Microcomputed Tomographic Analysis of Bone Reaction at Insertion of Orthodontic Mini-implants in Sheep

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1 Microcomputed Tomographic Analysis of Bone Reaction at Insertion of Orthodontic Mini-implants in Sheep Alberto Rebaudi, MD, DDS 1 /Nicola Laffi, MD, DDS 2 /Stefano Benedicenti, DDS 3 / Francesca Angiero, MD 4 /George E. Romanos, DDS, DMD, PhD 5 Purpose: To evaluate the effects on bone of forced insertion of self-tapping orthodontic mini-implants and thus obtain biomechanical data to develop insertion protocols and optimize drills for implant site preparation. Materials and Methods: After implant site preparation, 39 orthodontic mini-implants (OMI), mm each, were inserted into the hard bone of sheep mandible; 24 were placed with a 1-mm bone drill and 15 were placed with a standard-diameter (1.2-mm) drill. Removal torque was measured immediately (group A) and 8 weeks after insertion (group B). Eight OMIs (group C) were removed from the mandible in block sections of appropriate size for microcomputed tomographic morphometric and morphologic analyses. Results: All OMIs were placed without complications, with mean insertion torque of (± 1.71) Ncm (test groups) and (± 1.41) (control groups) and were stable at reentry. Group A implants showed a reduction in removal torque of 5.66%, while in group B, removal torque was reduced by 43.25%. In the control groups (ie, OMIs placed with a 1.2-mm drill), removal torque immediately after placement was reduced by 5.64%, and 8 weeks after insertion, removal torque had declined by 18.2%. Microcomputed tomographic bone morphometric analysis for both test and control groups showed that bone-implant contact was lower than expected in cortical bone 8 weeks after insertion. Morphologic analysis revealed cavities in the cortical bone close to the surface and microcalli in soft bone. Cavities in the cortical bone may have been caused by bone trauma during insertion. Conclusions: The use of a narrow drill for site preparation increased orthodontic screw insertion torque, but it also damaged the bone and decreased removal torque. Standard histologic examination may clarify whether cavities in hard bone are actually signs of bone resorption that results from the activation of remodeling. (INT J ORAL MAXILLOFAC IMPLANTS 2011;26:XXX XXX) Key words: anchorage, bone, bone biomechanics, microcomputed tomography, mini-implants, orthodontic implants 1 Contract Professor, University of Genoa, Italy; Secretary, Biomaterials Clinical Research Association, Pescara, Italy; Private Practice, Genova, Italy. 2 Private Practice, Genoa, Italy. 3 Associate Professor, University of Genoa, Italy. 4 Contract Professor, University of Milan-Bicocca, Italy; Anatomia Patologica Ospedale S. Gerardo, Monza, Italy. 5 Professor of Clinical Dentistry, Eastman Institute for Oral Health, University of Rochester, Rochester, New York. Correspondence to: Dr Alberto Rebaudi, Piazza della Vittoria 8/12, Genova 16121, Italy. Fax: al.reb@tin.it For optimal results, dental implants should be inserted into bone of adequate quality and quantity. 1 5 Some studies 3,6 10 have stressed that the placement of implants in posterior zones of the jaws should be avoided based on the intrinsic mechanical properties of the bone in those areas. Specifically, soft bone (D4) is frequently not conducive to implant retention. Moreover, it has been reported that long-term success cannot be expected if the biomechanical parameters that regulate bone behavior at loading are not respected.4 Frost, who put forth a mechanostat theory describing the enhancement of bone density, stated that when the load exceeds a certain physiologic threshold in cortical bone, bone hypertrophy results, in turn causing an increase in modeling and a decrease in remodeling. According to Burr et al, 14,15 bone hypertrophy occurs upon the application of a load able to induce a deformation of 2,500 to 4,000 µε in the bone matrix, while deformations exceeding 4,000 µε activate bone microdamage, leading to fatigue failure. Animal studies and clinical and histologic case reports have shown that loading above a certain threshold induces bone loss, while other studies indicate that static loading may induce corticalization Roberts et al 16 observed a marked change in bone volume, shape, and mass following the application of a continuous load to endosseous implants. Different techniques have been developed over the years to evaluate the reaction of peri-implant bone The International Journal of Oral & Maxillofacial Implants 1

2 Fig 1 The mini-screw used in this study has a dual thread that enables it to pass through bone without oscillation. The self-tapping apex of the screw easily self-penetrates into the cancellous bone and also into cortical bone up to 2 mm thick. For compact bone that is more than 2 mm thick, the mini-implant requires a drill for implant site preparation. The head of the miniscrew incorporates orthodontic biomechanics (a ball attachment for elastic bands and springs and slot for rectangular arches). and its structure. Several three-dimensional (3D) procedures have been proposed to overcome some of the limitations of analyzing two-dimensional histologic sections; these include stereo- or scanning microscopy 13 and serial sectioning. 14 These methods enable bone connectivity to be measured and are proposed as alternative approaches to outline and quantify bone in three dimensions. 12,15 These methods make it possible to evaluate and measure both the cancellous and the compact components of bone biopsy specimens, enabling 3D evaluation of bone biomechanics and of hard tissue healing after implant placement. The orthodontic miniscrew implant (OMI), also described as orthodontic screw, microscrew, orthodontic implant, orthodontic mini-implant, or orthodontic microimplant, is a temporary anchorage device that is inserted into the bone of the oral cavity. It is generally loaded immediately, with the goal of obtaining anchorage for orthodontic therapy The OMI is an easy, inexpensive, predictable, effective, and well-tolerated means of providing anchorage 27 with excellent patient compliance. 28 Although retreatment may sometimes be required, studies have shown that OMIs are easily replaced when lost. 29 Successful use of OMIs seems to be fairly comparable in the mandible and the maxilla, with little effect according to the orthodontic forces applied or the time of activation of the load. Primary stability, 30 bone quality, 31,32 placement site, time in function, 33 and learning curve 27 are reported to be important factors determining the success rate of OMIs. OMIs should remain stable for the entire time required for orthodontic therapy, but a percentage of them may fail. 27,29,32,34,35 The subsequent loss of immediately loaded dental implants and the loss of OMIs appear to result from micromovements at the implant site, which may be caused by the application in soft bone of a load exceeding the threshold of bone resistance. 32,34,36 Displacement of 0.0 to 1.6 mm of otherwise functional OMIs as a result of orthodontic traction has also been described. 36 Therefore, the present in vivo study aimed to evaluate the effects on bone of forced insertion of a self-tapping OMI (Miki Screw, Ti+Bone) to obtain biomechanical data that would be useful in developing insertion protocols and optimizing drills for implant site preparation. MATERIALS AND METHODS Twenty-four Miki-Screws (Fig 1) in three test groups of eight animals each (groups A, B and C) and 15 Miki- Screws in three control groups of five animals each (groups a, b, c) were inserted into sheep mandibles with a cortical bone layer at least 4 mm thick. The Miki- Screw is 1.6 mm in diameter. Its threaded intraosseous portion is 7.5 mm in length, and it is made of grade 5 titanium alloy (Ti-6Al-4V) with a machined surface. To prevent excessive insertion torque, site preparation with a drill is needed prior to Miki-Screw insertion when the cortical bone layer is very hard or thick. The manufacturer recommends using a 1.2-mm-diameter drill and passing it through the cortical bone layer before insertion of the Miki-Screw. In this study, after fullthickness flap elevation, a narrower drill (1 mm) was used for implant site preparation for the test groups, and the manufacturer-recommended 1.2-mm drill was used for the control groups; both were run at 700 rpm under irrigation with cooled physiologic solution. The purpose of the different drills was to determine the effects of bone stress at forced implant insertion and to verify whether narrower preparation would improve the stability of the Miki-Screws. Insertion was performed with a screwdriver with dynamometric control, since Miki-Screws cannot withstand more than 20 Ncm of torque. The experiment was carried out with the approval of the ethical committee for animal care within the project entitled Evaluation of implants with different surfaces in native bone (DL , Office of Veterinary Services ). Miki-Screws generally heal unsubmerged, but in this case, they healed in a submerged fashion, since the thickness of soft tissue in the sheep covered the implant heads. Eight Miki-Screws (group A) were immediately unscrewed after insertion, and removal torque was measured. The remaining 16 OMIs were left to heal in living bone for 8 weeks, after which eight were unscrewed and the removal torque was measured (group B). The remaining eight OMIs were harvested from the mandible in block sections of appropriate size for microcomputed tomographic (microct) morphologic and histomorphometric analysis (group C). In the control groups (a, b, and c), procedures were identical to that of the test groups (A, B, and C), except that five Miki-Screws were used in each group. 2 Volume 26, Number 6, 2011

3 Fig 2 Two-dimensional microct scan showing a typical situation at the neck of the test implant (white). Signs of remodeling leading to the formation of pores around the coronal part of the screw involving a layer of bone 1 mm thick are evident. These pores may fuse together, reducing BIC, and they might also reduce the mechanical properties of the bone (grey) (magnification 8). Fig 3 Three-dimensional microct of one miniscrew tested showing BIC. In the coronal part, where the bone is dense, some cavities are visible in the neighborhood of the implant. In the endosseous portion, the intermediate part of the orthodontic implant is poorly osseointegrated because it is made of smooth titanium that has no osteoconductive properties. At the apex, the implant appears to be in contact with bone trabeculae (magnification 8). Red = bone contact; green = no bone contact. Fig 4 Two-dimensional microct. Evaluation of BIC on one of the implants that was forcefully inserted without site preparation. Points of contact with mineralized bone (light blue) are shown in red, while points without contact are outlined in green (magnification 8). Statistical Analysis Statistical analyses were performed using the SPSS statistical package, version 12.0 for Windows (SPSS Inc). One-way analyses of variance for repeated measures with the Scheffé post hoc tests were used to test for statistical differences in removal torque between groups A and B (test) and between groups a and b (controls). The data are summarized as the mean ± standard deviation (SD) or given as percentages, depending on the variable. A P value (two-sided) of.05 or less was considered indicative of a statistically significant difference. MicroCT Sample Preparation and Analyses All biopsies were fixed in 10% neutral buffered formalin and sent to the hard tissue laboratory of BioCRA (Biomaterials Clinical-Histological Research Association). The specimens were processed for histology, dehydrated in an ascending series of alcohol rinses, and then embedded in methacrylate resin. After polymerization, the specimens were scanned with a highresolution microct system (µct-40, Scanco Medical) in multislice mode. Each 3D image dataset consisted of approximately 500 microct slice images (1,024 1,024 pixels with 16-bit grey levels). The specimens were scanned in high resolution with an x-, y-, z-axis resolution of approximately 20 µ m. The voxel size was µm 3. Scanning time for each specimen was approximately 12 hours. Morphologic analysis was by accurate observation of the two-dimensional sections (Fig 2) and the 3D reconstructions (Fig 3). The morphometric analysis enabled calculation of actual bone-to-implant contact (BIC), expected bone-to-implant contact (EBC), bone volume (BV), and standard morphometric indices. BIC is a histologic concept that is traditionally evaluated by calculating the amount of the implant surface that is directly attached to mineralized bone without the interposition of soft connective tissue. BIC was calculated by microct (automatic measurement of bone density) (Fig 4). EBC is a virtual value; it was calculated by superimposing the implant thread profile over the bone image at various distances from the actual implant site (1.0, 1.25, or 1.5 mm) (Fig 5) and then counting the amount of bone that would be in contact with the implant surface, as described by Trisi et al. 31 The International Journal of Oral & Maxillofacial Implants 3

4 A 1 mm Fig 5 Two-dimensional microct. This figure shows the techniques used to measure BIC and EBC. Points of contact with the mineralized bone are shown in red, while points without contact are outlined in green. EBC was calculated by superimposing the profile of the implant threads on the bone image at small increments from the actual implant site (1.0, 1.25, or 1.5 mm) and counting the amount of bone that should be in contact with the implant surface (magnification 8). A = BIC (no increment); B = EBC (1.0-mm increment); C = EBC (1.5-mm increment). B C Table 1 Comparison of Insertion Torque (IT) and Removal Torque (RT) in Group A OMI no. IT (Ncm) RT (Ncm) IT RT (Ncm and %) (5.26) (6.25) (5.88) (6.25) (5.55) (0) (11.11) (5) Mean (5.66) SD Table 2 Comparison of IT and RT in Group B OMI no. IT (Ncm) RT (Ncm) IT RT (Ncm and %) (50) (37.5) (43.75) (42.10) (47.06) (42.10) (31.25) (53.33) Mean (43.25) SD RESULTS Implant site preparation was achieved without complications. All implants were successfully inserted in the dense cortical bone of the sheep mandible, with a mean insertion torque of 18 Ncm (Table 1). Removal Torque Findings The immediate removal torque in group A implants was also very high (17 Ncm) and about 6% lower than insertion torque (Table 1). All implants of groups B and C were found to be stable upon reopening. After 8 weeks, the mean removal torque of group B was 9 Ncm, which was 43% lower than the insertion torque (Table 2). The results of the control groups are summarized in Tables 3 and 4. No implants fractured upon insertion or removal. One-way analysis of variance for repeated measurements with Scheffé post hoc test showed that there is a significant overall difference (P <.0001) between the mean change in torque (insertion torque minus reverse torque) of group A versus the mean change in torque of group B (Fig 6). MicroCT Results MicroCT morphologic analysis of the group C biopsy specimens revealed several large cavities of about 200 to 300 µm in diameter within the dense structure of the cortical bone. These cavities were observed in all specimens and were visible only in the neighborhood of the OMIs, involving a layer of bone about 1 mm thick. The cavities appeared to have markedly reduced bone density in the neighborhood of each miniscrew. 4 Volume 26, Number 6, 2011

5 Table 3 Comparison of IT and RT in Group a (Control) OMI no. IT (Ncm) RT (Ncm) IT RT (Ncm and %) (5.55) (5.88) (5.26) (6.25) (5.26) Mean (5.64) SD Table 4 Comparison of IT and RT in Group b (Control) OMI no. IT (Ncm) RT (Ncm) IT RT (Ncm and %) (16.67) (12.50) (15.79) (25.00) (21.05) Mean (18.202) SD Mean IT RT A a B b Group Fig 6 Comparison of mean changes in torque (IT RT). There was a significant overall difference (P <.0001) between the mean change seen for group A and that seen for group B. Error bars indicate 95% confidence intervals. Table 5 BIC and EBC in Cortical and Cancellous Bone in the Test Group (1.0-mm Drill) and Control Group (1.2-mm Drill) Group Test group BIC in cortical bone (%) EBC in cortical bone (%) BIC in cancellous bone (%) EBC in cancellous bone (%) Mean SD Control Mean SD Fig 7 (left) Three-dimensional microct of an implant. Note the formation of woven bone around the apex of the implant. Fig 8 (right) Three-dimensional microct. With the image subtraction technique, a detail of the previous figure becomes clear: a microcallus has formed around the apex of this implant. In some cases, the cavities were so close to one another that larger cavities were formed. In some of the sections, large cavities seemed to cause a net loss of bone contact, especially evident in the coronal part of the screw (Fig 7). The actual BIC with cortical bone was thus much lower than the EBC (Table 5). Group c showed only a slight difference between BIC and EBC. On the microct slides, it was shown in all cases that the threaded part of the Miki-Screw (7.5 mm) exceeded the thickness of the cortical bone layer of the sheep mandible and penetrated into the underlying low-density cancellous bone (Fig 8), histologically classified as soft D4 bone via microct morphologic and morphometric analysis. In many cases, the morphologic analysis revealed formation of considerable woven bone around the implant apex, organized in a globular structure, resembling that of a microcallus (Fig 9). However, in spite of the newly formed woven bone (microcalli) at the implant apex, BIC was not higher than the EBC in the cancellous bone. [AU: There is no Figure 9 with your manuscript, but Fig 9 is cited. Please clarify.] The International Journal of Oral & Maxillofacial Implants 5

6 DISCUSSION All implants were found to be stable at reopening, 2 months after undisturbed healing. This finding agrees with studies that have shown excellent stability of OMIs several months after placement and success rates ranging from 80% to 100%. 33,35 The present study found mean removal torque values that were 43.25% below insertion torque values at 8 weeks after implant insertion. This is in agreement with the study of Okazaki et al, 30 who evaluated the effect of primary stability in the healing phase after insertion of mini-implants 1.2 mm in diameter in 1.0- and 1.2-mm cavities prepared in the femurs of beagle dogs. The authors measured implant stability by evaluating removal torque values. Implants inserted in 1.0-mm cavities displayed a steady decrease in removal torque over the first 6 weeks, with average values of Ncm immediately, 8.83 Ncm at 1 week, 7.20 Ncm at 3 weeks, and 5.12 Ncm at 6 weeks postinsertion. This translates into average torque losses of 19.58% at 1 week, 34.43% at 3 weeks, and 53.37% at 6 weeks. Thus, removal torque values of mini-implants placed in 1.2-mm cavities were 11-fold lower than those placed in the 1.00-mm cavities, which demonstrated a significant increase in strength from 3 weeks (1.35 Ncm) to 6 weeks (5.17 Ncm) postinsertion (P <.01). Measurements performed 6, 9, and 12 weeks postinsertion were similar to those in the 1.0-mm cavity. Based on this line of evidence, Okazaki et al30 concluded that primary stability of OMIs is necessary and that an unstable implant should be replaced or isolated to await better stability. The decrease in removal torque values observed in the present study may have been caused by the activation of a biologic response to the effects of bone damage at implant insertion. Such bone damage at OMI insertion was recently described by Wawrzinek et al 37 in a study that investigated microstructural alterations in cortical bone by overtightening of orthodontic miniscrews during the insertion procedure in fresh pelvic porcine bone segments. Employing electron microscopy techniques, the group observed several cracks in the peri-implant bone and concluded that bone microdamage may diminish the stability of immediately loaded OMIs because of the biologic activation of bone remodeling initiated by microdamage. In contrast with the activation of bone resorption caused by bone remodeling, another mechanical hypothesis might explain the reduction in removal torque values, namely, that bone is a viscoelastic material that, if loaded above the threshold of resistance, may suffer relaxation, which then produces a loss of mechanical resistance. 37 However, this latter hypothesis would appear insufficient to explain such a marked loss in removal torque values. Perhaps bone relaxation alone may not account completely the loss but it may work in conjunction with activation of bone remodeling in reducing the removal torque values. Indeed, in agreement with the studies by Okazaki et al 30 and Wawrzinek et al, 37 the in vivo loss of removal torque values observed in the present study is apparently a result of the biologic bone remodeling process leading to bone resorption initiated by microdamage. This hypothesis appears more likely for the present study, since cavities were observed in the cortical bone around the implants and may have therefore caused a reduction in BIC. No signs of cracks were evident on microct scans in the peri-implant bone 8 weeks after OMI placement, possibly because the repair process through active remodeling may have hidden any signs of bone damage. To fully demonstrate an active peri-implant bone resorption process, which could confirm this important hypothesis, standard histologic preparation would be preferable. Specifically, ground sections for histologic examination, compared to microct, provide better resolution and allow bone cells to be observed, as well as the resorption activity and bone formation to be detected. The results of the present study suggest that forced insertion of OMIs into hard bone may result in reduced stability after 8 weeks. For this reason, further studies are required to verify whether this remodeling/resorption process stops or continues for a longer period of time. Another point to be clarified is the effect of the surface treatment on the healing of OMIs. The surface of the Miki-Screw is machined to a smooth texture and thus lacks the high osteoconductivity required to facilitate implant removal. In general, osseointegration of osteoconductive surfaces of standard implants significantly enhances BIC and improves performance and survival after the first 8 weeks, 38,39 but OMIs may differ in performance since the applied load distribution at implant insertion is different. OMIs are very thin, and the insertion torque is relatively high; it may therefore be expected that the load applied to the peri-implant bone is heavy. This hypothesis is confirmed by a recent study by Chaddad et al, 40 who found that the insertion torque statistically influenced the survival rate of OMIs, whereas surface treatment did not. Although the removal torque values of OMIs in the present study decreased significantly during the first 8 weeks after placement, the final mean removal torque measurements, at around 10 Ncm, were still high and implant stability was more than adequate for the clinical use of mini-implants (ie, orthodontic anchorage). This is in agreement with several studies showing high survival and success rates for OMIs in clinical use; thus the problem of initial loss of stability is not considered to be a determinant of failure. Further studies are needed to investigate the behavior of OMIs after longer observation periods. 6 Volume 26, Number 6, 2011

7 In the trabecular bone around the apex of most of the Miki-Screws analyzed, the morphologic microct analysis also revealed globular structures of woven bone that resembled microcalluses. These have been described in the orthopedic 41,42 and dental literature32 as organized structures surrounding fragments of bone trabeculae. Microcalluses are able to repair and stabilize bone and have also been observed in cancellous bone in close proximity to dental implants subjected to orthodontic loads. 32 Formation of microcalluses is the physiologic expression of a bone repair process, and during this phase, entire new trabeculae, which are a prerequisite for reconstruction of rarefied bone structure, can form. Although the formation of microcalluses indicates instability of the bone structure, the microcalluses also stabilize and regenerate the bone structure. The nature of these microcalluses is still the subject of discussion in the orthopedic field, and various hypotheses have been formulated. They may play a role in hip fracture, bone remodeling, and prosthesis loosening. It appears noteworthy that bone repair was activated via two different mechanisms in compact and cancellous bone. Generally, mini-implants are immediately loaded in clinical practice. However, in the present study, experiments were carried out on healed, unloaded miniimplants. Therefore, since implant loading may affect bone adaptation, healing, and remodeling, 16,22,23,32,34 the results of the present study may differ from studies reporting on functionally loaded implants. Also, the present study was carried out in dense cortical bone of about 4 mm in thickness. Thus, the results may differ from studies based on clinical specimens, where cortical bone rarely exceeds 1 mm in the maxilla and 3 mm in the mandible. 43,44 CONCLUSIONS This study detected signs compatible with remodeling activity and bone relaxation in bone subjected to forced insertion of orthodontic mini-implants. Remodeling may cause resorption of cortical bone and formation of new woven bone in cancellous bone. The resorption process is undesirable because the smooth surface of the mini-implant examined here is not osteoconductive. As a consequence, bone contact lost at the end of the entire remodeling process will probably not be regained. Forced insertion of orthodontic mini-implants in cancellous bone, in contrast, seems to stimulate woven bone formation, but the newly formed bone is apparently unable to enhance boneimplant contact, since orthodontic mini-implants have a smooth surface. Therefore, the results of the study suggest that further histologic studies are needed to confirm activation of bone remodeling and that in vitro and in vivo biomechanical studies are needed to better calibrate the ideal diameter of the tools used to prepare orthodontic implant sites. Meanwhile, it can be affirmed that a larger diameter of drill for implant site preparation may reduce compression and damage of cortical bone, probably without affecting the primary stability of the orthodontic mini-implant. REFERENCES 1. Adell R, Lekholm U, Rockler B, Brånemark P-l. A 15-year study of osseointegrated implants in the treatment of the edentulous jaw. Int J Oral Surg 1981;10: Adell R, Eriksson B, Lekholm U, Brånemark P-I, Jemt, T. Long-term follow-up study of osseointegrated implants in the treatment of totally edentulous jaws. Int J Oral Maxillofac Implants 1990;3: Jemt T, Lekholm U, Adell R. 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8 22. Gotfredsen K, Berglundh T, Lindhe J. Bone reactions adjacent to titanium implants subjected to static load. A study in the dog (I). Clin Oral Implants Res 2001;12: Melsen B, Lang NP. Biological reactions of alveolar bone to orthodontic loading of oral implants. Clin Oral Implants Res 2001;12: Lebus S. Application of orthodontic mini-implants. J Prosthodont 2008;17(7):601. [AU: Is this an abstract or a 1-page article? If not, please provide ending page number of article.] 25. Fletcher JL. Using mini-screws for orthodontic anchorage. Int J Orthod Milwaukee 2008;19(3): Serra G, Morais LS, Elias CN, et al. Sequential bone healing of immediately loaded mini-implants. Am J Orthod Dentofacial Orthop 2008;134(1): Garfinkle JS, Cunningham LL Jr, Beeman CS, Kluemper GT, Hicks EP, Kim MO. Evaluation of orthodontic mini-implant anchorage in premolar extraction therapy in adolescents. Am J Orthod Dentofacial Orthop 2008;133(5): Hoste S, Vercruyssen M, Quirynen M, Willems G. Risk factors and indications of orthodontic temporary anchorage devices: A literature review. Aust Orthod J 2008;24(2): Justens E, De Bruyn H. Clinical outcome of mini-screws used as orthodontic anchorage. Clin Implant Dent Relat Res 2008;10(3): Okazaki J, Komasa Y, Sakai D, et al. A torque removal study on the primary stability of orthodontic titanium screw mini-implants in the cortical bone of dog femurs. Int J Oral Maxillofac Surg 2008;37(7): Trisi P, Lazzara R, Rao W, Rebaudi A. Bone-implant contact and bone quality: Evaluation of expected and actual bone contact on machined and Osseotite implant surfaces. Int J Periodontics Restorative Dent 2002;22(6): Trisi P, Rebaudi A. Peri-implant bone reaction to immediate, early, and delayed orthodontic loading in humans. Int J Periodontics Restorative Dent 2005 Aug;25(4): Moon CH, Lee DG, Lee HS, Im JS, Baek SH. Factors associated with the success rate of orthodontic miniscrews placed in the upper and lower posterior buccal region. Angle Orthod 2008;78(1): Trisi P, Rebaudi A. Progressive bone adaptation of titanium implants during and after orthodontic load in humans. Int J Periodontics Restorative Dent 2002;22(1): Janssen KI, Raghoebar GM, Vissink A, Sandham A. Skeletal anchorage in orthodontics A review of various systems in animal and human studies. Int J Oral Maxillofac Implants 2008;23(1): Wang YC, Liou EJ. Comparison of the loading behavior of selfdrilling and predrilled miniscrews throughout orthodontic loading. Am J Orthod Dentofacial Orthop 2008;133(1): Wawrzinek C, Sommer T, Fischer-Brandies H. Microdamage in cortical bone due to the overtightening of orthodontic microscrews. J Orofac Orthop 2008;69(2): Trisi P, Rao W, Rebaudi A. A histometric comparison of smooth and rough titanium implants in human low-density jawbone. Int J Oral Maxillofac Implants 1999;14(5): Trisi P, Lazzara R, Rebaudi A, Rao W, Testori T, Porter SS. Boneimplant contact on machined and dual acid-etched surfaces after 2 months of healing in the human maxilla. J Periodontol 2003;74(7): Chaddad K, Ferreira AF, Geurs N, Reddy MS. Influence of surface characteristics on survival rates of mini-implants. Angle Orthod 2008;78(1): Mosekilde L. The effect of modelling and remodelling on human vertebral body architecture. Technol Health Care 1998;6: Mosekilde L. Consequences of remodelling process for vertebral trabecular bone structure: A scanning electron microscopy study (uncoupling of unloaded structures). Bone Miner 1990;10: Fernandes AC, Rossi MA, Schaffner IS, Machado LA, Sampaio AA. Lateral cortical bone thickness of human mandibles in region of mental foramen. J Oral Maxillofac Surg 2010 Dec;68(12): Abrahams JJ. Anatomy of the jaw revisited with a dental CT software program. AJNR Am J Neuroradiol 1993 Jul Aug;14(4): Volume 26, Number 6, 2011