Survey
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
SCIENTIFIC ARTICLE Australian Dental Journal 2007;52:(4):282-287 Effects of pulsed electromagnetic field vibration on tooth movement induced by magnetic and mechanical forces: a preliminary study M Ali Darendeliler,* A Zea,† G Shen,‡ H Zoellner§ Abstract Background: This study was designed to determine whether or not high-frequency and low-magnitude vibration affects orthodontic tooth movement caused by magnetic or/and mechanical forces. Methods: Forty-four 7-week-old Wistar rats were randomly divided into four groups, with each group further divided into experimental and control subgroups. Neodymium-Iron-Boron (Nd-Fe-B) magnets and Sentalloy closed coil springs were placed between maxillary or mandibular first molars and incisors to activate tooth movement. The animals of experimental subgroups were exposed to the vibration induced by pulsed electromagnetic fields (PEMF) whilst the control subgroups were under normal atmosphere. The experiment lasted for 14 days and all of the animals were sacrificed for examination. The changes in the space between the molar and incisor were measured to indicate the amount of tooth movement. Results: The coil springs, either with sham or active magnets, move molar much more than magnets alone, regardless of absence or presence of PEMF (p<0.001). Under PEMF, the coil spring moved significantly more amount of tooth movement than that of coil–magnet combination (p<0.01), as did the magnets compared to sham magnets (p<0.019). Under a non-PEMF scenario, there was no significant difference in tooth movement between coil spring and coil–magnets combination, nor was there difference between magnets and sham magnets. Conclusions: It is suggested that the PEMF-induced vibration may enhance the effect of mechanical and magnetic forces on tooth movement. Key words: Tooth movement, Nd-Fe-B magnet, PEMF vibration. *Professor and Chair, Department of Orthodontics, Faculty of Dentistry, The University of Sydney, New South Wales. †Postgraduate student, Department of Orthodontics, Faculty of Dentistry, The University of Sydney, New South Wales. ‡Associate Professor, Department of Orthodontics, Faculty of Dentistry, The University of Sydney, New South Wales. §Associate Professor, Department of Oral Pathology and Oral Medicine, Faculty of Dentistry, Sydney Dental Hospital, The University of Sydney, New South Wales. 282 Abbreviations and acronyms: ME = method analysis; Nd-Fe-B = Neodymium-Iron-Boron; PEMF = pulsed electromagnetic field. (Accepted for publication 21 February 2007.) INTRODUCTION It has been shown that applied electrical fields can alter the normal electrical states of bone and cartilage, induce increased rates of cellular division and metabolism, and thus promote increased healing of bony and cartilaginous defects.1,2 Bassett3 proposed that tissue integrity and function could be restored by applying electrical and/or mechanical energy to the area of injury. Electrical currents were applied to nonhealing fractures in animal studies4,5 and in clinical trials6,7 and successfully helped the healing process. It appears that electrical energy, whether applied as a direct current or a pulsed electromagnetic field (PEMF), has the ability to affect both the depository and resorptive activities of bone and cartilage cells.8-10 It is believed that orthodontic tooth movement is accompanied by site-specific bone remodelling with inflammatory nature.11 Alveolar bone remodelling is essential for tooth movement and is characterized by tandem periods of osteoclastic recruitment, bone resorption, reversal and bone formation.12 This process involves the periodontal ligament and is dependent on the magnitude and consistency of the force being applied. In the area of periodontal ligament compression, osteoclasts proliferate and initial resorption of superficial bone occurs.13,14 In the region of periodontal ligament tension, the periodontal fibres unwind, fibroblasts appear and osteoblasts form a non-mineralized collagenous matrix called osteoid. The osteoid is later mineralized, trapping some osteocytes in lacunae within the bone. Previous animal and clinical studies have shown that mechanical stimulation, in particular low intensity pulsed ultrasound, improves the rate of bone healing via up-regulation of cartilage formation and maturation of endochondral bone formation.15,16 Australian Dental Journal 2007;52:4. Table 1. Experimental design and animal grouping Experimental subgroups (with PEMF vibration) Group Group Group Group 1 2 3 4 (n=20) (n=8) (n=8) (n=8) Control subgroups (without PEMF vibration) Left side Right side Left side Right side Sham magnet Magnet Sham magnet Coil+sham magnet Magnet Coil+magnet Coil+sham magnet Coil+magnet Sham magnet Magnet Sham magnet Coil+sham magnet Magnet Coil+magnet Coil+sham magnet Coil+magnet In addition, the results of earlier studies show that high-frequency (30Hz), low-magnitude vibrations induce increased anabolic activity in bone.17 Since it has been hypothesized that there is an increase in metabolic activity of bone, it is reasonable to assume that there should be an increase in the rate of orthodontic tooth movement under the influence of mechanical vibration. Therefore, the primary aim of this study was to determine whether or not high-frequency and lowmagnitude mechanical vibration affects orthodontic tooth movement when it is integrated with magnetic and/or elastic forces. MATERIALS AND METHODS Experimental design Forty-four 7-week-old Wistar strain rats weighing 210–250 g were used (ethics approval: Westmead Hospital Animal Ethics Committee protocol no. 141.04-04). The animals were randomly divided into four groups, with each group further divided into the experimental and control subgroups (Table 1). Group 1 (n=20): Demagnetized sham magnets were bonded onto the mesial aspect of the maxillary or mandibular left first molars and the distal aspect of the incisors. Neodymium-Iron-Boron (Nd-Fe-B) magnets were bonded on the contralateral side (Fig 1). Half of the animals (n=10) were designated as experimental subgroup (Group 1P) which were exposed to PEMF vibration in a Helmholtz configuration eight hours a day.18 Another half of the animals were the control subgroup (Group 1C) which were not exposed to the vibration. Magnets and sham magnets were bonded on the maxillary first molars of six rats of Group 1P and Group 1C. Subsequently, it was found that the coil springs were more securely attached to the mandibular teeth than maxillary teeth due to the concavity of the maxillary teeth. Therefore, magnets and coil springs were attached between the first molar and the incisors of the mandible for the remaining sample groups. Group 2 (n=8): Nd-Fe-B magnets were bonded on the mesial aspect of the left first molars and the distal aspect of the incisors, and the 25 g Sentalloy closed coil springs (GAC Cat No:10-000-26) plus Nd-Fe-B magnets were placed on the contralateral side. Half of the animals (n=4) were exposed to PEMF eight hours a day (Group 2P) and the other half of the animals were not (Group 2C). Group 3 (n=8): Demagnetized sham magnets were bonded between left first molars and incisors, and the Australian Dental Journal 2007;52:4. 25 g Sentalloy closed coil springs plus permanently demagnetized sham magnets were placed on the contralateral side. Half of the group (n=4) were exposed to PEMF eight hours a day (Group 3P) and the other half (n=4) were not (Group 3C). Group 4 (n=8): 25 g Sentalloy closed coil springs with demagnetized sham magnets were placed between the molars and the incisors, and 25 g Sentalloy closed coil springs with Nd-Fe-B magnets were placed on the contralateral side. Half of the group (n=4) were exposed to PEMF eight hours a day (Group 4P) and the other half (n=4) were not (Group 4C). The rats were administered an appropriate amount of anaesthetic agent: Xylazine (10 mg/kg) and Ketamine (90 mg/kg). Polyvinyl siloxane hydrophilic impressions of the rat’s dentition were taken as records (3M Imprint II Garant Quick Step Regular Body Cat No. 9579). Then Nd-Fe-B magnets (1 mm length x 1 mm width x 0.5 mm thickness) were bonded onto the mesial surface of the rat upper first molars in relevant groups with 3M Transbond light cure composite resin (Ref No. 712036) and 3M Transbond Moisture Insensitive Primer (Ref No. 712-025). The Nd-Fe-B Fig 1. Ne-Fe-B magnets and permanently demagnetized sham magnets bonded on mesial surface of the maxillary first molars in a Wistar rat. 283 above via the standard analogue sound output channel. Field strength was controlled via the amplifier power output. Throughout this experiment, the PEMF generated high-frequency and low-magnitude vibration featuring 30Hz pulses, a positive duration (T) of 200 microseconds, a magnetic field (B) of 1.8 mT and a positive rate (dB/dT) of 9 tesla/second. The magnetic field intensity was controlled via the amplifier power output to provide two Gauss as measured using Holaday ELF Magnetic Field Meter (Holaday Industries Inc., USA). Fig 2. PEMF coils surrounding circular lexan cage produces high-frequency and low-magnitude vibration. magnets produced energy of 190 kilojoules/m3 with attractive force at 1 mm of 0.5 mT (Tesla). Permanently demagnetized sham magnets of the same dimension were bonded onto maxillary molars on the contralateral side. The magnetization of the magnet was in mesiodistal direction. Sentalloy closed coil springs of 25 g (GAC Cat No:10-000-26) were used to move the mandibular molars forward, decreasing the length of the interdental space between the first molar and the incisor. The orthodontic tooth movement model was adapted from Kobayashi et al.19 and Brudvik and Rygh.20 In appropriate groups, Nd-Fe-B magnets and permanently demagnetized sham magnets were bonded onto 25 g Sentalloy closed coil springs before ligating onto the first mandibular molars. After ligation with 3.0 silk suture, composite resin was used to bond magnets and sham magnets onto the mesial surface of first molars to ensure contact with tooth structure. The springs were then fixed anteriorly using ligature wire loops placed around the incisal thirds of both lower incisors. Composite resin was placed over ligature wire ends to prevent mucosal trauma. Following recovery, the rats were housed in circular lexan cages. Generation of pulsed electromagnetic field (PEMF) The electromagnetic field generating coils of internal diameter of 40 cm which were placed above and below the cage in the PEMF groups were arranged parallel to each other with a separation of 20 cm (Fig 2). This design, known as a Helmholtz configuration, produced an even magnetic field in the space between the coils. The principle of apparatus setup was based on the proposal by Darendeliler et al.18 The field coil was driven by a linear amplifier with a variable power output of up to 800 Watts RMS (Panasonic Pty. Ltd.). Field parameters including frequency and growth/decay character can be precisely controlled via a computer interface. This waveform generator comprised a MacIntosh computer, hosting a software signal generator (Mac the Scope, Channel D Corporation, Trenton NJ) with the output being passed to the amplifier described 284 Examination of tooth movement The rats were sacrificed on day 14 by carbon dioxide asphyxiation. Polyvinyl siloxane impressions of rat dentition were taken as post-treatment records. Casts of before and after treatment were prepared in plaster from the impressions. Measurements were taken with digital millimetre callipers (Orthopli Electronic Digital Callipers Model 50001, USA) to determine the distance between the midpoint of the incisors to the most mesial cervical point of the first molar (interdental space). The data were analysed with the univariate analysis of variance and estimated marginal means, using Statistical Package for Social Sciences program (SPSS for Windows, version 12 SPSS Inc., Chicago, USA). Each measurement was recorded three times on different days to reduce error. Method error (ME) analysis was calculated by the formula: where d is the difference between the two registrations of a pair and n is the number of double registrations. Paired t tests were performed to compare the two registrations. There was no significant difference among the separate registrations. RESULTS Univariate analysis of variance was conducted to identify the differences in amount of tooth movement (changes in interdental spaces) between PEMF, magnets, coil spring and coil spring combined with magnets (Table 2). It was found that the effect of coil spring alone, i.e., with sham magnet (Group 4, p=0.000) was more prominent than when coil springs were used in combination with Nd-Fe-B magnets (Group 2, p=0.014). The effect of magnets (Group 1, Table 2. Univariate analysis of variance testing the effects of different modalities on tooth movement (dependent variable: tooth movement) Sources Intercept Effect of PEMF Inter-rat differences Effect of coil Effect of magnet Coil–magnet interaction Significance (P) 0.000 0.577 0.002 0.000 0.097 0.014 Australian Dental Journal 2007;52:4. Table 3. Univariate analysis of variance testing the effects of different modalities on tooth movement with presence and absence of PEMF (dependent variable: tooth movement) Sources With PEMF Without PEMF Significance (P) Significance (P) 0.003 0.000 0.019 0.004 0.001 0.002 0.001 0.408 0.050 0.884 Intercept Effect of coil Effect of magnet Inter-rat effect Coil–magnet interaction p=0.097), on the other hand, was less prominent than combination of coil spring and magnets (Group 2, p=0.014), indicating that magnets would have increased effect on molar tooth movement in the presence of coil spring. It was also found that the amount of tooth movement under the influence of PEMF vibration (experimental subgroups) was not significantly different from that without PEMF (control subgroups) (p=0.577). The amount of tooth movement between different animals with rat as a variable was statistically significant (p=0.002). To further examine the effects of PEMF vibration on molar tooth movement under different force modalities, i.e., coil spring, magnet and combined coil spring and magnet, the univariate analysis of variance for the presence and absence of PEMF was conducted (Table 3). It was found that the effect of combined coil spring and magnets under PEMF vibration was more significant (p=0.001) than that without PEMF (p=0.884). The effects of magnets only (p=0.019) and coil spring only (p=0.000) under PEMF vibration were also greater than those without PEMF (magnets p=0.408, coils spring p=0.001). These data suggested that the effect of magnets on tooth movement increased when magnets were integrated with PEMF vibration. To have a comprehensive and overall evaluation of the differences in tooth movement between different force modalities (magnetic, mechanic and combined forces) under different scenarios (with and without PEMF), a statistical plot analysis was conducted (Fig 3). This plot revealed the following: (1) The coil springs, either with sham or active magnets, move molar much more than magnets alone, regardless of the absence or presence of PEMF (p<0.001); (2) Under PEMF, the coil spring moved significantly more amount of tooth movement than that of coil–magnet combination (p<0.01), as did the magnets compared to sham magnets (p<0.019); (3) Under a non-PEMF scenario, there was no significant difference in tooth movement between coil spring and coil–magnets combination, nor was there any difference between magnets and sham magnets. DISCUSSION This study was designed in such a way that the NdFe-B magnet bonded onto the molar tooth of the rat Australian Dental Journal 2007;52:4. Fig 3. Statistical plot depicting the overall effects of Ne-Fe-B magnets. Sentalloy coil springs and their interaction in the absence and presence of PEMF. PCM stands for the following possible combinations of the factors: … = Sham; ..m = magnet; .c. = coil; .cm = coil plus magnet; p.. = PEMF; p.m = PEMF plus magnet; pc. = PEMF plus coil; pcm = PEMF plus coil and magnet. would interact with the PEMF, resulting in mesiodistal vibratory stimulus to that molar. The direction of PEMF will affect the direction of pulsating movement of the magnet. The direction of vibration in relation to the PEMF may have been changed, depending on the orientation of the head. However, the variation in PEMF direction would not cause significant bias as the chance of being subject to this variation was even between the animals. It was shown that Nd-Fe-B magnets bonded onto rat molars in the presence of PEMF vibration (Group 1P) resulted in a more decreased interdental space than that in sham magnet group (Group 1C) and this was statistically significant (p=0.019) (Fig 3). This difference in interdental space could be partly due to growth in craniofacial complex of the animal. However, the matched control groups could eliminate or minimize the influence of the growth factor. The experimental duration lasted for 14 days in this study where 7-week-old rats were used. It has been reported that the laboratory rats grow in a pubertal spurt between 7 and 9 weeks of age, the time suitable for growth modification.21 It should be noted that magnets and sham magnets were bonded on the maxillary first molars of the first six rats of Group 1P and Group 1C, followed by the placement moving into the mandibular counterparts. The data from the maxillary device were still included for statistical analysis due to the fact that the matched controls could factor out any deviations that may cause. Some reports described asymmetric voltage waveforms from mechanically deformed live bone.4,5 These changes were presumed to occur in bone during physical activity as a result of mechanical forces. Polarity is dependent on the direction of bending; areas under pressure are in an electropositive state which is usually associated with osteoclastic activity and areas under tension are in an electronegative state which is associated with osteoblastic activity. It is therefore 285 conceivable that under the situation of alveolar bone on the present study with vibrating stimulus, the areas under pressure will shortly become the areas under tension and vice versa. It is also possible that an area of alveolar bone is associated with both increased osteoblastic activity and osteoclastic activity. It was shown in this study that, influenced by Nd-FeB magnet (without coil spring) together with PEMF, the interdental spaces increased much less than when influenced by sham magnets (p<0.019) (Fig 3). This indicated that the static magnetic field produced by NdFe-B magnet would have effect on tooth displacement. The effect of magnetic field on bone healing is well documented in the literature;22 however, the mechanism of action is not clear. Bassett3 stated that magnetic field could initiate increased localized calcium deposition, which neutralizes the tissues net negative charge, allows for subsequent vascularization and initiation of osteogenesis. It seems that this static magnetic effect caused by the Nd-Fe-B magnet alone could be accentuated in the presence of PEMF which causes vibration (Table 3). It appeared that although the effect on tooth movement of PEMF alone was not statistically significant, it affected the linear measurements of the interdental space of the experimental samples compared with the controls (Table 3). It is well documented in the literature that PEMF at low frequency significantly accelerates bone fracture healing in clinical trials6,7 and osteotomy healing in animal studies,4,5 especially with non-unions and delayed fracture unions. It has been suggested by Rubin et al.4 that bone resorption which accompanies disuse can be prevented or even reversed by the exogenous induction of electric fields. However, the precise mechanism of action remains unclear. Satake et al.23 found that calcium concentration in human periodontal ligament fibroblast cells was increased in the presence of PEMF. At the cellular level, Rodan et al.24 observed that cyclic nucleotides and calcium vehicles carry extracellular messages across the cell membrane. Interactions with diffusible ions, such as Ca2+ and K+, may convey an electric signal for DNA synthesis and cell division. One of the aims of this study was to evaluate whether PEMF vibration will affect conventional orthodontic tooth movement produced by closed coil spring and Nd-Fe-B magnet. It was found that 25 g Sentalloy closed coil spring moved the tooth more when it was used alone than when combined with magnets (Table 2), and it was especially so in the presence of PEMF where this interaction remained highly significant (p<0.01) (Table 3, Fig 3). This demonstrates a possible synergistic effect of the PEMF on the rate of tooth movement caused by the Nd-Fe-B magnet and coil springs. In addition, it was also interesting to note that the interdental space either became slightly increased when magnets worked alone, or decreased slowly when combined with coil spring, 286 regardless of the presence or absence of PEMF (Fig 3), indicating that the magnets hinder orthodontic tooth movement. The reasons behind the phenomenon may be the pulsating effect of the magnet that causes the molar tooth to remain relatively stationary. Another explanation may lie in the fact that the attractive forces by the magnets faded down significantly due to the large distance between the molar and incisor, and therefore hardly overcome the natural tendency of molar distal drift.25 The pulsating movement caused by the interaction of the PEMF and the Nd-Fe-B magnet could have a greater effect than as detected because the amount and/or direction of movement may be masked by that produced by the coil springs. As mentioned earlier, the Nd-Fe-B magnet alone and together with the closed coil spring appeared to slow down the changes in decreased interdental space. The closed coil spring, on the other hand, moved tooth faster when exposed to PEMF than it did without PEMF vibration (Fig 3). This phenomenon indicates that PEMF increases the rate of tooth movement produced by the closed coil springs. This is in agreement with the findings of Darendeliler et al.18 They found that a combined use of PEMF with coil springs was successful in increasing the rate of tooth movement compared with that produced by the coil springs alone. The mechanism of this effect has been suggested by some researchers to involve a reduction in “lag” phase which is common in orthodontic tooth movement.18 We therefore postulate that the PEMF, although it did not appear to produce much effect on tooth movement independently (p=0.577) (Table 2), has a synergistic effect on tooth movement when it is applied in conjunction with coil springs (p<0.001) (Table 3). It is also worth noting that whilst there was no significant difference between magnets and sham magnets in the absence of PEMF (p=0.408) (Table 3), it became significantly different when PEMF was imposed where the interdental space increased much less with magnets than with sham magnets (p=0.019) (Table 3). This clearly demonstrated that, when taking into consideration overcoming molar distal migration and magnets’ long working distance, PEMF was effective in encouraging magnets to move tooth towards favourable direction. It is therefore safe to contend that when combined with coil springs or magnets, PEMF could be applied, especially at the beginning of orthodontic treatment, to reduce the initial “lag” phase of orthodontic tooth movement and consequently to shorten the treatment time. CONCLUSIONS The effect of conventional mechanic forces, e.g., coil springs, on orthodontic tooth movement is enhanced with the exposure to PEMF-induced vibration. With reasonable working distance, the magnetic forces may be effective in enhancing tooth movement under PEMF-induced vibration. Australian Dental Journal 2007;52:4. ACKNOWLEDGEMENTS We thank the Australian Society of Orthodontics for funding this project. We also thank Associate Professor P Petocz of the Department of Statistics, Macquarie University for his statistical assistance. Thanks also go to Mr Paul Bowker, Senior Lecturer (clinical), The University of Sydney; Ms Janice Mathews from the Cellular and Molecular Pathology Research Unit, The University of Sydney; all the staff of the Westmead Animal Holding Facility and Dr. Allan Jones from the Electron Microscopy Unit, The University of Sydney. REFERENCES 13. Sato Y, Sakai H, Kobayashi Y, Sasaki, T. Bisphosphonate adminstration alters subcellular localisation of vacuolar-type H(+)-ATPase and cathepsin K in osteoclasts during experimental movement of rat molars. Anat Rec 2000;260:72-80. 14. Sato Y, Shibasaki Y, Sasaki T. Effects of bisphosphonate administration on root and bone resorption during experimental movement of rat molars. In: Davidovitch Z, Mah J, eds. Biological mechanisms of tooth movement and craniofacial adaptation. Birmingham: EBSCO;2000:243-252. 15. Rubin C, Turner S, Bain S, Mallinckrodt C, McLeod K. Anabolism: Low mechanical signals strengthen long bones. Nature 2001;412:603-604. 16. Rubin C, Xu G, Judex S. The anabolic activity of bone tissue, suppressed by disuse, is normalized by brief exposure to extremely low-magnitude mechanical stimuli. FASEB J 2001;15:2225-2229. 1. Norton JB, Young SO, Kenner GH. Epiphyseal cartilage cAMP changes produced by electrical and mechanical perturbations. Clin Orthop 1977;48:915-923. 17. Nolte PA, Klein-Nulend J, Albers GH, et al. Low intensity ultrasound stimulates endochondral ossification in vitro. J Orthop Res 2001;19:301-307. 2. Martin RB, Gutman W. The effect of electric fields on osteoporosis of disease. Calcif Tissue Int 1978;5:23-27. 18. Darendeliler MA, Sinclair PM, Kusy RP. The effects of samariumcobalt magnets and pulsed electromagnetic fields on tooth movement. Am J Orthod Dentofacial Orthop 1995;107:578-588. 3. Bassett CA. Beneficial effects of electromagnetic fields. J Cell Biochem 1993;51:387-393. 4. Rubin CT, Donahue HJ, Rubin JE, McLeod KJ. Optimisation of electric field parameters for the control of bone remodelling: exploitation of an indigenous mechanism for the prevention of osteopenia. J Bone Miner Res 1993;8 Suppl 2:S573-581. 5. Yonemori K, Matsunaga S, Ishidou Y, Maeda S, Yoshida H. Early effects of electrical stimulation on osteogenesis. Bone 1996;19:173-180. 6. Scott G, King JB. A prospective, double-blind trial of electrical capacitive coupling in the treatment of non-union of long bones. J Bone Joint Surg Am 1994;76:820-826. 7. Hulme J, Robinson V, DeBie R, Wells G, Judd M, Tugwell, P. Electromagnetic fields for the treatment of osteoarthritis. Cochrane Database Syst Rev 2002;1:CD003523. 8. Quittan M, Schuhfried O, Wiesinger GF, Fialka-Moser V. Clinical effectiveness of magnetic field therapy – a review of the literature. Acta Med Austraca 2002;27:61-68. 9. Ibiwoye MO, Powell KA, Grabiner MD, et al. Bone mass is preserved in a critical-sizes osteotomy by low energy pulsed electromagnetic fields as quantitated by in vivo micro-computed tomography. J Orthop Res 2004;22:1086-1093. 10. Inoue N, Ohnishi I, Chen D, Deitz LW, Schwardt JD, Chao EY. Effect of pulsed electromagnetic fields (PEMF) on late-phase osteotomy gap healing in a canine tibial model. J Orthop Res 2002;20:1106-1114. 11. Vandevska-Radunovic V. Neural modulation of inflammatory reactions in dental tissues incident to orthodontic tooth movement. A review of the literature. Eur J Orthod 1999;21:231247. 12. Miyajima K, Kasai R, Kahn AJ, Hayakawa T, Iizuka T. Biological mechanisms of tooth movement: in vitro analysis and clinical application. In: Davidovitch Z, Mah J, eds. The biological mechanisms of tooth movement and craniofacial adaptation. Birmingham: EBSCO;1992:311-317. Australian Dental Journal 2007;52:4. 19. Kobayashi Y, Hashimoto F, Miyamoto H, et al. Force-induced osteoclast apoptosis in vivo is accompanied by elevation in transforming growth factor beta and osteoprotegerin expression. J Bone Miner Res 2000;15:1924-1934. 20. Brudvik P, Rygh P. The initial phase of orthodontic root resorption incident to local compression of the periodontal ligament. Eur J Orthod 1993;15:249-263. 21. Shen G, Hägg U, Rabie AB, Kalurachchi K. Identification of temporal pattern of mandibular growth – A molecular and biochemical study. Orthod Craniofacial Res 2005;8:114-122. 22. Linovitz RJ, Pathria M, Bernhardt M, et al. Combined magnetic fields accelerate and increase spine fusion in double-blind, randomised, placebo controlled study. Spine 2002;27:1383-1389; discussion 1389. 23. Satake T, Yasu N, Kakai Y, et al. Effect of pulsed electromagnetic fields on human periodontal ligament in vivo. Alterations of intracellular Ca2+. Kanagawa Shigaku 1990;24:735-742. 24. Rodan GA, Bourret LA, Norton LA. DNA synthesis in cartilage cells is stimulated by oscillating electric fields. Science 1978;199:690-692. 25. Roux D, Meunier C, Woda A. A biometric analysis in the rat of the horizontal component of physiological tooth migration and its response to altered occlusal function. Arch Oral Biol 1993;38:957-963. Address for correspondence/reprints: Professor M Ali Darendeliler Department of Orthodontics Faculty of Dentistry The University of Sydney Level 2, 2 Chalmers Street Surry Hills, New South Wales 2010 Email: [email protected] 287