Evaluation of Bone Heating, Drill Deformation, and Drill Roughness After Implant Osteotomy: Guided Surgery and Classic Drilling Procedure Pâmela Letícia dos Santos, DDS, MSc, PhD1/Thallita Pereira Queiroz, DDS, MSc, PhD2/ Rogério Margonar, DDS, MSc, PhD3/Abrahão Cavalcante Gomes de Souza Carvalho, DDS, MSc4/ Walter Betoni Jr, DDS, MSc, PhD5/Regis Rocha Rodrigues Rezende, DDS, MSc6/ Paulo Henrique dos Santos, PhD7/Idelmo Rangel Garcia Jr, DDS, MSc, PhD8 Purpose: This study evaluated and compared bone heating, drill deformation, and drill roughness after several implant osteotomies in the guided surgery technique and the classic drilling procedure. Materials and Methods: The tibias of 20 rabbits were used. The animals were divided into a guided surgery group (GG) and a control group (CG); subgroups were then designated (G0, G1, G2, G3, and G4, corresponding to drills used 0, 10, 20, 30 and 40 times, respectively). Each animal received 10 sequential osteotomies (5 in each tibia) with each technique. Thermal changes were quantified, drill roughness was measured, and the drills were subjected to scanning electron microscopy. Results: Bone temperature generated by drilling was significantly higher in the GG than in the CG. Drill deformation in the GG and CG increased with drill use, and in the CG a significant difference between G0 and groups G3 and G4 was observed. In the GG, a significant difference between G0 and all other groups was found. For GG versus CG, a significant difference was found in the 40th osteotomy. Drill roughness in both groups was progressive in accordance with increased use, but there was no statistically significant difference between subgroups or between GG and CG overall. Conclusion: During preparation of implant osteotomies, the guided surgery technique generated a higher bone temperature and deformed drills more than the classic drilling procedure. The increase in tissue temperature was directly proportional to the number of times drills were used, but neither technique generated critical necrosisinducing temperatures. Drill deformation was directly proportional to the number of times the drills were used. The roughness of the drills was directly proportional to the number of reuses in both groups but tended to be higher in the GG group. Int J Oral Maxillofac Implants 2014;29:51–58. doi: 10.11607/jomi.2919 Key words: bone overheating, dental implants, osteotomy
I
mplant dentistry constitutes a highly predictable and successful means of rehabilitation of the stomatognathic system, with success rates between 89% and
1 Assistant
Professor, Discipline of Oral and Maxillofacial Surgery and Integrated Clinic, Department of Oral Biology, Postgraduate Studies, Universidade do Sagrado Coração (USC), Bauru, São Paulo, Brazil. 2 Assistant Professor, Discipline of Oral and Maxillofacial Surgery and Integrated Clinic, University Center of Araraquara (UNIARA), Araraquara, São Paulo, Brazil; Assistant Professor, Postgraduate Course of Dental Implantology, UNIARA. 3Assistant Professor, Discipline of Periodontology and Integrated Clinic, University Center of Araraquara, UNIARA, Araraquara, São Paulo, Brazil; Coordinating Professor, Postgraduate Course of Dental Implantology, UNIARA, Araraquara, São Paulo, Brazil. 4PhD Student, Department of Surgery and Integrated Clinic, Discipline of Oral and Maxillofacial Surgery, Dentistry School of Araçatuba, São Paulo State University (UNESP), Araçatuba, São Paulo, Brazil.
95%.1 The high success rate with the osseointegration of dental implants is, among other factors, related to primary bone repair of the site where implants have 5Assistant
Professor, Department of Oral Surgery, University of Cuiabá (UNIC), Cuiabá, Brazil; Assistant Professor, Specialization in Dental Implantology, Dental School of Cuiabá, Mato Grosso, Brazil. 6Specialist in Implantology, University Center Barretos (UniFEB), São Paulo, Brazil. 7Associate Professor, Department of Dental Materials and Prosthodontics, Discipline of Dental Materials, UNESP, Araçatuba, São Paulo, Brazil. 8 Professor, Department of Surgery, Discipline of Oral and Maxillofacial Surgery, Dentistry School of Araçatuba, UNESP, Araçatuba, São Paulo, Brazil. Correspondence to: Pâmela Letícia dos Santos, Rua José Bonifácio 1193, CEP: 16015-050, Araçatuba, SP, Brazil. Email: [email protected] ©2014 by Quintessence Publishing Co Inc.
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been placed.2 Therefore, adequate preparation of the receptor bed and the presence of healthy bone tissue are critical conditions in the repair process.3,4 Preparation of the implant receptor bed can cause mechanical and thermal damage. The bone heating generated during this procedure can produce necrosis in a discrete cortical area or affect the whole region, including adjacent soft tissue.5 This occurs because thermal bone necrosis causes irreversible injuries to the organic portion of bone tissue and to the cells present in the local blood circulation. The extent of this necrosis varies according to the following factors: (1) osteotomy technique in relation to the velocity, pressure, and duration of the osteotomy; (2) drill characteristics, such as size, shape, and cutting capacity; (3) external factors, including the irrigation technique.4,6–8 Eriksson and Albrektsson5,8 proved that bone tissue is more susceptible to thermal injury than previously thought. They confirmed that the critical temperature is 47°C when drilling for less than 1 minute, or 50°C when drilling for 30 seconds. Repeated use of drills during preparation of the receptor bed can increase wear, which reduces drilling efficiency and consequently generates more frictional heat.9–11 However, in guided surgery, because of scarce information about the life span of drills, the dental practitioner’s decision to substitute them remains empirical, which might result in thermal and mechanical compromise of the receptor bed and subsequent bone repair. The use of guided surgery for dental implants is a helpful tool for the diagnosis, planning, and treatment of patients with no teeth or partial dentition. In guided surgery, an individualized surgical guide is created using a stereolithographic model based on computed tomography. However, this device limits direct irrigation from the active point of the drill.4,10 Considering the harmful impact of bone overheating on bone tissue repair and the osseointegration of implants, the overutilization of drills during osteotomy may influence the temperature generated in bone tissue. Furthermore, guided surgery can limit direct irrigation from the active point of the drill because metal sleeves must be used to guide the drilling. Therefore, the purpose of this study was to evaluate bone tissue heating, drill deformation, and drill roughness after implant osteotomy, comparing classic drilling with guided surgery and verifying the influence of surgical drill reuse on bone heating.
MATERIAL AND METHODS The project was reviewed and approved by the animal care and use committee at the Dentistry School of Araçatuba, São Paulo State University (protocol no.
2010-004687). Twenty male white rabbits (Oryctolagus cunilicus, New Zealand) with body weight between 3 and 4 kg were used. The animals were divided into a guided surgery group (GG) and a classic drilling procedure control group (CG); these were then each divided into five subgroups—G0, G1, G2, G3, and G4—corresponding to drills used for 0, 10, 20, 30, and 40 osteotomies, respectively. There is no information to indicate the ideal quantity of perforations for the studied drill system.
Surgery
The animals were sedated intramuscularly with a combination of ketamine (50 mg/kg, Vetaset, Fort Dodge Saúde Animal) and xylazine hydrochloride (5 mg/kg, Dopaser, Laboratório Calier do Brasil). After anesthesia was obtained, an incision was made in the medial portion of the right and left tibia of every rabbit, followed by the dissection of soft tissue and detachment of the periosteum for the creation of the osteotomies. An electric motor at a speed of 1,600 rpm, connected to a reducer handpiece 20:1 (Kavo), was used to create the osteotomies.10 Every animal received 10 sequential osteotomies (5 GG, 5 CG) at random in both tibiae. Receptor bed preparation of the CG began with a spear drill to delimit the drilling locations and to pierce the cortical bone. Next, 2.0-mm, 2.8-mm, 3.0-mm, and 3.15-mm twist drills (Conexão Sistemas de Prótese) were used sequentially to a constant depth of 4 mm (Fig 1).10 Therefore, only the superior cortex was drilled, corresponding to type 1 bone.12 External irrigation was performed with 0.9% sodium chloride solution (Darrow). The preparation of GG sites consisted of an incision, tissue detachment, and a drilling sequence similar to the CG. However, for the GG, a surgical guide was made of acrylic resin, obtained from the cast of a rabbit tibia. The guide was positioned on the tibia and used during receptor bed preparation to simulate the guided surgery technique (Fig 2). External irrigation was performed with 0.9% sodium chloride solution (Darrow). Although the pressure exerted on bone tissue during the osteotomies was not measured, intermittent drilling with little applied pressure allowed for the removal of detached bone and free access of the irrigation solution. Euthanasia was performed immediately postoperative with an intramuscularly administered dose of 30% chloral hydrate (2 mL/kg).
Bone Heating Analysis
Thermal quantification was performed with a digital thermometer (Salvterm 700C, sensor type J, Salgas Indústria e Comércio) that registered the bone surface temperature before drilling (initial temperature) and the
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dos Santos et al
Fig 1 Initial drilling in the CG with twist drill under abundant irrigation with saline.
Fig 2 Sequential drilling for implants in the GG with a twist drill.
Fig 3 SEM illustrating area of substance loss from the active tip of the drill.
Fig 4 SEM showing condensation of steel flakes abraded from the drill points.
temperature in the osteotomies after drilling (final temperature). The maximum variation of the values (final temperature – initial temperature) was then registered.13 The data were subjected to the Mann-Whitney test (α = .05) for nonparametric comparison between the GG and CG techniques.
Microscopic Investigation of Drills
The drills used for the osteotomies were analyzed with a scanning electron microscope (SEM) (XL series, type XL 30 TMP, equipped with an Oxford incaX-sight detector, Philips). Two photomicrographs (front and back, magnified 200 times) were obtained from the active point of each drill before and after their use for 10, 20, 30, and 40 osteotomies. Next, areas of deformation were quantified, including areas of substance loss, condensation of steel flakes abraded from the drill points, cavity-shaped defects, wear, and abrasion (Figs 3 to 5). To enable quantification of areas of substance loss in the spear drills, a template of a new unused drill was superimposed on the images of used drills (Fig 6). The obtained images were processed in the program ImageLab 2000. Using the tools select region, calculate
Fig 5 SEM illustrating deformation and melting of the active tip of the drill.
regions, and calculation spreadsheet, all areas of deformation were demarcated, calculated in pixels, and added together. Subsequently, the percentage of the deformed area in relation to the total area of the photomicrograph of each drill was calculated. The International Journal of Oral & Maxillofacial Implants 53
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dos Santos et al
4.5
CG GG
Thermal oscillation (°C)
4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0
Temperature (°C)
Fig 6 To enable quantification of areas of substance loss in the spear drills, a template of a new unused drill was superimposed on the images of the used drills. 34 33 32 31 30 29 28.3 28 27 26.1 26 25 24 0
CG GG
28.4 27.3
30.9
27.9
28.5
26.4
10
20 30 No. of osteotomies
40
50
Fig 8 Comparison of bone heating with the number of osteotomies performed.
To assess the groups separately, the data were subjected to variance analysis using the Holm-Sidak method with significance level set at .05. The t test and Pearson correlation coefficients were used to compare groups.
Investigation of Drill Roughness
H2.0 mm H2.8 mm H3.0 mm H3.15 mm Type of drill
Fig 7 Comparison of thermal oscillation with drill type between the CG and GG. H = twist drill.
RESULTS Bone Heating Analysis
31.8 30.3
Spear
The average surface roughness (Ra), average depth of roughness (Rz), and maximum roughness (Rmax) were all determined (in microns) with a roughness meter (SJ-401, Mitutoyo) with a cutoff of 0.80 mm, totaling 5.6 mm of reading length over the cutting area of the drills. For each surface, three readings were performed at different positions on the drill, and the average was calculated. The surface roughness values were measured for unused drills (G0) and after 10 (G1), 20 (G2), 30 (G3), and 40 osteotomies (G4). The reading parameters were the same for all evaluation periods. Data were analyzed statistically by the Kolmogorov-Smirnov test and further with the Kruskal-Wallis and Mann-Whitney tests (α = 5%).
The average predrilling bone temperature was 28°C. Maximum temperatures observed in the CG and GG were 30.5°C and 34.6°C, respectively, with maximum oscillations of 5.1°C and 5.8°C. Comparing each group separately, no statistically significant correlation was found between the temperature increase and the type of drill used (Fig 7). However, it was noted that the average temperature oscillations were 2.8°C and 4.1°C when spear drills were used and 0.81°C and 3.15°C when twist drills were used in the CG and GG, respectively. A statistically significant difference in thermal oscillation between CG and GG was found. Regardless of drill type (spear or twist), bone heating was about three times higher in the GG. Bone temperature increased with the number of times the drills were used in both groups (Fig 8).
SEM Observation
The unused drills of the GG and CG were compared with the drills used for different numbers of osteotomies using image analysis. In the G0 groups, some fabrication errors were observed and quantified in the analysis as initial defects. The percentage values of these defects in GG and CG drills covered an average of 9.23% and 5.12% of the active point, respectively. In the CG, spear drills underwent more deformation than twist drills. The former showed an average surface area deformation of 33.88%, whereas the latter had 22.79% deformation. In the GG, however, spear drills had less deformation than twist drills, with areas of deformation averaging 31.25% and 33.9%, respectively. In subgroups G1, G2, G3, and G4, a gradual increase in drill deformation was observed, varying proportionally with the increase in the number of times a drill was used in both the GG and CG (Fig 9).
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CG 50 47.07% GG 45 40 34.31% 35 28.33% 30 25 27.95% 18.24% 24.84% 20 21.35% 15 9.26% 17.86% 10 5 5.20% 0 0 10 20 30 40 50 No. of osteotomies
CG GG
0.8 0.7 0.6 Ra (µm)
No. of deformation
dos Santos et al
0.5 0.4 0.3 0.2 0.1 0
0
10
20 30 No. of osteotomies
40
50
Fig 9 Percentage average drill deformation versus the number of osteotomies performed.
Fig 10 Average Ra values for CG and GG as a function of the number of osteotomies performed.
Comparisons between subgroups of the CG using the Holm-Sidak method revealed a statistically significant difference between G0 and G3 and between G0 and G4. Comparisons between the remaining groups did not produce significant results. The subgroups of GG were submitted to the same test, which revealed significant differences between G0 and G1, G2, G3, and G4, as well as a difference between G1 and G2, compared to G4. GG and CG were compared using the t test, which did not reveal statistically significant differences between GG1 and CG1, GG2 and CG2, and GG3 and CG3. However, a significant difference between GG4 and CG4 was observed. Quantification of the areas of deformation made it possible to verify a strong and directly proportional correlation between the variables “deformation” and “number of times used” in the CG (Pearson r = 0.984). In the GG, a moderate directly proportional correlation between the same variables was observed (Pearson r = 0.635).
up to the 20th drill reuse (G2), and after the 30th drill reuse there was a tendency toward increased Ra values (Fig 10). Although no significant difference was observed between the CG and GG for Rz (P > .05), the GG exhibited absolute greater roughness than CG (Fig 11). For CG, the Rz value was constant for all periods evaluated; on the other hand, a directly proportional increase in Rz values was noted for GG as the reuse of drills increased. Additionally, the values for Rmax did not differ significantly between CG and GG groups (P > .05). Figure 12 shows that the Rmax values remained constant up to the 30th drill reuse (G3), with an increase in surface roughness after this period for both osteotomy techniques. GG drills exhibited a tendency toward increased Rmax value when compared to the CG drills for all subgroups.
Investigation of Drill Roughness
Drill deformation and its consequent influence on the viability of the receptor bed after implant osteotomy has been studied by various authors,10,11,14,15 who predominantly made use of rabbit tibiae in their in vivo assessments of osseointegration. This choice is related to the fact that rabbit tibiae allow for the use of implants and drills of a size that is compatible with the human oral cavity. Furthermore, the superior cortex of the rabbit tibia possesses a bone quality similar to type 1 bone, and rabbits are easy to handle and inexpensive.11,16,17 Because of technologic advances, this issue remains relevant, and there is much discussion about the life span of drills used for implants.6 Until now, no in vivo studies have yet assessed bone heating, drill deformation, and drill roughness with the guided surgery technique.
In the G0 subgroups, the presence of some artifacts from the manufacturer was observed, and these were considered and quantified during the initial roughness evaluations. The initial Ra, Rz, and Rmax for the CG were 0.415 µm, 2.325 µm, and 0.518 µm, respectively. For the GG, these measurements were 0.356 µm, 1.596 µm, and 0.4235 µm, respectively. No significant difference was observed between the CG and GG after 10, 20, 30, and 40 osteotomies for all roughness parameters (P > .05). In the subgroups G1, G2, G3, and G4, a gradual increase of surface roughness was noted. In other words, as the use of the drill increased, its surface roughness also increased for both groups. Similar Ra values were observed for the CG and GG (P > .05). For both groups, the roughness was constant
DISCUSSION
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dos Santos et al
CG GG
1.6
0.6
1.4
0.5
1.2
Rmax (µm)
Rz (µm)
0.7
0.4 0.3 0.2
1.0 0.8 0.6 0.4
0.1 0
CG GG
1.8
0.2 0
10
20 30 No. of osteotomies
40
50
0
0
10
20 30 No. of osteotomies
40
50
Fig 11 Rz values for CG and GG groups as a function of the number of osteotomies performed.
Fig 12 Rmax values for CG and GG groups as a function of the number of osteotomies performed.
Even in less traumatic surgical procedures, a necrotic zone is formed during receptor bed preparation. This zone interferes in the osseointegration and is related to several factors, including surgical technique and bone heating, as mentioned in this study.4,7,18 The quantity of frictional heat generated is directly related to the magnitude of force used, drill size and form, and drilling time.7 Clinically, there is no measurement of the pressure exerted on a handpiece during osteotomy preparation. Therefore, if the speed is kept constant, it is possible for the operator to apply greater pressure when working on cortical bone, thereby increasing the frictional heat and consequently the bone tissue temperature.13 Moreover, in the present study, drillings were performed in dense cortical bone (type 1) at a constant speed of 1,600 rpm, and only one surgeon performed all the osteotomies to ensure standardization of the surgical technique, following the protocol previously described by Queiroz et al10 and dos Santos et al.19 The depth of drilling was a constant factor in this research. The anatomy of the rabbit tibia presents a thicker cortex of approximately 4 mm; this was passed through completely during milling of the osteotomies, following the methodology of previous studies.10,13,19 Misir et al4 verified bone heating after drill reutilization in guided surgery and concluded that, after 35 utilizations, the drills caused increased heating. The results of the present study also showed a tendency toward increased temperatures, although it was not statistically significant. However, Allsobrook et al20 stated that drills used for up to 50 osteotomies did not appear to elevate bone temperatures to a harmful level. Guided surgery generated more heat than conventional drilling, although the highest recorded temperature of 33°C was well below the critical temperature of 47°C indicated by Eriksson and Albrektsson.8
Among the factors that may influence bone heating is drill shape.10,21 In this study, the use of spear drills caused higher thermal oscillation during drilling in both groups. Drill wear is defined by the United Nations Organization for Economic Cooperation and Development as progressive damage that involves loss of material. Several studies have conducted SEM analyses of drill wear and its association with bone heating using the classic drilling method.10,11,22 However, the absence of quantitative data concerning the deformed areas and differences in the adopted experimental models have made it impossible to compare those studies.4,14 This study is the first in the literature to quantify and compare drill deformation after repeated osteotomies, using both the classic drilling method and guided surgery. It was possible to verify that the active point of spear drills used in classic drilling was slightly more deformed than those used in guided surgery. For twist drills, the opposite was seen, which is probably related to the fact that during the use of twist drills in guided surgery the drill-sleeve distance is smaller. The heat exchange between these metallic elements generates a higher temperature and, consequently, more deformation. Furthermore, because an acrylic resin guide with metal sleeves is present, direct irrigation in this technique is not possible, which also contributes to a higher temperature and more drill deformation.4 The main method to prevent bone overheating is irrigation. Lavelle and Wedgwood23 affirmed that internal irrigation was more effective than external irrigation in reducing friction during osteotomy. More recently, Misir et al4 conducted a study that showed higher temperatures when external irrigation was used in combination with internal irrigation, compared to the use of external irrigation only. The authors attributed this to the involvement of dense cortical bone that obstructed the internal irrigation points.
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According to Harris and Kohles,14 another factor that influences the cutting capacity of drills is the repetition of sterilization cycles by autoclave. Jochum and Reichart,24 however, found no statistically significant difference in bone heating between reused drills that were washed and sterilized and drills that were washed only. The present study did not consider this factor. Ercoli et al9 analyzed the influence of wear on the cutting capacity of drills and related this factor to bone heating. They concluded that the durability and cutting efficiency of a drill are directly related to its design and fabrication material. On the other hand, Chacon et al22 found no significant differences between drills of different brands. In this study, only one commercial brand was used to keep this factor constant. When the number of times a drill was used and deformation were examined, it was possible to observe a directly proportional relationship between those factors in the GG as well as in the CG using the Pearson correlation coefficient. The direct effect of drill reuse on deformation was confirmed by statistical analysis, which revealed a significant difference between the unused drills and drills used 10, 20, 30, and 40 times in the GG and between unused drills and those used 30 and 40 times in the CG. However, group comparison (GG and CG) showed a significant difference only for the 40th osteotomy. These results can be explained by the fixed inclination of the drill during an osteotomy with guided surgery, which uses an acrylic resin guide with metal sleeves. This procedure may cause less substance loss and deformation on the active point than classical drilling, where the absence of a surgical guide allows for changes in inclination during osteotomy. Golin25 investigated the Ra of unused steel drills and of those used for 20 osteotomies through the conventional technique of implant surgery in bovine ribs. It was concluded that both 2- and 3-mm-diameter drills exhibited an increase in surface roughness. Sartori et al,26 using the same experimental model and conventional technique of implant insertion, investigated the Ra, Rz, and Rmax of steel drills after 10, 20, 30, and 40 osteotomies and observed no significant difference in surface roughness, regardless of the number of osteotomies performed. In this study, both techniques exhibited similar behavior, although a tendency toward increased roughness was observed for the GG technique for all roughness parameters. To avoid a negative influence on osseointegration, it is important for dental professionals to be aware of the importance of minimizing the factors that may contribute to bone heating during implant osteotomy. These include selection of the least traumatic surgery technique, increases in the volume of irrigation to ensure that irrigation reaches the drill/receptor bed
interface, and minimization of the force applied during drilling. Taking these measures is of particular importance when using a guided surgery protocol, as this technique generates more heat than classic drilling.
CONCLUSION Based on the methods adopted for the present study, it can be concluded that: 1. The guided surgery technique generated a higher bone temperature than the classic drilling technique during osteotomies for implant receptor bed preparation. The increase in tissue temperature was directly proportional to the number of times drills were used. However, neither technique generated the critical temperature that bone can tolerate without necrosis. 2. Drill deformation was directly proportional to the number of times drills were used in both groups. The tendency toward drill deformation was stronger in guided surgery, particularly in the 40th osteotomy. 3. The surface roughness of the drill was directly proportional to the number of uses for both osteotomy techniques, and the guided surgery technique tended to increase the surface roughness of the drills.
Acknowledgments The authors would like to thank Conexão Sistema de Prótese for their assistance and for supplying the implant drills used in this study. The authors reported no conflicts of interest related to this study.
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7. Tehemar SH. Factors affecting heat generation during implant site preparation: A review of biologic observations and future considerations. Int J Oral Maxillofac Implants 1999;14:127–136. 8. Eriksson RA, Albrektsson T. The effect of heat on bone regeneration: An experimental study in rabbits using the bone growth chamber. J Oral Maxillofac Surg 1984;42:705–711. 9. Ercoli C, Funkenbusch PD, Lee HJ, Moss ME, Graser GN. The influence of drill wear on cutting efficiency and heat production during osteotomy preparation for dental implants: A study of drill durability. Int J Oral Maxillofac Implants 2004;19:335–349. 10. Queiroz TP, Souza FA, Okamoto R, et al. Evaluation of immediate bone-cell viability and of drill wear after implant osteotomies: Immunohistochemistry and scanning electron microscopy analysis. J Oral Maxillofac Surg 2008;66:1233–1240. 11. Almeida EO, Pellizzer EP, Goiato MC, et al. Computer-guided surgery in implantology: Review of basic concepts. J Craniofac Surg 2010;21:1917–1921. 12. Brånemark PI, Zarb GA, Albrektsson T. Tissue-Integrated Prostheses: Osseointegration in Clinical Dentistry. Chicago: Quintessence, 1985:199–210. 13. Carvalho AC, Queiroz TP, Okamoto R, Margonar R, Garcia IR Jr, Magro Filho O. Evaluation of bone heating, immediate bone cell viability, and wear of high-resistance drills after the creation of implant osteotomies in rabbit tibias. Int J Oral Maxillofac Implants 2011;26(6):1193–1201. 14. Harris BH, Kohles SS. Effects of mechanical and thermal fatigue on dental drill performance. Int J Oral Maxillofac Implants 2001;16(6): 819–826. 15. Reingewirtz Y, Szmukler-Moncler S, Senger B. Influence of different parameters on bone heating and drilling time in implantology. Clin Oral Implants Res 1997;8(3):189–197.
16. Ellingsen JE, Johansson CB, Wennerberg A, Holmén A. Improved retention and bone-to-implant contact with fluoride-modified titanium implants. Int J Oral Maxillofac Implants 2004;19:659–666. 17. Margonar R, Sakakura CE, Holzhausen M, Pepato MT, Alba RC, Marcantonio E. The influence of diabetes mellitus and insulin therapy on biomechanical retention around dental implants: A study in rabbits. Implant Dent 2003;12(4):333–339. 18. Wiggins KL, Malkin S. Drilling of bone. J Biomech 1976;9:553–559. 19. dos Santos PL, Queiroz TP, Margonar R, et al. Guided implant surgery: What is the influence of this new technique on bone cell viability? J Oral Maxillofac Surg 2013;71(3):505–512. 20. Allsobrook OFL, Leichter J, Holborow D, Swain M. Descriptive study of the longevity of dental implant surgery drills. Clin Implant Dent Relat Res 2011;13(3):244–254. 21. Cordioli G, Majzoub Z. Heat generation during site preparation: An in vitro study. Int J Oral Maxillofac Implants 1997;12:186–193. 22. Chacon GE, Bower DL, Larsen PE, McGlumphy EA, Beck M. Heat production by 3 implant drill systems after repeated drilling and sterilization. J Oral Maxillofac Surg 2006;64:265–269. 23. Lavelle C, Wedgwood D. Effect of internal irrigation on frictional heat generated from bone drilling. J Oral Surg 1980;38(7):499–503. 24. Jochum RM, Reichart PA. Influence of multiple use of Timedurtitanium cannon drills: Thermal response and scanning electron microscopic findings. Clin Oral Implants Res 2000;11:139–143. 25. Golin AL. Análise do comportamento de ferramentas de cortes com diferentes revestimentos e seu efeito sobre a geração de calor no osso [thesis]. Paraná, Brazil: Pontifícia Universidade Católica do Paraná, 2005. 26. Sartori EM, Shinohara EH, Ponzoni D, Padovan LE, Valgas L, Golin AL. Evaluation of deformation, mass loss, and roughness of different metal burs after osteotomy for osseointegrated implants. J Oral Maxillofac Surg 2012;70(11):e608–621.
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I
mplant dentistry constitutes a highly predictable and successful means of rehabilitation of the stomatognathic system, with success rates between 89% and
1 Assistant
Professor, Discipline of Oral and Maxillofacial Surgery and Integrated Clinic, Department of Oral Biology, Postgraduate Studies, Universidade do Sagrado Coração (USC), Bauru, São Paulo, Brazil. 2 Assistant Professor, Discipline of Oral and Maxillofacial Surgery and Integrated Clinic, University Center of Araraquara (UNIARA), Araraquara, São Paulo, Brazil; Assistant Professor, Postgraduate Course of Dental Implantology, UNIARA. 3Assistant Professor, Discipline of Periodontology and Integrated Clinic, University Center of Araraquara, UNIARA, Araraquara, São Paulo, Brazil; Coordinating Professor, Postgraduate Course of Dental Implantology, UNIARA, Araraquara, São Paulo, Brazil. 4PhD Student, Department of Surgery and Integrated Clinic, Discipline of Oral and Maxillofacial Surgery, Dentistry School of Araçatuba, São Paulo State University (UNESP), Araçatuba, São Paulo, Brazil.
95%.1 The high success rate with the osseointegration of dental implants is, among other factors, related to primary bone repair of the site where implants have 5Assistant
Professor, Department of Oral Surgery, University of Cuiabá (UNIC), Cuiabá, Brazil; Assistant Professor, Specialization in Dental Implantology, Dental School of Cuiabá, Mato Grosso, Brazil. 6Specialist in Implantology, University Center Barretos (UniFEB), São Paulo, Brazil. 7Associate Professor, Department of Dental Materials and Prosthodontics, Discipline of Dental Materials, UNESP, Araçatuba, São Paulo, Brazil. 8 Professor, Department of Surgery, Discipline of Oral and Maxillofacial Surgery, Dentistry School of Araçatuba, UNESP, Araçatuba, São Paulo, Brazil. Correspondence to: Pâmela Letícia dos Santos, Rua José Bonifácio 1193, CEP: 16015-050, Araçatuba, SP, Brazil. Email: [email protected] ©2014 by Quintessence Publishing Co Inc.
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dos Santos et al
been placed.2 Therefore, adequate preparation of the receptor bed and the presence of healthy bone tissue are critical conditions in the repair process.3,4 Preparation of the implant receptor bed can cause mechanical and thermal damage. The bone heating generated during this procedure can produce necrosis in a discrete cortical area or affect the whole region, including adjacent soft tissue.5 This occurs because thermal bone necrosis causes irreversible injuries to the organic portion of bone tissue and to the cells present in the local blood circulation. The extent of this necrosis varies according to the following factors: (1) osteotomy technique in relation to the velocity, pressure, and duration of the osteotomy; (2) drill characteristics, such as size, shape, and cutting capacity; (3) external factors, including the irrigation technique.4,6–8 Eriksson and Albrektsson5,8 proved that bone tissue is more susceptible to thermal injury than previously thought. They confirmed that the critical temperature is 47°C when drilling for less than 1 minute, or 50°C when drilling for 30 seconds. Repeated use of drills during preparation of the receptor bed can increase wear, which reduces drilling efficiency and consequently generates more frictional heat.9–11 However, in guided surgery, because of scarce information about the life span of drills, the dental practitioner’s decision to substitute them remains empirical, which might result in thermal and mechanical compromise of the receptor bed and subsequent bone repair. The use of guided surgery for dental implants is a helpful tool for the diagnosis, planning, and treatment of patients with no teeth or partial dentition. In guided surgery, an individualized surgical guide is created using a stereolithographic model based on computed tomography. However, this device limits direct irrigation from the active point of the drill.4,10 Considering the harmful impact of bone overheating on bone tissue repair and the osseointegration of implants, the overutilization of drills during osteotomy may influence the temperature generated in bone tissue. Furthermore, guided surgery can limit direct irrigation from the active point of the drill because metal sleeves must be used to guide the drilling. Therefore, the purpose of this study was to evaluate bone tissue heating, drill deformation, and drill roughness after implant osteotomy, comparing classic drilling with guided surgery and verifying the influence of surgical drill reuse on bone heating.
MATERIAL AND METHODS The project was reviewed and approved by the animal care and use committee at the Dentistry School of Araçatuba, São Paulo State University (protocol no.
2010-004687). Twenty male white rabbits (Oryctolagus cunilicus, New Zealand) with body weight between 3 and 4 kg were used. The animals were divided into a guided surgery group (GG) and a classic drilling procedure control group (CG); these were then each divided into five subgroups—G0, G1, G2, G3, and G4—corresponding to drills used for 0, 10, 20, 30, and 40 osteotomies, respectively. There is no information to indicate the ideal quantity of perforations for the studied drill system.
Surgery
The animals were sedated intramuscularly with a combination of ketamine (50 mg/kg, Vetaset, Fort Dodge Saúde Animal) and xylazine hydrochloride (5 mg/kg, Dopaser, Laboratório Calier do Brasil). After anesthesia was obtained, an incision was made in the medial portion of the right and left tibia of every rabbit, followed by the dissection of soft tissue and detachment of the periosteum for the creation of the osteotomies. An electric motor at a speed of 1,600 rpm, connected to a reducer handpiece 20:1 (Kavo), was used to create the osteotomies.10 Every animal received 10 sequential osteotomies (5 GG, 5 CG) at random in both tibiae. Receptor bed preparation of the CG began with a spear drill to delimit the drilling locations and to pierce the cortical bone. Next, 2.0-mm, 2.8-mm, 3.0-mm, and 3.15-mm twist drills (Conexão Sistemas de Prótese) were used sequentially to a constant depth of 4 mm (Fig 1).10 Therefore, only the superior cortex was drilled, corresponding to type 1 bone.12 External irrigation was performed with 0.9% sodium chloride solution (Darrow). The preparation of GG sites consisted of an incision, tissue detachment, and a drilling sequence similar to the CG. However, for the GG, a surgical guide was made of acrylic resin, obtained from the cast of a rabbit tibia. The guide was positioned on the tibia and used during receptor bed preparation to simulate the guided surgery technique (Fig 2). External irrigation was performed with 0.9% sodium chloride solution (Darrow). Although the pressure exerted on bone tissue during the osteotomies was not measured, intermittent drilling with little applied pressure allowed for the removal of detached bone and free access of the irrigation solution. Euthanasia was performed immediately postoperative with an intramuscularly administered dose of 30% chloral hydrate (2 mL/kg).
Bone Heating Analysis
Thermal quantification was performed with a digital thermometer (Salvterm 700C, sensor type J, Salgas Indústria e Comércio) that registered the bone surface temperature before drilling (initial temperature) and the
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dos Santos et al
Fig 1 Initial drilling in the CG with twist drill under abundant irrigation with saline.
Fig 2 Sequential drilling for implants in the GG with a twist drill.
Fig 3 SEM illustrating area of substance loss from the active tip of the drill.
Fig 4 SEM showing condensation of steel flakes abraded from the drill points.
temperature in the osteotomies after drilling (final temperature). The maximum variation of the values (final temperature – initial temperature) was then registered.13 The data were subjected to the Mann-Whitney test (α = .05) for nonparametric comparison between the GG and CG techniques.
Microscopic Investigation of Drills
The drills used for the osteotomies were analyzed with a scanning electron microscope (SEM) (XL series, type XL 30 TMP, equipped with an Oxford incaX-sight detector, Philips). Two photomicrographs (front and back, magnified 200 times) were obtained from the active point of each drill before and after their use for 10, 20, 30, and 40 osteotomies. Next, areas of deformation were quantified, including areas of substance loss, condensation of steel flakes abraded from the drill points, cavity-shaped defects, wear, and abrasion (Figs 3 to 5). To enable quantification of areas of substance loss in the spear drills, a template of a new unused drill was superimposed on the images of used drills (Fig 6). The obtained images were processed in the program ImageLab 2000. Using the tools select region, calculate
Fig 5 SEM illustrating deformation and melting of the active tip of the drill.
regions, and calculation spreadsheet, all areas of deformation were demarcated, calculated in pixels, and added together. Subsequently, the percentage of the deformed area in relation to the total area of the photomicrograph of each drill was calculated. The International Journal of Oral & Maxillofacial Implants 53
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dos Santos et al
4.5
CG GG
Thermal oscillation (°C)
4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0
Temperature (°C)
Fig 6 To enable quantification of areas of substance loss in the spear drills, a template of a new unused drill was superimposed on the images of the used drills. 34 33 32 31 30 29 28.3 28 27 26.1 26 25 24 0
CG GG
28.4 27.3
30.9
27.9
28.5
26.4
10
20 30 No. of osteotomies
40
50
Fig 8 Comparison of bone heating with the number of osteotomies performed.
To assess the groups separately, the data were subjected to variance analysis using the Holm-Sidak method with significance level set at .05. The t test and Pearson correlation coefficients were used to compare groups.
Investigation of Drill Roughness
H2.0 mm H2.8 mm H3.0 mm H3.15 mm Type of drill
Fig 7 Comparison of thermal oscillation with drill type between the CG and GG. H = twist drill.
RESULTS Bone Heating Analysis
31.8 30.3
Spear
The average surface roughness (Ra), average depth of roughness (Rz), and maximum roughness (Rmax) were all determined (in microns) with a roughness meter (SJ-401, Mitutoyo) with a cutoff of 0.80 mm, totaling 5.6 mm of reading length over the cutting area of the drills. For each surface, three readings were performed at different positions on the drill, and the average was calculated. The surface roughness values were measured for unused drills (G0) and after 10 (G1), 20 (G2), 30 (G3), and 40 osteotomies (G4). The reading parameters were the same for all evaluation periods. Data were analyzed statistically by the Kolmogorov-Smirnov test and further with the Kruskal-Wallis and Mann-Whitney tests (α = 5%).
The average predrilling bone temperature was 28°C. Maximum temperatures observed in the CG and GG were 30.5°C and 34.6°C, respectively, with maximum oscillations of 5.1°C and 5.8°C. Comparing each group separately, no statistically significant correlation was found between the temperature increase and the type of drill used (Fig 7). However, it was noted that the average temperature oscillations were 2.8°C and 4.1°C when spear drills were used and 0.81°C and 3.15°C when twist drills were used in the CG and GG, respectively. A statistically significant difference in thermal oscillation between CG and GG was found. Regardless of drill type (spear or twist), bone heating was about three times higher in the GG. Bone temperature increased with the number of times the drills were used in both groups (Fig 8).
SEM Observation
The unused drills of the GG and CG were compared with the drills used for different numbers of osteotomies using image analysis. In the G0 groups, some fabrication errors were observed and quantified in the analysis as initial defects. The percentage values of these defects in GG and CG drills covered an average of 9.23% and 5.12% of the active point, respectively. In the CG, spear drills underwent more deformation than twist drills. The former showed an average surface area deformation of 33.88%, whereas the latter had 22.79% deformation. In the GG, however, spear drills had less deformation than twist drills, with areas of deformation averaging 31.25% and 33.9%, respectively. In subgroups G1, G2, G3, and G4, a gradual increase in drill deformation was observed, varying proportionally with the increase in the number of times a drill was used in both the GG and CG (Fig 9).
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CG 50 47.07% GG 45 40 34.31% 35 28.33% 30 25 27.95% 18.24% 24.84% 20 21.35% 15 9.26% 17.86% 10 5 5.20% 0 0 10 20 30 40 50 No. of osteotomies
CG GG
0.8 0.7 0.6 Ra (µm)
No. of deformation
dos Santos et al
0.5 0.4 0.3 0.2 0.1 0
0
10
20 30 No. of osteotomies
40
50
Fig 9 Percentage average drill deformation versus the number of osteotomies performed.
Fig 10 Average Ra values for CG and GG as a function of the number of osteotomies performed.
Comparisons between subgroups of the CG using the Holm-Sidak method revealed a statistically significant difference between G0 and G3 and between G0 and G4. Comparisons between the remaining groups did not produce significant results. The subgroups of GG were submitted to the same test, which revealed significant differences between G0 and G1, G2, G3, and G4, as well as a difference between G1 and G2, compared to G4. GG and CG were compared using the t test, which did not reveal statistically significant differences between GG1 and CG1, GG2 and CG2, and GG3 and CG3. However, a significant difference between GG4 and CG4 was observed. Quantification of the areas of deformation made it possible to verify a strong and directly proportional correlation between the variables “deformation” and “number of times used” in the CG (Pearson r = 0.984). In the GG, a moderate directly proportional correlation between the same variables was observed (Pearson r = 0.635).
up to the 20th drill reuse (G2), and after the 30th drill reuse there was a tendency toward increased Ra values (Fig 10). Although no significant difference was observed between the CG and GG for Rz (P > .05), the GG exhibited absolute greater roughness than CG (Fig 11). For CG, the Rz value was constant for all periods evaluated; on the other hand, a directly proportional increase in Rz values was noted for GG as the reuse of drills increased. Additionally, the values for Rmax did not differ significantly between CG and GG groups (P > .05). Figure 12 shows that the Rmax values remained constant up to the 30th drill reuse (G3), with an increase in surface roughness after this period for both osteotomy techniques. GG drills exhibited a tendency toward increased Rmax value when compared to the CG drills for all subgroups.
Investigation of Drill Roughness
Drill deformation and its consequent influence on the viability of the receptor bed after implant osteotomy has been studied by various authors,10,11,14,15 who predominantly made use of rabbit tibiae in their in vivo assessments of osseointegration. This choice is related to the fact that rabbit tibiae allow for the use of implants and drills of a size that is compatible with the human oral cavity. Furthermore, the superior cortex of the rabbit tibia possesses a bone quality similar to type 1 bone, and rabbits are easy to handle and inexpensive.11,16,17 Because of technologic advances, this issue remains relevant, and there is much discussion about the life span of drills used for implants.6 Until now, no in vivo studies have yet assessed bone heating, drill deformation, and drill roughness with the guided surgery technique.
In the G0 subgroups, the presence of some artifacts from the manufacturer was observed, and these were considered and quantified during the initial roughness evaluations. The initial Ra, Rz, and Rmax for the CG were 0.415 µm, 2.325 µm, and 0.518 µm, respectively. For the GG, these measurements were 0.356 µm, 1.596 µm, and 0.4235 µm, respectively. No significant difference was observed between the CG and GG after 10, 20, 30, and 40 osteotomies for all roughness parameters (P > .05). In the subgroups G1, G2, G3, and G4, a gradual increase of surface roughness was noted. In other words, as the use of the drill increased, its surface roughness also increased for both groups. Similar Ra values were observed for the CG and GG (P > .05). For both groups, the roughness was constant
DISCUSSION
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dos Santos et al
CG GG
1.6
0.6
1.4
0.5
1.2
Rmax (µm)
Rz (µm)
0.7
0.4 0.3 0.2
1.0 0.8 0.6 0.4
0.1 0
CG GG
1.8
0.2 0
10
20 30 No. of osteotomies
40
50
0
0
10
20 30 No. of osteotomies
40
50
Fig 11 Rz values for CG and GG groups as a function of the number of osteotomies performed.
Fig 12 Rmax values for CG and GG groups as a function of the number of osteotomies performed.
Even in less traumatic surgical procedures, a necrotic zone is formed during receptor bed preparation. This zone interferes in the osseointegration and is related to several factors, including surgical technique and bone heating, as mentioned in this study.4,7,18 The quantity of frictional heat generated is directly related to the magnitude of force used, drill size and form, and drilling time.7 Clinically, there is no measurement of the pressure exerted on a handpiece during osteotomy preparation. Therefore, if the speed is kept constant, it is possible for the operator to apply greater pressure when working on cortical bone, thereby increasing the frictional heat and consequently the bone tissue temperature.13 Moreover, in the present study, drillings were performed in dense cortical bone (type 1) at a constant speed of 1,600 rpm, and only one surgeon performed all the osteotomies to ensure standardization of the surgical technique, following the protocol previously described by Queiroz et al10 and dos Santos et al.19 The depth of drilling was a constant factor in this research. The anatomy of the rabbit tibia presents a thicker cortex of approximately 4 mm; this was passed through completely during milling of the osteotomies, following the methodology of previous studies.10,13,19 Misir et al4 verified bone heating after drill reutilization in guided surgery and concluded that, after 35 utilizations, the drills caused increased heating. The results of the present study also showed a tendency toward increased temperatures, although it was not statistically significant. However, Allsobrook et al20 stated that drills used for up to 50 osteotomies did not appear to elevate bone temperatures to a harmful level. Guided surgery generated more heat than conventional drilling, although the highest recorded temperature of 33°C was well below the critical temperature of 47°C indicated by Eriksson and Albrektsson.8
Among the factors that may influence bone heating is drill shape.10,21 In this study, the use of spear drills caused higher thermal oscillation during drilling in both groups. Drill wear is defined by the United Nations Organization for Economic Cooperation and Development as progressive damage that involves loss of material. Several studies have conducted SEM analyses of drill wear and its association with bone heating using the classic drilling method.10,11,22 However, the absence of quantitative data concerning the deformed areas and differences in the adopted experimental models have made it impossible to compare those studies.4,14 This study is the first in the literature to quantify and compare drill deformation after repeated osteotomies, using both the classic drilling method and guided surgery. It was possible to verify that the active point of spear drills used in classic drilling was slightly more deformed than those used in guided surgery. For twist drills, the opposite was seen, which is probably related to the fact that during the use of twist drills in guided surgery the drill-sleeve distance is smaller. The heat exchange between these metallic elements generates a higher temperature and, consequently, more deformation. Furthermore, because an acrylic resin guide with metal sleeves is present, direct irrigation in this technique is not possible, which also contributes to a higher temperature and more drill deformation.4 The main method to prevent bone overheating is irrigation. Lavelle and Wedgwood23 affirmed that internal irrigation was more effective than external irrigation in reducing friction during osteotomy. More recently, Misir et al4 conducted a study that showed higher temperatures when external irrigation was used in combination with internal irrigation, compared to the use of external irrigation only. The authors attributed this to the involvement of dense cortical bone that obstructed the internal irrigation points.
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dos Santos et al
According to Harris and Kohles,14 another factor that influences the cutting capacity of drills is the repetition of sterilization cycles by autoclave. Jochum and Reichart,24 however, found no statistically significant difference in bone heating between reused drills that were washed and sterilized and drills that were washed only. The present study did not consider this factor. Ercoli et al9 analyzed the influence of wear on the cutting capacity of drills and related this factor to bone heating. They concluded that the durability and cutting efficiency of a drill are directly related to its design and fabrication material. On the other hand, Chacon et al22 found no significant differences between drills of different brands. In this study, only one commercial brand was used to keep this factor constant. When the number of times a drill was used and deformation were examined, it was possible to observe a directly proportional relationship between those factors in the GG as well as in the CG using the Pearson correlation coefficient. The direct effect of drill reuse on deformation was confirmed by statistical analysis, which revealed a significant difference between the unused drills and drills used 10, 20, 30, and 40 times in the GG and between unused drills and those used 30 and 40 times in the CG. However, group comparison (GG and CG) showed a significant difference only for the 40th osteotomy. These results can be explained by the fixed inclination of the drill during an osteotomy with guided surgery, which uses an acrylic resin guide with metal sleeves. This procedure may cause less substance loss and deformation on the active point than classical drilling, where the absence of a surgical guide allows for changes in inclination during osteotomy. Golin25 investigated the Ra of unused steel drills and of those used for 20 osteotomies through the conventional technique of implant surgery in bovine ribs. It was concluded that both 2- and 3-mm-diameter drills exhibited an increase in surface roughness. Sartori et al,26 using the same experimental model and conventional technique of implant insertion, investigated the Ra, Rz, and Rmax of steel drills after 10, 20, 30, and 40 osteotomies and observed no significant difference in surface roughness, regardless of the number of osteotomies performed. In this study, both techniques exhibited similar behavior, although a tendency toward increased roughness was observed for the GG technique for all roughness parameters. To avoid a negative influence on osseointegration, it is important for dental professionals to be aware of the importance of minimizing the factors that may contribute to bone heating during implant osteotomy. These include selection of the least traumatic surgery technique, increases in the volume of irrigation to ensure that irrigation reaches the drill/receptor bed
interface, and minimization of the force applied during drilling. Taking these measures is of particular importance when using a guided surgery protocol, as this technique generates more heat than classic drilling.
CONCLUSION Based on the methods adopted for the present study, it can be concluded that: 1. The guided surgery technique generated a higher bone temperature than the classic drilling technique during osteotomies for implant receptor bed preparation. The increase in tissue temperature was directly proportional to the number of times drills were used. However, neither technique generated the critical temperature that bone can tolerate without necrosis. 2. Drill deformation was directly proportional to the number of times drills were used in both groups. The tendency toward drill deformation was stronger in guided surgery, particularly in the 40th osteotomy. 3. The surface roughness of the drill was directly proportional to the number of uses for both osteotomy techniques, and the guided surgery technique tended to increase the surface roughness of the drills.
Acknowledgments The authors would like to thank Conexão Sistema de Prótese for their assistance and for supplying the implant drills used in this study. The authors reported no conflicts of interest related to this study.
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The International Journal of Oral & Maxillofacial Implants 57 © 2014 BY QUINTESSENCE PUBLISHING CO, INC. PRINTING OF THIS DOCUMENT IS RESTRICTED TO PERSONAL USE ONLY. NO PART MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM WITHOUT WRITTEN PERMISSION FROM THE PUBLISHER.
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16. Ellingsen JE, Johansson CB, Wennerberg A, Holmén A. Improved retention and bone-to-implant contact with fluoride-modified titanium implants. Int J Oral Maxillofac Implants 2004;19:659–666. 17. Margonar R, Sakakura CE, Holzhausen M, Pepato MT, Alba RC, Marcantonio E. The influence of diabetes mellitus and insulin therapy on biomechanical retention around dental implants: A study in rabbits. Implant Dent 2003;12(4):333–339. 18. Wiggins KL, Malkin S. Drilling of bone. J Biomech 1976;9:553–559. 19. dos Santos PL, Queiroz TP, Margonar R, et al. Guided implant surgery: What is the influence of this new technique on bone cell viability? J Oral Maxillofac Surg 2013;71(3):505–512. 20. Allsobrook OFL, Leichter J, Holborow D, Swain M. Descriptive study of the longevity of dental implant surgery drills. Clin Implant Dent Relat Res 2011;13(3):244–254. 21. Cordioli G, Majzoub Z. Heat generation during site preparation: An in vitro study. Int J Oral Maxillofac Implants 1997;12:186–193. 22. Chacon GE, Bower DL, Larsen PE, McGlumphy EA, Beck M. Heat production by 3 implant drill systems after repeated drilling and sterilization. J Oral Maxillofac Surg 2006;64:265–269. 23. Lavelle C, Wedgwood D. Effect of internal irrigation on frictional heat generated from bone drilling. J Oral Surg 1980;38(7):499–503. 24. Jochum RM, Reichart PA. Influence of multiple use of Timedurtitanium cannon drills: Thermal response and scanning electron microscopic findings. Clin Oral Implants Res 2000;11:139–143. 25. Golin AL. Análise do comportamento de ferramentas de cortes com diferentes revestimentos e seu efeito sobre a geração de calor no osso [thesis]. Paraná, Brazil: Pontifícia Universidade Católica do Paraná, 2005. 26. Sartori EM, Shinohara EH, Ponzoni D, Padovan LE, Valgas L, Golin AL. Evaluation of deformation, mass loss, and roughness of different metal burs after osteotomy for osseointegrated implants. J Oral Maxillofac Surg 2012;70(11):e608–621.
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