 9.80 2.40 9.54 21.60 35.50 21.60 23.70 20.30 19.40
39.60 65.20 42.50 64.30 70.10 72.90 64.75 71.80 58.75 70.50
26.30 3.00 14.35 2.10 0.50 1.90 0.85 0.75 3.55 0.35
72.87 234.50 73.72 197.83 266.48 391.81 74.00 217.71 81.84 86.88
(144.46) (213.71) (36.06) (126.37) (216.42) (399.59) (675.82) (346.27) (392.66) (266.23)
(0.70) (0.58) (0.18) (0.76) (2.41) (2.68) (2.46) (2.00) (0.95) (1.58)
(9.97) (4.74) (3.79) (4.42) (1.49) (3.12) (5.27) (1.51) (4.14) (0.82)
(5.53) (1.20) (4.67) (0.66) (0.33) (1.02) (0.82) (0.75) (1.21) (0.53)
(6.94) (25.20) (5.06) (15.88) (32.89) (34.52) (18.01) (36.65) (5.22) (10.94)
Table 2 Pearson correlation coefficients for all parameters studied in polyurethane foam; all correlations are significant at a level of a ¼ 0.05. Strain gauge signal [mm/m] Strain gauge signal [mm/m] Insertion torque [N cm] Osstell [ISQ] Periotest [PTV] Elastic modulus [MPa]
Insertion torque [N cm]
Osstell [ISQ]
Periotest [PTV]
Elastic modulus [MPa]
0.810
0.471 0.753
0.458 0.746 0.871
0.387 0.575 0.572 0.490
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Table 3 Multiple comparisons between the different polyurethane foam materials based on the strain readings measured on the contra angle handpiece; p-values <0.05 designate significant differences. C10 C10 C10 & S40 C20 C20 & S40 S10 S10 & S40 S20 S20 & S40 S30 S40
C10 & S40
C20
C20 & S40
S10
S10 & S40
S20
S20 & S40
S30
S40
0.000
1.000 0.000
0.004 1.000 0.086
1.000 0.000 1.000 0.046
0.000 1.000 0.000 1.000 0.000
1.000 0.000 1.000 0.013 1.000 0.000
0.000 1.000 0.000 0.319 0.000 1.000 0.000
0.043 0.025 1.000 1.000 0.555 0.006 0.170 0.000
0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.001 0.000
Table 4 Mean values and standard deviations for all parameters determined in human cadaver bone.
Maxilla ant. Maxilla post. Mandible ant. Mandible post.
Drilling resistance [1-2-3-4]
Strain gauge signal [mm/m]
Insertion torque [N cm]
Osstell [ISQ]
Elastic modulus [MPa]
Cortical bone thickness [mm]
Trabecular bone density [1-2-3]
2.83 2.85 1.34 1.60
1193.03 439.22 2323.80 3243.02
16.68 9.33 29.72 30.53
63.75 64.92 75.39 78.46
381.38 475.97 770.00 516.21
1.58 0.74 1.63 1.76
1.90 1.75 2.16 1.88
(0.72) (0.80) (0.70) (0.72)
(888.02) (334.60) (1830.96) (3803.27)
(11.66) (5.31) (13.27) (12.18)
(12.99) (11.23) (6.31) (6.21)
(311.74) (279.98) (296.17) (369.94)
(1.03) (0.38) (0.95) (0.77)
(0.57) (0.45) (0.45) (0.58)
Table 5 Correlation coefficients for all parameters determined in human cadaver bone (Pearson’s productemoment correlation); correlation coefficients p < 0.05 designate significant correlations. Drilling resistance Drilling resistance Strain gauge signal Insertion torque Resonance frequency analysis Compressive test Cortical bone thickness Trabecular bone density
Strain gauge signal
Insertion torque
Resonance frequency analysis
Compressive test
Cortical bone thickness
Trabecular bone density
0.33
0.69 0.16
0.47 0.29 0.46
0.23 0.02 0.37 0.17
0.38 0.23 0.57 0.44 0.29
0.06 0.16 0.19 0.12 0.53 0.07
Table 6 Welch two sample tests for differences with respect to jaw type based on measurements in human cadaver bone. p-values <0.05 designate significant differences. Parameter
Jaw type
n
Mean
SD
Drilling resistance
Maxilla Mandible Maxilla Mandible Maxilla Mandible Maxilla Mandible Maxilla Mandible Maxilla Mandible Maxilla Mandible
25 85 25 85 25 85 25 85 11 39 22 84 22 84
2.840 1.501 801.052 2896.962 12.856 30.228 64.360 77.306 424.375 594.298 1.1233 1.7107 1.818 1.988
0.7461 0.7175 751.7649 3223.7187 9.5110 12.5274 11.8669 6.3906 287.0313 364.8232 0.8440 0.8410 0.5010 0.5487
Strain gauge signal Insertion torque Osstell Elastic modulus Cortical bone thickness Trabecular bone density
modulus and trabecular bone density it was possible to differentiate mandibular from maxillary bone using all the measurement techniques (Table 6). 4. Discussion In experimental research, micro computed tomography and microradiographs are frequently used for objective evaluation of bone quality as represented by measurements of bone mineral density and bone microstructure (Matsuo et al., 2011; Nolff et al., 2010; Pekkan et al., 2011). For clinical application these techniques are not available and computed tomography (CT) or CBCT is used instead. However, it has recently been pointed out that
t
df
p
7.9272
38.029
0.000
5.5066
105.331
0.000
7.4341
50.951
0.000
5.2359
28.210
0.000
1.6274
20.093
0.1192
2.9078
32.779
0.006
1.3875
35.378
0.1740
considerable limitations exist with the use of CBCT for evaluating bone quality (Hohlweg-Majert et al., 2010). With current clinical methods being inappropriate for evaluating alveolar bone quality and dental implant stability (Nkenke et al., 2003; Ribeiro-Rotta et al., 2007) it was the aim of this study to investigate whether strain measurements conducted on the shaft of a contra angle handpiece during implant bed preparation could be used for the objective classification of alveolar bone (Lekholm and Zarb, 1985; Vercellotti and Vercellotti, 2009). The major advantage of that approach would be that, in contrast to measurement systems for dental implant stability such as the Osstell or Periotest device (Tricio et al., 1995; Friberg et al., 1999b; Al-Nawas et al., 2006), no additional step would be added to the
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surgical protocol. Similar to measuring implant insertion torque (Beer et al., 2003; Johansson et al., 2004), which has also been shown to provide only rough estimations, strain measurements on the contra angle handpiece can be carried out as part of the regular protocol applied in dental implant surgery. In contrast to radiographic assessments of bone quality (Norton and Gamble, 2001), which have also been found to show high variations (Shapurian et al., 2006; Turkyilmaz et al., 2007), the patient would not be exposed to radiation (Aranyarachkul et al., 2005). With the measurements being done at an early stage of implant surgery, the treatment protocol could be modified to account for low levels of bone quality. In such a case, finalizing the implant hole could, for instance, be done using undersized drilling (Beer et al., 2007) and the osteotome technique respectively in order to increase local bone density and subsequently primary implant stability (Nkenke et al., 2002; Gulsahi et al., 2007). Despite the fact that significant correlations of strain readings with other measurement techniques could be set up based on the experiments conducted in polyurethane foam, it was not possible to reliably distinguish materials differing in density and structure based on the strain values obtained from the contra angle handpiece. In particular, the presence of a simulated cortical plate made it impossible to differentiate the underlying bone types showing varying densities and architectural properties. The major problem involved with the approach presented appears to be the fact that axial feed and contact pressure cannot be standardized in manual drilling of implant sockets in a setting resembling clinical practice. For that reason, the strain measurements have been conducted during the second drilling step (2.8 mm twist drill) following the creation of a pilot hole with a diameter of 2.2 mm. Although time expenditure for the second drill step was more consistent as compared to the first drill step, a number of measurements had to be excluded from analysis as substantial deviations in the time needed for completing the 2.8 mm drilling occurred. With that operation being carried out, reasonably good correlations of strain values and the other parameters determined could be established. For the experiments based on human cadaver bone, a comparable standardization procedure could not be carried out as measurements on unique samples showing high levels of variation had to be analyzed. As a result of this, fewer correlations with other parameters have been found. However, variations in quality between maxillary and mandibular bone have obviously been great enough to allow for a statistically significant difference between the respective strain measurements to be detected. With respect to the use of polyurethane foam material and human cadaver bone for simulating the clinical conditions of dental implant surgery, the following limitations have to be taken into account. Although it has been claimed that from a structural point of view, bone is comparable to foam materials (Gibson, 1985), the polyurethane material used drastically differed from human bone in terms of clinical handling characteristics. The human cadaver bone used in the second experiment also bears considerable shortcomings as the mechanical properties of bone undergo changes post mortem and may also be influenced by storage conditions and time (Linde and Sørensen, 1993). This may have also been one reason why differentiating between anterior and posterior implant sites was not possible using any of the diagnostic methods used. 5. Conclusion Within the limitations of this study, it appears that the use of strain measurements on a contra angle handpiece for the classification of bone quality is only applicable in uniform single layer
materials when axial feed and contact pressure can be standardized. As neither of these requirements can be fulfilled in clinical practice, this approach seems to be inappropriate for setting up an objective classification system for alveolar bone quality. Sources of support None. Conflict of interest None of the authors have any conflict of interest. Acknowledgments The authors wish to thank Anthony Simpson, Institute of Anatomy, University of Erlangen-Nuremberg for assistance with human cadaver specimens, Dr. Felix Kölpin, Department of Prosthodontics, University of Erlangen-Nuremberg for conducting the compressive tests and Dr. Friedrich Graef, Department of Applied Mathematics, University of Erlangen-Nuremberg, for statistical data analysis. References 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 21: 726e732, 2006 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 20: 416e424, 2005 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 34: 359e366, 2007 Beer A, Gahleitner A, Holm A, Tschabitscher M, Homolka P: Correlation of insertion torques with bone mineral density from dental quantitative CT in the mandible. Clin Oral Implants Res 14: 616e620, 2003 Beer A, Gahleitner A, Holm A, Birkfellner W, Homolka P: Adapted preparation technique for screw-type implants: explorative in vitro pilot study in a porcine bone model. Clin Oral Implants Res 18: 103e107, 2007 Brunski JB: Biomechanics of oral implants: future research directions. J Dent Educ 52: 775e787, 1988 Friberg B, Sennerby L, Grondahl K, Bergstrom C, Back T, Lekholm U: On cutting torque measurements during implant placement: a 3-year clinical prospective study. Clin Implant Dent Relat Res 1: 75e83, 1999a Friberg B, Sennerby L, Meredith N, Lekholm U: A comparison between cutting torque and resonance frequency measurements of maxillary implants. A 20-month clinical study. Int J Oral Maxillofac Surg 28: 297e303, 1999b Gibson LJ: The mechanical behaviour of cancellous bone. J Biomech 18: 317e328, 1985 Gulsahi A, Paksoy CS, Yazıcıoglu N, Arpak N, Kucuk NO, Terzioglu H: Assessment of bone density differences between conventional and bone-condensing techniques using dual energy x-ray absorptiometry and radiography. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 104: 692e698, 2007 Hohlweg-Majert B, Metzger MC, Kummer T, Schulze D: Morphometric analysis e cone beam computed tomography to predict bone quality and quantity. J Craniomaxillofac Surg. doi:10.1016/j.jcms.2010.10.002, 2010 Johansson B, Back 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 6: 9e15, 2004 Lekholm U, Zarb GA: Patient selection and preparation. In: Branemark P-I, Zarb GA, Albrektsson T (eds), Tissue integrated prostheses: osseointegration in clinical dentistry. Chicago: Quintessence Publ Co, 199e209, 1985 Linde F, Sørensen HC: The effect of different storage methods on the mechanical properties of trabecular bone. J Biomech 26: 1249e1252, 1993 Matsuo A, Chiba H, Takahashi H, Toyoda J, Hasegawa O, Hojo S: Bone quality of mandibles reconstructed with particulate cellular bone and marrow, and plateletrich plasma. J Craniomaxillofac Surg. doi:10.1016/j.jcms.2011.01.003, 2011 Meredith N: Assessment of implant stability as a prognostic determinant. Int J Prosthodont 11: 491e501, 1998 Nkenke E, Kloss F, Wiltfang J, Schultze-Mosgau S, Radespiel-Tröger M, Loos K, et al: Histomorphometric and fluorescence microscopic analysis of bone remodelling after installation of implants using an osteotome technique. Clin Oral Implants Res 13: 595e602, 2002 Nkenke E, Hahn M, Weinzierl K, Radespiel-Troger M, Neukam FW, Engelke K: Implant stability and histomorphometry: a correlation study in human cadavers using stepped cylinder implants. Clin Oral Implants Res 14: 601e609, 2003 Nolff MC, Kokemueller H, Hauschild G, Fehr M, Bormann KH, Spalthoff S, et al: Comparison of computed tomography and microradiography for graft
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Applicability of strain measurements on a contra angle handpiece for the determination of alveolar bone quality during dental implant surgery Tim Krafft, Werner Winter, Manfred Wichmann, Matthias Karl* Department of Prosthodontics (Head: Prof. Dr. M. Wichmann), School of Dental Medicine, University of Erlangen-Nuremberg, 91054 Erlangen, Germany
a r t i c l e i n f o
a b s t r a c t
Article history: Paper received 10 April 2011 Accepted 30 July 2011
Alveolar bone quality is considered to be an important prognostic factor in dental implant stability. Although numerous methods have been described, no technique allows for reliable diagnostics. The purpose of this study was to determine if strain measurements on the shaft of a contra angle handpiece during implant bed preparation could be used for the determination of bone quality. Experiments in polyurethane foam and human cadaver bone were conducted to investigate whether strain measurements could be correlated with other diagnostic parameters, such as the surgeon’s tactile sensation during drilling, implant insertion torque, implant stability, elastic modulus of bone and bone quality as assessed radiographically. Tests were also performed to determine if strain measurements could be used to distinguish various types of bone. As axial feed and contact pressure during the drilling process could not be standardized under simulated clinical conditions, substantial deviations in the time needed to complete the drilling occurred. Under controlled circumstances using polyurethane foam, this problem could be addressed by a normalization procedure, but great variations occurred in human cadaver bone. As bone quality could not be reliably determined, especially when a cortical layer was present, strain measurements on a contra angle handpiece appears to be inappropriate for this purpose. Ó 2011 European Association for Cranio-Maxillo-Facial Surgery.
Keywords: Bone density Dental implant stability Mechanical testing Strain gauge Implant bed preparation
1. Introduction The quality of alveolar bone has been shown to affect treatment planning, the surgical and loading protocol applied as well as the long term success of dental implants (Brunski, 1988; Norton and Gamble, 2001). For treatment planning purposes, preoperative assessment methods based on radiographic examinations as well as specific classification systems have been described (Vercellotti and Vercellotti, 2009). Based on the partially contradictory results presented in the literature, it appears that these techniques do have specific limitations in the field of implant dentistry. The widely applied classification system for alveolar bone quality introduced by Lekholm and Zarb allows for a clinically relevant classification of alveolar bone in four categories ranging from solid, mainly cortical bone to soft trabecular bone providing limited primary stability for dental implants (Lekholm and Zarb, 1985). This classification system in its original form is based on the surgeon’s tactile sensation during implant site preparation using varying sets of drills (Trisi and Rao, 1999; Alsaadi et al., 2007). It has been shown that with this technique differentiating between * Corresponding author. Zahnklinik 2, Department of Prosthodontics, Glueckstrasse 11, 91054 Erlangen, Germany. Tel.: þ49 91318535802; fax: þ49 9131 8536781. E-mail address: [email protected] (M. Karl).
the two extreme classes described above is possible, but differentiating between the two intermediate classes as well as between neighboring classes is not possible (Trisi and Rao, 1999; Shapurian et al., 2006). Given the variability in design and surgical protocol of the different implant systems available, it appears that an objective classification cannot be established using subjective hand feelings. Implant related measurement techniques allowing for assumptions to be made about the underlying bone quality have also been introduced. Besides implant insertion torque measurements (Friberg et al., 1999a; Beer et al., 2003; Johansson et al., 2004), evaluating the primary stability of dental implants by means of resonance frequency and damping capacity assessments are being used (Schulte et al., 1992; Tricio et al., 1995; Meredith, 1998; Nkenke et al., 2003; Turkyilmaz et al., 2006). With varying correlations of the resulting measurement values with other factors related to bone architecture and the differences in the implant systems available, it appears to be impossible to establish a valid classification system based on these approaches. Based on the clinical observation that the pressure exerted on the contra angle handpiece during implant bed preparation depends on the drilling resistance experienced by the surgeon, it was the aim of this investigation to determine whether strain gauge measurements on the shaft of the contra angle handpiece could be used for setting up an objective classification system for alveolar bone.
1010-5182/$ e see front matter Ó 2011 European Association for Cranio-Maxillo-Facial Surgery. doi:10.1016/j.jcms.2011.07.013
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2. Materials and methods
2.3. Testing in human cadaver bone
2.1. Modification of a contra angle handpiece for strain measurements during implant bed preparation
Segments of embalmed human mandibles and maxillas were obtained from the Institute of Anatomy, University of ErlangenNuremberg and subject to cone beam computed tomography
A unidirectional strain gauge (LY11-0.6/120; 120 U reference resistance; Hottinger Baldwin Messtechnik GmbH, Darmstadt, Germany) was attached to a contra angle handpiece (E20RI, NSK Europe, Eschborn, Germany; gear ratio 20:1) with the sensing element being oriented in the anterioreposterior direction (Fig. 1). A measurement amplifier (Spider 8Ò; Hottinger Baldwin) and analyzing software (BEAM for Spider 8Ò; AMS Gesellschaft für Angewandte Mess-und Systemtechnik GmbH, Flöha, Germany) allowed recording of the strains occurring in the contra angle handpiece during drilling.
Testing in polyurethane foam materials Commercially available polyurethane foam blocks (Sawbones Europe AB, Malmö, Sweden) differing in structure and density (given in pound per cubic foot; pcf) were used as bone surrogate material for preliminary testing (Gibson, 1985): Blocks with a solid, homogeneous structure (Solid Rigid Polyurethane Foam 10 pcf, 20 pcf, 30 pcf, 40 pcf) Blocks with a cellular structure (Cellular Rigid Polyurethane Foam 10 pcf, 20 pcf) Blocks with a simulated cortical layer (Solid Rigid Polyurethane Foam 10 pcf, 20 pcf laminated with one sheet of Solid Rigid Polyurethane Foam 40 pcf; Cellular Rigid Polyurethane Foam 10 pcf, 20 pcf laminated with one sheet of Solid Rigid Polyurethane Foam 40 pcf) Ten sockets 3.5 mm in diameter and 11 mm in length were prepared for the placement of screw-shaped cylindrical implants with a diameter of 4.1 mm and 10 mm length (Straumann Standard Implant; Institut Straumann AG, Basel, Switzerland) in each of the materials. The implant positions were marked with a round burr and a set of twist drills 2.2 mm, 2.8 mm and 3.5 mm in diameter was used in combination with a surgical motor (KaVo INTRAsurg 1000; KaVo Dental GmbH, Biberach, Germany) to create standardized implant beds. For drilling with the 2.8 mm twist drill, the strain gauge equipped contra angle handpiece was used and the strains occurring at the contra angle handpiece during drilling were recorded (Fig. 2). Mean values for the time required to complete the 2.8 mm drilling were calculated for each material and measurements showing deviations from the mean value greater than 0.9 s were excluded from analysis. For valid measurements, strain readings over time were approximated using a polynomial of 5th degree and the integral value was taken for analysis. Implants were installed using the surgical motor (KaVo INTRAsurg 1000) which also allowed for measuring the maximum torque needed to seat the implants. Primary implant stability was determined by means of damping capacity assessment (Periotest, Medizintechnik Gulden, Modautal, Germany) and resonance frequency measurements (Osstell mentor, Osstell AB, Gothenburg, Sweden). Ten standardized cylinders 6 mm in diameter and 10 mm in length were harvested from each material using trephine burrs (Meisinger Bone Management, Meisinger, Neuss, Germany). The elastic moduli of the cylinders were determined by compressive testing in a universal testing machine (Inspekt mini 3kN; Hegewald & Peschke, Nossen, Germany) at a crosshead speed of 1 mm/min until 1 mm compression was reached.
Fig. 1. Total view of the modified contra angle handpiece used for strain measurements during dental implant surgery. The strain gauge is positioned with the sensing element in the anterioreposterior direction and in conjunction with a measurement amplifier allows for strain measurements during implant bed preparation.
Fig. 2. Following the creation of an initial 2.2 mm osteotomy, a 2.8 mm twist drill in combination with the strain gauged contra angle handpiece was used to further prepare the implant site while the strains occurring were measured.
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(CBCT) scans (3D Accuitomo, J. Morita Europe GmbH, Dietzenbach, Germany). A total of 110 sites were identified radiographically to be suitable for implant placement and were classified according to their location in the oral cavity (maxilla/mandible; anterior/ posterior). During implant bed preparation with the 2.2 mm twist drill, the surgeon subjectively rated bone quality according to the Lekholm and Zarb classification system (Lekholm and Zarb, 1985). Strain readings over time occurring at the contra angle handpiece during drilling with the 2.8 mm twist drill were approximated using a polynomial of 5th degree and the integral value was taken for analysis. As no reference values could be established, all measurements were used for analysis. Additionally, maximum values for implant insertion torque (KaVo INTRAsurg 1000) were recorded and primary implant stability was determined by means of resonance frequency measurements (Osstell mentor). Whenever possible, bone cylinders 6 mm in diameter and 10 mm in length were harvested from the vicinity of the implant sites and subject to compressive testing in a universal testing machine (Inspekt mini 3kN) at a crosshead speed of 1 mm/min until 1 mm compression was reached. Based on a second CBCT scan (3D Accuitomo) following removal of the implants, the thickness of cortical bone at the implant sites was measured and the density of trabecular bone was subjectively classified based on the surgeon’s experience as low (1), medium (2) or high (3) according to the classification system proposed by Vercellotti and Vercellotti (2009).
2.4. Statistical analysis of measurement values obtained from polyurethane foam materials As a box test of homogeneity of covariances revealed significant differences among groups (p ¼ 0.000), statistical analysis (SPSS 14.0 for Windows, SPSS Inc, Chicago, Ill.) of the measurement values obtained was done by multivariate analysis of variance (MANOVA) with Pillai’s trace, which is robust to heterogeneous variances (Olson, 1974; Olson, 1976). The level of significance was set at a ¼ 0.05. Pairwise comparisons between groups were conducted applying Bonferroni correction for multiple comparisons. In addition, Pearson correlation coefficients were calculated for all combinations of parameters.
2.5. Statistical analysis of measurement values obtained from human cadaver bone Pearson productemoment correlation coefficients were calculated for all combinations of parameters (level of significance a ¼ 0.05). Multivariate analysis of variance (MANOVA) did not indicate any significant influence of the fixed factors dental status and position (anterior, posterior) on measurement results. For that reason, all implant sites were classified according to the jaw type (maxilla, mandible). For comparing the different implant sites two sample t-tests were conducted for all parameters with the level of significance set at a ¼ 0.05. 3. Results 3.1. Testing in polyurethane foam materials The mean values and standard deviations for all parameters obtained are given in Table 1. Significant correlations between all parameters were found based on Pearson correlation coefficients (Table 2). Global multivariate analysis of variance (MANOVA) with Pillai’s trace revealed a significant influence of the different polyurethane foam materials on all measurement results (p ¼ 0.000). Pairwise comparisons based on the strain values determined (Table 3), showed that it was not possible to distinguish polyurethane foam blocks differing in density and structure when a cortical layer was present (p ¼ 0.319; p ¼ 1.000). Differentiating materials showing the same density but different structure (Cellular vs. Solid) was not possible (p ¼ 1.000). The only material which could consistently be identified was Solid 40 where significant differences in strain values were found for all comparisons (p ¼ 0.000; p ¼ 0.001). All other comparisons were inconsistent. 3.2. Testing in human cadaver bone The mean values and standard deviations for all parameters obtained are given in Table 4. In contrast to testing in polyurethane foam, only three significant correlations of the strain gauge signals with other parameters (Drilling resistance 0.33; Implant insertion torque 0.16; Resonance frequency analysis 0.29) could be established (Table 5). With the exception of the parameters elastic
Table 1 Mean values and standard deviations for all parameters determined in different polyurethane foam materials.
Cellular 10 Cellular 20 Solid 10 Solid 20 Solid 30 Solid 40 Cellular 10 & Solid 40 Cellular 20 & Solid 40 Solid 10 & Solid 40 Solid 20 & Solid 40
Strain gauge signal [mm/m]
Insertion torque [N cm]
Osstell [ISQ]
Periotest [PTV]
Elastic modulus [MPa]
210.28 373.58 104.50 293.20 771.22 2870.20 1392.80 1119.00 1617.00 1803.33
1.79 9.80 2.40 9.54 21.60 35.50 21.60 23.70 20.30 19.40
39.60 65.20 42.50 64.30 70.10 72.90 64.75 71.80 58.75 70.50
26.30 3.00 14.35 2.10 0.50 1.90 0.85 0.75 3.55 0.35
72.87 234.50 73.72 197.83 266.48 391.81 74.00 217.71 81.84 86.88
(144.46) (213.71) (36.06) (126.37) (216.42) (399.59) (675.82) (346.27) (392.66) (266.23)
(0.70) (0.58) (0.18) (0.76) (2.41) (2.68) (2.46) (2.00) (0.95) (1.58)
(9.97) (4.74) (3.79) (4.42) (1.49) (3.12) (5.27) (1.51) (4.14) (0.82)
(5.53) (1.20) (4.67) (0.66) (0.33) (1.02) (0.82) (0.75) (1.21) (0.53)
(6.94) (25.20) (5.06) (15.88) (32.89) (34.52) (18.01) (36.65) (5.22) (10.94)
Table 2 Pearson correlation coefficients for all parameters studied in polyurethane foam; all correlations are significant at a level of a ¼ 0.05. Strain gauge signal [mm/m] Strain gauge signal [mm/m] Insertion torque [N cm] Osstell [ISQ] Periotest [PTV] Elastic modulus [MPa]
Insertion torque [N cm]
Osstell [ISQ]
Periotest [PTV]
Elastic modulus [MPa]
0.810
0.471 0.753
0.458 0.746 0.871
0.387 0.575 0.572 0.490
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Table 3 Multiple comparisons between the different polyurethane foam materials based on the strain readings measured on the contra angle handpiece; p-values <0.05 designate significant differences. C10 C10 C10 & S40 C20 C20 & S40 S10 S10 & S40 S20 S20 & S40 S30 S40
C10 & S40
C20
C20 & S40
S10
S10 & S40
S20
S20 & S40
S30
S40
0.000
1.000 0.000
0.004 1.000 0.086
1.000 0.000 1.000 0.046
0.000 1.000 0.000 1.000 0.000
1.000 0.000 1.000 0.013 1.000 0.000
0.000 1.000 0.000 0.319 0.000 1.000 0.000
0.043 0.025 1.000 1.000 0.555 0.006 0.170 0.000
0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.001 0.000
Table 4 Mean values and standard deviations for all parameters determined in human cadaver bone.
Maxilla ant. Maxilla post. Mandible ant. Mandible post.
Drilling resistance [1-2-3-4]
Strain gauge signal [mm/m]
Insertion torque [N cm]
Osstell [ISQ]
Elastic modulus [MPa]
Cortical bone thickness [mm]
Trabecular bone density [1-2-3]
2.83 2.85 1.34 1.60
1193.03 439.22 2323.80 3243.02
16.68 9.33 29.72 30.53
63.75 64.92 75.39 78.46
381.38 475.97 770.00 516.21
1.58 0.74 1.63 1.76
1.90 1.75 2.16 1.88
(0.72) (0.80) (0.70) (0.72)
(888.02) (334.60) (1830.96) (3803.27)
(11.66) (5.31) (13.27) (12.18)
(12.99) (11.23) (6.31) (6.21)
(311.74) (279.98) (296.17) (369.94)
(1.03) (0.38) (0.95) (0.77)
(0.57) (0.45) (0.45) (0.58)
Table 5 Correlation coefficients for all parameters determined in human cadaver bone (Pearson’s productemoment correlation); correlation coefficients p < 0.05 designate significant correlations. Drilling resistance Drilling resistance Strain gauge signal Insertion torque Resonance frequency analysis Compressive test Cortical bone thickness Trabecular bone density
Strain gauge signal
Insertion torque
Resonance frequency analysis
Compressive test
Cortical bone thickness
Trabecular bone density
0.33
0.69 0.16
0.47 0.29 0.46
0.23 0.02 0.37 0.17
0.38 0.23 0.57 0.44 0.29
0.06 0.16 0.19 0.12 0.53 0.07
Table 6 Welch two sample tests for differences with respect to jaw type based on measurements in human cadaver bone. p-values <0.05 designate significant differences. Parameter
Jaw type
n
Mean
SD
Drilling resistance
Maxilla Mandible Maxilla Mandible Maxilla Mandible Maxilla Mandible Maxilla Mandible Maxilla Mandible Maxilla Mandible
25 85 25 85 25 85 25 85 11 39 22 84 22 84
2.840 1.501 801.052 2896.962 12.856 30.228 64.360 77.306 424.375 594.298 1.1233 1.7107 1.818 1.988
0.7461 0.7175 751.7649 3223.7187 9.5110 12.5274 11.8669 6.3906 287.0313 364.8232 0.8440 0.8410 0.5010 0.5487
Strain gauge signal Insertion torque Osstell Elastic modulus Cortical bone thickness Trabecular bone density
modulus and trabecular bone density it was possible to differentiate mandibular from maxillary bone using all the measurement techniques (Table 6). 4. Discussion In experimental research, micro computed tomography and microradiographs are frequently used for objective evaluation of bone quality as represented by measurements of bone mineral density and bone microstructure (Matsuo et al., 2011; Nolff et al., 2010; Pekkan et al., 2011). For clinical application these techniques are not available and computed tomography (CT) or CBCT is used instead. However, it has recently been pointed out that
t
df
p
7.9272
38.029
0.000
5.5066
105.331
0.000
7.4341
50.951
0.000
5.2359
28.210
0.000
1.6274
20.093
0.1192
2.9078
32.779
0.006
1.3875
35.378
0.1740
considerable limitations exist with the use of CBCT for evaluating bone quality (Hohlweg-Majert et al., 2010). With current clinical methods being inappropriate for evaluating alveolar bone quality and dental implant stability (Nkenke et al., 2003; Ribeiro-Rotta et al., 2007) it was the aim of this study to investigate whether strain measurements conducted on the shaft of a contra angle handpiece during implant bed preparation could be used for the objective classification of alveolar bone (Lekholm and Zarb, 1985; Vercellotti and Vercellotti, 2009). The major advantage of that approach would be that, in contrast to measurement systems for dental implant stability such as the Osstell or Periotest device (Tricio et al., 1995; Friberg et al., 1999b; Al-Nawas et al., 2006), no additional step would be added to the
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surgical protocol. Similar to measuring implant insertion torque (Beer et al., 2003; Johansson et al., 2004), which has also been shown to provide only rough estimations, strain measurements on the contra angle handpiece can be carried out as part of the regular protocol applied in dental implant surgery. In contrast to radiographic assessments of bone quality (Norton and Gamble, 2001), which have also been found to show high variations (Shapurian et al., 2006; Turkyilmaz et al., 2007), the patient would not be exposed to radiation (Aranyarachkul et al., 2005). With the measurements being done at an early stage of implant surgery, the treatment protocol could be modified to account for low levels of bone quality. In such a case, finalizing the implant hole could, for instance, be done using undersized drilling (Beer et al., 2007) and the osteotome technique respectively in order to increase local bone density and subsequently primary implant stability (Nkenke et al., 2002; Gulsahi et al., 2007). Despite the fact that significant correlations of strain readings with other measurement techniques could be set up based on the experiments conducted in polyurethane foam, it was not possible to reliably distinguish materials differing in density and structure based on the strain values obtained from the contra angle handpiece. In particular, the presence of a simulated cortical plate made it impossible to differentiate the underlying bone types showing varying densities and architectural properties. The major problem involved with the approach presented appears to be the fact that axial feed and contact pressure cannot be standardized in manual drilling of implant sockets in a setting resembling clinical practice. For that reason, the strain measurements have been conducted during the second drilling step (2.8 mm twist drill) following the creation of a pilot hole with a diameter of 2.2 mm. Although time expenditure for the second drill step was more consistent as compared to the first drill step, a number of measurements had to be excluded from analysis as substantial deviations in the time needed for completing the 2.8 mm drilling occurred. With that operation being carried out, reasonably good correlations of strain values and the other parameters determined could be established. For the experiments based on human cadaver bone, a comparable standardization procedure could not be carried out as measurements on unique samples showing high levels of variation had to be analyzed. As a result of this, fewer correlations with other parameters have been found. However, variations in quality between maxillary and mandibular bone have obviously been great enough to allow for a statistically significant difference between the respective strain measurements to be detected. With respect to the use of polyurethane foam material and human cadaver bone for simulating the clinical conditions of dental implant surgery, the following limitations have to be taken into account. Although it has been claimed that from a structural point of view, bone is comparable to foam materials (Gibson, 1985), the polyurethane material used drastically differed from human bone in terms of clinical handling characteristics. The human cadaver bone used in the second experiment also bears considerable shortcomings as the mechanical properties of bone undergo changes post mortem and may also be influenced by storage conditions and time (Linde and Sørensen, 1993). This may have also been one reason why differentiating between anterior and posterior implant sites was not possible using any of the diagnostic methods used. 5. Conclusion Within the limitations of this study, it appears that the use of strain measurements on a contra angle handpiece for the classification of bone quality is only applicable in uniform single layer
materials when axial feed and contact pressure can be standardized. As neither of these requirements can be fulfilled in clinical practice, this approach seems to be inappropriate for setting up an objective classification system for alveolar bone quality. Sources of support None. Conflict of interest None of the authors have any conflict of interest. Acknowledgments The authors wish to thank Anthony Simpson, Institute of Anatomy, University of Erlangen-Nuremberg for assistance with human cadaver specimens, Dr. Felix Kölpin, Department of Prosthodontics, University of Erlangen-Nuremberg for conducting the compressive tests and Dr. Friedrich Graef, Department of Applied Mathematics, University of Erlangen-Nuremberg, for statistical data analysis. References 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 21: 726e732, 2006 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 20: 416e424, 2005 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 34: 359e366, 2007 Beer A, Gahleitner A, Holm A, Tschabitscher M, Homolka P: Correlation of insertion torques with bone mineral density from dental quantitative CT in the mandible. Clin Oral Implants Res 14: 616e620, 2003 Beer A, Gahleitner A, Holm A, Birkfellner W, Homolka P: Adapted preparation technique for screw-type implants: explorative in vitro pilot study in a porcine bone model. Clin Oral Implants Res 18: 103e107, 2007 Brunski JB: Biomechanics of oral implants: future research directions. J Dent Educ 52: 775e787, 1988 Friberg B, Sennerby L, Grondahl K, Bergstrom C, Back T, Lekholm U: On cutting torque measurements during implant placement: a 3-year clinical prospective study. Clin Implant Dent Relat Res 1: 75e83, 1999a Friberg B, Sennerby L, Meredith N, Lekholm U: A comparison between cutting torque and resonance frequency measurements of maxillary implants. A 20-month clinical study. Int J Oral Maxillofac Surg 28: 297e303, 1999b Gibson LJ: The mechanical behaviour of cancellous bone. J Biomech 18: 317e328, 1985 Gulsahi A, Paksoy CS, Yazıcıoglu N, Arpak N, Kucuk NO, Terzioglu H: Assessment of bone density differences between conventional and bone-condensing techniques using dual energy x-ray absorptiometry and radiography. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 104: 692e698, 2007 Hohlweg-Majert B, Metzger MC, Kummer T, Schulze D: Morphometric analysis e cone beam computed tomography to predict bone quality and quantity. J Craniomaxillofac Surg. doi:10.1016/j.jcms.2010.10.002, 2010 Johansson B, Back 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 6: 9e15, 2004 Lekholm U, Zarb GA: Patient selection and preparation. In: Branemark P-I, Zarb GA, Albrektsson T (eds), Tissue integrated prostheses: osseointegration in clinical dentistry. Chicago: Quintessence Publ Co, 199e209, 1985 Linde F, Sørensen HC: The effect of different storage methods on the mechanical properties of trabecular bone. J Biomech 26: 1249e1252, 1993 Matsuo A, Chiba H, Takahashi H, Toyoda J, Hasegawa O, Hojo S: Bone quality of mandibles reconstructed with particulate cellular bone and marrow, and plateletrich plasma. J Craniomaxillofac Surg. doi:10.1016/j.jcms.2011.01.003, 2011 Meredith N: Assessment of implant stability as a prognostic determinant. Int J Prosthodont 11: 491e501, 1998 Nkenke E, Kloss F, Wiltfang J, Schultze-Mosgau S, Radespiel-Tröger M, Loos K, et al: Histomorphometric and fluorescence microscopic analysis of bone remodelling after installation of implants using an osteotome technique. Clin Oral Implants Res 13: 595e602, 2002 Nkenke E, Hahn M, Weinzierl K, Radespiel-Troger M, Neukam FW, Engelke K: Implant stability and histomorphometry: a correlation study in human cadavers using stepped cylinder implants. Clin Oral Implants Res 14: 601e609, 2003 Nolff MC, Kokemueller H, Hauschild G, Fehr M, Bormann KH, Spalthoff S, et al: Comparison of computed tomography and microradiography for graft
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