tooth movement into distraction regenerate: when should we start?

ORIGINAL ARTICLE

Tooth movement into distraction regenerate:When should we start?

Fouad Aly El Sharaby,a Nader Nabil El Bokle,b Dalia Mohamed El Boghdadi,c and Yehya Ahmed Mostafad

Cairo, Egypt

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482

Introduction: The aim of this study was to evaluate clinically, radiographically, and histologically orthodontictooth movement into bone regenerate after mandibular distraction osteogenesis to elucidate the optimal timingfor initiating tooth movement.Methods: The study sample consisted of 9 male mongrel dogs. An average eden-tulous space of 9 mm was created by using a custom-made bone-borne distractor fixed on the mandibularcorpus of each dog. The dogs were equally divided into 3 groups, and tooth movement began into thedistraction gap after 1, 3, or 6 weeks of consolidation. The rate and type of tooth movement as well as theadverse tissue reactions (root resorption and crestal bone loss) were evaluated.Results:Radiographic and his-tologic analyses showed analogous adverse tissue reactions in association with early tooth movement into theregenerate bone. Furthermore, the rate and type of toothmovement were variable in the 3 groups.Conclusions:Early tooth movement into the distraction regenerate is not recommended because it could result in adverse tis-sue reactions. Moreover, radiographic examination of the distraction regenerate is advisable and could be usedas a guide before starting tooth movement. (Am J Orthod Dentofacial Orthop 2011;139:482-94)

Distraction osteogenesis (DO) is the process of gener-ating new bone in a gap between 2 bone segmentsin response to the application of graduated tensile

stress across the bone gap. The DO surgical concept was in-troduced by Codivilla1 in 1905 and implemented 50 yearslater by Ilizarov.2,3 DO has opened new horizons for theorthodontist in treating crowded dental arches, especiallythose associated with craniofacial anomalies.

In most of the current mandibular osteodistractionreports, the osteotomies are done in nontooth-bearingareas posterior to the alveolar process with lengtheningof the ramus and the body as the common target.4 Onthe other hand, fewer studies reported midline interden-tal osteotomies for transverse mandibular expansion,particularly in patients with severe anterior dentalcrowding. In general, avoidance of osteotomies in thetooth-bearing body of the mandible is partly the resultof the limited data about the consequences of recon-structing the interdental gaps created after distraction

the Faculty of Oral and Dental Medicine, Cairo University, Cairo, Egypt.tant lecturer, Orthodontic Department.rer, Oral and Maxillofacial Surgery Department.rer, Orthodontic Department.ssor, Orthodontic Department.uthors report no commercial, proprietary, or financial interest in the prod-r companies described in this article.t requests to: Yehya Ahmed Mostafa, PO Box 60, Mina Garden City, Octo-ty, Cairo 12582, Egypt; e-mail, [email protected], February 2009; revised and accepted, May 2009.5406/$36.00ight � 2011 by the American Association of Orthodontists..1016/j.ajodo.2009.05.041

by either orthodontically moving teeth or placingimplants into the newly formed bone.

Although the clinical possibility of moving teeth intoregenerate alveolar bone is no longer disputed, the tim-ing of initiating orthodontic tooth movement into thenewly created bone remains a topic of discussion.Some authors suggested that tooth movement shouldnot begin until the regenerate bone has consolidatedfor 8 to 12 weeks.5-14 However, others have shownthat tooth movement can begin much earlier in theconsolidation period.15-18 This study was designed toevaluate clinically, radiographically, and histologicallyorthodontic tooth movement into bone regeneratecreated after mandibular DO to elucidate the optimaltiming for starting tooth movement.

MATERIAL AND METHODS

The sample for this study consisted of 9 adult malemongrel dogs with an average weight of 13 to 17 kg,aged 11 to 15 months. In all dogs, osteotomies for dis-traction were done in tooth-bearing areas of the mandi-ble between the third and fourth premolars. The dogswere divided equally into 3 groups based on the timeof initiating tooth movement into the regenerate bonecreated after distraction. Tooth movement began after1, 3, and 6 weeks of consolidation in groups I, II, andIII, respectively, and continued for 8 weeks or until com-plete contact between the third and fourth premolars.Bilateral mandibular distraction was done in all dogs,

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Fig 1. The flap design, osteotomy, and distractor fixed inplace.

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except for 1 dog in each group that had only unilateralmandibular distraction. This dog was killed before toothmovement to examine the quality of the formed regen-erate at that time.

In this study, a custom-made intraoral bone-bornedistractor was used that was made up of a rapid palatalexpander (Forestadent, Pforzheim, Germany), 2/0 straightstainless steel surgical miniplates (KLS Martin, Jackson-ville, Florida), and 6 titanium bone screws (11 mm) forbicortical fixation (Fig 1).

The surgical protocol was as follows: An intraoralsoft-tissue 4-cm vestibular incision was made from thesecond premolar to the first molar with a number 15blade. A mucoperiosteal flap was reflected inferiorly, ex-posing the inferior border of the mandible with minimaldissection superiorly enough to expose the area of theplanned osteotomy and to maintain the integrity ofthe gingival tissue. A mandibular buccal osteotomywas initiated by using a reciprocating saw blade, andthen the device was fixed in place with 3 bicortical min-iscrews on each side of the osteotomy. The osteotomywas completed by using a spatula osteotome. The os-teotomy was made closer to the fourth premolar; this re-sulted in root injury in some dogs. This was done toprovide enough bone coverage distal to the third premo-lar root and to prevent its possible injury during the os-teotomy procedure (Fig 1). The mucosal flap was thenclosed with a continuous 3-0 polyglactin 910 suture.An indentation was made on the middle of the labial sur-face of the canine with a round bur to be used as a distantreference point for monitoring the amount and rate oftooth movement. The other reference point was the tipof the crown of the third premolar.

The distraction protocol was as follows: The dogswere carefully monitored after surgery. Oral chlorhexi-dine was used for irrigation twice daily for 4 days post-operatively and when signs of inflammation wereobserved.

The bone segments were maintained in a neutral po-sition for 7 days (latency period). On the eighth postop-erative day, activation of the appliance began at a rate of1 mm per day divided into 2 increments of 0.5 mm for 12days followed by either 1, 3, or 6 weeks of consolidationbefore initiating tooth movement. In all animals, the de-vice was maintained in position during tooth movement.

The tooth movement protocol was as follows:Custom-made crowns for the third and fourth premolarswere fabricated. On the labial surface of each alreadyprepared crown, a stainless steel molar tube (0.022 30.028 in) was soldered in such a way that it alloweda high-gauge straight stainless steel wire (0.019 30.025 in) to slide through freely. The crowns were ce-mented with glass ionomer cement. A calibrated

American Journal of Orthodontics and Dentofacial Orthoped

nickel-titanium coil spring with a force of 150 g was at-tached to the hooks of the soldered molar tubes to movethe third premolar into the edentulous segment createdby distraction. Meanwhile, the fourth premolar was pre-vented from movement by ligation with the first molarwith a ligature wire (Fig 2).

All animals were monitored postsurgically for wounddehiscences, infection, and loosening or breakage of thedistractor.

At the end of the distraction phase, the amount ofdistraction on each side was measured from the tip ofthe third premolar crown to the tip of the fourth premo-lar crown by using a sliding caliper.

During the tooth movement phase, the distance fromthe third premolar crown tip and the indentation madeon the middle of the labial surface of the canine of thesame side was measured at the start of tooth movementand repeated every 2 weeks for 8 weeks to estimate theamount and rate of tooth movement in each group.

At the end of the experiment in each group, the dogswere humanely killed with an intravenous overdose ofpentobarbital (40-50 mg/kg).

Digital periapical radiographs were then taken for thehemi-mandibles by using phosphor storage plates (Di-gora, Soredex,Tuusula, Finland). The radiographs wereevaluated for signs of new bone formation in the distrac-tion gaps. Moreover, the densities of the formed regen-erate bone in each group were measured at the proximalends of the osteotomized segments as well as at the cen-ter of the newly formed bone and compared by usingsoftware (Digora for Windows, version 2.5; Soredex).

The tissues were prepared as follows. The mandibularsegments including the fourth premolar, distracted newbone, and the third premolar were dissected en bloc. The

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Fig 2. A, The tooth movement assembly; B, stabilizingthe position of the fourth premolar by ligation with the firstmolar during third premolar retraction.

Fig 3. A, Normal maxillary-mandibular relationship in thecanine model; B, anterior crossbite that developed afterdistraction.

484 El Sharaby et al

specimens were processed according to the method ofCallis.19 After complete decalcification, the specimenswere embedded in paraffin with the conventional tech-nique, and sagittal serial sections, 6 mm thick, werestained with hematoxylin and eosin for examination.

Statistical analysis

The amounts and rates of tooth movement in the 3groups were analyzed and compared by using analysisof variance (ANOVA) followed by Scheff�e post-hoc tests.Statistical significance was established at a P value of0.05.

RESULTS

Throughout this experiment, all animals tolerated thesurgical procedures well, ate without problems, and con-sistently gained weight postoperatively.

During the latency period, 3 cases of wound dehiscencewere observed in 3 animals. No infections were reported,and the dehiscences weremanagedwith oral chlorhexidineirrigation twice daily until complete healing.

In all animals, the area between the distractor and thebuccal mucosa was perceived to be an area of food stag-nation, and it was difficult to maintain good hygiene.

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Accordingly, in some cases (6 of 15 distraction sites; 2in group I, 1 in group II, and 3 in group III), a slight buccalgingival inflammationwas observed at the area of distrac-tion and was managed by oral chlorhexidine irrigationtwice daily until complete resolution of the inflammation.

At the end of the distraction phase, all animals withbilateral mandibular distraction developed increasedprognathism of the mandible compared with the maxilla.The increase in the sagittal body of the mandible con-comitant with distraction accompanied the creation ofan edentulous segment with an average of 9.02 62.42 mm as measured from the tip of the third premolarcrown to the tip of the fourth premolar crown. It was ob-served that in all cases the edentulous alveolar ridge cre-ated by distraction had a saddle-shaped appearance.Furthermore, all dogs with unilateral mandibular dis-traction developed a unilateral mandibular shift to thecontralateral side that was obvious clinically (Fig 3).

With progressive retraction of the third premolars atthe time planned for each group, the teeth were success-fully moved distally about two thirds of the length of thecreated edentulous space, except in group I wherethe teeth moved only about one third of the length ofthe edentulous space. The premolars were distalizedabout 3.65 6 0.95 mm in group I, 9.38 6 2.04 mm ingroup II, and 7.72 6 2.04 mm in group III. The rate oftooth movement was steady over the 8 weeks of the ex-periment in all groups, except in group II where it in-creased in the last 4 weeks of tooth movement. Therates of tooth movement were about 0.46 6 0.12 mmper week for group I, 1.176 0.26 mm per week in groupII, and 0.97 6 0.26 mm per week for group III (Table I).

Journal of Orthodontics and Dentofacial Orthopedics

Table I. Amounts and rates of tooth movement ineach group

Mean 6 SD (mm)

Amount Rate (weeks 0-4) Rate (weeks 4-8)Group I 3.65 6 0.95 0.44 6 0.13 0.48 6 0.08Group II 9.38 6 2.04* 1.07 6 0.25 1.27 6 0.17Group III 7.72 6 2.04* 1.03 6 0.49 0.9 6 0.11

*The rates were significantly greater in groups II and III (P\0.05)than in group I.

Fig 4. Time courses of tooth movements in the groups.


The rates of tooth movement were significantlygreater in groups II and III (P \0.05) than in group I(Fig 4).

In this study, attempts to use rigid sliding mechanicsfor orthodontic tooth movement did not guarantee purebodily movement in all situations. The results of this ex-periment showed severe tipping movements in 3 of 4premolars in group II, with the fourth one showing mod-erate tipping during retraction into the distraction re-generate. On the other hand, all premolars in groups Iand III demonstrated bodily movement, with the excep-tion of 1 premolar in group I that had a severe tippingmovement during retraction into the regenerate bone.

Radiographs taken for the distraction gap after 1week of consolidation (group I) showed sharp demarca-tions of the osteotomy line. The distraction gap ap-peared to be mostly radiolucent with areas ofradiopacities indicating new bone starting to form atthe osteotomized end of the segments proceeding to-ward the center of the distraction gap (Fig 5, A).

After 3 weeks of consolidation (group II), the osteot-omy line started to be less evident with an increase in ra-diopacity of the distraction gap, denoting furtherextension of bone formation (Fig 5, B).

After 6 weeks of consolidation (group III), the distrac-tion gap had a saddle-shaped appearance and was per-ceived to be homogenously radiopaque andindistinguishable from the host bone (Fig 5, C).

When we compared bone density measurementsamong the groups, we found a gradual increase in thebone density of the distraction regenerate concomitantwith the increase in the consolidation period; this inturn reflected the increase in mineralization (Table II).

Radiographic evaluation after tooth movement intothe distraction regenerate in group I showed severe ex-ternal apical and lateral resorption of the distal root ofthe third premolar with loss of the lamina dura. Mean-while, an irregular band of radiolucency was observedat the center of the distraction gap, denoting incompletemineralization of the distraction regenerate at that time.It was noticed that the third premolar maintained an


upright position while moving into the distraction gap.At the same time, moderate to severe crestal bone losswas detected with preservation of the interseptal bone(Fig 6, A).

In group II, there was mild root resorption with pres-ervation of the lamina dura especially in the area of theroot apex. The distraction regenerate was more or lessindistinguishable from the host bone at that time, indi-cating greater regenerate mineralization than in group I.In this group, the tipping type of tooth movement wasmanifested with mild reduction in crestal bone levels(Fig 6, B).

In group III, there was no radiographically detectableroot resorption with preservation of the lamina dura.Similar to group II, the distraction regenerate was indis-tinguishable from the host bone, indicating progressiveregenerate mineralization. In this group, bodily toothmovement was manifested despite the greater distanceof tooth movement than in group I (Fig 6, C).

The histologic appearance of the canine mandiblebones was normal (Fig 7). The control bone biopsy sam-ple showed regular lamellar structure with well-developed interstitial lamella and haversian canaliculi.Additionally, organized osteon structures were observedin the section with multiple trapped osteocytes in calci-fied matrix. Neither osteoclasts nor osteoblasts were ob-served in the haversian canaliculi. On the other hand,some medium-sized vessels were detected.

Examination of the histologic appearance of the dis-traction regenerate in group I (Fig 8) showed a gap filledwith fibrovascular tissue comprising most of the totalregenerate area and organized as centrally arrangedcollagen bundles with interspersed vascular channels.No evidence of cartilage tissue was seen in the distrac-tion gap. On the other hand, there was some evidenceof new bone formation as small areas of bone trabec-ulae at the host bone margins oriented parallel to thedirection of distraction with widely interspersed bone


Fig 5. A,Radiograph showing the distraction gap after 1 week of consolidation;B, radiograph showingthe distraction gap after 3 weeks of consolidation; C, radiograph showing the distraction gap after 6weeks of consolidation.

Table II. Bone density measurements of the distrac-tion regenerates in the groups

Proximal end Central area Distal endGroup I 155.77 145.02 156.33Group II 163.31 156.78 158.85Group III 176.30 167.19 176.30


marrow spaces. Furthermore, the upper border of thedistraction regenerate displayed the typical saddle-shaped appearance that was evident both clinicallyand radiographically.

The histologic appearance of the distraction regener-ate in group II (Fig 9) showed more progression towardmaturation with marked reduction in the dimension ofthe fibrous interzone; it was wider at the upper than atthe lower part of the regenerate. The newly formedbone maintained the parallel orientation of trabeculaeto the direction of distraction, particularly near the lowerborder adjacent to the inferior cortex.

The newly formed bone appeared more mature andless vascularized than that in group I. Small islands ofcartilage tissue were observed in the subapical regionof the distraction regenerate close to the inferior alveolarcanal. The chondrocytes of this cartilage tissue were ar-ranged in an irregular pattern with no clearly definedcellular orientation.

There was no significant difference in osteogenesisbetween the proximal and distal segments of the mandi-ble. On the other hand, bone regeneration seemed to bemore pronounced in the lower portion compared withthe upper part of the mandible.

The histologic appearance of the distraction regener-ate in group III (Fig 10) showed further progression to-ward maturation accompanied by completeobliteration of the fibrous interzone with newly formedbone trabeculae interspersed with wide marrow spaces.

At this stage, a network of thin trabeculae of newlyformed nonlamellar bone was observed. These trabeculaeoccupied most of the distraction gap and did not displaythe parallel arrangement to the distraction vector. Thenewly formed trabeculae were lined by osteoblasts ar-ranged in a palisading manner and were laying downan osteoid matrix. On the other hand, moremature lamel-lar bone was found near the lower border of the mandiblewith no evidence of cartilage tissue at this stage.


The histologic appearance of the periodontal struc-tures of the third premolar of the canine model beforeattempting tooth movement was normal (Fig 11).

The histologic sections showed the alveolar processformed of 2 types of bone: bundle and lamellar. Fibersof the periodontal ligament were attached to the bundlebone. It was perforated by many foramina transmittingnerves and blood vessels to the periodontal ligament.Next to the bundle bone was a thick layer of lamellarbone with some of its lamellae arranged parallel to the sur-face of adjacent marrow spaces, whereas others formedosteons that were arranged around the haversian canals.The canals contained 1 or 2 small blood vessels andwere connected with each other and with the free surfaceby transverse or horizontal channels (Volkmann’s canals).

The periodontal ligament fibers appeared to beformed of well-arranged collagen bundles. Wide inter-stitial spaces were obvious between the fibers’ bundles,where blood vessels, lymph vessels, and nerves werelocated surrounded by loose connective tissue.

We studied the histologic appearance of the peri-odontal structures of the third premolar of the caninemodel after tooth movement into the regenerate bone.

In group I on the pressure side (Fig 12,A), severe rootresorption extending into the dentin reducing its thick-ness to more than half of normal was seen. Areas ofgranulation tissue appeared in the direction of the mov-ing tooth with multiple resorption lacunae appearing onthe surface of the neighboring bone trabeculae denotingextensive osteoclastic activity.


Fig 6. A, Periapical radiograph showing tooth movement into the distraction regenerate in group I (no-tice the amount of external apical and lateral root resorption); B, periapical radiograph showing toothmovement into the distraction regenerate in group II (notice tipping of the tooth while moving into thedistraction regenerate); C, periapical radiograph showing tooth movement into the distraction regener-ate in group III (notice the bodily movement of the third premolar with no radiographically detectableroot resorption and injury of the fourth premolar root during the osteotomy).

Fig 7. A,Photomicrograph showing the normal histologicappearance of the canine mandible bone (hematoxylinand eosin staining; 1X); B, the same photomicrographwith higher magnification showing the regular lamellarstructure with well-developed interstitial lamella (IL) andhaversian canaliculi (H) and organized osteon (O) struc-tures in some areas (hematoxylin and eosin staining;magnification, 100 times).

Fig 8. A, Photomicrograph showing the histologic ap-pearance of the distraction regenerate after 1 week ofconsolidation, demonstrating the classic 3 zonal regener-ate with fibrous interzone (FIZ) bounded on either side byareas of bony trabeculae (BT) originating from the hostbone (HB) margins (arrows refer to screw positions) (he-matoxylin and eosin staining; 1X);B, higher magnificationshowing the newly formed bone trabeculae arranged inthe direction of tension with osteoblastic rimming of themargins (arrow) (hematoxylin and eosin staining; magni-fication, 100 times).


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Fig 9. A, Photomicrograph showing the histologic ap-pearance of the distraction regenerate after 3 weeks ofconsolidation demonstrating the classic 3 zonal regener-ate with more than a 50% reduction in the size of the fi-brous interzone (FIZ) (arrows refer to previous screwpositions) (hematoxylin and eosin staining; 1X); B, highermagnification showing areas of endochondral bone for-mation located close to the inferior alveolar canal (hema-toxylin and eosin staining; magnification, 100 times).

Fig 10. A, Photomicrograph showing the histologic ap-pearance of the distraction regenerate after 6 weeks ofconsolidation and the complete disappearance of thefibrous interzone, which was replaced by newly formedbone trabeculae (hematoxylin and eosin staining; 1X);B, higher magnification showing the network of newlyformed trabeculae of nonlamellar bone with osteoblastsarranged in a palisading manner (hematoxylin and eosinstaining; magnification, 100 times).


The periodontal ligament showed fewer vascularchannels and was more or less uniform in thicknesswith widespread disarrangement of its fibers.

On the tension side of group I (Fig 12, B), widening ofthe periodontal ligament was observed with stretchingof the fibers in the direction of tooth movement. Noresorption lacunae or infrabony defects were observed.

In group II (Fig 13,A and B) on the pressure side, nar-rowing of the periodontal ligament with an irregular


arrangement of fibers was seen. Focal areas of resorptionlacunae were observed on both the root surface and theneighboring alveolar bone.

The root resorption extended to the dentin but toa much lesser extent than in group I. Additionally, tissuehyalinization was minimal along the length of the peri-odontal ligament.

The alveolar bone demonstrated the typical scallopedappearance of the multiple osteoclasts lining Howship’slacunae.

In group II on the tension side (Fig 13, C-E), the peri-odontal ligament was wider with its fibers stretched in


Fig 11. A, Photomicrograph showing the normal histologic appearance of the periodontal structures ofthe mandibular third premolar before tooth movement (hematoxylin and eosin staining; 1X); B, photo-micrograph showing the normal arrangement of the periodontal ligament fibers (PDL), Sharpey’s fibers(arrow), cememtum (C), and alveolar bone (A) (hematoxylin and eosin staining; magnification, 100times).


the direction of tooth movement. Additionally, increasesin the numbers of both fibroblasts and osteoblasts wereobserved.

New bone trabeculae were observed in the form ofspecules projecting in the direction of tooth movement.The newly formed trabeculae were lined with osteoblastsarranged in a palisading manner, denoting active boneformation.

In group III on the pressure side (Fig 14, B), similar tothe observations in group II, an irregular arrangement ofthe periodontal ligament fibers was observed.

Limited focal areas of resorption lacunae were seenon both the alveolar bone surface and the root, whereit was limited to the cementum.

In group III on the tension side (Fig 14, A), wideningof the periodontal ligament was evident with newlyformed bone trabeculae at the area of bifurcation pro-jecting in the direction of tooth movement. The boneapical to the moving tooth was perceived to be maturelamellar bone with wide marrow spaces.


DISCUSSION

In clinical orthodontics, DO has been applied formandibular advancement and widening. The interdentalgap created after osteodistraction when the osteotomy ismade in a tooth-bearing area could be reconstructedeither orthodontically by moving teeth or prostheticallyby placing an implant into the newly formed bone.

Several clinical and experimental studies have beenconducted to prove the feasibility of moving teeth intobone regenerate created after DO. These studies haveevolved into a relatively well-established protocol forsuch procedure. Yet, the optimum timing for movingteeth into the regenerate bone is still a matter of debate.

In our study, dogs were chosen as the experimentalmodel, since the canine mandible was reported to bethe most appropriate model when DO will be accompa-nied by an orthodontic procedure.20 The area of thebody of the mandible between the third and fourth pre-molars was chosen as the site for the osteotomy because


Fig 12. A, Photomicrographs showing extensive root resorption in the dirction of tooth movement ingroup I (hematoxylin and eosin staining; magnification, 40 times); B, photomicrographs showing wid-ening of the periodontal ligament on the tension side in group I (C, cememtum; B, alveolar bone; PDL,periodontal ligament) (hematoxylin and eosin staining; magnification, 100 times).


it is free from occlusion; hence, this decreased any over-load from the bite on the distraction device or the mov-ing tooth. The area in the midline of the mandible(mandibular symphysis) was avoided because it was re-ported to be an area of dense fibrous tissue that couldinterfere with the distraction process.21

The amount of distraction achieved was measuredfrom the tip of the third premolar crown to the tip ofthe fourth premolar crown. Additionally, a mark on thecanine—stable because of its inherently long roots—was used as a reference point for measuring the amountand rate of third premolar movement into the distractionregenerate.

In this study, an intraoral distraction device was ad-vocated over an extraoral one. Extraoral devices, despitehaving the advantage of controlling the vector duringthe distraction phase, were criticized for problems suchas pin-tract infection and high risk of traumatic dis-lodgement of the pins.14,22 Moreover, a bone-borne dis-tractor was favored over a tooth-borne one because thelatter can allow a greater amount of dental or dentoal-veolar than skeletal expansion.14,23-27

The stiffness of the fixation system is an importantparameter in achieving clinical success.2 Hence, fixation


stiffness of the device in this study comparable to otherstudies was enhanced by using 6 titanium bone screws(11 mm) for bicortical fixation.4,12,27

The sample was divided into 3 groups with toothmovement into the distraction regenerate initiated aftercessation of distraction device activation at 1, 3, and 6weeks, respectively. In most clinical studies where thedistraction was performed in a tooth-bearing area, con-solidation periods of at least 8 to 12 weeks have been ad-vocated before attempting tooth movement into thenewly formed bone.5-14 On the other hand, fewerstudies have reported successful early tooth movementinto the distraction regenerate with no periodontalproblems or postoperative complications.4,15-18,28

According to Conley and Legan,29 early tooth move-ment into the gap created by DO can lead to periodontaland bony defects in addition to potential loss of at least1 tooth.

Several studies have reported the use of radiographsfor evaluating the formed regenerate without mention-ing a technique for standardization.4,27,28 In our study,regenerate bone density was evaluated and comparedamong the groups by using standardized digitalradiography. The obtained radiographic images were


Fig 13. A, Photomicrograph showing the histologic appearance of the periodontal structures of thethird premolar in group II while moving into the distraction regenerate (pressure side) (hematoxylinand eosin staining; 1X). Arrow indicates direction of tooth movement; B, higher magnification showingthe resorption lacunae on both the root (R) and the alveolar bone (A) (hematoxylin and eosin staining;magnification, 100 times); C, photomicrograph showing the histologic appearance of the periodontalstructures of the third premolar in group II while moving into the distraction regenerate (tension side)(hematoxylin and eosin staining; 1X). Arrow indicates direction of tooth movement; D, higher magnifi-cation showing the stretched periodontal ligament fibers and the newly formed trabeculae in the direc-tion of tooth movement (hematoxylin and eosin staining; magnification, 100 times); E, highermagnification showing the newly formed bone trabeculae lined with osteoblasts and projecting in thedirection of tooth movement (hematoxylin and eosin staining; magnification, 400 times).


analyzed with the Digora software to eliminate anyprocessing variables.

In this study, all dogs developed an anterior cross-bite as the mandibular distal segments were


distracted anteriorly. The average length of the eden-tulous segment created by 12 mm of device activa-tion was 9.02 6 2.42 mm, which was comparablewith other studies.4,24,27,30


Fig 14. A, Photomicrograph showing the histologic appearance of the periodontal structures of the thirdpremolar in group III while moving into the distraction regenerate (hematoxylin and eosin staining; 1X).Arrow indicates direction of tooth movement;B, higher magnification showing the resorption lacunae (ar-rows) on both cementum (C) and bone (B) (hematoxylin and eosin staining; magnification, 100 times).


Saddle-shaped depressions of the alveolar ridge wereseen where new bone was created. The saddle-shapeddepression might be due to contraction of the fibrocel-lular tissue formed at the early stages of regenerate for-mation to the center of the distraction gap before itbecame completely mineralized. Similar findings havebeen demonstrated in other studies.24,26,27,31

Radiographic analysis of the distraction gap in the 3groups showed increasing radiodensity, reflecting grad-ual bone formation and mineralization. These results arein accordance with those of other studies.4,24,27,30,32,33

In this study, rate of tooth movement, type of toothmovement, root resorption, and adverse tissue effectswere the main parameters used to determine the opti-mum timing for initiating tooth movement into boneregenerate after DO.

The average rate of orthodontic tooth movement ofthe dog premolar in nondistracted bone was reportedto be 0.3 mm per week regardless of the amount of forceapplied.34 In our study, the rates of orthodontic toothmovement into the distraction regenerate were about0.46, 1.17, and 0.97 mm per week for groups I, II, andIII, respectively, with a significant difference betweengroups I and II. The faster rate of tooth movement ingroup II compared with the other groups could be due


to the emergence of osteoclasts in the calcified callus 2weeks after distraction as reported by Maffuli andFixsen35; this could have promoted bone resorption inthe direction of the moving tooth.

Despite the rigid sliding mechanics we used, a tippingtooth movement was evident in group II compared withbodily movement in the other groups. The possible rea-son for that might have been the faster rate of toothmovement in group II aided by the reduced resistanceof the distraction regenerate at that time. These resultsagree with those of Nakamoto et al,27 where a tippingmovement was reported despite the use of similar slidingmechanics for tooth movement.

Tooth movement into the distraction regenerate wasassociated with distal or apical resorption of the thirdpremolar root. To accurately compare the degree ofroot resorption between the 3 groups, a scale for evalu-ation was set with a plus sign for resorption limited tocementum only, 2 plus signs for resorption of less than50% into dentin, and 3 plus signs for resorption ofmore than 50% into dentin. Statistical analysis of thedata with the Kruskal-Wallis test showed that group Ihad significantly more root resorption than did groupsII and III. There was no significant difference betweengroups II and III, suggesting decreases in root resorption


Table III. The degree of root resorption in the groups

Factor Group I Group II Group III P value*Root resorptionmedian 31(a) 1.51(b) 11(b) 0.029

2-3 1-2 1-2

*P values#0.05 were considered significant. Groupmedians sharingthe same letter were not significantly different from each other.


with the increasing consolidation period (Table III). Copeet al4 reported focal regions of irregular root surface areasuggesting possible root resorption when teeth weremoved into the distraction regenerate after 1 week ofconsolidation.

Nakamoto et al27 reported root resorption extendinginto the dentin of the moving teeth in both experimentalgroups regardless of the timing of starting tooth move-ment into the distraction regenerate. They suggested 3possible explanations for this root resorption. The firstwas that a greater force magnitude (100 g) for a longtime (3 months) was used during tooth retraction com-pared with other experiments.16,28 The secondexplanation was the expression of growth factorsincluding transforming growth factor, insulin-likegrowth factor, and bone morphogenetic proteins inthe bone regenerate after distraction and during theconsolidation period. They added that these growth fac-tors were important regulators of bone formation thatput the distraction regenerate in an active state of re-modeling with a high turnover rate, thus inducingboth bone and root resorption. The third explanationwas that tooth movement continued in their study untilthe animals were killed, hence impeding any possibilityfor subsequent repair during the experimental period.

Histologic evidence published regarding the opti-mum time for initiating tooth movement into regeneratebone created after DO was controversial. Some studiesdemonstrated the possibility of early tooth movementinto the distraction regenerate,4,16-18,28,36 whereasothers emphasized the importance of waiting for atleast an 8 to 12 week consolidation period.5-14

However, our radiographic and histologic findings,supported by other studies, showed that tissue reactionwas most favorable when tooth movement started 6weeks postdistraction, and that early tooth movementinto the regenerate bone is not advisable.26,27,30

The coincidence of our radiographic and histologicfindings is of great significance to clinicians. Increasedradiodensity of the distraction regenerate concomitantwith bone maturation and mineralization was confirmedby histologic analysis. Consequently, radiographic ex-amination of the distraction regenerate can be relied


on for determining the suitable timing for initiatingtooth movement into the distraction gap.

CONCLUSIONS

Based on these results, early tooth movement intothe distraction regenerate is not recommended becauseit could result in adverse effects to the roots and thesupporting structures of the moving teeth. Radio-graphic examination of the distraction regenerate isadvisable and should be used as a guide before initiat-ing tooth movement.

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tooth movement into distraction regenerate: when should we start?

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