Acceleration of orthodontic tooth movement by alveolar ... · ORIGINAL ARTICLE Acceleration of...

8
ORIGINAL ARTICLE Acceleration of orthodontic tooth movement by alveolar corticotomy in the dog Shoichiro Iino, a Sumio Sakoda, b Gakuji Ito, c Toshikazu Nishimori, d Tetsuya Ikeda, e and Shouichi Miyawaki f Kagoshima and Miyazaki, Japan Introduction: Tooth movement and alveolar bone reaction after corticotomies have not been thoroughly examined. In this study, the effects of corticotomies on orthodontic tooth movement and alveolar bone reaction were investigated in dogs. Methods: Corticotomies were performed on the cortical bone of the mandibular left third premolar region in 12 male adult beagles. The third premolars on the left experimental side and on the right sham side were moved mesially with a continuous force of 0.5 N. Results: Tooth movement velocities from 0 to 1 week and from 1 to 2 weeks after the corticotomies were significantly faster on the experimental side than on the sham side. Hyalinization of the periodontal ligament appeared only at 1 week after the corticotomies on the experimental sides, whereas it was observed from 1 to 4 weeks after the corticotomies on the sham sides. Tartrate-resistant-acid-phosphatase positive cells of the experimental side tended to work vigorously at an early time on the alveolar wall and in the bone marrow cavities. Conclusions: Orthodontic tooth movement increased for at least 2 weeks after the corticotomies. This might be brought about by rapid alveolar bone reaction in the bone marrow cavities, which leads to less hyalinization of the periodontal ligament on the alveolar wall. (Am J Orthod Dentofacial Orthop 2007;131: 448.e1-448.e8) A corticotomy on the alveolar bone makes orth- odontic tooth movement faster than in conven- tional orthodontic treatment; this leads to shorter orthodontic treatment times. 1-8 According to Hajji, 3 the active orthodontic treatment periods in patients with corticotomies were 3 to 4 times more rapid compared with patients without corticotomies. It was believed that a corticotomy makes tooth movement faster because the bone block moves with the tooth. 6-8 However, tooth movement after a corticotomy should be considered a combination of classical orthodontic tooth movement and the movement of bone blocks containing a tooth, because the force applied to a tooth is transmitted into the osteotomy gap through the periodontal ligament (PDL). Bone turnover is well known to be accelerated after bone fracture, osteotomy, or bone grafting. 9 This could be explained by a regional acceleratory phenomenon (RAP); ie, osteoclasts and osteoblasts increase by local multicellular mediator mechanisms containing precur- sors, supporting cells, blood capillaries, and lymph. RAP also occurs in the mandible. 10 Similarly, bone turnover is increased by RAP after a corticotomy. The velocity of orthodontic tooth movement is influenced by bone turnover, 11,12 bone density, 13 and hyalinization of the PDL. 14 Wilcko et al 4,5 mentioned, in cases of rapid orthodontics with corticotomies, that corticotomies could increase tooth movement by in- creasing bone turnover and decreasing bone density. However, the increase of tooth movement after a corticotomy was not always examined histologically. In our study, we intended to elucidate the mechanism of rapid tooth movement associated with corticotomies by investigating the amount of tooth movement and the alveolar bone reaction on the periodontal tissue of the compression side after corticotomies in beagle dogs. MATERIAL AND METHODS The experimental animals were 12 male adult beagles. They were caged individually with regu- lated light and temperature, and fed soft dog food a Assistant professor, Department of Orthodontics, Center of Developmental Dentistry, Medical and Dental Hospital, Kagoshima University, Kagoshima, Japan. b Professor and chair, Department of Oral and Maxillofacial Surgery, Miyazaki Medical College, University of Miyazaki, Miyazaki, Japan. c Professor emeritus, Kagoshima University, Kagoshima, Japan. d Professor and chair, Division of Biology, Miyazaki Medical College, Univer- sity of Miyazaki, Miyazaki, Japan. e Assistant professor, Division of Biology, Miyazaki Medical College, Univer- sity of Miyazaki, Miyazaki, Japan. f Professor and chair, Department of Orthodontics, Field of Developmental Medicine, Health Research Course, Graduate School of Medical and Dental Sciences, Kagoshima University, Kagoshima, Japan. Partially supported by grants-in-aid for scientific research for the first and sixth authors from the Japan Society for the Promotion of Science. Reprint requests to: Shouichi Miyawaki, Department of Orthodontics, Field of Developmental Medicine, Health Research Course, Graduate School of Med- ical and Dental Sciences, Kagoshima University, 8-35-1 Sakuragaoka, Ka- goshima 890-8544, Japan; e-mail, [email protected]. Submitted, May 2006; revised and accepted, August 2006. 0889-5406/$32.00 Copyright © 2007 by the American Association of Orthodontists. doi:10.1016/j.ajodo.2006.08.014 448.e1

Transcript of Acceleration of orthodontic tooth movement by alveolar ... · ORIGINAL ARTICLE Acceleration of...

ORIGINAL ARTICLE

Acceleration of orthodontic tooth movementby alveolar corticotomy in the dogShoichiro Iino,a Sumio Sakoda,b Gakuji Ito,c Toshikazu Nishimori,d Tetsuya Ikeda,e and Shouichi Miyawakif

Kagoshima and Miyazaki, Japan

Introduction: Tooth movement and alveolar bone reaction after corticotomies have not been thoroughlyexamined. In this study, the effects of corticotomies on orthodontic tooth movement and alveolar bonereaction were investigated in dogs. Methods: Corticotomies were performed on the cortical bone of themandibular left third premolar region in 12 male adult beagles. The third premolars on the left experimentalside and on the right sham side were moved mesially with a continuous force of 0.5 N. Results: Toothmovement velocities from 0 to 1 week and from 1 to 2 weeks after the corticotomies were significantly fasteron the experimental side than on the sham side. Hyalinization of the periodontal ligament appeared only at1 week after the corticotomies on the experimental sides, whereas it was observed from 1 to 4 weeks afterthe corticotomies on the sham sides. Tartrate-resistant-acid-phosphatase positive cells of the experimentalside tended to work vigorously at an early time on the alveolar wall and in the bone marrow cavities.Conclusions: Orthodontic tooth movement increased for at least 2 weeks after the corticotomies. This mightbe brought about by rapid alveolar bone reaction in the bone marrow cavities, which leads to lesshyalinization of the periodontal ligament on the alveolar wall. (Am J Orthod Dentofacial Orthop 2007;131:

448.e1-448.e8)

Acorticotomy on the alveolar bone makes orth-odontic tooth movement faster than in conven-tional orthodontic treatment; this leads to

shorter orthodontic treatment times.1-8 According toHajji,3 the active orthodontic treatment periods inpatients with corticotomies were 3 to 4 times morerapid compared with patients without corticotomies. Itwas believed that a corticotomy makes tooth movementfaster because the bone block moves with the tooth.6-8

However, tooth movement after a corticotomy shouldbe considered a combination of classical orthodontictooth movement and the movement of bone blocksaAssistant professor, Department of Orthodontics, Center of DevelopmentalDentistry, Medical and Dental Hospital, Kagoshima University, Kagoshima,Japan.bProfessor and chair, Department of Oral and Maxillofacial Surgery, MiyazakiMedical College, University of Miyazaki, Miyazaki, Japan.cProfessor emeritus, Kagoshima University, Kagoshima, Japan.dProfessor and chair, Division of Biology, Miyazaki Medical College, Univer-sity of Miyazaki, Miyazaki, Japan.eAssistant professor, Division of Biology, Miyazaki Medical College, Univer-sity of Miyazaki, Miyazaki, Japan.fProfessor and chair, Department of Orthodontics, Field of DevelopmentalMedicine, Health Research Course, Graduate School of Medical and DentalSciences, Kagoshima University, Kagoshima, Japan.Partially supported by grants-in-aid for scientific research for the first and sixthauthors from the Japan Society for the Promotion of Science.Reprint requests to: Shouichi Miyawaki, Department of Orthodontics, Field ofDevelopmental Medicine, Health Research Course, Graduate School of Med-ical and Dental Sciences, Kagoshima University, 8-35-1 Sakuragaoka, Ka-goshima 890-8544, Japan; e-mail, [email protected], May 2006; revised and accepted, August 2006.0889-5406/$32.00Copyright © 2007 by the American Association of Orthodontists.

doi:10.1016/j.ajodo.2006.08.014

containing a tooth, because the force applied to a toothis transmitted into the osteotomy gap through theperiodontal ligament (PDL).

Bone turnover is well known to be accelerated afterbone fracture, osteotomy, or bone grafting.9 This couldbe explained by a regional acceleratory phenomenon(RAP); ie, osteoclasts and osteoblasts increase by localmulticellular mediator mechanisms containing precur-sors, supporting cells, blood capillaries, and lymph.RAP also occurs in the mandible.10 Similarly, boneturnover is increased by RAP after a corticotomy.

The velocity of orthodontic tooth movement isinfluenced by bone turnover,11,12 bone density,13 andhyalinization of the PDL.14 Wilcko et al4,5 mentioned,in cases of rapid orthodontics with corticotomies, thatcorticotomies could increase tooth movement by in-creasing bone turnover and decreasing bone density.However, the increase of tooth movement after acorticotomy was not always examined histologically. Inour study, we intended to elucidate the mechanism ofrapid tooth movement associated with corticotomies byinvestigating the amount of tooth movement and thealveolar bone reaction on the periodontal tissue of thecompression side after corticotomies in beagle dogs.

MATERIAL AND METHODS

The experimental animals were 12 male adultbeagles. They were caged individually with regu-

lated light and temperature, and fed soft dog food

448.e1

American Journal of Orthodontics and Dentofacial OrthopedicsApril 2007

448.e2 Iino et al

and water to prevent any damage to the experimentalorthodontic appliance. All experimental procedureswere performed under intravenous anesthesia withsodium pentobarbital (25-30 mg per kilogram ofbody weight). The experimental conditions and pro-cedures were approved by the Animal Ethics Com-mittee of Miyazaki University.

The mandibular left and right third premolars (P3)were the experimental and sham sides, respectively.The mandibular second premolars were extracted onboth sides to prepare the space for mesial movement ofthe P3.

Healing, by the formation and mineralization ofcallus, usually requires 4 to 16 weeks after boneinjury.9 Therefore, at 16 weeks after extraction, thealveolar bone on the experimental side was corticoto-mized as follows: the gingival mucoperiosteal flapswere raised to expose cortical bone on both the buccaland the lingual sides of the P3. The horizontal cut lineof the corticotomy was made under the apices of the P3on the lingual side and at the level of mental foramenon the buccal side (Fig 1). The vertical cut lines weremade from the alveolar crests of the P3 to the horizontalcut lines on the buccal and lingual sides. The corti-cotomy process was performed with a #009 fissure burunder saline-solution irrigation. The width of bone cutswas approximately 1 mm, and the depth was carefullyadjusted to reach the bone marrow by confirmingbleeding through the cut lines. The mucoperiostealflaps were sutured with absorbable surgical sutures.

Orthodontic appliances were constructed on bothsides on the dental casts before the corticotomies(Figs 2 and 3). Orthodontic bands were cemented onthe mandibular canines and P3 teeth. Metal tubes(diameter, 1.14 mm; length, 4.6 mm; Tomy Interna-

Fig 1. Photograph of corticotomy on alveolar buccalsurface on experimental side. Same incision was madeon lingual side. White arrowhead, horizontal cut line wasmade beyond apices; black arrowhead, vertical cut linewas made from alveolar crest to horizontal cut line.

tional, Tokyo, Japan) were soldered to the orthodon-

tic bands of the P3. Orthodontic wires (diameter, 1.0mm; Dentsply-Sankin, Tokyo, Japan) were solderedto the mandibular canine bands and inserted throughthe metal tubes on the bands of the P3. The bandswere cemented to the teeth with glass ionomercement.

Immediately after the corticotomies, the P3 teeth ofthe experimental and sham sides were moved mesiallyalong the orthodontic wire with a continuous force of0.5 N by using nickel-titanium closed coil springs(Tomy International). One end of the spring was fixedto the bent loop of the orthodontic wire on the caninesite with a ligature wire, and the other side was fixed tothe metal tube with a ligature wire. The length of eachspring, which corresponded to a contractile force of 0.5N, was measured with a caliper and strain gauge, andthe activation of the spring was set at that length. Theappliance, teeth, and gingiva were checked once a dayand cleaned with a toothbrush and gauze with 0.02%chlorhexidine in water, and the force delivery wasmeasured once a week.

Standardized dental radiographs were taken at aconstant distance and angle by setting the film holderwith an attachment on the mandibular fourth premolar(Fig 4) before the corticotomy (T0) and at 1 (T1), 2(T2), 4 (T4), and 8 (T8) weeks after the corticotomy.Tracing and superimposition on the mandibular fourthpremolar were carried out. The distance of tooth move-ment was measured between the tip of protocone ofthe P3 at the various time points with a caliper on thetracing. The error of the method was calculated for thedistance of tooth movement based on double measure-

Fig 2. Schematic drawing of orthodontic appliance.One side of wire (external diameter 1.0 mm) was sol-dered to orthodontic band of mandibular canine, andother side ran freely through the 1.14 mm metal tube(internal diameter) on mandibular third premolar. Man-dibular third premolars on both sides were movedmesially with nickel-titanium coil springs. C, Canine; P3,third premolar; P4, fourth premolar.

ments on 10 randomly selected distances of tooth

American Journal of Orthodontics and Dentofacial OrthopedicsVolume 131, Number 4

Iino et al 448.e3

movement measurements and was estimated as S ���(d)2/2n, where n � number of paired measure-ments and d � deviations between the 2 measurements.The error of the method for measurement of toothmovement was 0.02 mm. The tooth movement veloci-ties (millimeters per week) from T0 to T1 (T0-1), T1 toT2 (T1-2), and T2 to T4 (T2-4) were calculated. Themean values of the distance and velocity of the toothmovement were estimated with the Mann-Whitney Utest. Three dogs were killed at T1, T2, T4, and T8 forhistologic examinations. Therefore, the numbers of dogswere 12, 9, 6, and 3 at T1, T2, T4, and T8, respectively.

The animals were perfused through the carotidartery with 1% paraformaldehyde and 1% glutaralde-hyde in 0.1 mol phosphate buffer (pH 7.4) under deepanesthesia. The blocks of mandibular bone were dis-sected and refixed in the same solution at 4°C for 24hours. The blocks were trimmed and decalcified in 10%ethylenediaminetetraacetic acid (EDTA-2Na; pH 7.4)at 4°C for 30 days. Subsequently, according to aconventional technique, serial mesiodistal paraffin sec-tions of 8 �m thickness were made and stained withhaematoxylin and eosin or tartrate-resistant-acid-phos-phatase (TRAP) with methylene blue as counterstain-

Fig 3. Photographs of orthodontic applianceB, closed-mouth view.

Fig 4. Standardized dental radiograph taken by settingfilm holder with attachment on mandibular fourthpremolar.

ing for detection of the osteoclasts. Although oste-

oclasts and osteoblasts are generally observed to assessbone turnover, we observed only osteoclasts to studythe tendency of bone turnover on the periodontal tissue

d for tooth movement: A, open-mouth view;

Fig 5. Comparison of distance of tooth movementbetween experimental and sham sides with Mann-Whitney U test. T1, 1 week; T2, 2 weeks; T4, 4 weeksafter corticotomy. *P �.05; ***P �.001.

Fig 6. Comparison of tooth movement velocity betweenexperimental and sham groups with Mann-Whitney U test.T0-1, Period from 0 to 1 week; T1-2, period from 1 to 2weeks; T2-4, period from 2 to 4 weeks after corticotomy.*P �.05; **P �.01; ***P �.001.

s use

and simplify our experiment.

my. O

American Journal of Orthodontics and Dentofacial OrthopedicsApril 2007

448.e4 Iino et al

Light microscopic observation was carried out onthe compression side of the P3 mesial root in theexperimental and sham sides at T1, T2, T4, and T8. AllP3 teeth of the experimental and sham sides weremoved mesially with slight tipping, so histologicalobservations were performed from the alveolar crest tohalfway apically at the compression side. The numbersof TRAP positive (TRAP�) cells were counted on themesial surface of the mesial root (alveolar wall) and inthe bone marrow cavities immediately adjacent to thealveolar wall according to the method of Noxon et al.15

Their numbers were counted from 3 midsagittal sec-tions per case in the experimental and sham sides at T1,T2, and T4. The timing of TRAP� cell increase(increasing bone turnover) and decrease (decreasingbone turnover) was observed on the alveolar wall and inthe bone marrow cavities.

RESULTS

The distances of the tooth movement on the exper-imental side were significantly greater than those on thesham sides at T1, T2, and T4 (Fig 5), approximatelydouble those on the sham side. Tooth movementincreased almost linearly from T0 to T4 on the exper-imental side. On the sham sides, tooth movementstopped from T1 to T2, but the distances increased from

Fig 7. Microphotographs of periodontal tissuestain. Hyalinization of PDL was observed only aAlveolar bone; H, hyalinization; PDL, periodonsame scale. T8 means 8 weeks after corticoto

T0 to T1 and from T2 to T4.

The movement velocity on the experimental sidewas also faster than that on the sham side throughoutthe experiment (Fig 6). There was a significant differ-ence between the experimental and sham sides at T0-1and T1-2; movement was 2 and 5 times faster on theexperimental side, respectively. There was no signifi-cant difference in movement velocity between T1-2 andT2-4 on the experimental side. On the sham side, thevelocity at T1-2 was significantly slower than that atT0-1 and T2-4.

On the experimental side, undermining resorptionwith hyalinization of the PDL was observed on thealveolar wall only at T1 (Figs 7 and 8). Underminingresorption disappeared, and direct resorption progressed atT2, T4, and T8. In the bone marrow cavities, underminingresorption was significant at T1. No root resorption wasobserved at any time point after corticotomy.

On the sham side, undermining resorption withhyalinization of the PDL also occurred on the alveolarwall at T1, T2, and T4 (Fig 9). Undermining resorptiondisappeared, and direct bone resorption progressed atT8. Remarkably, in the bone marrow cavities, under-mining resorption was found at T2. Root resorption wasobserved around the area of hyalinization at T4, and itwas more striking at T8 (arrows in Fig 8).

On the alveolar wall, the numbers of TRAP� cells

xperimental side with haematoxylin and eosinFramed areas of T1 are magnified in Fig 8. AB,ament; TR, tooth root. All photographs are atther abbreviations are shown in Fig 5.

on et T1. tal lig

increased from T1 on the experimental side (Fig 10);

are s

American Journal of Orthodontics and Dentofacial OrthopedicsVolume 131, Number 4

Iino et al 448.e5

the numbers increased gradually during the experimenton the sham side. Thus, TRAP� cells seemed to workvigorously at an early time on the experimental side(Figs 10 and 11).

In the bone marrow cavities, the numbers ofTRAP� cells decreased at T2 on the experimental side(Fig 9); the numbers increased at T2 and decreased atT4 on the sham side. Timing of increase and decreaseof TRAP� cells seemed to be hastened on the experi-mental side.

DISCUSSION

The average distance of tooth movement by anorthodontic force of 0.5 N on the sham side in this

Fig 8. Microphotographs of A, hyalinization oPhotographs are at same scale.

Fig 9. Microphotographs of periodontal tissueHyalinization of PDL was observed at T1, Tphotographs are at same scale. Abbreviations

study was 1 mm in 4 weeks, and this value is similar to

that in a previous dog study.16 The distance wasapproximately double on the experimental side at T1,T2, and T4 compared with the sham side. Moreover,tooth movement velocity on the experimental side wassignificantly faster than on the sham side at T0-1 andT1-2: 2 and 5 times faster on the experimental side,respectively. Therefore, it is suggested that orthodontictooth movement increased especially in the early stageafter the corticotomies.

Time-displacement curves of orthodontic toothmovement are divided and sequenced into 4 phases:initial, lag, acceleration, and constant linear phases.16,17

The initial phase (rate of tooth movement: about thedistance of PDL thickness) lasts 3 to 4 days or less, and

and B, undermining resorption in Fig 7 at T1.

ham side with haematoxylin and eosin stain.d T4. Arrowheads show root resorption. Allhown in Fig 7.

f PDL

on s2, an

its duration is never longer than 7 days, and the lag

American Journal of Orthodontics and Dentofacial OrthopedicsApril 2007

448.e6 Iino et al

Fig 10. Timing of increase and decrease of numbers of TRAP� cells on alveolar wall and in bonemarrow cavities. Abbreviations are shown in Fig 5. ●, Number of TRAP� cells in each tooth; �,

mean value of number of TRAP� cells at each time point.

Fig 11. Microphotographs of periodontal tissue on experimental (Exp.) and sham sides with TRAPstain at 1 week after corticotomy. There are many TRAP� cells (arrowheads) in experimental side.

Photographs are at same scale. Abbreviations are shown in Fig 7.

American Journal of Orthodontics and Dentofacial OrthopedicsVolume 131, Number 4

Iino et al 448.e7

phase (rate: quite small) lasts for an average of about 7days.16 On the sham side, tooth movement velocity wasalso quite slow at T1-2 (mean, 0.1 mm per week);therefore, T1-2 could be considered the lag phase.On the other hand, there was no observable lag phaseon the experimental side, because no significant differ-ence existed in tooth movement velocity between T1-2and T2-4. Several authors proposed that the lag phase isassociated with hyalinization in the PDL, and that theefficiency of tooth movement might be improved bypreventing hyalinization.16-20 Hyalinization of the PDLprecedes the root resorption process during orthodontictooth movement and can often be observed adjacent tothis process.21,22 In our study, hyalinization of the PDLat the compression side was observed only at T1 on theexperimental side, whereas it was found at T1, T2, andT4 on the sham side. Thus, hyalinization of the PDLwas eliminated at an early stage on the experimentalside. Furthermore, root resorption was not observed onthe experimental side, but it was observed on the shamside at T4 and T8. These results suggested that toothmovement after corticotomy increased without rootresorption, and this might be due to the disappearanceof the lag phase as evident by less hyalinization of thePDL in the early stage. However, tooth movementvelocity at T0-1 was still faster than that at T1-2 andT2-4 on the experimental side. The initial phase wasinterpreted as the initial movement of a tooth in itssocket, because the thickness of the PDL is reduced onthe compression side by the orthodontic force.16 Theincrease of tooth movement velocity at T0-1 on theexperimental side would be due to compression ofthe PDL and bare spongiose bone and, on the compres-sion side, by the orthodontic force. However, no alve-olar bone reaction in the osteotomy gaps was observedin this study. It would have been interesting to inves-tigate the alveolar bone reaction in the osteotomy gaps.

In our study, TRAP� cells of the experimental sideseemed to work vigorously at an early time on thealveolar wall and in the bone marrow cavities. Almostno TRAP� cells were found on the alveolar bone ofsections from dogs examined in our other previousstudy (data not shown). When hyalinization of the PDLoccurs, osteoclasts appear in the adjacent bone marrowcavities and begin attacking the underside of the boneadjacent to the area of hyalinization.18,23 Tooth move-ment in juveniles was faster than that in adults at anearly phase,24 because mediator levels in juveniles weremore responsive than those in adults in early toothmovement.25 Bone healing is accelerated by RAP aftersurgery.7 New bone formed in the trabecular boneadjacent to the incision site was caused by increasing

bone turnover in rabbits.26 Also, after the corticotomies

in our study, the alveolar bone reaction increasedsimultaneously with orthodontic tooth movement nearthe corticotomy by RAP at an early stage.

Clinically, it is generally believed that a heavierorthodontic force is needed for the en-masse movementof the bone block with the tooth after a corti-cotomy.1,2,6,7 However, our results suggest that con-ventional orthodontic force would increase the velocityof orthodontic tooth movement, possibly by accelera-tion of the bone turnover mechanism at an early stageafter a corticotomy.

Alveolar bone turnover of the mandible is acceler-ated by the raising of the gingival mucoperiosteal flapper se.10 Therefore, the side without a corticotomy inthis study might not be really a sham for the corti-cotomy in a strict sense. However, we considered thatorthodontic tooth movement after the corticotomy in-creased by an acceleration of bone turnover accompa-nied by the surgery of the corticotomy and raising ofthe gingival mucoperiosteal flaps. Wilcko et al4 men-tioned that bleeding of the corticotomy site is moreimportant than creating blocks of bone for rapid toothmovement. Therefore, a more simple surgery such asgingival mucoperiosteal incision or bone perforation4,5

might be used instead of a corticotomy. Furthermore, aproblem that could arise from the surgical proceduremight be dysfunction accompanied by pain or swellingimmediately after the corticotomy. Perhaps the effectsof simple surgeries on orthodontic tooth movement anddysfunction after corticotomy should be studied.

CONCLUSIONS

The alveolar corticotomy procedure increases orth-odontic tooth movement for at least 2 weeks after thecorticotomy and decreases the risk of root resorption.This process might be brought about by the rapidalveolar bone reaction in the bone marrow cavities,leading to less hyalinization of the PDL on the alveolarwall.

We thank Masanori Uemura and Tetsuya Matsugu-chi for their generous guidance and Abdullah Al-Kalalyfor his help with the English language.

REFERENCES

1. Köle H. Surgical operation on the alveolar ridge to correctocclusal abnormalities. Oral Surg Oral Med Oral Pathol OralRadiol Endod 1959;12:515-29.

2. Converse JM, Horwitz SL. The surgical orthodontic approach tothe treatment of dentofacial deformities. Am J Orthod 1969;55:217-43.

3. Hajji SS. The influence of accelerated osteogenic response onmandibular decrowding (thesis). St Louis: St Louis University;

2000.

American Journal of Orthodontics and Dentofacial OrthopedicsApril 2007

448.e8 Iino et al

4. Wilcko WM, Wilcko MT, Bouquot JE, Ferguson DJ. Rapidorthodontics with alveolar reshaping: two case reports of de-crowding. Int J Periodontics Restorative Dent 2001;21:9-19.

5. Wilcko WM, Ferguson DJ, Bouquot JE, Wilcko MT. Rapidorthodontic decrowding with alveolar augmentation: case report.World J Orthod 2003;4:197-205.

6. Chung KR, Oh MY, Ko SJ. Corticotomy-assisted orthodontics.J Clin Orthod 2001;35:331-9.

7. Hwang HS, Lee KH. Intrusion of overerupted molars by corti-cotomy and magnets. Am J Orthod Dentofacial Orthop 2001;120:209-15.

8. Suya H. Corticotomy in orthodontics. In: Hosl E, Baldauf A,editors. Mechanical and biological basics in orthodontic therapy.Heidelberg, Germany: Huthig Buch Verlag; 1991. p. 207-26.

9. Frost HM. The biology of fracture healing. An overview forclinicians. Part I. Clin Orthop Related Res 1989;248:283-93.

10. Yaffe A, Fine N, Binderman I. Regional accelerated phenome-non in the mandible following mucoperiosteal flap surgery.J Periodontol 1994;65:79-83.

11. Verna C, Dalstra M, Melsen B. The rate and the type oforthodontic tooth movement is influenced by bone turnover in arat model. Eur J Orthod 2000;22:343-52.

12. Verna C, Melsen B. Tissue reaction to orthodontic tooth move-ment in different bone turnover conditions. Orthod Craniofac Res2003;6:155-63.

13. Goldie RS, King GJ. Root resorption and tooth movement inorthodontically treated, calcium-deficient, and lactating rats.Am J Orthod 1984;85:424-30.

14. Bohl MV, Maltha JC, Von den Hoff JW, Kuijpers-JagtmanAM. Focal hyalinization during experimental tooth movementin beagle dogs. Am J Orthod Dentofacial Orthop 2004;125:615-23.

15. Noxon SJ, King GJ, Gu G, Huang G. Osteoclast clearance fromperiodontal tissues during orthodontic tooth movement. Am J

Orthod Dentofacial Orthop 2001;120:466-76.

16. Pilion JJGM, Kuijpers-Jagtman AM, Maltha JC. Magnitude oforthodontic forces and rate of bodily tooth movement: anexperimental study in beagle dogs. Am J Orthod DentofacialOrthop 1996;110:16-23.

17. Leeuwen EJ, Maltha JC, Kuijpers-Jagtman AM. Tooth move-ment with light continuous and discontinuous forces in beagledogs. Eur J Oral Sci 1999;107:468-74.

18. Proffit WR. Biomechanics and mechanics. In: Rudolph P,editor. Contemporary orthodontics. St Louis: Mosby; 2000. p.296-361.

19. Driel WD, Leeuwen EJ, Hoff JW, Maltha JC, Kuijpers-JagtmanAM. Time-dependent mechanical behavior of the periodontalligament. Proc Inst Mech Eng 2000;214:497-504.

20. Reitan K. Continuous bodily tooth movement and its histologicalsignificance. Acta Odont Scand 1947;6:115-44.

21. Brudvik P, Rygh P. The initial phase of orthodontic rootresorption incident to local compression of periodontal ligament.Eur J Orthod 1993;15:249-63.

22. Kurol J, Owman-Moll P. Hyalinization and root resorptionduring early orthodontic tooth movement in adolescents. AngleOrthod 1998;68:161-5.

23. Lindskog S, Lilja E. Scanning electron microscopic study oforthodontically induced injuries to the periodontal membrane.Scand J Dent Res 1984;92:334-43.

24. Ren Y, Maltha JC, Von den Hoff JW, Kuijpers-Jagtman AM.Age effect on orthodontic tooth movement in rats. J Dent Res2003;82:38-42.

25. Ren Y, Maltha JC, Bohl MV, Von den Hoff JW, Kuijpers-Jagtman AM, Ding Z. Cytokine levels in crevicular fluid are lessresponsive to orthodontic force in adults than in juveniles. J ClinPeriodontol 2002;29:757-62.

26. Bogoch E, Gschwend N, Rahn B, Moran E, Perren S. Healing ofcancellous bone osteotomy in rabbits - Part I: regulation of bonevolume and the regional acceleratory phenomenon in normal

bone. J Orthop Res 1993;11:285-91.