Manipulating the Mandibular Distraction Site at Different Stages of Consolidation

J Oral Maxillofac Surg 65:840-846, 2007

Manipulating the Mandibular Distraction Site at Different Stages of Consolidation Shang Wei, DDS,* Miriam Scadeng, MD,† Dennis Duke Yamashita, DDS,‡ Harvey Pollack, MD,§ Omar Faridi, BA,¶ Binh Tran, BA,储 Charles Shuler, DMD, PhD,# and Stephen Yen, DMD, PhD** Purpose: The purpose of this study was to define optimal timing and conditions for correcting an open

bite side effect by manipulating the distraction site with orthodontic springs after mandibular distraction. Materials and Methods: At 0, 1, 2, 3, and 8 weeks postdistraction, interarch springs were attached for 2 weeks to close distraction-produced open bites in 45 rabbits. Distractors were removed in half of the animals receiving spring treatment. Segment position was recorded by weekly direct measurements and radiographs. Tissue samples were collected at the end of spring application for microcomputerized tomography analysis and measurements of lateral symmetry. Results: Orthodontic springs closed the open bite with or without distractors in place immediately after distraction and partially corrected the bite at later stages of bone consolidation. Distractor removal produced more rapid bite closure but also introduced lateral buckling of the distraction site during early consolidation. The lateral buckling was not observed if springs were applied after 2 weeks of consolidation. The amount of bite correction with orthodontic springs correlated with mineralization of the distraction site. Conclusion: During the consolidation period, a distraction site can be callus manipulated with orthodontic springs to correct an open bite. The amount of correction depended on when springs were placed and whether distractors were removed at the time of spring application. © 2007 American Association of Oral and Maxillofacial Surgeons J Oral Maxillofac Surg 65:840-846, 2007 Distraction osteogenesis is a technique for lengthening bone by the gradual separation of bony ends in a healing fracture callus and has been used to lengthen mandibles in patients with congenital deformities. Individual variations in occlusal forces, muscle pull, skeletal anatomy, and bone thickness can make a mandibular distraction procedure difficult to control. Mandibular distraction requires continual adjustments in different planes of space to maintain the intended

direction of lengthening. The result of poor control or unexpected interferences (muscular, soft tissue, dental) can be a poor occlusion or an inability to close the mouth. In order to compensate for problems that occur during lengthening, orthodontic elastics or springs can be used to guide the distracted segment back into an occlusal position by placing elastics from the unoperated maxilla to the distracted mandibular segment (Figs 1A,B). We reported that guiding springs 储Orthodontic Resident, St Louis University, St Louis, MO.

*Formerly, Visiting Scholar, Center for Craniofacial Molecular Biology, Childrens Hospital Los Angeles, Los Angeles, CA; and Currently, Chairman, Oral and Maxillofacial Surgery Department, Affiliated Medical College, Qingdao University, Shandong, China. †Formerly, Research Associate, Department of Radiology, Childrens Hospital Los Angeles, Los Angeles, CA; and Currently, Assistant Professor, Department of Radiology, School of Medicine, University of California, San Diego, San Diego, CA. ‡Chairman, Department of Oral and Maxillofacial Surgery, University of Southern California, Los Angeles, CA. §Formerly, Research Associate, Department of Radiology, Childrens Hospital Los Angeles, Los Angeles, CA. ¶Oral and Maxillofacial Surgery Resident, University of Southern California, Los Angeles, CA.

#Director, Center for Craniofacial Molecular Biology, University of Southern California, Los Angeles, CA. **Assistant Professor, Center for Craniofacial Molecular Biology, University of Southern California, Los Angeles, CA; and Director, Craniofacial Orthodontics, Childrens Hospital Los Angeles, Los Angeles, CA. Address correspondence and reprint requests to Dr Yen: Center for Craniofacial Molecular Biology, University of Southern California School of Dentistry, CSA 103, 2250 Alcazar Street, Los Angeles, CA 90033; e-mail: [email protected] © 2007 American Association of Oral and Maxillofacial Surgeons

0278-2391/07/6505-0003$32.00/0 doi:10.1016/j.joms.2005.10.037

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A

B

g g g rin in ing p rin pr p spr p s up p s s p T0 gro T1 rou T2 rou T3 rou g g g

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1 wk

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Latency (1 wk)

Distraction Period (total of 2 wks)

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2 wk

3 wk

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g rin p s p T8 rou g

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Consolidation Period (total of 8 wks)

FIGURE 1. Rabbit model. A, 8-mm open bite produced by bilateral mandibular distraction. B, Closure of open bite by 8-oz vertical springs. Experimental timetable; arrows indicate when springs were added. Wei et al. Manipulating the Mandibular Distraction Site. J Oral Maxillofac Surg 2007.

or elastics caused a bending of the distraction site,1,2 a phenomenon also called “callus molding.”3,4 A guiding movement by orthodontic elastics can produce 3-dimensional repositioning of osteotomized segments and improve distraction outcomes.5-9 However, the time period for intervening with orthodontic elastics and springs has not been established, and the relationship between segment stability and molding has not been studied. Recent prescriptions for manipulating a distraction callus by removing the distractors at the time of elastic placement10,11 raised a clinical dilemma. It was not known whether the unsupported distraction site would behave like an unreduced fracture site and cause fibrous union or nonunion. This study was undertaken to define the optimal conditions for redirecting a distraction procedure with orthodontic springs or elastics.

Materials and Methods Forty-five young New Zealand White (NZW) rabbits (7.5 lbs) underwent bilateral mandibular distraction using a previously published protocol1,2 approved by the Institutional Animal Care and Use Committee at the University of Southern California (Figs 1A,B). The NZW rabbit was large enough to produce an 8-mm anterior open bite by altering the position of 4 distractor screws. Animals were randomly assigned into

3 groups of 15 animals (spring activation, spring activation with distractor removal, control without springs). Each group was subdivided into triplicate animals for 5 time points when orthodontic springs would be applied. Eight-ounce nickel titanium springs were attached for 2 weeks at the end of distraction, 1, 2, 3, and 8 weeks of consolidation. Sham controls were distracted without springs. To help animals adjust to their changing bite, each animal was hand fed for 20 minutes with a water-softened pellet mix during distraction and spring correction. SURGERY AND DISTRACTION

Bilateral osteotomies were made perpendicular to the occlusal plane in the midmolar region. To produce a skeletal open bite during mandibular lengthening, the distractor was attached 30 degrees to the occlusal plane to allow the anterior segment to rotate inferiorly as the segment was lengthened.1,2 Elizabethan collars were used to prevent dislodgement of the distractors. Vertical springs were attached between the anterior maxilla and mandible using a wire that was inserted through the alveolar bone between the incisors with a spinal needle. After a latency period of 1 week, the distractors were lengthened 1 mm/day for 2 weeks. Nickel titanium springs were ligated at 8 oz of tension as measured by a tension gauge at 0, 1, 2, 3, and 8 weeks after distraction was completed.

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Amount of open bite correction when 8 oz. springs were applied at different times.

Bite Opening (mm)

To

T1

T2

T3

T8

Previous work indicated that 8 oz of spring force could close an 8-mm anterior open bite within 10 days during distraction.1,2

8

INTRAORAL MEASUREMENTS

4

0

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4

weeks Consolidation

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2 months w/ distractors w/out distractors sham control

FIGURE 2. Changes with bite opening at different times of spring application. (TO) Applying springs immediately after distraction was stopped. (T1) Springs applied after 1 week of consolidation. (T2) Springs applied after 2 weeks of consolidation. (T3) Springs applied after 3 weeks. (T8) Springs applied after 8 weeks of consolidation. The bite opening of sham controls with distractors in place did not change with time. Wei et al. Manipulating the Mandibular Distraction Site. J Oral Maxillofac Surg 2007.

Open bite measurements were recorded prior to surgery, prior to spring application, and after each week of spring application. All rabbits were sedated for open bite measurements, photographs, and radiographs (lateral and basilar radiographs). Overbite was measured from the gingival margins because the incisors were continuously erupting (Fig 2A). Basilar films of the mandible were taken while the rabbits’ heads were supported with foam supports and surgical tape. To assess lateral deviations, these radiographs were traced using the maxillary midline and zygomatic arches as references for a skeletal midline that bisected the maxilla. Left and right perpendicular distances from the midline were measured to the anterior and posterior borders of tooth-bearing alveolar ridge. Spring tension was checked and adjusted during daily animal feeding. C. MicroCt Scan of Distraction Site Normalized for Host Bone

A.

100

Percent Luminescence

90 80 70 60 50

host bone transition

40

center

30 20 10 0

0 wk

1w k

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Mean luminosity units 75(fibrous center) 117(mineralizing bone) 256(host bone)

B. D. FIGURE 3. Microcomputerized tomography analysis of distraction sites. A, Diagram of sagittal and transverse CT planes. B, Image analysis and quantitation. C, Changes in luminescence with time. Fibrous center and intermediate values were compared as a fraction of host bone values. D, Transverse image showing corticalization of distraction site. Wei et al. Manipulating the Mandibular Distraction Site. J Oral Maxillofac Surg 2007.

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A Early Removal of Distractor

a a’

b b’

B Late Removal of Distractor

FIGURE 4. Measurement of lateral asymmetry. A, Example of perpendicular distances from midline when distractors were removed immediately after distraction was completed and after 3 weeks of consolidation. B, Ratios of measurements on side of midline shift to opposite side (‘). P ⬍ .05 for lateral deviation between experimental groups without distractor and with distractor measurements for T1, T2, but P ⬎ .05 after springs are placed at T3. Wei et al. Manipulating the Mandibular Distraction Site. J Oral Maxillofac Surg 2007.

MICROCOMPUTERIZED TOMOGRAPHY MEASUREMENTS

After 2 weeks of spring application, the animals were euthanized, radiographed, and measured. Mandibular halves were fixed in 10% formaldehyde for 2 days and dehydrated in ethanol. These specimens were scanned using microcomputerized tomography (MicroCT) (ImTek Inc, Knoxville, TN) at 1,000 slices per cm of bone in the sagittal and transverse planes (Fig 3A). Quantitation of the radiodensity of bone was estimated using luminosity values between 0 and 256 grayscale (Photoshop; Adobe Systems Inc, San Jose, CA) for sites in the center of the distraction site, the adjacent host bone, and a site between the center and host bone (Fig 3B). Two calibrated researchers measured 3 different areas of equal pixel size for each site to produce an average luminosity value.

Results SPRING CORRECTION OF OPEN BITE AT DIFFERENT STAGES OF CONSOLIDATION

The control animals were distracted to produce an 8-mm anterior open bite by an inferior rotation of the anterior mandibular segment. None of the control animals were given springs to close the anterior open bite. The 8-mm anterior open bite remained during the consolidation period and did not spontaneously self-correct after 0, 1, 2, 3, or 8 weeks of consolidation. The experimental animals were also distracted to produce an 8-mm anterior open bite but were given vertical orthodontic springs attached to the anterior maxilla and mandible. If distractors were left in place

while the vertical springs were used to close the anterior open bites, there was a difference in how quickly the bite was corrected. When vertical 8-oz springs were applied immediately after distraction, bite closure was rapid, and complete closure was obtained with 2 weeks of spring application. The rate of bite correction slowed as the distraction site consolidated. If the springs were added after the third week of consolidation, only partial correction of the open bite was observed with 2 weeks of spring wear (Fig 3). If the springs were applied after 2 months of consolidation, no measurable change in open bite (⬍ 1 mm) was observed after 2 weeks of spring correction. None of the mandibular specimens showed fibrous union. A second group of experimental animals were distracted to produce an 8-mm anterior open bite. At different times during the consolidation period, springs were added to close the bite. In addition, the mandibular distractors were removed at the time of spring treatment. Removal of distractors allowed vertical bite closure to occur more rapidly than the experimental group with the distractors left in place (Fig 2) at all of the time points during distraction and the consolidation stage of treatment. Although distractor removal appeared to facilitate bite correction with springs, there were additional complications when springs were applied during early consolidation: the distraction site buckled laterally with one side bending in and the other side bending out. The vertical spring pressure also produced malformed and asymmetric mandibles (Fig 4A) with a pronounced shift of the symphyseal midline. Perpendicular line distances to the midline in basilar films showed that the mandibular midline deviated to one side as one side of the mandible buckled inward at the distraction site (Fig 4B, Table 1). The degree of lateral buckling of the distraction site was most pronounced when springs were applied to the unsupported distraction site immediately after distraction (⬎3 mm difference between left and right distances). The buckling of the distraction site and lateral difference in midline were less obvious after 1 week of consolidation, (1.5–3 mm difference) and not observed after 2 weeks of consolidation. MicroCT ANALYSIS OF MANDIBULAR HALVES

The mineralization of the distraction site was monitored by microCT in order to determine whether the mineralization of the distraction site correlated with the observed changes in bite closure with vertical springs. As in tissue histology, the distraction sites mineralized from the host bone toward a fibrous center. Comparisons in luminosity among the 3 sites—center, intermediate zone, and host bone—showed the low-

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Table 1. EFFECT OF EARLY DISTRACTOR REMOVAL ON LATERAL SYMMETRY AS DESCRIBED BY RATIOS OF LEFT/ RIGHT SIDE TO MIDLINE MEASUREMENTS

Mean ⫹ SD Distractor removed A/A’ B/B’ Midline deviation Distractor in place A/A B/B Midline deviation

T0

T1

T2

T3

1.67 ⫹ 0.17 0.67 ⫹ 0.04 8 mm

1.32 ⫹ 0.1 0.8 ⫹ 0.07 4 mm

1.08 ⫹ 0.03 0.98 ⫹ 0.4 ⬍1 mm

1.02 ⫹ 0.3 0.97 ⫹ 0.4 ⬍1 mm

0.97 ⫹ 0.04 1.0 ⫹ 0.07 ⬍1 mm

0.98 ⫹ 0.1 0.99 ⫹ 0.1 ⬍1 mm

1.02 ⫹ .03 0.97 ⫹ .02 ⬍1 mm

0.98 ⫹ 0.03 1.05 ⫹ 0.07 ⬍1 mm

Abbreviations: T0, distractors removed immediately after distraction; T1, distractors removed at 1 week on consolidation; T2, distractors removed at 2 weeks of consolidation; T3, distractors removed at 3 weeks of consolidation. Wei et al. Manipulating the Mandibular Distraction Site. J Oral Maxillofac Surg 2007.

est luminosity at the center of the distraction site and the highest luminosity in the host bone, with intermediate values in the intermediate zone of bone. All 3 sites increased in luminosity as the distraction site aged and consolidated. According to the lateral deviation measurements, after 2 weeks of consolidation, the distraction site had consolidated enough to prevent the buckling of the distraction site when distractors were removed and springs were applied. The microCT allowed these distraction sites to be analyzed in different planes of space. In the sagittal view, the fibrous center was only 20% the luminosity of the adjacent host bone at the end of the second week. When the view was rotated 90 degrees and observed in transverse cross sections, a thin wall of outer cortical plate (⬍1 mm) accounted for the 20% luminosity. The different views of microCT images suggest that the faint luminosity observed in the lateral view is actually an image of a thin cortical wall of bone that spans the distraction site. ANALYSIS OF DATA

Bite opening measurements. The 3 groups were compared for differences in bite opening at different time points with a 1-way analysis of variance. The amount of bite closure observed in the spring-treated groups was significantly different from the control group that did not have any bite closure (P ⬍ .01). Additionally, the group with the distractors removed had significantly more bite change than the experimental group with distractors left in place (P ⬍ .05). Luminosity values. With consolidation and aging of the distraction site, 2 observations were noted: a decrease in amount of bite closure per 2-week spring treatment and an increase in luminosity of the center of the distraction site. Bite closure measurements in the spring-treated groups correlated with luminosity values of the distraction site (linear regression analysis

P ⬍ .01; F ⫽ 199.29) during the first 3 weeks of consolidation. Midline deviation measurements. A/A’ and B/B’ measurements estimated right and left lateral deviation from 2 positions (Fig 4A). If the fraction equaled 1, then the 2 sides were symmetric. For each time period (Table 1), multiple Student’s t tests showed a significant difference in lateral deviation only in the group with the distractors removed (P ⬍ .01) during the first 2 weeks of consolidation. After 2 weeks of consolidation, these differences were not observed in any of the groups (P ⬎ .05).

Discussion The use of orthodontic appliances and elastics to assist a mandibular distraction procedure has been advocated by different craniofacial teams. The “floating bone technique” as described by Hoffmeister et al10,11 prescribed the removal of mandibular distractors after 2 weeks of osseous consolidation and the use of interarch orthodontic elastics to correct the anterior open bite. Bite correction was usually followed by several weeks of intermaxillary fixation to maintain the bite correction. Although orthodontic elastic and spring forces have been used to control mandibular distraction procedures, the timing of such interventions has not been studied, and the relationship between callus manipulation and mineralization has not been investigated. This study supports the use of guiding elastic and spring forces to prevent or correct side effects such as an anterior open bite that developed during bilateral lengthening of the mandible. As in our previous studies, an 8-oz vertically applied spring force did not cause fibrous union or nonunion. The amount of correction and rate of bite closure varied according to when this intervention was attempted

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during the consolidation period. A linear correlation between radiographic luminescence and bite correction by orthodontic springs provided a timetable for orthodontic intervention. Complete bite correction was attainable during the first 2 weeks of consolidation, but only partial bite correction was possible at later stages of bony consolidation. We hypothesized that partial mineralization of the distraction site inhibited manipulation of the callus by orthodontic springs. The changes in luminosity values of the distraction center were difficult to interpret if only the sagittal view were used in microCT images. A faint image in the sagittal view later proved to be a thin wall of cortical bone that spanned the distraction site by the third week when observed in a transverse view. A similar thin layer of cortical bone has been observed by our surgeons when distraction sites prematurely consolidate and require surgical release. MicroCT was useful in discovering the thin cortical plate spanning the distraction site, which might have been lost in histology sections or left undetected in 2-dimensional radiographs such as the lateral cephalometric and panoramic radiographs. According to our experiments, Hoffmeister’s prescription of waiting for 2 weeks of consolidation before removing distractors for orthodontic spring corrections represents a narrow window of opportunity for removing distractors while permitting enough lateral stabilization to prevent buckling of the segments. If attempted later, then the bite correction would proceed at a slower rate because mineralization of the cortical plate would limit manipulation of the distraction site. If attempted earlier, then there was a risk of lateral buckling of the distraction site. Hence, callus molding has 2 conflicting requirements: 1) early stabilization of the distraction site to prevent lateral movement and 2) enough flexibility to permit redirection of the distraction process with orthodontic springs. During the second and third week of consolidation, there appeared to be enough stability and flexibility to satisfy both requirements; therefore, this would be the optimal time for using the “floating bone technique.” Alternatively, our experiments indicated that orthodontic springs could be used earlier if the distractors were left in place to stabilize the distraction site. In clinical applications, orthodontic elastics placed bilaterally may serve to prevent some of the lateral buckling observed with anterior springs in our rabbit model. These experiments suggest that once the distraction site is produced, distractors or spring forces can move the distracted segments toward a target position. In the animal model, orthodontic appliances and springs can correct for distractors that

track linearly and along a path that does not lead to complete closure of the bite.6 We extrapolated certain principles of early correction from the animal model to human patients because the rate of bone healing followed the timetable for a young small mandible; however, the timing for manipulating the callus may be modified by other factors such as age, size and density of the bone, which were not examined in this study. In the future, orthodontists may be called upon to finish the mandibular distraction procedure by moving segments into an optimal bite position after bony lengthening is completed. A distraction model in which a distraction site is created and then the segments are guided into position with orthodontic spring forces has been used in several new distraction osteogenesis applications for cleft lip and palate patients.12,13 The biology of redirecting and manipulating a distraction site by orthodontic spring forces is also known as “callus molding.” This phenomenon is not well understood. Luchs et al14 confirmed that bony union occurred after molding of the regenerate. The present study suggests that timing and mineralization of the distraction site determines how much callus manipulation is possible. The mechanism of callus manipulation is likely to be a series of different bone responses that develop as the distraction site mineralizes. Further studies on redirecting a distraction procedure with spring forces are needed to delineate how the callus bends at different stages of mineralization. Acknowledgments This research was supported by a grant from the Oral and Maxillofacial Surgery Foundation and donated surgical screws from KLS Martin. We wish to express our appreciation to Drs Li Wei, Seketu Patel, David Moose, Paul Bohman, Ramtin Vahadi, Daniel Brunner, Alexander Kim, Peter Krakowiak, and Andisheh Afsharpanah for their help in animal surgeries and care.

References 1. Yen SL, Shang W, Shuler C, et al: Orthodontic spring guidance of bilateral mandibular distraction in rabbits. Am J Orthod Dentofacial Orthop 120:425, 2001 2. Yen SL, Shang W, Li S, et al: Bending of the distraction site during mandibular distraction osteogenesis: A model for studying segment control and side effects. J Oral Maxillofac Surg 59:779, 2001 3. Peltomaki T, Grayson BH, Vendittelli BL: Moulding of the generate to control open bite during mandibular distraction osteogenesis. Eur J Orthod 24:639, 2002 4. McCarthy JG, Hopper RA, Hollier LH, et al: Molding of the regenerate in mandibular distraction: Clinical experience. Plast Reconstr Surg 112:1239, 2003 5. Kunz C, Hammer B, Prein J: Manipulation of the callus after linear distraction: A “lifeboat” or an alternative to multivetorial distraction of the mandible? Plast Reconstr Surg 105:674, 2000 6. Yen SL, Gross J, Yamashita DD, et al: Correcting an anterior open side effect during distraction with spring forces. Plast Reconstr Surg 110:1476, 2002 7. Suhr MA, Kreusch T: Technical considerations in distraction osteogenesis. Int J Oral Maxillofac Surg 33:89, 2004

846 8. Politi M, Sembronio S, Robiony M, et al: The floating bone technique of the vertical ramus in hemifacial microsomia: A case report. Int J Adult Orthdon Orthognath Surg 17:223, 2002 9. Grayson BH, Santiago PE: Treatment planning and biomechanics of distraction osteogenesis from an orthodontic perspective. Semin Orthod 5:9, 1999 10. Hoffmeister B, Marks CH, Wolf KD: The floating bone concept in distraction osteogenesis. J Craniomaxillofac Surg 26:S67, 1998 11. Hoffmeister B, Marcks CH, Wolff KP: Intraoral callus distraction using the floating bone concept. Proceedings of the 55th Annual Meeting of the American Cleft Palate-Craniofacial Association, Baltimore, MD, 1998

MANIPULATING THE MANDIBULAR DISTRACTION SITE 12. Yen SL, Yamashita DD, Gross J, et al: Combining orthodontic tooth movement with distraction osteogenesis to close cleft spaces and improve maxillary arch form in cleft lip and palate patients. Am J Orthod Dentofacial Orthop 127:224, 2005 13. Lauwers F, Mayorca-Guiliani A, Lopez R, et al: Maxillofacial intraoral distraction osteogenesis followed by elastic traction in cleft maxillary deformity. Int J Oral Maxillofac Surg 34:85, 2005 14. Luchs JS, Stelnicki EJ, Rowe NM: Molding of the regenerate in mandibular distraction: Part 1. Laboratory study. J Craniofac Surg 13:205, 2002