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Mandibular Lengthening by Distraction Osteogenesis: Role of Periosteum and Endosteum
Nuntanaranont, Vongvatcharanon Asian J OralSattayasunskul, Maxillofac Surg 2004;16:21-33. ORIGINAL RESEARCH
Mandibular Lengthening by Distraction Osteogenesis: Role of Periosteum and Endosteum Thongchai Nuntanaranont, Wilad Sattayasunskul, Surapong Vongvatcharanon Department of Oral and Maxillofacial Surgery, Faculty of Dentistry, Prince of Songkla University, Songkhla, Thailand
Abstract Objective: To study the role of the periosteum and endosteum in new bone formation by distraction osteogenesis. Materials and Methods: Twenty four rabbits were divided into 3 groups of perieosteum destruction (group P), endosteum destruction (group E), and a control group (group C). After right mandibular body osteotomy followed by distractor placement, the buccal periosteum in the segment between the second and third screws was removed by scalpel in group P. In group E, the endosteum was scraped out from both bone ends between the second and third screws. In group C, both periosteum and endosteum were preserved during the surgical operation. After a latency period of 3 days, bone lengthening was started at a rate of 1 mm per day for 10 days, after which the newly formed bone was allowed to consolidate for 6 weeks with the device serving as an external fixator. Radiographs were taken at the following time intervals: 2 weeks, 4 weeks, and 6 weeks after completion of distraction and 6 months after consolidation. The animals were sacrificed 6 weeks after completion of distraction and 6 months after consolidation for the gross macroscopic, histological, and radiological examinations and stability measurement of the distracted segment. Results: New bone was generated in all animal groups. The buccal cortex was incompletely formed in groups P and E but was completely formed and indistinguishable in the control group after 6 months. Histologically, the newly formed bone in the control group had a more mature appearance and better organised bone spicules than in groups P and E. In addition the remodelling process occurred more rapidly in the control group. However, quantitative analysis of the newly formed bone by densitometry revealed no statistically significant differences at each time interval among the 3 groups except for a decline in density in the control group after 6 months due to the bone remodelling process. The stability of the regenerated bone of the lengthened segment was best in the control group, with groups P and E showing marked changes in the length of the distracted distance. Conclusion: Although groups P and E exhibited slower new bone maturation, the amount of newly formed bone was equal in all groups. It could be stated that the periosteum and endosteum are probably not indispensable or particularly important for adequate callus formation. This may be due to the rich blood supply of the craniofacial skeleton. However the instability of the segment caused by the slow maturation and remodelling of the newly formed bone in groups P and E should be noted, and a longer consolidation period is recommended to avoid instability of the regenerated segment in such cases. Key words: Distraction osteogenesis, Mandible, Periosteum
Introduction Distraction osteogenesis is a method of producing unlimited quantities of living bone directly from a Correspondence: Thongchai Nuntanaranont, Department of Oral and Maxillofacial Surgery, Faculty of Dentistry, Prince of Songkla University, Songkhla, Hat Yai, Thailand 90110. Tel/Fax: (66 74) 429876; E-mail: [email protected]
Asian J Oral Maxillofac Surg Vol 16, No 1, 2004
special osteotomy by controlled mechanical distraction of the bone segments. The new bone spontaneously bridges the gap and rapidly remodels to a normal macrostructure similar to local bone.1-5 Distraction osteogenesis is a concept of bone lengthening first described by Codivilla in 1905, who used it to elongate a femur by repeated pulling forces.6 However, the technique of bone lengthening by 21
Mandibular Lengthening by Distraction Osteogenesis
gradual distraction was further developed and refined by Ilizarov in 1951.3,7 The use of distraction osteogenesis in the craniofacial skeleton was first reported by Snyder et al who used monofocal distraction to lengthen the mandible in a canine model.8 Successful clinical bone lengthening in craniofacial surgery was first described by McCarthy et al in 1992.9 Since then several clinical reports followed,10-12 and a wide variety of techniques are now available to lengthen bone segments or entire maxillary and mandibular arches.13-16 Recent advances and innovations in surgical techniques and equipment have made bone lengthening by osteodistraction both easier and safer. Many successful clinical cases have been reported,17,18 but only limited information is available regarding the importance of the periosteum and endosteum in the distraction area in relation to the quality and quantity of newly formed bone, especially in the craniofacial region. Ilizarov stated that the degree of damage to the periosteal and endosteal tissue at the time of osteotomy is one of the most critical factors to determine new bone regeneration, and maximum preservation of the periosteal and intraosseous soft tissue should enhance bone formation during limb lengthening by distraction osteogenesis.4 Any damage to the bone marrow in the distraction area inhibits osteogenesis resulting in retarded and poorly formed bone. On the basis of these previous studies on long bone lengthening, osteotomy with protection of the bone marrow during operation has been emphasised, and a carefully limited corticotomy recommended.17-21 Kojimoto et al, in a rabbit tibial model, reported marked disturbance and failure of callus formation when the periosteum was removed during the operation. 22 These researchers concluded that preservation of the periosteum is essential if bone lengthening by callus distraction is to succeed, and this effect is more prominent than with the preservation of endosteal tissue. Although some controversy exists, it seems that the periosteum and endosteum are both important factors for optimal new bone regeneration by 22
distraction osteogenesis. The role of the periosteum and endosteum in new bone formation in long bones was also expected to apply to craniofacial bones, which are membranous in embryological origin. However, a study that confirms this hypothesis in craniofacial osteodistraction is lacking. The majority of reports assessed the results by estimation based on clinical observation or qualitative evaluation.23-25 Craniofacial bones indeed possess different and complex anatomical structures with high vascular supply when compared with long bones. Thus the influence of periosteum and endosteum on new bone regeneration by distraction osteogenesis in craniofacial bones could well be different from long bones. Additionally, in most circumstances, the periosteum and endosteum in the craniofacial area are difficult to preserve during the osteotomy process due to their fine structure and difficult access. In some situations, the recommended limited corticotomy used in long bones cannot be achieved in the craniofacial bone region. The surgical approach to the operation site and complete osteotomy by bone saw or rotary bur inevitably creates mechanical and thermal injury both to the periosteal and endosteal soft tissues. The purpose of the present study was to investigate the effect of periosteal and endosteal soft tissues in and around the distraction area on new bone formation by distraction osteogenesis in craniofacial bones.
Materials and Methods Twenty four healthy male New Zealand white rabbits, aged 5 to 7 months and weighing 3.0 to 3.5 kg, served as experimental animals. The animals were divided equally into 3 groups: a periosteum destruction group (group P), endosteum destruction group (group E), and a control group (group C), in which both periosteal and endosteal soft tissues were protected and preserved. The distraction device used in this study was modified from an orthodontic palatal expansion screw (Hyrax) with the capacity of opening up to 10 mm. The rod ends of the device were bent and soldered to the preformed alloy extension rods with 2 holes on each side. Therefore, each bone segment could be fixed and secured by 2 titanium microscrews (Figure 1). Asian J Oral Maxillofac Surg Vol 16, No 1, 2004
Nuntanaranont, Sattayasunskul, Vongvatcharanon
A
B C Figure 1. Modified distraction device. Abbreviations: A = activator part; B = extension rod; C = fixation holes for micro-titanium screws.
The surgical procedure was performed under aseptic conditions. All animals were anaesthetised with an intramuscular injection of ketamine hydrochloride 25 mg/kg and diazepam 5 mg/kg, repeated if required. Penicillin G sodium 0.5 million units was administered intramuscularly preoperatively. A 2 cm linear incision was made along the inferior border of the rabbit mandible. The body of the mandible was exposed subperiosteally from the anterior region to the antegonial notch. The mental nerve was preserved. The osteotomy cut was made vertically from the area posterior to the mental nerve just anterior to the premolar teeth downward to the lower border of the mandible. Every effort was made to preserve the inferior alveolar nerve running past the osteotomy line. The osteotomy was completed and the mobility of the fragments checked by rotational movement of the osteotome until complete separation was achieved. Before placement of the distraction device, each animal was treated according to its group. For group P, the periosteum lining the bone segments between the second and third screws was removed by scalpel followed by thermal electrocautery. For group E, the endosteum and bone marrow were scraped out of both ends of the bone stumps on either side of the osteotomy, between the second and third screws. For the control group C, both the periosteum and endosteum were preserved during the surgical operation. The distraction device was fixed to the proximal and distal bone stumps using 2 bicortical self-tapping titanium microscrews on each side. The wound was closed in 3 layers leaving the activator Asian J Oral Maxillofac Surg Vol 16, No 1, 2004
Figure 2. The active part of the distractor was left outside the surgical wound.
part of the distraction device outside the surgical wound (Figure 2). Analgesics and antimicrobial medication were given for 3 consecutive days postoperatively. After device placement, distraction was delayed for 3 days, the ‘latency period’. The distractor was activated to separate the bone stumps by 0.5 mm twice a day to gain 1 mm distraction length per day. The distraction was performed for 10 consecutive days to achieve a 10 mm distraction gap for new bone formation. The newly formed bone was allowed to consolidate for 6 weeks with the device serving as external fixation. A mandibular cross-sectional occlusal radiograph using paediatric periapical film (Eastman Kodak Company, Rochester, USA) was taken (10 milliamparage, 50 kilovoltage peak, 0.42 seconds) using the same dental radiographic machine (Gendex, Gendex Co, Illinois, USA). The radiographic examination was standardised using a customised parallel film holder specifically made for each rabbit to achieve the same distance, angulation, and spatial position at each time interval. The radiographs were taken at 2, 4, and 6 weeks after completion of distraction and after a 6-month consolidation period. All films were processed by the same automatic film processor (Dent X 9000, Dent X/Logetronics GmbH, Kornberg, Germany). These radiographs served for both the qualitative evaluation of the newly formed bone, and quantitative measurement of radiographic density in the expanded 23
Mandibular Lengthening by Distraction Osteogenesis
sodium pentobarbitone. The mandible was removed from the cadaver and stripped of surrounding soft tissues. The specimen initially served for gross morphological examination, and was then fixed and decalcified in 10% formic acid and embedded in paraffin block. A section of 5 micron thickness, which included both the newly formed bone and native bone stump, was stained with hematoxylin and eosin for histological study under light microscope.
Figure 3. Radiographic digital image can be manipulated by the image processing software to enhance the ability to precisely choose the area of new bone regeneration in the distraction gap. The radiopacity in this area will be calculated and serves for the quantitative analysis.
gap by the Densitometer (Bio-Rad [GS-700] Imaging Densitometer, Bio-Rad Pacific, Hong Kong, China). The radiograph was placed in the scanner. The digital image of each film was transferred into the digital image analysis system to calculate the radiodensity of the distraction area reported in the optical density (OD) scale. Percentage volume, area, volume, mean OD, maximum OD, and minimum OD were obtained. The imaging system can be calibrated and adjusted to enhance the ability to discriminate the desired area from the native bone stump (Figure 3). The animals were killed in 2 groups, at 6 weeks after completion of distraction and 6 months after consolidation, with an intravenous bolus overdose of
In the 6 months experimental group, the distractor was removed when the consolidation period was complete. The screws adjacent to the distraction site were reinserted, one on each side, into the corresponding screw holes. The distance between the centres of the heads of the 2 screws was measured by a digital veneer caliper (Digital Caliper, Mitutoyo, Tokyo, Japan). The surgical wound was re-entered 6 months later. The distance between the centres of the screwheads was measured and recorded by the same method. The data were compared to determine the stability of the lengthened segment. The animal experimental design was approved by the ethics committee of the Prince of Songkla University. The schema of the experiment is shown in Figure 4. The quantitative data related to bone density of the lengthened gap and segment stability assessment were analysed by the Kruskawalis test followed by post-comparison test and Mann-Whitney U test, respectively. The statistical significance was determined when p < 0.05.
Lengthened segment measurement Insert distractor
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Figure 4. Schema of the experiment.
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Figure 5. Clinical appearance of the rabbit after completion of activation. Obvious cross bite of the incisor teeth and deviation of the chin to the left side (arrow) developed as a result of mandibular lengthening on the right side. The overgrowth of the incisor teeth is also noted.
Figure 6. Comparison of the hemimandible length on the same animal after completion of distraction. The distraction side (lower) was markedly longer than the non-operated side (upper). The arrows represent the regenerated tissue in the expanding gap.
Results
all specimens. According to observational findings at 6 weeks, the buccal cortex was noticeably incompletely formed, resulting in a soft and irregular outer surface in both the P and E groups. The thin discontinuous cortex-like structures were observed in cross section specimens of the distraction area. In the control group, on the other hand, initial formation of a structural cortex was evidenced by the rather hard and smooth outer surface of the lengthened gap. The continuous band of whitish cortex-like structure was seen in the cross section of the expanded gap (Figure 7).
Clinical Evaluation All animals tolerated the anaesthetic and surgical procedures and recovered well without any accident or death. A 2-day period of anorexia was frequently observed, after which all animals could eat independently without any disturbance from the distraction device. After 10 consecutive days of distraction, the rabbits developed a severe cross bite of the anterior teeth and an expected overgrowth of the incisors caused by continual eruption of the teeth (Figure 5). After completion of activation, the animals were able to take regular food for the remaining part of the study. No significant weight loss was observed in the experimental animals. Ten consecutive days of distraction were achieved in all animals without any failure of the distractor appliances. Gross Morphological Observation The distraction procedure produced separation of the bone stumps of up to 10 mm. Clinical observation of the mandible after removal of the attached soft tissues in all groups showed a lengthened gap filled with new callus-like tissue. The distracted side of the half mandible was significantly longer than the nonoperated contralateral half (Figure 6). The lingual cortex of the distracted area was intact and indistinguishable from the neighbouring bone in Asian J Oral Maxillofac Surg Vol 16, No 1, 2004
At 6 months, the formation of the buccal cortex in groups P and E had slowly progressed. The surface of the newly formed bone in the distraction gap was still irregular and softer than the normal nearby bone and could be readily distinguished from the original native bone stumps. From the cross section specimen of the distraction gap, only a thin continuous line of cortical bone was detected. Conversely, the control group had a buccal cortex that was well formed, with a thick continuous cortical plate resembling the lingual cortex seen in the cross section specimen. The buccal surface was completely formed and blended into adjacent bone. A medullary structure was found in both native bone ends of the distraction gap in all groups. However, in the control group, this remodelling process was found to be more advanced than in groups P and E and was similar 25
Mandibular Lengthening by Distraction Osteogenesis
a
b
c
Figure 7. Gross morphological appearance of the lengthened mandible at 6 weeks. (a) Periosteum destruction and (b) endosteum destruction showed incompletely formed buccal cortex that has a soft and irregular surface, (c) whereas a rather hard and smooth surface is seen in the control group. The arrows represent the expanded gap. The arrowheads show the buccal cortical structure of the distraction gap viewed from the cross section surface. A better formed cortex was noticed in the control group (c).
to the normal corticomedullary complex of the mandible (Figure 8). Histological Evaluation Newly formed bone was observed in the distraction gap, particularly near the native bone stumps and the periosteal tissue, in all animals. At 6 weeks in groups P and E, small trabeculae of bone with many active osteoblasts were scattered throughout the distraction gap. Woven pattern bone was observed. The buccal cortical bone contained many large and round osteoblastic cells in lacunae. In the control group at 6 weeks, small bone spicules with little osteoblastic rimming were seen. These bony trabeculae were better organised — a more mature lamellar pattern cortical bone with small shrunken osteoblasts in their lacunae was seen (Figure 9). a
b
At 6 months in groups P and E, the regenerated bone increased in maturation but many small bony trabeculae with osteoblasts lying on the surface could still be observed. The cortical bone structure appeared to have a more lamellar pattern. However, large osteoblasts were still found in some of the lacunae. On the other hand, in the control group, the remodelling process was complete. Few tiny mature bone spicules were seen surrounded by abundant normal fatty tissue. Cortical bone with a completely developed normal Harversian system and osteons was observed. Small flattened osteoblasts in lacunae or empty lacunae were noted. The histological structure of the corticomedullary complex in this group could not be distinguished from the adjacent native bone (Figure 10). c
Figure 8. Gross morphological appearance of the lengthened mandible at 6 months. (a) Periosteum destruction and (b) endosteum destruction still possessed an irregular and softer consistency than the nearby native bone stump (arrows). A thin continuous cortical layer was seen in the cross section of the expanded gap (arrowheads). (c) The control group showed a completely formed buccal cortex that had a hard consistency similar to the adjacent normal bone. As a result, it blended with the native bone stump (arrows). A thick cortical plate with normal corticomedullary structures were seen from the cross section specimen (arrowheads).
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a
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Figure 9. Histological findings of the distraction area at 6 weeks. (a) The periosteum destruction and (b) endosteum destruction groups showed bone trabeculae with active osteoblastic rimming. Cortical bone with round osteoblastic cells in their lacunae was seen. (c) More mature bone spicules surrounded by fatty tissue and well organised mature cortical bone were observed in the control group. (Hematoxylin and eosin stain.) Abbreviations: S = bone spicules; C = cortical bone.
a
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Figure 10. Histological findings of the distraction gap at 6 months. (a) The periosteum destruction and (b) endosteum destruction groups showed a nearly complete maturation pattern of the cortical bone and remodelling process of the medullary cavity. (c) Complete maturation of the cortical bone structure and complete remodelling process of the medullary cavity were observed in the control group. (Hematoxylin and eosin stain.) Abbreviations: C = cortical bone; S = bone spicule. Asian J Oral Maxillofac Surg Vol 16, No 1, 2004
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Mandibular Lengthening by Distraction Osteogenesis
Radiographic Evaluation Radiographic examination was performed at 2, 4, and 6 weeks after completion of distraction and 6 months after the consolidation period. At 2 weeks, the radiopaque area was found throughout the expanded gap in all animals, especially close to both native bone stumps. The radiodensity streaks extended from the bone stumps and tended to align themselves in a parallel manner with each other and with the distraction vector. This radiographic pattern was distributed evenly in both the cortical and medullary regions. Thus, neither radiographic structure of the cortical layer nor a medullary cavity of normal mandible was seen at this stage. However, the radiopaque streaks did not extend through to the central region. As a result, a unique 3-zonal structure that was observed comprised an anterior and posterior radiopaque region near the bone stumps with a central radiolucent band. The noticeable 3 zones were quite readily distinguishable from each other and from the adjacent bone stumps (Figure 11). At 4 weeks, the radiopacity in the distraction gap had increased in all groups when compared with 2 weeks. The radiopaque areas were scattered throughout the distraction gap, and the radiolucent a
b
central zone disappeared at this stage. The typical alignment of the radiopaque streaks parallel to the direction of distraction vector could still be observed. A thin and delicate radiopaque cortical layer was seen on the buccal side of the lengthened gap in the control group, while the cortical plate in groups P and E was not well established, and an irregular and discontinuous buccal cortex was observed (Figure 12). At 6 weeks, the radiodensity in the lengthened gap was further increased, particularly in the buccal cortical area. The cortical plate of the expanded gap in the control group was markedly thickened and blended with the outer cortex of the adjacent bone stumps. The buccal cortical plate of the lengthened gap in groups P and E was better established than at 4 weeks. However, the radiopacity was still thin and ill defined. In the control group, a decrease in radiodensity of the medullary area of the expanded gap when compared with 4 weeks was observed. This implied the beginning of the remodelling process to form the medullary complex of the new bone regenerated (Figure 13). After 6 months, the buccal cortical bone in the control group increased in radiodensity and thickness to form a fully mature cortex. The radiographic c
Figure 11. Radiographic appearance of the distraction area at 2 weeks showing (a) the periosteum destruction, (b) endosteum destruction, and (c) control groups. A distraction gap of 10 mm on average was obtained (arrows). The fine radiopaque streaks parallel to the distraction vector (double headed arrows) extending from both native bone stumps were noticed in all groups. The unique 3-zonal radiographic structure was established.
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a
c
b
Figure 12. Radiographic appearance of the distraction area at 4 weeks showing (a) the periosteum destruction, (b) endosteum destruction, and (c) control groups. The radiopaque area was scattered throughout the expanded gap. The 3-zonal structure disappeared. A thin radiopaque cortex-like structure was observed in the control group, whereas a discontinuous irregular radiopaque cortex in the periosteum and endosteum destruction groups was noted (arrows).
structure was similar to the nearby normal cortex. The regenerated cortex was continuous with the cortex of the normal bone and indistinguishable from the adjacent native bone stumps. The parallel radiopaque streaks feature disappeared. The radiopacity of the central medullary region of the expanded gap due to the remodelling process had further decreased and a radiographic medullary structure, similar to a
b
that of the normal mandible, was established. At this stage, the lengthened segment of the control group possessed all of the radiographic features of the corticomedullary structure of normal bone. The radiodensity of the cortical layer of the expanded gap in groups P and E had increased but remained less than that of the control group. The cortical plate was thin and not clearly defined. In addition, the c
Figure 13. Radiographic appearance of the distraction area at 6 weeks showing (a) the periosteum destruction, (b) endosteum destruction, and (c) control groups. Increase in radiodensity of the expanded area was noticed in all groups. However the radiographic structure of the cortical plate of the control group was better established than in the periosteum and endosteum destruction groups (arrows). The beginning of the decrease of radiopacity in the medullary region was also observed in the control group. Asian J Oral Maxillofac Surg Vol 16, No 1, 2004
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Mandibular Lengthening by Distraction Osteogenesis
a
c
b
Figure 14. Radiographic appearance of the distraction area 6 months after the consolidation period. Thin radiopaque cortical structure and initial resorption of the marrow cavity due to the remodelling process were seen in (a) the periosteum and (b) endosteum destruction groups. (c) Complete cortical bone formation and remodelling process to achieve the normal corticomedullary structure of the mandible were established in the control group.
Bone Density of the Lengthened Gap The radiodensity of the regenerated bone of the expanded gap was measured from the mandibular cross-sectional occlusal film at 2, 4, and 6 weeks after completion of distraction and 6 months after the consolidation phase in each experimental animal. The radiodensity of the expanded gap was assessed in each group according to the timing of the study (Figure 15). Quantitative analysis of the newly formed bone by the densitometer revealed no statistically significant difference at each time point between the 3 groups except for a marked decrease in density in the control group at 6 months (p < 0.05) when compared with groups P and E at the same time interval. Stability Evaluation The mean distance in millimetres between the centres of the heads of the screws of groups P, E, and C was compared between the complete consolidation period and after 6 months. A significant difference was found in groups P and E between the measurement at the end of the consolidation period and the measurement 6 months later (Figure 16). 30
Discussion The technique of distraction osteogenesis involves the creation of new bone by gradual separation of 2 or more bony fragments following their surgical division. The amount of new bone formation depends on several factors, including the existing periosteum Periosteum Endosteum Control
0.19 0.17 0.15 Optical density
radiodensity of the medullary cavity of the lengthened gap had not decreased as markedly as in the control group (Figure 14).
*
0.13 0.11 0.09 0.07 0.05
2 weeks
4 weeks
6 weeks
6 months
Time
Figure 15. Measurement of the radiodensity of the newly formed bone in the distraction area in optical density scale at 2, 4, and 6 weeks after completion of distraction and 6 months after the consolidation period in all groups compared at the same time interval. Bone density of the control group was markedly decreased when compared with the other groups after 6 months. The asterisk indicates a significant difference (p < 0.05). Asian J Oral Maxillofac Surg Vol 16, No 1, 2004
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*
*
Distraction length (mm)
16
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14 12 10 8 6 4 2 0
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Figure 16. Bar graphs comparing the distraction length in millimeters of the periosteum destruction, endosteum destruction, and control groups 6 weeks after completion of distraction and 6 months after the consolidation period. The asterisks indicate significant difference (p < 0.05). Abbreviations: P = periosteum group; E = endosteum group; C = control group.
and endosteum in the planned distraction site. In this study, the rabbit was used as an experimental model. When considering animal models, it has been suggested that the choice of animal in any experiment should be related to the level of hypothesis testing and that the degree of phylogenetic affinity between the animal model and humans depends upon the level of experimental manipulation and hypothesis testing.26 In the present study, the rabbit was used to assess the process of bone formation by mandibular distraction osteogensis in various conditions that depended on the existence of periosteal and endosteal soft tissue. This level of descriptive process only required the use of ‘generic’ animals, such as the rabbit, rather than animals that are phylogenetically closer to man.26 The results of this study revealed that new bone formation occurred in all experimental groups, and that the amount of newly formed bone showed no statistically significant difference at each time point between the 3 groups based on histological and radiographic observation. These data were also confirmed quantitatively by densitometry. Nevertheless, the Asian J Oral Maxillofac Surg Vol 16, No 1, 2004
new bone regeneration process in groups P and E achieved maturation at a slower rate than in group C, as detected by histological and radiographic analysis at the same time intervals. In addition, the remodelling process in the control group was more rapid than in groups P and E, as evidenced by the marked decline of the OD value of the control group measured by densitometry. Since the quantity of bone obtained from each group showed no difference, it could be stated that the presence of periosteum and endosteum at the site of distraction was probably not indispensable or a particularly important factor for new bone regeneration in mandibular osteodistraction. Therefore, new bone formation by mandibular distraction can take place despite poverty of periosteal and endosteal tissue. This is probably due to the rich blood supply in the craniofacial region,27,28 which can tolerate a more liberal elevation of the periosteum and a complete osteotomy. On this basis, the osteotomy in distraction osteogenesis of the craniofacial skeleton could be performed with subperiosteal dissection and complete osteotomy even by the heat-producing rotary bur which destroys the contact endosteum without disturbing the amount of new bone formation that can be expected. The limited careful osteotomy that is highly recommended for long bone osteodistraction,17,19-21 can be avoided. This is a great benefit in view of the limited and difficult access for surgical bone separation in the craniofacial region. The results of the present study suggest that distraction osteogenesis in the craniofacial skeleton is a promising procedure for new bone regeneration even in circumstances of depletion or poor quality periosteal and endosteal tissue at the distraction site. Therefore, distraction osteogenesis in the craniofacial area might be used in cases such as previous osteotomy with scarring, grafted bone, or irradiated bone where conventional reconstruction procedures may be expected to fail. With regard to the stability of the lengthened segment, the control group showed minimal change in the length of the distraction segment with no statistically significant difference between measurements at the 31
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complete consolidation period and after 6 months. However, a statistically significant difference was noted in groups P and E between these 2 time intervals. This instability of the lengthened segment might be the result of delayed maturation and remodelling process when compared with the control group and implies that the consolidation period in cases with poor or destroyed periosteum and endosteum probably needs to be longer than the normal consolidation time in cases with intact periosteum and endosteum to prevent instability of the lengthened segment.
Conclusion Distraction osteogenesis is a reliable method for new bone regeneration and can be used in the maxillofacial skeleton with good bone formation outcome. Due to the high vascular supply of the craniofacial skeleton, the presence of periosteal and endosteal tissue was probably not the most important factor for new bone formation. Thus, this procedure offered the promise of providing new bone regeneration even in the poor or destroyed periosteal and endosteal host bed at the site of planned distraction. This may mean it could be used for cases involving previous osteotomy with scarring, grafted bone, or irradiated bone with acceptable results. However, slow bone maturation and remodelling process in this situation should be expected. A longer consolidation period when compared with the normal soft tissue bed is recommended to prevent instability of the lengthened segment.
Acknowledgements This study was supported by a grant for academic research from the Prince of Songkla University, Songkhla, Thailand. We would like to thank the animal house, Faculty of Science; Center of Research Equipment, Postgraduate School, Pathology Division and Radiographic Division, Department of Stomatology, Faculty of Dentistry for their kind suggestions and cooperation.
References 1. Aronson J. The biology of distraction osteogenesis. In: Chapman MW, Madison M, editors. Operative orthopaedics. Philadelphia: JB Lippincott; 1993:873-882. 2. Aronson J, Johnson E, Harp JH. Local bone transportation for treatment of intercalary defects 32
by Ilizarov technique. Biomechanical and clinical considerations. Clin Orthop 1989;243:71-79. 3. Ilizarov GA. The tension-stress effect on the genesis and growth of tissue: Part I. The influence of stability of fixation and soft-tissue preservation. Clin Orthop 1989;238:263-281. 4. Ilizarov GA. The tension-stress effect on the genesis and growth of tissues: Part II. The influence of the rate and frequency of distraction. Clin Orthop 1989;239:263-273. 5. Ilizarov GA. Clinical application of the tensionstress effect for limb lengthening. Clin Orthop 1990;250:8-26. 6. Codivilla A. On the means of lengthening, in the lower limbs, the muscles and tissues which are shortened through deformity. Am J Orthop Surg 1905;2:353-369. 7. Ilizarov GA. The principles of Ilizarov method. Bull Hosp Jt Dis 1997;56:49-53. 8. Snyder CC, Levine GA, Swanson HM, Browne EZ. Mandibular lengthening by gradual distraction. Plast Reconstr Surg 1973;5:506-508. 9. McCarthy JG, Schreiber J, Karp N, Thorne CH, Grayson BH. Lengthening the human mandible by gradual distraction. Plast Reconstr Surg 1992; 89:1-10. 10. Havlik RJ, Bartlett SP. Mandibular distraction lengthening in the severely hypoplastic mandible: a problematic case with tongue aplasia. J Craniofac Surg 1994;5:305-310. 11. Losken HW, Patterson GT, Lazarou SA, Whitney T. Planning mandibular distraction: preliminary report. Cleft Palate J 1995;32:71-76. 12. Klein C, Howaldt HP. Lengthening of the hypoplastic mandible by gradual distraction in childhood — a preliminary report. J Cranio Maxillofac Surg 1995;23:68-74. 13. Chin M, Toth BA. Distraction osteogenesis in maxillofacial using internal devices. J Oral Maxillofac Surg 1996;54:45-53. 14. Block MS, Chang A, Crawford C. Mandibular alveolar ridge augmentation in the dog using distraction osteogenesis. J Oral Maxillofac Surg 1996;54:309-314. 15. Altuna G, Walker DS, Freeman E. Rapid orthopedic lengthening of the mandible in primates by sagittal split osteogenesis. A pilot study. Int J Adult Orthod Orthognath Surg 1995;10:59-64. Asian J Oral Maxillofac Surg Vol 16, No 1, 2004
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16. Rachmiel A, Levy M, Laufer D. Lengthening of the mandible by distraction osteogenesis: report of cases. J Oral Maxillofac Surg 1995; 53:838-846. 17. De Bastiani G, Aldegheri R, Renzi-Brivio L, Trivella G. Limb lengthening by callus distraction (callotasis). J Pediatr Orthop 1987;7:129-134. 18. Molina F, Ortiz-Monasterio F. Mandibular elongation and remodeling by distraction: a farewell to major osteotomy. Plast Reconstr Surg 1995;96:825-840. 19. Kawamura B. Limb lengthening. Orthop Clin North Am 1978;9:155-165. 20. Ilizarov GA, Lediaev VI, Shitin VP. Techenie reparativnof regeneratsii kompaktnof kosti pri distraktsionnom osteosinteze v razlichnykh usloviiakh fiksatsii kostnykh otiomkov (eksperimental noeissledovanie). Eksp Khir Anesteziol 1969;14(6):3-12. 21. Dal Monte A, Donzelli O. Tibial lengthening according to Ilizarov in congenital hypophysia of the leg. J Pediatr Orthop 1987;7:135-138. 22. Kojimoto H, Yasui N, Goto T, Matsuda S,
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Shimomura Y. Bone lengthening in rabbit by callus distraction. J Bone Joint Surg 1988;70B:3-9. 23. Muhonen A, Muhonen J, Lindholm T, Minn H, Klossner J, Kuumala J, Happonen R. Osteodistraction of a previously irradiated mandible with or without adjunctive hyperbaric oxygenation: an experimental study in rabbits. Int J Oral Maxillofac Surg 2002;31:519-524. 24. Gantous A, Phillips JH, Catton P, Holmberg D. Distraction osteogenesis in the irradiated canine mandible. Plast Reconstr Surg 1994;93:164-168. 25. Ozerdem OR, Kivanc O, Tunccer I, Acarturk S, Gocenler L, Gumurdulu D. Callotasis in nonvascularized bone grafts and the role of periosteum: a new contribution to the concept of distraction osteogenesis. Ann Plast Surg 1998; 41:148. 26. Siegel MI, Mooney MP. Appropriate animal models for craniofacial biology. Cleft Palate J 1990;27:18-25. 27. Havlik RJ, Bartlett SP. Mandibular distraction lengthening in the severely hypoplastic mandible: a problematic case with tongue aplasia. J Craniofac Surg 1994;5:305.
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Mandibular Lengthening by Distraction Osteogenesis: Role of Periosteum and Endosteum Thongchai Nuntanaranont, Wilad Sattayasunskul, Surapong Vongvatcharanon Department of Oral and Maxillofacial Surgery, Faculty of Dentistry, Prince of Songkla University, Songkhla, Thailand
Abstract Objective: To study the role of the periosteum and endosteum in new bone formation by distraction osteogenesis. Materials and Methods: Twenty four rabbits were divided into 3 groups of perieosteum destruction (group P), endosteum destruction (group E), and a control group (group C). After right mandibular body osteotomy followed by distractor placement, the buccal periosteum in the segment between the second and third screws was removed by scalpel in group P. In group E, the endosteum was scraped out from both bone ends between the second and third screws. In group C, both periosteum and endosteum were preserved during the surgical operation. After a latency period of 3 days, bone lengthening was started at a rate of 1 mm per day for 10 days, after which the newly formed bone was allowed to consolidate for 6 weeks with the device serving as an external fixator. Radiographs were taken at the following time intervals: 2 weeks, 4 weeks, and 6 weeks after completion of distraction and 6 months after consolidation. The animals were sacrificed 6 weeks after completion of distraction and 6 months after consolidation for the gross macroscopic, histological, and radiological examinations and stability measurement of the distracted segment. Results: New bone was generated in all animal groups. The buccal cortex was incompletely formed in groups P and E but was completely formed and indistinguishable in the control group after 6 months. Histologically, the newly formed bone in the control group had a more mature appearance and better organised bone spicules than in groups P and E. In addition the remodelling process occurred more rapidly in the control group. However, quantitative analysis of the newly formed bone by densitometry revealed no statistically significant differences at each time interval among the 3 groups except for a decline in density in the control group after 6 months due to the bone remodelling process. The stability of the regenerated bone of the lengthened segment was best in the control group, with groups P and E showing marked changes in the length of the distracted distance. Conclusion: Although groups P and E exhibited slower new bone maturation, the amount of newly formed bone was equal in all groups. It could be stated that the periosteum and endosteum are probably not indispensable or particularly important for adequate callus formation. This may be due to the rich blood supply of the craniofacial skeleton. However the instability of the segment caused by the slow maturation and remodelling of the newly formed bone in groups P and E should be noted, and a longer consolidation period is recommended to avoid instability of the regenerated segment in such cases. Key words: Distraction osteogenesis, Mandible, Periosteum
Introduction Distraction osteogenesis is a method of producing unlimited quantities of living bone directly from a Correspondence: Thongchai Nuntanaranont, Department of Oral and Maxillofacial Surgery, Faculty of Dentistry, Prince of Songkla University, Songkhla, Hat Yai, Thailand 90110. Tel/Fax: (66 74) 429876; E-mail: [email protected]
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special osteotomy by controlled mechanical distraction of the bone segments. The new bone spontaneously bridges the gap and rapidly remodels to a normal macrostructure similar to local bone.1-5 Distraction osteogenesis is a concept of bone lengthening first described by Codivilla in 1905, who used it to elongate a femur by repeated pulling forces.6 However, the technique of bone lengthening by 21
Mandibular Lengthening by Distraction Osteogenesis
gradual distraction was further developed and refined by Ilizarov in 1951.3,7 The use of distraction osteogenesis in the craniofacial skeleton was first reported by Snyder et al who used monofocal distraction to lengthen the mandible in a canine model.8 Successful clinical bone lengthening in craniofacial surgery was first described by McCarthy et al in 1992.9 Since then several clinical reports followed,10-12 and a wide variety of techniques are now available to lengthen bone segments or entire maxillary and mandibular arches.13-16 Recent advances and innovations in surgical techniques and equipment have made bone lengthening by osteodistraction both easier and safer. Many successful clinical cases have been reported,17,18 but only limited information is available regarding the importance of the periosteum and endosteum in the distraction area in relation to the quality and quantity of newly formed bone, especially in the craniofacial region. Ilizarov stated that the degree of damage to the periosteal and endosteal tissue at the time of osteotomy is one of the most critical factors to determine new bone regeneration, and maximum preservation of the periosteal and intraosseous soft tissue should enhance bone formation during limb lengthening by distraction osteogenesis.4 Any damage to the bone marrow in the distraction area inhibits osteogenesis resulting in retarded and poorly formed bone. On the basis of these previous studies on long bone lengthening, osteotomy with protection of the bone marrow during operation has been emphasised, and a carefully limited corticotomy recommended.17-21 Kojimoto et al, in a rabbit tibial model, reported marked disturbance and failure of callus formation when the periosteum was removed during the operation. 22 These researchers concluded that preservation of the periosteum is essential if bone lengthening by callus distraction is to succeed, and this effect is more prominent than with the preservation of endosteal tissue. Although some controversy exists, it seems that the periosteum and endosteum are both important factors for optimal new bone regeneration by 22
distraction osteogenesis. The role of the periosteum and endosteum in new bone formation in long bones was also expected to apply to craniofacial bones, which are membranous in embryological origin. However, a study that confirms this hypothesis in craniofacial osteodistraction is lacking. The majority of reports assessed the results by estimation based on clinical observation or qualitative evaluation.23-25 Craniofacial bones indeed possess different and complex anatomical structures with high vascular supply when compared with long bones. Thus the influence of periosteum and endosteum on new bone regeneration by distraction osteogenesis in craniofacial bones could well be different from long bones. Additionally, in most circumstances, the periosteum and endosteum in the craniofacial area are difficult to preserve during the osteotomy process due to their fine structure and difficult access. In some situations, the recommended limited corticotomy used in long bones cannot be achieved in the craniofacial bone region. The surgical approach to the operation site and complete osteotomy by bone saw or rotary bur inevitably creates mechanical and thermal injury both to the periosteal and endosteal soft tissues. The purpose of the present study was to investigate the effect of periosteal and endosteal soft tissues in and around the distraction area on new bone formation by distraction osteogenesis in craniofacial bones.
Materials and Methods Twenty four healthy male New Zealand white rabbits, aged 5 to 7 months and weighing 3.0 to 3.5 kg, served as experimental animals. The animals were divided equally into 3 groups: a periosteum destruction group (group P), endosteum destruction group (group E), and a control group (group C), in which both periosteal and endosteal soft tissues were protected and preserved. The distraction device used in this study was modified from an orthodontic palatal expansion screw (Hyrax) with the capacity of opening up to 10 mm. The rod ends of the device were bent and soldered to the preformed alloy extension rods with 2 holes on each side. Therefore, each bone segment could be fixed and secured by 2 titanium microscrews (Figure 1). Asian J Oral Maxillofac Surg Vol 16, No 1, 2004
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A
B C Figure 1. Modified distraction device. Abbreviations: A = activator part; B = extension rod; C = fixation holes for micro-titanium screws.
The surgical procedure was performed under aseptic conditions. All animals were anaesthetised with an intramuscular injection of ketamine hydrochloride 25 mg/kg and diazepam 5 mg/kg, repeated if required. Penicillin G sodium 0.5 million units was administered intramuscularly preoperatively. A 2 cm linear incision was made along the inferior border of the rabbit mandible. The body of the mandible was exposed subperiosteally from the anterior region to the antegonial notch. The mental nerve was preserved. The osteotomy cut was made vertically from the area posterior to the mental nerve just anterior to the premolar teeth downward to the lower border of the mandible. Every effort was made to preserve the inferior alveolar nerve running past the osteotomy line. The osteotomy was completed and the mobility of the fragments checked by rotational movement of the osteotome until complete separation was achieved. Before placement of the distraction device, each animal was treated according to its group. For group P, the periosteum lining the bone segments between the second and third screws was removed by scalpel followed by thermal electrocautery. For group E, the endosteum and bone marrow were scraped out of both ends of the bone stumps on either side of the osteotomy, between the second and third screws. For the control group C, both the periosteum and endosteum were preserved during the surgical operation. The distraction device was fixed to the proximal and distal bone stumps using 2 bicortical self-tapping titanium microscrews on each side. The wound was closed in 3 layers leaving the activator Asian J Oral Maxillofac Surg Vol 16, No 1, 2004
Figure 2. The active part of the distractor was left outside the surgical wound.
part of the distraction device outside the surgical wound (Figure 2). Analgesics and antimicrobial medication were given for 3 consecutive days postoperatively. After device placement, distraction was delayed for 3 days, the ‘latency period’. The distractor was activated to separate the bone stumps by 0.5 mm twice a day to gain 1 mm distraction length per day. The distraction was performed for 10 consecutive days to achieve a 10 mm distraction gap for new bone formation. The newly formed bone was allowed to consolidate for 6 weeks with the device serving as external fixation. A mandibular cross-sectional occlusal radiograph using paediatric periapical film (Eastman Kodak Company, Rochester, USA) was taken (10 milliamparage, 50 kilovoltage peak, 0.42 seconds) using the same dental radiographic machine (Gendex, Gendex Co, Illinois, USA). The radiographic examination was standardised using a customised parallel film holder specifically made for each rabbit to achieve the same distance, angulation, and spatial position at each time interval. The radiographs were taken at 2, 4, and 6 weeks after completion of distraction and after a 6-month consolidation period. All films were processed by the same automatic film processor (Dent X 9000, Dent X/Logetronics GmbH, Kornberg, Germany). These radiographs served for both the qualitative evaluation of the newly formed bone, and quantitative measurement of radiographic density in the expanded 23
Mandibular Lengthening by Distraction Osteogenesis
sodium pentobarbitone. The mandible was removed from the cadaver and stripped of surrounding soft tissues. The specimen initially served for gross morphological examination, and was then fixed and decalcified in 10% formic acid and embedded in paraffin block. A section of 5 micron thickness, which included both the newly formed bone and native bone stump, was stained with hematoxylin and eosin for histological study under light microscope.
Figure 3. Radiographic digital image can be manipulated by the image processing software to enhance the ability to precisely choose the area of new bone regeneration in the distraction gap. The radiopacity in this area will be calculated and serves for the quantitative analysis.
gap by the Densitometer (Bio-Rad [GS-700] Imaging Densitometer, Bio-Rad Pacific, Hong Kong, China). The radiograph was placed in the scanner. The digital image of each film was transferred into the digital image analysis system to calculate the radiodensity of the distraction area reported in the optical density (OD) scale. Percentage volume, area, volume, mean OD, maximum OD, and minimum OD were obtained. The imaging system can be calibrated and adjusted to enhance the ability to discriminate the desired area from the native bone stump (Figure 3). The animals were killed in 2 groups, at 6 weeks after completion of distraction and 6 months after consolidation, with an intravenous bolus overdose of
In the 6 months experimental group, the distractor was removed when the consolidation period was complete. The screws adjacent to the distraction site were reinserted, one on each side, into the corresponding screw holes. The distance between the centres of the heads of the 2 screws was measured by a digital veneer caliper (Digital Caliper, Mitutoyo, Tokyo, Japan). The surgical wound was re-entered 6 months later. The distance between the centres of the screwheads was measured and recorded by the same method. The data were compared to determine the stability of the lengthened segment. The animal experimental design was approved by the ethics committee of the Prince of Songkla University. The schema of the experiment is shown in Figure 4. The quantitative data related to bone density of the lengthened gap and segment stability assessment were analysed by the Kruskawalis test followed by post-comparison test and Mann-Whitney U test, respectively. The statistical significance was determined when p < 0.05.
Lengthened segment measurement Insert distractor
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Completed distraction
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Radiograph Radiograph Radiograph 3 days Day 0
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Figure 4. Schema of the experiment.
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Figure 5. Clinical appearance of the rabbit after completion of activation. Obvious cross bite of the incisor teeth and deviation of the chin to the left side (arrow) developed as a result of mandibular lengthening on the right side. The overgrowth of the incisor teeth is also noted.
Figure 6. Comparison of the hemimandible length on the same animal after completion of distraction. The distraction side (lower) was markedly longer than the non-operated side (upper). The arrows represent the regenerated tissue in the expanding gap.
Results
all specimens. According to observational findings at 6 weeks, the buccal cortex was noticeably incompletely formed, resulting in a soft and irregular outer surface in both the P and E groups. The thin discontinuous cortex-like structures were observed in cross section specimens of the distraction area. In the control group, on the other hand, initial formation of a structural cortex was evidenced by the rather hard and smooth outer surface of the lengthened gap. The continuous band of whitish cortex-like structure was seen in the cross section of the expanded gap (Figure 7).
Clinical Evaluation All animals tolerated the anaesthetic and surgical procedures and recovered well without any accident or death. A 2-day period of anorexia was frequently observed, after which all animals could eat independently without any disturbance from the distraction device. After 10 consecutive days of distraction, the rabbits developed a severe cross bite of the anterior teeth and an expected overgrowth of the incisors caused by continual eruption of the teeth (Figure 5). After completion of activation, the animals were able to take regular food for the remaining part of the study. No significant weight loss was observed in the experimental animals. Ten consecutive days of distraction were achieved in all animals without any failure of the distractor appliances. Gross Morphological Observation The distraction procedure produced separation of the bone stumps of up to 10 mm. Clinical observation of the mandible after removal of the attached soft tissues in all groups showed a lengthened gap filled with new callus-like tissue. The distracted side of the half mandible was significantly longer than the nonoperated contralateral half (Figure 6). The lingual cortex of the distracted area was intact and indistinguishable from the neighbouring bone in Asian J Oral Maxillofac Surg Vol 16, No 1, 2004
At 6 months, the formation of the buccal cortex in groups P and E had slowly progressed. The surface of the newly formed bone in the distraction gap was still irregular and softer than the normal nearby bone and could be readily distinguished from the original native bone stumps. From the cross section specimen of the distraction gap, only a thin continuous line of cortical bone was detected. Conversely, the control group had a buccal cortex that was well formed, with a thick continuous cortical plate resembling the lingual cortex seen in the cross section specimen. The buccal surface was completely formed and blended into adjacent bone. A medullary structure was found in both native bone ends of the distraction gap in all groups. However, in the control group, this remodelling process was found to be more advanced than in groups P and E and was similar 25
Mandibular Lengthening by Distraction Osteogenesis
a
b
c
Figure 7. Gross morphological appearance of the lengthened mandible at 6 weeks. (a) Periosteum destruction and (b) endosteum destruction showed incompletely formed buccal cortex that has a soft and irregular surface, (c) whereas a rather hard and smooth surface is seen in the control group. The arrows represent the expanded gap. The arrowheads show the buccal cortical structure of the distraction gap viewed from the cross section surface. A better formed cortex was noticed in the control group (c).
to the normal corticomedullary complex of the mandible (Figure 8). Histological Evaluation Newly formed bone was observed in the distraction gap, particularly near the native bone stumps and the periosteal tissue, in all animals. At 6 weeks in groups P and E, small trabeculae of bone with many active osteoblasts were scattered throughout the distraction gap. Woven pattern bone was observed. The buccal cortical bone contained many large and round osteoblastic cells in lacunae. In the control group at 6 weeks, small bone spicules with little osteoblastic rimming were seen. These bony trabeculae were better organised — a more mature lamellar pattern cortical bone with small shrunken osteoblasts in their lacunae was seen (Figure 9). a
b
At 6 months in groups P and E, the regenerated bone increased in maturation but many small bony trabeculae with osteoblasts lying on the surface could still be observed. The cortical bone structure appeared to have a more lamellar pattern. However, large osteoblasts were still found in some of the lacunae. On the other hand, in the control group, the remodelling process was complete. Few tiny mature bone spicules were seen surrounded by abundant normal fatty tissue. Cortical bone with a completely developed normal Harversian system and osteons was observed. Small flattened osteoblasts in lacunae or empty lacunae were noted. The histological structure of the corticomedullary complex in this group could not be distinguished from the adjacent native bone (Figure 10). c
Figure 8. Gross morphological appearance of the lengthened mandible at 6 months. (a) Periosteum destruction and (b) endosteum destruction still possessed an irregular and softer consistency than the nearby native bone stump (arrows). A thin continuous cortical layer was seen in the cross section of the expanded gap (arrowheads). (c) The control group showed a completely formed buccal cortex that had a hard consistency similar to the adjacent normal bone. As a result, it blended with the native bone stump (arrows). A thick cortical plate with normal corticomedullary structures were seen from the cross section specimen (arrowheads).
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a
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Figure 9. Histological findings of the distraction area at 6 weeks. (a) The periosteum destruction and (b) endosteum destruction groups showed bone trabeculae with active osteoblastic rimming. Cortical bone with round osteoblastic cells in their lacunae was seen. (c) More mature bone spicules surrounded by fatty tissue and well organised mature cortical bone were observed in the control group. (Hematoxylin and eosin stain.) Abbreviations: S = bone spicules; C = cortical bone.
a
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Figure 10. Histological findings of the distraction gap at 6 months. (a) The periosteum destruction and (b) endosteum destruction groups showed a nearly complete maturation pattern of the cortical bone and remodelling process of the medullary cavity. (c) Complete maturation of the cortical bone structure and complete remodelling process of the medullary cavity were observed in the control group. (Hematoxylin and eosin stain.) Abbreviations: C = cortical bone; S = bone spicule. Asian J Oral Maxillofac Surg Vol 16, No 1, 2004
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Mandibular Lengthening by Distraction Osteogenesis
Radiographic Evaluation Radiographic examination was performed at 2, 4, and 6 weeks after completion of distraction and 6 months after the consolidation period. At 2 weeks, the radiopaque area was found throughout the expanded gap in all animals, especially close to both native bone stumps. The radiodensity streaks extended from the bone stumps and tended to align themselves in a parallel manner with each other and with the distraction vector. This radiographic pattern was distributed evenly in both the cortical and medullary regions. Thus, neither radiographic structure of the cortical layer nor a medullary cavity of normal mandible was seen at this stage. However, the radiopaque streaks did not extend through to the central region. As a result, a unique 3-zonal structure that was observed comprised an anterior and posterior radiopaque region near the bone stumps with a central radiolucent band. The noticeable 3 zones were quite readily distinguishable from each other and from the adjacent bone stumps (Figure 11). At 4 weeks, the radiopacity in the distraction gap had increased in all groups when compared with 2 weeks. The radiopaque areas were scattered throughout the distraction gap, and the radiolucent a
b
central zone disappeared at this stage. The typical alignment of the radiopaque streaks parallel to the direction of distraction vector could still be observed. A thin and delicate radiopaque cortical layer was seen on the buccal side of the lengthened gap in the control group, while the cortical plate in groups P and E was not well established, and an irregular and discontinuous buccal cortex was observed (Figure 12). At 6 weeks, the radiodensity in the lengthened gap was further increased, particularly in the buccal cortical area. The cortical plate of the expanded gap in the control group was markedly thickened and blended with the outer cortex of the adjacent bone stumps. The buccal cortical plate of the lengthened gap in groups P and E was better established than at 4 weeks. However, the radiopacity was still thin and ill defined. In the control group, a decrease in radiodensity of the medullary area of the expanded gap when compared with 4 weeks was observed. This implied the beginning of the remodelling process to form the medullary complex of the new bone regenerated (Figure 13). After 6 months, the buccal cortical bone in the control group increased in radiodensity and thickness to form a fully mature cortex. The radiographic c
Figure 11. Radiographic appearance of the distraction area at 2 weeks showing (a) the periosteum destruction, (b) endosteum destruction, and (c) control groups. A distraction gap of 10 mm on average was obtained (arrows). The fine radiopaque streaks parallel to the distraction vector (double headed arrows) extending from both native bone stumps were noticed in all groups. The unique 3-zonal radiographic structure was established.
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a
c
b
Figure 12. Radiographic appearance of the distraction area at 4 weeks showing (a) the periosteum destruction, (b) endosteum destruction, and (c) control groups. The radiopaque area was scattered throughout the expanded gap. The 3-zonal structure disappeared. A thin radiopaque cortex-like structure was observed in the control group, whereas a discontinuous irregular radiopaque cortex in the periosteum and endosteum destruction groups was noted (arrows).
structure was similar to the nearby normal cortex. The regenerated cortex was continuous with the cortex of the normal bone and indistinguishable from the adjacent native bone stumps. The parallel radiopaque streaks feature disappeared. The radiopacity of the central medullary region of the expanded gap due to the remodelling process had further decreased and a radiographic medullary structure, similar to a
b
that of the normal mandible, was established. At this stage, the lengthened segment of the control group possessed all of the radiographic features of the corticomedullary structure of normal bone. The radiodensity of the cortical layer of the expanded gap in groups P and E had increased but remained less than that of the control group. The cortical plate was thin and not clearly defined. In addition, the c
Figure 13. Radiographic appearance of the distraction area at 6 weeks showing (a) the periosteum destruction, (b) endosteum destruction, and (c) control groups. Increase in radiodensity of the expanded area was noticed in all groups. However the radiographic structure of the cortical plate of the control group was better established than in the periosteum and endosteum destruction groups (arrows). The beginning of the decrease of radiopacity in the medullary region was also observed in the control group. Asian J Oral Maxillofac Surg Vol 16, No 1, 2004
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Mandibular Lengthening by Distraction Osteogenesis
a
c
b
Figure 14. Radiographic appearance of the distraction area 6 months after the consolidation period. Thin radiopaque cortical structure and initial resorption of the marrow cavity due to the remodelling process were seen in (a) the periosteum and (b) endosteum destruction groups. (c) Complete cortical bone formation and remodelling process to achieve the normal corticomedullary structure of the mandible were established in the control group.
Bone Density of the Lengthened Gap The radiodensity of the regenerated bone of the expanded gap was measured from the mandibular cross-sectional occlusal film at 2, 4, and 6 weeks after completion of distraction and 6 months after the consolidation phase in each experimental animal. The radiodensity of the expanded gap was assessed in each group according to the timing of the study (Figure 15). Quantitative analysis of the newly formed bone by the densitometer revealed no statistically significant difference at each time point between the 3 groups except for a marked decrease in density in the control group at 6 months (p < 0.05) when compared with groups P and E at the same time interval. Stability Evaluation The mean distance in millimetres between the centres of the heads of the screws of groups P, E, and C was compared between the complete consolidation period and after 6 months. A significant difference was found in groups P and E between the measurement at the end of the consolidation period and the measurement 6 months later (Figure 16). 30
Discussion The technique of distraction osteogenesis involves the creation of new bone by gradual separation of 2 or more bony fragments following their surgical division. The amount of new bone formation depends on several factors, including the existing periosteum Periosteum Endosteum Control
0.19 0.17 0.15 Optical density
radiodensity of the medullary cavity of the lengthened gap had not decreased as markedly as in the control group (Figure 14).
*
0.13 0.11 0.09 0.07 0.05
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4 weeks
6 weeks
6 months
Time
Figure 15. Measurement of the radiodensity of the newly formed bone in the distraction area in optical density scale at 2, 4, and 6 weeks after completion of distraction and 6 months after the consolidation period in all groups compared at the same time interval. Bone density of the control group was markedly decreased when compared with the other groups after 6 months. The asterisk indicates a significant difference (p < 0.05). Asian J Oral Maxillofac Surg Vol 16, No 1, 2004
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Consolidation
*
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6 months later
14 12 10 8 6 4 2 0
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C Group
Figure 16. Bar graphs comparing the distraction length in millimeters of the periosteum destruction, endosteum destruction, and control groups 6 weeks after completion of distraction and 6 months after the consolidation period. The asterisks indicate significant difference (p < 0.05). Abbreviations: P = periosteum group; E = endosteum group; C = control group.
and endosteum in the planned distraction site. In this study, the rabbit was used as an experimental model. When considering animal models, it has been suggested that the choice of animal in any experiment should be related to the level of hypothesis testing and that the degree of phylogenetic affinity between the animal model and humans depends upon the level of experimental manipulation and hypothesis testing.26 In the present study, the rabbit was used to assess the process of bone formation by mandibular distraction osteogensis in various conditions that depended on the existence of periosteal and endosteal soft tissue. This level of descriptive process only required the use of ‘generic’ animals, such as the rabbit, rather than animals that are phylogenetically closer to man.26 The results of this study revealed that new bone formation occurred in all experimental groups, and that the amount of newly formed bone showed no statistically significant difference at each time point between the 3 groups based on histological and radiographic observation. These data were also confirmed quantitatively by densitometry. Nevertheless, the Asian J Oral Maxillofac Surg Vol 16, No 1, 2004
new bone regeneration process in groups P and E achieved maturation at a slower rate than in group C, as detected by histological and radiographic analysis at the same time intervals. In addition, the remodelling process in the control group was more rapid than in groups P and E, as evidenced by the marked decline of the OD value of the control group measured by densitometry. Since the quantity of bone obtained from each group showed no difference, it could be stated that the presence of periosteum and endosteum at the site of distraction was probably not indispensable or a particularly important factor for new bone regeneration in mandibular osteodistraction. Therefore, new bone formation by mandibular distraction can take place despite poverty of periosteal and endosteal tissue. This is probably due to the rich blood supply in the craniofacial region,27,28 which can tolerate a more liberal elevation of the periosteum and a complete osteotomy. On this basis, the osteotomy in distraction osteogenesis of the craniofacial skeleton could be performed with subperiosteal dissection and complete osteotomy even by the heat-producing rotary bur which destroys the contact endosteum without disturbing the amount of new bone formation that can be expected. The limited careful osteotomy that is highly recommended for long bone osteodistraction,17,19-21 can be avoided. This is a great benefit in view of the limited and difficult access for surgical bone separation in the craniofacial region. The results of the present study suggest that distraction osteogenesis in the craniofacial skeleton is a promising procedure for new bone regeneration even in circumstances of depletion or poor quality periosteal and endosteal tissue at the distraction site. Therefore, distraction osteogenesis in the craniofacial area might be used in cases such as previous osteotomy with scarring, grafted bone, or irradiated bone where conventional reconstruction procedures may be expected to fail. With regard to the stability of the lengthened segment, the control group showed minimal change in the length of the distraction segment with no statistically significant difference between measurements at the 31
Mandibular Lengthening by Distraction Osteogenesis
complete consolidation period and after 6 months. However, a statistically significant difference was noted in groups P and E between these 2 time intervals. This instability of the lengthened segment might be the result of delayed maturation and remodelling process when compared with the control group and implies that the consolidation period in cases with poor or destroyed periosteum and endosteum probably needs to be longer than the normal consolidation time in cases with intact periosteum and endosteum to prevent instability of the lengthened segment.
Conclusion Distraction osteogenesis is a reliable method for new bone regeneration and can be used in the maxillofacial skeleton with good bone formation outcome. Due to the high vascular supply of the craniofacial skeleton, the presence of periosteal and endosteal tissue was probably not the most important factor for new bone formation. Thus, this procedure offered the promise of providing new bone regeneration even in the poor or destroyed periosteal and endosteal host bed at the site of planned distraction. This may mean it could be used for cases involving previous osteotomy with scarring, grafted bone, or irradiated bone with acceptable results. However, slow bone maturation and remodelling process in this situation should be expected. A longer consolidation period when compared with the normal soft tissue bed is recommended to prevent instability of the lengthened segment.
Acknowledgements This study was supported by a grant for academic research from the Prince of Songkla University, Songkhla, Thailand. We would like to thank the animal house, Faculty of Science; Center of Research Equipment, Postgraduate School, Pathology Division and Radiographic Division, Department of Stomatology, Faculty of Dentistry for their kind suggestions and cooperation.
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