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Does the sheep mandible relapse following lengthening by distraction osteogenesis?
Journal of Cranio-Maxillofacial Surgery (2000) 28, 251–257 # 2000 European Association for Cranio-Maxillofacial Surgery doi:10.1054/jcms.2000.0153, available online at http://www.idealibrary.com on
Does the sheep mandible relapse following lengthening by distraction osteogenesis? James McTavish,1 Damian D. Marucci,2 S. Fiona Bonar,3 William R. Walsh,2 Michael D. Poole1 1
Department of Plastic & Reconstructive Surgery, St George Hospital, Kogarah, NSW, Australia; Orthopaedic Research Laboratories, Prince of Wales Hospital, Division of Surgery, University of New South Wales, Randwick, NSW, Australia; 3Douglass Hanly Moir Pathology, Sydney, Australia 2
SUMMARY. Aim: Distraction osteogenesis is a technique used to lengthen the shortened mandible. However, the long term stability of the distracted mandibular bone is not known. The aim of this study was to assess if the sheep mandible relapses following lengthening, and to assess the quality of distracted bone up to 1 year post lengthening. Methods: Twenty-four sheep had bilateral external mandibular distractors applied, with three sheep as controls. Titanium marker screws were positioned both proximal and distal to the distraction zone in all sheep. Following a 5 day latency period, the interdental gap was distracted 1 mm/day for 20 days, with a subsequent 20 day consolidation period. Ante-mortem serial X-rays were used to assess for relapse by measuring the distance between the screws. The animals were sacrificed at either 3, 6, 9 or 12 months post-distraction. At post mortem, the distance between the screws was re-measured. The distracted bone was assessed mechanically and histologically. Results: The mean mandibular lengthening obtained was 13.2 mm. There was no relapse of the mandible over 12 months. The distracted bone had attained the strength and stiffness of undistracted bone by 6 months postdistraction (p50.05). Histological evaluation revealed significant amounts of lamellar bone by 6 months postdistraction. Conclusions: No relapse occurred for 12 months post distraction lengthening. The bone formed following distraction was stable and of good quality. These findings lend support to the use of distraction osteogenesis in clinical practice. # 2000 European Association for Cranio-Maxillofacial Surgery
The mandibles of 24 adult Wethers sheep were bilaterally distracted with external distraction devices using an established model (Tavakoli et al., 1998; Fig. 1). Four titanium marker screws (Mondeal cross fit screws 1.763 mm) were inserted into the mandible bilaterally, two on either side of the osteotomy/distraction gap to monitor relapse (Fig. 2). The distance between the screws was recorded to within 0.1 mm with a hand held Vernier calliper. The 24 sheep were allocated to four experimental groups of six (A, B, C and D; Table 1). Three additional sheep, acting as controls, had marker screws inserted but were not distracted, to measure any changes in mandibular length during the study period, such as may occur due to growth. Distraction commenced after a 5 day latency period, at a rate of 0.5 mm 12 hourly, for 20 consecutive days. A 20 day consolidation period was observed. On day 45 following insertion of the distractors, the sheep returned to the operating theatre and the distance between the screws was measured. All other metal hardware was removed and the mandibles X-rayed. Sheep were followed up for 3, 6, 9 and 12 months after removal of the distractors (six sheep per group) and sacrificed. Radiographs were taken at 3 monthly intervals as shown in Table 1. After sacrifice, the mandibles were excised and the distance between the marker screws measured again directly on the mandible.
INTRODUCTION Traditionally, bilateral sagittal ramus split osteotomy has been used to lengthen the retrognathic mandible. Relapse is the tendency for bone and soft tissue to return to pre-lengthened status, and is a frequent but unpredictable complication of this technique (Van Sickels et al., 1988). The more the mandible is advanced the more it tends to relapse even with internal fixation of the bone fragments (Lake et al., 1981). Distraction osteogenesis is now an established technique for lengthening the hypoplastic mandible (McCarthy et al., 1992). Despite the widespread use of this technique the long-term stability of distracted bone in the mandible is not known. In the mandible, relapse may have severe functional and aesthetic consequences as there is little room for error with respect to issues such as dental occlusion. This study used a sheep model to assess whether the regenerate bone relapses following distraction osteogenesis of the mandible. MATERIAL AND METHODS All experiments were performed after authorization by the Animal Care and Ethics Committee of the University of New South Wales (UNSW) and complied with the Australian Code of Practice for the Care and Use of Animals for Scientific Purposes (National Health and Medical Research Council, 1997). 251
252 Journal of Cranio-Maxillofacial Surgery
Fig. 1 – Schematic drawing of sheep skull demonstrating (A) the position of the distractor in relation to the interdental space and (B) mandibular lengthening post-distraction.
Type SCM-1, Showa Xray Ltd, Tokyo, Japan ) using Super HG 30 Fuji medical film. All radiographs were taken 125 cm from the source. At this fixed focal distance there was no measurable magnification effect. (This was confirmed by using a dry mandible with marker screws inserted as a standard). The machine was set at 40 kV and 3.0 mAs. Post mortem investigations The following investigations were performed on the resected hemimandibles following sacrifice of the animal. Fig. 2 – Two titanium marker screws inserted into mandible on either side of osteotomy site (indicated by line). Table 1 – Summary of experimental protocol
Radiology The mandibles were radiographed at a fixed focal distance using a portable X-ray machine as previously described.
Quantity 3 months 6 months 9 months 12 months
In vivo investigations
Histology One hemimandible was fixed in 10% buffered formalin and subsequently decalcified in 10% formic acidformalin solution. The section of mandible containing the distraction zone was processed for light microscopy, by sectioning longitudinally in the axial plane and embedding in paraffin. All sections were stained with haemotoxylin and eosin and examined by light microscopy and under polarised light.
Radiology The mandibles were radiographed in the anaesthetised animal at 3, 6 and 9 months post distraction, using a portable X-ray machine (Tecnomed Medecon
Biomechanical testing The other hemimandible was mechanically tested using an MTS 858 servo-hydraulic materials testing machine (MTS Systems Corporation, Minneapolis,
Group A Group B Group C Group D Controls
6 6 6 6 3
Sacrifice X-ray X-ray X-ray X-ray
Sacrifice X-ray X-ray X-ray
Sacrifice X-ray X-ray
Sacrifice Sacrifice
Distraction osteogenesis 253
Fig. 3 – Three-point mechanical testing to determine strength and stiffness of regenerate bone.
MN, USA; Fig. 3). The specimens were stored frozen in 0.9% sodium chloride at 7188C, and defrosted on the day of testing. Three point bending to destruction was performed at a rate of 2 mm/min, with the specimens placed lingual side down and the central loading point situated in the centre of the distraction zone (Elovic et al., 1994; Tavakoli et al., 1998; Farhadieh et al., 2000). Load and displacement data was collected by computer. Peak load and stiffness were calculated for each sample. Data was analysed using a one way Analysis of Variance followed by a post-hoc multiple comparison when appropriate (Statistica, Statsoft, Tulsa, OK, USA). RESULTS Clinical A class III malocclusion was produced in all sheep. Sheep were able to feed normally on a diet of lucerne hay, 1 kg of lucerne chaff fodder and 800 g of water softened nuts per day. A superficial infection rate of 50% was observed initially but this was reduced to 17% by adopting a more aggressive antimicrobial policy. Two sheep died and had to be replaced. Both deaths occurred under general anaesthesia during removal of the external distraction devices (Day 45 post insertion). An autopsy was performed by a veterinary pathologist with the cause of death suspected to be a cardiac arrhythmia.
Mandible lengthening obtained Following lengthening of the bilateral distraction devices by 20 mm, the mean lengthening obtained at the level of the mandible was 13.2 mm (range 6–16.5 mm, SD 2.35), as measured by direct measurement of the mandible marker screws to the nearest 0.1 mm. In group A some marker screws fell out bilaterally in two sheep and unilaterally in three sheep, but because four marker screws had been placed, measurement of the interdental gap was still possible. In only two sheep did the lengthening of each side of the mandible correlate exactly. The mean difference in lengthening between the left and right hemimanibles was 2.06 mm (SD¼1.49). Sheep were radiographed and sacrificed in accordance with Table 1. Radiologic analysis (Fig. 4) revealed no change in the length of the distraction gap in any sheep over the study period. This was confirmed post mortem, when the inter screw distances were measured directly. There was no relapse in any sheep over the 12 month follow-up period. There was no growth of the control mandibles over the study period as confirmed by radiologic and direct measurements. Histology Histological evaluation of the sheep mandibles 3 months post distraction (Group A) showed bony union, in which the bone within the distraction zone
254 Journal of Cranio-Maxillofacial Surgery
was predominantly woven in nature and the trabeculae were mainly arranged longitudinally (Fig. 5). The original osteotomy site was well healed in all but one sheep, which had a fibrous non-union secondary to osteomyelitis. At 6 and 9 months post-distraction, increasing quantities of lamellar bone demonstrating orderly maturation were seen. At 9 months (Group C), the majority of the trabeculae were lamellar in nature arranged predominantly longitudinally in the distraction zone and union was complete in all cases (Fig. 6). At 12 months post distraction (Group D), very little woven bone was demonstrated. Merging of the distraction zone with original mandible anteriorly and posteriorly was practically imperceptible. Biomechanical testing Three-point biomechanical testing of the post mortem hemimandibles was performed to determine strength and stiffness of the distracted bone. The distracted bone attained the same strength as undistracted bone by 6 months post-distraction (p50.05; Fig. 7). The stiffness of bone was determined from the gradient of the load vs displacement curve generated for each three-point testing experiment. As with bone strength, the distracted bone attained the same stiffness as undistracted bone by 6 months postdistraction (p50.05; Fig. 8). Fig. 4 – Radiograph of sheep 3 months following removal of distraction device. Marker screws are clearly visible on either side of radiolucent bone in the distraction zone.
DISCUSSION There is no consensus from clinical work as to whether the mandible relapses following distraction
Fig. 5 – Regenerate bone at 3 months demonstrating an irregular arrangement of collagen fibres, typical of immature woven bone (Polarisation microscopy 640).
Distraction osteogenesis 255
Fig. 6 – (A) Regenerate bone at 9 months demonstrating collagen fibres arranged in a predominantly lamellar pattern (Polarisation microscopy 640). This is comparable to the arrangement of mature lamellar cortical bone in an (B) undistracted control animal (Polarisation microscopy 620).
Fig. 7 – Peak load (strength) of the regenerate bone formed by distraction osteogenesis.
Fig. 8 – Stiffness of the regenerate bone formed by distraction osteogenesis.
256 Journal of Cranio-Maxillofacial Surgery
osteogenesis. It is important to establish if it occurs as any relapse can affect the dental occlusion, the anatomy of the pharynx when distraction is performed for airway obstruction, and overall cosmetic result. If relapse could be quantified perhaps some overcorrection could be incorporated into the initial lengthening procedure. No change was observed in the distances between the marker screws on either side of the distraction zone up to 12 months post distraction. An uniform distraction distance of 20 mm was applied to the device. However, the mean lengthening obtained in the mandible was 13.2 mm (range 6–16.5 mm). These varying amounts of lengthening may be accounted for in part due to bending of the K-wires which are not rigid during the distraction period and occasional cheese wire effect of the K-wires through the mandible and soft tissues. Bone formed following distraction in the sheep mandible using the present conditions is permanent and stable. Distracted bone can also adapt to the functional demands of the native mandible, as evidenced by the remodelling observed with union by mature lamellar bone. This contrasts with bone imported into the mandible as grafts from distant sites, e.g. iliac crest, which is initially dead and cannot readily respond and adapt to the local milieu. In distraction lengthening of the mandible there was a gradual stretching of the para-mandibular soft tissues over 20 days, which were held in position for a further 20 days during the consolidation period. This presumably allowed the soft tissue envelope to accommodate more readily than it does when the mandible is fully advanced in a one off procedure as in osteotomy and advancement. The functional demands on the mandible in this model were not those of normal occlusion as the sheep were prognathic and had class III bite after distraction. However, one would expect this to predispose to relapse rather than protect against it. In this model, the vector of distraction was opposed by the longitudinal genial muscles, which would also be predicted to predispose the mandible to relapse. Dental occlusion is used to assess relapse but compensatory changes in the dentition may mask any small movements. Cephalometry can also be used to monitor postoperative changes but this may be inaccurate (Wall and Rosenquist, 1996). Changes may be due to factors other than regenerate bone relapse, such as growth in the mandible or lack of it (Grayson et al., 1997; Carls and Sailer, 1998). ‘Relapse’ documented by cephalometric or occlusal relationships could also be due to resorption or translation of other areas of bone, such as the mandibular condyle, due to alterations in functional demand. If the lengthening of the regenerate bone is not measured precisely, it is difficult to assess the exact extent and nature of subsequent relapse. Klein and Howaldt (1995) found cephalometric relapse occurring in one patient out of nine following distraction lengthening of the mandible. They advocated immediate postoperative orthodontic treatment
to prevent relapse. Shomura et al. (1999) reported cephalometric ‘relapse’ in three patients following mandibular distraction, possibly due to factors mentioned above. Other authors have found no relapse of the mandible following distraction osteogenesis based on dental occlusion and cephalometry (Molina and Monasterio, 1995). In the sheep midface relapse of 2–3 mm was recorded over 1 year following distraction lengthening, with relapse occurring in the first 3 months as measured by radiography of marker screws (Rachmiel et al., 1995). In a primate model there was no relapse of the distracted maxilla but the follow-up period was only 6 weeks post distraction and only two animals were used (Altuna et al., 1995). Cedars et al. (1999) distracted the midface of 14 patients and found excellent stability at the occlusal level. At the level of orbitale, a horizontal advancement of 15 mm was obtained – at 1 year follow-up this had relapsed by 1 mm. The sheep model seems to be a reasonable predictor of the behaviour of the human midface. Clinically, the regenerate bone formed in midface distraction is not comparable to that in the mandible and is of a more fibrocartilaginous nature for a longer period macroscopically. Distraction osteogenesis and sagittal split osteotomy are different methods for lengthening the mandible. Relapse is a frequent complication of sagittal split osteotomy. We did not demonstrate any relapse after distraction osteogenesis in the sheep mandible. Direct comparison and extrapolation to the human mandible is difficult and caution must be taken. Whether distraction osteogenesis will offer less relapse after human mandibular lengthening compared to other methods remains to be seen.
CONCLUSION This is the first animal study to specifically address the issue of whether the regenerate bone of the mandible relapses following bilateral distraction lengthening. At 12 months there was no relapse of distracted bone. The bone formed by distraction osteogenesis in the mandible underwent normal remodelling and was stable by 12 months following distraction. References Altuna G, Walker DA, Freeman E: Surgically assisted-rapid orthopedic lengthening of the maxilla in primates – relapse following distraction osteogenesis. Int J Adult Orthodon Orthognath Surg 10: 269–275, 1995 Carls FR, Sailer HF: Seven years clinical experience with mandibular distraction in children. J CranioMaxillofac Surg 26: 197–208, 1998 Cedars MG, Linck DL, Chin C, Toth BA: Advancement of the midface using distraction techniques. Plast Reconstr Surg 103: 429–441, 1999 Elovic RP, Hipp J, Hayes WA: A method for measuring the structural properties of the rat mandible. Archs Oral Biol 39: 1029–1033, 1994
Distraction osteogenesis 257 Farhadieh RD, Dickson R, Gianoutsos M, Walsh WR: Effect of distraction on biomechanical, mineralisation and histologic properties of an ovine mandible model. Plast Reconstr Surg 105: 889–895, 2000 Grayson BH, McCormick S, Santiago PE, McCarthy JG: Vector of device placement and trajectory of mandibular distraction. J Craniofac Surg 8: 473–482, 1997 Klein C, Howaldt HP: Lengthening of the hypoplastic mandible by gradual distraction in childhood – a preliminary report. J CranioMaxillofac Surg 23: 68–74, 1995 Lake SL, McNeill RW, Little RM, West RA: Surgical mandibular advancement: a cephalometric analysis of treatment response. Am J Orthod 80: 376–393, 1981 McCarthy JG, Schreiber J, Karp N, Thorne CH, Grayson BH: Lengthening the human mandible by gradual distraction. Plast Reconstr Surg 89: 1–8, 1992 Molina F, Monasterio FO: Mandibular elongation and remodeling by distraction: a farewell to major osteotomies. Plast Reconstr Surg 96: 825–840, 1995 National health and medical research council: Australian code of practice for the care and use of animals for scientific purposes. Australian Government Publishing Services, Canberra 1997, 1–82 Rachmiel A, Jackson IT, Potparic Z, Laufer D: Midface advancement in sheep by gradual distraction: a 1-year followup study. J Oral Maxillofac Surg 50: 525–529, 1995 Shomura K, Inoue R, Kuroe K, Mimura T, Sugihara K, Ito G. Skeletal relapse after mandibular distraction – 3 case reports. Transactions of 2nd International Congress on Cranial and Facial Bone Distraction Processes, Paris, France 1999; 353–357
Tavakoli K, Walsh WR, Bonar F, Smart R, Wulf S, Poole MD: The role of latency in mandibular osteodistraction. J CranioMaxillofac Surg 26: 209–219, 1998 Van Sickels JE, Larsen AJ, Thrash WJ: A retrospective study of relapse in rigidly fixated sagittal split osteotomies: contributing factors. Am J Orthod Dentofacial Orthop 93: 413–418, 1988 Wall G, Rosenquist B: Accuracy of cephalometry in measurements of postoperative migration of the maxilla after Le Fort I osteotomy. Int J Adult Orthod Orthognath Surg 11: 105–115, 1996
Prof. M. D. Poole Department of Plastic and Reconstructive Surgery The St George Hospital 30 Gray Street Kogarah NSW 2217 Australia Tel: +61 2 9350 2755 Fax: +61 2 9350 2756 E-mail: [email protected] Paper received 18 October 1999 Accepted 15 September 2000 Published online 20 November 2000
Does the sheep mandible relapse following lengthening by distraction osteogenesis? James McTavish,1 Damian D. Marucci,2 S. Fiona Bonar,3 William R. Walsh,2 Michael D. Poole1 1
Department of Plastic & Reconstructive Surgery, St George Hospital, Kogarah, NSW, Australia; Orthopaedic Research Laboratories, Prince of Wales Hospital, Division of Surgery, University of New South Wales, Randwick, NSW, Australia; 3Douglass Hanly Moir Pathology, Sydney, Australia 2
SUMMARY. Aim: Distraction osteogenesis is a technique used to lengthen the shortened mandible. However, the long term stability of the distracted mandibular bone is not known. The aim of this study was to assess if the sheep mandible relapses following lengthening, and to assess the quality of distracted bone up to 1 year post lengthening. Methods: Twenty-four sheep had bilateral external mandibular distractors applied, with three sheep as controls. Titanium marker screws were positioned both proximal and distal to the distraction zone in all sheep. Following a 5 day latency period, the interdental gap was distracted 1 mm/day for 20 days, with a subsequent 20 day consolidation period. Ante-mortem serial X-rays were used to assess for relapse by measuring the distance between the screws. The animals were sacrificed at either 3, 6, 9 or 12 months post-distraction. At post mortem, the distance between the screws was re-measured. The distracted bone was assessed mechanically and histologically. Results: The mean mandibular lengthening obtained was 13.2 mm. There was no relapse of the mandible over 12 months. The distracted bone had attained the strength and stiffness of undistracted bone by 6 months postdistraction (p50.05). Histological evaluation revealed significant amounts of lamellar bone by 6 months postdistraction. Conclusions: No relapse occurred for 12 months post distraction lengthening. The bone formed following distraction was stable and of good quality. These findings lend support to the use of distraction osteogenesis in clinical practice. # 2000 European Association for Cranio-Maxillofacial Surgery
The mandibles of 24 adult Wethers sheep were bilaterally distracted with external distraction devices using an established model (Tavakoli et al., 1998; Fig. 1). Four titanium marker screws (Mondeal cross fit screws 1.763 mm) were inserted into the mandible bilaterally, two on either side of the osteotomy/distraction gap to monitor relapse (Fig. 2). The distance between the screws was recorded to within 0.1 mm with a hand held Vernier calliper. The 24 sheep were allocated to four experimental groups of six (A, B, C and D; Table 1). Three additional sheep, acting as controls, had marker screws inserted but were not distracted, to measure any changes in mandibular length during the study period, such as may occur due to growth. Distraction commenced after a 5 day latency period, at a rate of 0.5 mm 12 hourly, for 20 consecutive days. A 20 day consolidation period was observed. On day 45 following insertion of the distractors, the sheep returned to the operating theatre and the distance between the screws was measured. All other metal hardware was removed and the mandibles X-rayed. Sheep were followed up for 3, 6, 9 and 12 months after removal of the distractors (six sheep per group) and sacrificed. Radiographs were taken at 3 monthly intervals as shown in Table 1. After sacrifice, the mandibles were excised and the distance between the marker screws measured again directly on the mandible.
INTRODUCTION Traditionally, bilateral sagittal ramus split osteotomy has been used to lengthen the retrognathic mandible. Relapse is the tendency for bone and soft tissue to return to pre-lengthened status, and is a frequent but unpredictable complication of this technique (Van Sickels et al., 1988). The more the mandible is advanced the more it tends to relapse even with internal fixation of the bone fragments (Lake et al., 1981). Distraction osteogenesis is now an established technique for lengthening the hypoplastic mandible (McCarthy et al., 1992). Despite the widespread use of this technique the long-term stability of distracted bone in the mandible is not known. In the mandible, relapse may have severe functional and aesthetic consequences as there is little room for error with respect to issues such as dental occlusion. This study used a sheep model to assess whether the regenerate bone relapses following distraction osteogenesis of the mandible. MATERIAL AND METHODS All experiments were performed after authorization by the Animal Care and Ethics Committee of the University of New South Wales (UNSW) and complied with the Australian Code of Practice for the Care and Use of Animals for Scientific Purposes (National Health and Medical Research Council, 1997). 251
252 Journal of Cranio-Maxillofacial Surgery
Fig. 1 – Schematic drawing of sheep skull demonstrating (A) the position of the distractor in relation to the interdental space and (B) mandibular lengthening post-distraction.
Type SCM-1, Showa Xray Ltd, Tokyo, Japan ) using Super HG 30 Fuji medical film. All radiographs were taken 125 cm from the source. At this fixed focal distance there was no measurable magnification effect. (This was confirmed by using a dry mandible with marker screws inserted as a standard). The machine was set at 40 kV and 3.0 mAs. Post mortem investigations The following investigations were performed on the resected hemimandibles following sacrifice of the animal. Fig. 2 – Two titanium marker screws inserted into mandible on either side of osteotomy site (indicated by line). Table 1 – Summary of experimental protocol
Radiology The mandibles were radiographed at a fixed focal distance using a portable X-ray machine as previously described.
Quantity 3 months 6 months 9 months 12 months
In vivo investigations
Histology One hemimandible was fixed in 10% buffered formalin and subsequently decalcified in 10% formic acidformalin solution. The section of mandible containing the distraction zone was processed for light microscopy, by sectioning longitudinally in the axial plane and embedding in paraffin. All sections were stained with haemotoxylin and eosin and examined by light microscopy and under polarised light.
Radiology The mandibles were radiographed in the anaesthetised animal at 3, 6 and 9 months post distraction, using a portable X-ray machine (Tecnomed Medecon
Biomechanical testing The other hemimandible was mechanically tested using an MTS 858 servo-hydraulic materials testing machine (MTS Systems Corporation, Minneapolis,
Group A Group B Group C Group D Controls
6 6 6 6 3
Sacrifice X-ray X-ray X-ray X-ray
Sacrifice X-ray X-ray X-ray
Sacrifice X-ray X-ray
Sacrifice Sacrifice
Distraction osteogenesis 253
Fig. 3 – Three-point mechanical testing to determine strength and stiffness of regenerate bone.
MN, USA; Fig. 3). The specimens were stored frozen in 0.9% sodium chloride at 7188C, and defrosted on the day of testing. Three point bending to destruction was performed at a rate of 2 mm/min, with the specimens placed lingual side down and the central loading point situated in the centre of the distraction zone (Elovic et al., 1994; Tavakoli et al., 1998; Farhadieh et al., 2000). Load and displacement data was collected by computer. Peak load and stiffness were calculated for each sample. Data was analysed using a one way Analysis of Variance followed by a post-hoc multiple comparison when appropriate (Statistica, Statsoft, Tulsa, OK, USA). RESULTS Clinical A class III malocclusion was produced in all sheep. Sheep were able to feed normally on a diet of lucerne hay, 1 kg of lucerne chaff fodder and 800 g of water softened nuts per day. A superficial infection rate of 50% was observed initially but this was reduced to 17% by adopting a more aggressive antimicrobial policy. Two sheep died and had to be replaced. Both deaths occurred under general anaesthesia during removal of the external distraction devices (Day 45 post insertion). An autopsy was performed by a veterinary pathologist with the cause of death suspected to be a cardiac arrhythmia.
Mandible lengthening obtained Following lengthening of the bilateral distraction devices by 20 mm, the mean lengthening obtained at the level of the mandible was 13.2 mm (range 6–16.5 mm, SD 2.35), as measured by direct measurement of the mandible marker screws to the nearest 0.1 mm. In group A some marker screws fell out bilaterally in two sheep and unilaterally in three sheep, but because four marker screws had been placed, measurement of the interdental gap was still possible. In only two sheep did the lengthening of each side of the mandible correlate exactly. The mean difference in lengthening between the left and right hemimanibles was 2.06 mm (SD¼1.49). Sheep were radiographed and sacrificed in accordance with Table 1. Radiologic analysis (Fig. 4) revealed no change in the length of the distraction gap in any sheep over the study period. This was confirmed post mortem, when the inter screw distances were measured directly. There was no relapse in any sheep over the 12 month follow-up period. There was no growth of the control mandibles over the study period as confirmed by radiologic and direct measurements. Histology Histological evaluation of the sheep mandibles 3 months post distraction (Group A) showed bony union, in which the bone within the distraction zone
254 Journal of Cranio-Maxillofacial Surgery
was predominantly woven in nature and the trabeculae were mainly arranged longitudinally (Fig. 5). The original osteotomy site was well healed in all but one sheep, which had a fibrous non-union secondary to osteomyelitis. At 6 and 9 months post-distraction, increasing quantities of lamellar bone demonstrating orderly maturation were seen. At 9 months (Group C), the majority of the trabeculae were lamellar in nature arranged predominantly longitudinally in the distraction zone and union was complete in all cases (Fig. 6). At 12 months post distraction (Group D), very little woven bone was demonstrated. Merging of the distraction zone with original mandible anteriorly and posteriorly was practically imperceptible. Biomechanical testing Three-point biomechanical testing of the post mortem hemimandibles was performed to determine strength and stiffness of the distracted bone. The distracted bone attained the same strength as undistracted bone by 6 months post-distraction (p50.05; Fig. 7). The stiffness of bone was determined from the gradient of the load vs displacement curve generated for each three-point testing experiment. As with bone strength, the distracted bone attained the same stiffness as undistracted bone by 6 months postdistraction (p50.05; Fig. 8). Fig. 4 – Radiograph of sheep 3 months following removal of distraction device. Marker screws are clearly visible on either side of radiolucent bone in the distraction zone.
DISCUSSION There is no consensus from clinical work as to whether the mandible relapses following distraction
Fig. 5 – Regenerate bone at 3 months demonstrating an irregular arrangement of collagen fibres, typical of immature woven bone (Polarisation microscopy 640).
Distraction osteogenesis 255
Fig. 6 – (A) Regenerate bone at 9 months demonstrating collagen fibres arranged in a predominantly lamellar pattern (Polarisation microscopy 640). This is comparable to the arrangement of mature lamellar cortical bone in an (B) undistracted control animal (Polarisation microscopy 620).
Fig. 7 – Peak load (strength) of the regenerate bone formed by distraction osteogenesis.
Fig. 8 – Stiffness of the regenerate bone formed by distraction osteogenesis.
256 Journal of Cranio-Maxillofacial Surgery
osteogenesis. It is important to establish if it occurs as any relapse can affect the dental occlusion, the anatomy of the pharynx when distraction is performed for airway obstruction, and overall cosmetic result. If relapse could be quantified perhaps some overcorrection could be incorporated into the initial lengthening procedure. No change was observed in the distances between the marker screws on either side of the distraction zone up to 12 months post distraction. An uniform distraction distance of 20 mm was applied to the device. However, the mean lengthening obtained in the mandible was 13.2 mm (range 6–16.5 mm). These varying amounts of lengthening may be accounted for in part due to bending of the K-wires which are not rigid during the distraction period and occasional cheese wire effect of the K-wires through the mandible and soft tissues. Bone formed following distraction in the sheep mandible using the present conditions is permanent and stable. Distracted bone can also adapt to the functional demands of the native mandible, as evidenced by the remodelling observed with union by mature lamellar bone. This contrasts with bone imported into the mandible as grafts from distant sites, e.g. iliac crest, which is initially dead and cannot readily respond and adapt to the local milieu. In distraction lengthening of the mandible there was a gradual stretching of the para-mandibular soft tissues over 20 days, which were held in position for a further 20 days during the consolidation period. This presumably allowed the soft tissue envelope to accommodate more readily than it does when the mandible is fully advanced in a one off procedure as in osteotomy and advancement. The functional demands on the mandible in this model were not those of normal occlusion as the sheep were prognathic and had class III bite after distraction. However, one would expect this to predispose to relapse rather than protect against it. In this model, the vector of distraction was opposed by the longitudinal genial muscles, which would also be predicted to predispose the mandible to relapse. Dental occlusion is used to assess relapse but compensatory changes in the dentition may mask any small movements. Cephalometry can also be used to monitor postoperative changes but this may be inaccurate (Wall and Rosenquist, 1996). Changes may be due to factors other than regenerate bone relapse, such as growth in the mandible or lack of it (Grayson et al., 1997; Carls and Sailer, 1998). ‘Relapse’ documented by cephalometric or occlusal relationships could also be due to resorption or translation of other areas of bone, such as the mandibular condyle, due to alterations in functional demand. If the lengthening of the regenerate bone is not measured precisely, it is difficult to assess the exact extent and nature of subsequent relapse. Klein and Howaldt (1995) found cephalometric relapse occurring in one patient out of nine following distraction lengthening of the mandible. They advocated immediate postoperative orthodontic treatment
to prevent relapse. Shomura et al. (1999) reported cephalometric ‘relapse’ in three patients following mandibular distraction, possibly due to factors mentioned above. Other authors have found no relapse of the mandible following distraction osteogenesis based on dental occlusion and cephalometry (Molina and Monasterio, 1995). In the sheep midface relapse of 2–3 mm was recorded over 1 year following distraction lengthening, with relapse occurring in the first 3 months as measured by radiography of marker screws (Rachmiel et al., 1995). In a primate model there was no relapse of the distracted maxilla but the follow-up period was only 6 weeks post distraction and only two animals were used (Altuna et al., 1995). Cedars et al. (1999) distracted the midface of 14 patients and found excellent stability at the occlusal level. At the level of orbitale, a horizontal advancement of 15 mm was obtained – at 1 year follow-up this had relapsed by 1 mm. The sheep model seems to be a reasonable predictor of the behaviour of the human midface. Clinically, the regenerate bone formed in midface distraction is not comparable to that in the mandible and is of a more fibrocartilaginous nature for a longer period macroscopically. Distraction osteogenesis and sagittal split osteotomy are different methods for lengthening the mandible. Relapse is a frequent complication of sagittal split osteotomy. We did not demonstrate any relapse after distraction osteogenesis in the sheep mandible. Direct comparison and extrapolation to the human mandible is difficult and caution must be taken. Whether distraction osteogenesis will offer less relapse after human mandibular lengthening compared to other methods remains to be seen.
CONCLUSION This is the first animal study to specifically address the issue of whether the regenerate bone of the mandible relapses following bilateral distraction lengthening. At 12 months there was no relapse of distracted bone. The bone formed by distraction osteogenesis in the mandible underwent normal remodelling and was stable by 12 months following distraction. References Altuna G, Walker DA, Freeman E: Surgically assisted-rapid orthopedic lengthening of the maxilla in primates – relapse following distraction osteogenesis. Int J Adult Orthodon Orthognath Surg 10: 269–275, 1995 Carls FR, Sailer HF: Seven years clinical experience with mandibular distraction in children. J CranioMaxillofac Surg 26: 197–208, 1998 Cedars MG, Linck DL, Chin C, Toth BA: Advancement of the midface using distraction techniques. Plast Reconstr Surg 103: 429–441, 1999 Elovic RP, Hipp J, Hayes WA: A method for measuring the structural properties of the rat mandible. Archs Oral Biol 39: 1029–1033, 1994
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Tavakoli K, Walsh WR, Bonar F, Smart R, Wulf S, Poole MD: The role of latency in mandibular osteodistraction. J CranioMaxillofac Surg 26: 209–219, 1998 Van Sickels JE, Larsen AJ, Thrash WJ: A retrospective study of relapse in rigidly fixated sagittal split osteotomies: contributing factors. Am J Orthod Dentofacial Orthop 93: 413–418, 1988 Wall G, Rosenquist B: Accuracy of cephalometry in measurements of postoperative migration of the maxilla after Le Fort I osteotomy. Int J Adult Orthod Orthognath Surg 11: 105–115, 1996
Prof. M. D. Poole Department of Plastic and Reconstructive Surgery The St George Hospital 30 Gray Street Kogarah NSW 2217 Australia Tel: +61 2 9350 2755 Fax: +61 2 9350 2756 E-mail: [email protected] Paper received 18 October 1999 Accepted 15 September 2000 Published online 20 November 2000