Distraction osteogenesis of the mandible

Distraction osteogenesis of the mandible

Research; development Distraction osteogenesis of the mandible T. Karaharju-Suvanto 1, ,I. Peltonen 4, A. Kahri 2, E. O. Karaharju a Departments of...

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Research; development

Distraction osteogenesis of the mandible

T. Karaharju-Suvanto 1, ,I. Peltonen 4,

A. Kahri 2, E. O. Karaharju a Departments of 1Paedodontics and Orthodontics, 2Pathology and 3Orthopaedics and Traumatology, University of Helsinki, and 4The Orthopaedic Hospital of Invalid Foundation, Helsinki, Finland

An experimentalstudyon sheep T. Karaharju-Suvanto, J. Peltonen, A. Kahri, E. O. Karaharju: Distraction osteogenesis of the mandible. An experimental study on sheep. J. Oral Maxillofac. Surg. 1992; 21: 118-121. Abstract. Distraction bone healing has been studied in long bones but there are only few experiments reported in relation to the mandible. The histological pattern of the healing process after m a n d i b u l a r distraction is described. After osteotomy the mandibles of 17 growing sheep were lengthened by gradual distraction using an external fixation device. The follow-up varied from 0 to 52 weeks. The results indicate that bone healing in mandibles is principally the same as in long bones. Four phases can be observed during the repair process: 1) formation of collagen aligned in the direction of distraction, 2) bone formation over the collagen template, 3) bone union across the distraction gap, and 4) remodelling of the lengthened segment. Some increased osteoblast activity was also seen in the control side.

Accepted for publication 21 December 1991

Distraction of long bone fragments after osteotomy results in bony healing and consolidation of the lengthened segment 13. Distraction bone healing apparently is a specific repair process which differs from callus formation or direct osteonal (primary) bone healing 7. According to ILIZAROV5'6 the quality and quantity of the new bone depends u p o n 4 main factors: 1) the rigidity of the fixation, 2) the degree of damage to the bone marrow, periosteal soft tissues and blood supply, 3) the rate of distraction, and 4) the rhythm of distraction. Studies concerning the application of the distraction principle on mandibles have been few, and, at least to our knowledge, only experimental studies have been performed. SNYDER et al. 14 were the first to examine the lengthening of mandibles in dogs, proving that the idea of bone lengthening can be applied to the mandible. MICHIELI & MIOTT111 used an orthodontic type of lengthening appliance in dogs and first reported histological changes and showed that collagen fibers align according to the distraction force. KARP et al. 9 also used dogs and histologically showed that the newly formed bone was less organized and had larger vascular channels compared to the nonoperated side. COSTANTINO et al. 4 reported that newly formed bone close to

drilled into the ascending ramus. An incision was made at the mandibular angle and the masseter muscle was stripped off. Using the external fixation frame as guide the 2 remaining half-pins were fixed to the angle of the mandible. A horizontal bone cut was made in the middle of the ascending ramus using an oscillating saw while trying to preserve as much of the periosteum as possible (Fig. 1). During this procedure cooling was achieved with sterile saline solution. The frame, which was developed for this experiment, was applied to fix the osteotomy in neutral position. The incision was closed in layers. The animals were given procain penicillin 300 000 i.m. after the operation and for 3 consecutive days. After the operation the animals were able to eat normally and as sheep are ruminate animals strong biting forces were conducted to the frame. After 5 days of neutral fixation, gradual distraction was started at a rate of 0.5-1.0 mm/day which was continued for 4-16 days. After the distraction period the device was kept in place for a period similar to the distraction time. On removal of the frame the stability of the mandibles was clinically tested. The animals were killed up to 1 (5 sheep), 5 (4 sheep), 20 (4 sheep), 35 (2 sheep) and 52 (2 sheep) weeks after distraction. Some animals in Group 1 were killed already during the distraction period. The heads of the sheep were sawn in a mid-sagittal plane. Thereafter, the mandibles were harvested preserving the periosteum. The distraction areas were identified and cut and divided along the long axis (Fig. 2). Half of the area was fixed in buffered formaldehyde for conventional histology and

the end of the gap was more calcified and that the regenerated bone was less dense and more cellular and vascular than in the non-operated side. KARAHARJU-SUVANTO et al. 8, using sheep, documented the roentgenological healing pattern. They observed that the beginning of bone healing could be noticed already at the end of the distraction period and that bone u n i o n was achieved in all cases 16 weeks after the distraction period. The purpose of this study was, histologically, to evaluate bone regeneration after distraction of the mandible. The osteogenesis at the early distraction phase, during distraction, and the bone structure after long-term follow-up, were studied.

Material and methods A total of 17 growing sheep aged 13.5 to 19 weeks, weighing 15-34 kg, were used as experimental animals. Anesthesia for the operation included a ketamin-domitor combination which is widely approved for this kind of operation. Preoperatively, the animals fasted for 2 days. For anesthesia they were given intravenously 25 /~g/kg Domitor® (medetomin hydrochlorid, L~i/ikefarmos Oy) and 1 /~g/kg Ketamin® (Ketamin hydrochlorid, Parke-Davis Oy). Two self-drilling, self-tapping half-pins 1.6 mm in diameter (Howmedica Apex) were

Key words: mandible; distraction bone healing; bone lengthening; external fixation.

Distraction osteogenesis o f the mandible

Fig. 1. The osteotomy line (A) and half-pin (B) and the frame (C) in ramus of the sheep mandible. the other half was preserved for further studies. The bone specimenswere decalcified in 10% formic acid, embedded in paraffin, cut into sections and stained with hematoxylin and eosin, van Gieson and alcian-blue. The sections were also examined under polarized light microscopy. The non-operated side of the mandible was used as control. Results

In all animals in which the distraction procedure was completed (i.e. distraction period and healing period) the mandibular gap had healed resulting in solid bone. A superficial pinhole infection was observed in 13% of the pinholes but no pseudoarthrosis or delayed union were seen. In the living animals when the frame was removed all the mandibles were clinically stable. During the first week (5 sheep) after distraction, the gap between the bone ends appeared to contain fibroblasts and collagen bundles, which were for

the most part aligned in the direction of the distraction (Fig. 3). Non-organized connective tissue and solitary islands of cartilaginous cells were also seen. Bone formation had already started in some specimens and in these a layer of osteoblasts was seen lining the thin stripes of of newly formed bone. The control side showed normal lamellar bone. Up to 5 weeks (4 sheep) new bone was seen from the bone margins towards the centre of the gap, where the collagen bundles formed a frame for the new bone across the distraction gap. The direction of the bundles was longitudinal in the direction of the distraction (Fig. 4). Separate cartilage cells and islands were also seen (Fig. 5). In some specimens the distraction line was no longer visible. In some control samples the periosteum appeared thicker, with many osteoblasts, indicating active bone formation in contrast to the control specimens of the first week. Up to 20 weeks (4 sheep) the distraction gap was mostly filled with bone and the centre of the gap was closed and in most cases no longer visible. The periosteum was in some cases thickened and there was active bone formation. In the control side the periosteum was thickened in all cases but no active bone formation was noted as only a few solitary osteoblasts were seen. At 35 weeks (2 sheep) the bone union was complete and the remodelling had started. The distraction gap was no longer visible and the periosteum appeared normal in both specimens. Osteoclasts were seen in the area, indicating an active remodelling process. At 52 weeks (2 sheep) the bone in the operated side resembled the control side with only few solitary isles of connective tissue inside the bone. Discussion

Even though distraction bone healing has been widely studied in long bones, studies of the mandible have been few and experimental. In a previous study it

Fig. 2. Sampling technique: the distraction gap was first cut off. Then the gap was sawn longitudinally and half of the section preserved for histological studies in buffered formaldehyde (A).

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Fig. 3. In this picture taken in polarized light the collagen bundles (arrow) are oriented according to the direction of distraction in the central part of the gap. Alcian-blue staining, original magnification x 175.

was shown that the pattern of radiological healing in mandible resembles that of tubular bone lengthening8. Similarities between the mandibles of humans and sheep have been studied by BOSANQUET • GOSS3. The sheep mandible is large enough for adequate insertion of external pin fixation. The experiment was carried out in growing animals, as the system might be applicable in growing patients. In this model distraction was applied by an external device attached to the mandible with 4 half-pins. MICHIELI & MIOTTIH used a frame that was fixed to the teeth and was thus more like an orthodontic appliance. SNVD~R et al. TM used an external fixation frame with 2 pins. KARP et al. 9 and COSTANTINOet al. 4 used different kinds of external fixation devices with 4 pins. The device used provided adequate stability for successful lengthening and allowed for easy daily distraction. The external fixation device with 4 half-pins appeared to be a good alternative for mandibular distraction. The ketamin-domitor anesthesia, which is generally accepted for this kind of operation, appeared to be adequate. The animals showed no signs of pain during the operation and no visible side effects after wakening.

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}Fig. 4. The new bone (A) forming according to the collagen template (B). Alcian-blue staining, original magnification x 375.

When performing the osteotomy we endeavoured to preserve as much of the periosteum as possible so as not to disturb its osteogenic potential in the distraction area 5,1°.Although sawing the mandible destroyed part of the periosteum, it did not appear to affect healing since all gaps were healed within 16 weeks after the distraction. In the studies on long bones it has been emphasized that an intact intramedullary blood circulation is essential to allow bone regeneration after lengthening5. In this study the vessels inside the bone were cut; however, this did not appear to affect bone healing. There has been some controversy as to when distraction should commence after the osteotomy. For long bones IHZAROV6 recommends 5-7 days' delay before starting gradual distraction. In mandibular distraction SNYD~R et al. 14 waited 1 week and KARP et al. 9 and COSTANTINO et al. 4 10 days. According to PANIKAROVSKIet al) 2 the optimal time to start distraction is 14 to 21 days. Considering the healing capacity of mandibles2 and the relative young age of the animals a waiting period of 5 days seemed reasonable. Different rates of daily distraction have been reported in earlier studies. The most commonly used rate has been 1 mm/day 4,9,14. In our study the daily distraction was within the limits of 0.5-1 mm/day which has shown to be optimal for long bone lengthening. Even though the amount of daily distraction was less than in most of the studies, no premature closures had occurred. Histologically, it appears that bone healing after distraction in mandibles follows the same pattern as seen after long bone lengthening. Four main

Fig. 5. Cartilage cell island in the distraction gap, Alcian-blue staining, original magnification × 375.

phases in distraction bone healing can be observed: formation of the collagen template, mineralization of the distraction gap, bone union, and remodelling of the lengthened bone segment. In some specimens chondroid tissue was observed in the distraction area for up to 5 weeks. One possible explanation is movement in the distraction gap due to strong biting forces being conducted to the frame. Movement in the distraction area perhaps disturbs the local vascular regeneration, diminishing oxygen tension and changing the bone formation via cartilaginous tissue. Thickening of the periosteum in the control side was seen at 5 5 0 weeks. A possible explanation might be that the forces created by lengthening had affected the control side. The control side returned to normal indicating that remodelling occurred. These histological results support the previously reported radiographic results8. During distraction bone healing the centrally situated radiolucent line corresponded with the collagen area in the middle of the gap. This area has been called "growth zone" of the distraction area I. Although the structure and origin of the long bones and mandible are different, the healing process after bone distraction appears to be similar. The basic reparative events are the same in both bones. Remodelling of the distracted bone segment occurs relatively rapidly, resulting in complete repair. The method described might be clinically applicable for patients with hemifacial microsomia or hypoplastic mandibles although further experiments are needed to establish the best possible technique.

Acknowledgements.. This study was supported by the Sivi/i Kosti foundation, the Paulo foundation and the Academy of Finland.

References

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Address: Terhi Karaharju-Suvanto Vesilinnankatu 27 as 4 SF-O0510 Helsinki Finland