- Email: [email protected]
Continuous and intermittent bone distraction using a microhydraulic cylinder: an experimental study in minipigs
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British Journal of Oral and Maxillofacial Surgery (2001) 39, 2–7 © 2001 The British Association of Oral and Maxillofacial Surgeons doi: 10.1054/bjom.2000.0564, available online at http://www.idealibrary.com on
BRITISH
Journal of Oral and Maxillofacial Surgery
Continuous and intermittent bone distraction using a microhydraulic cylinder: an experimental study in minipigs J. Wiltfang,* P. Keßler,* H.-A. Merten,† F. W. Neukam* *Department of Oral and Maxillofacial Surgery, University of Erlangen-Nuremberg; †Department of Oral and Maxillofacial Surgery, University of Göttingen, Germany SUMMARY. Distraction osteogenesis of the mandible is an option in the treatment of mandibular hypoplasia. Today, only intermittent distraction devices are available for clinical application. The aim of this study in minipigs was to evaluate continuous bone distraction using a microhydraulic cylinder. After a seven-day interval, continuous or intermittent distraction of 1.5 mm/day was established for 10 days. Immediately after active distraction, two animals and 20 days later the other four animals were killed and radiographs taken. The mandible was then removed en bloc and the distracted bone examined histologically. Intermittent distraction forces of up to 2500 kPa were necessary to move the cylinders’ piston. The pressure needed for continuous distraction was considerably lower (1200–1300 kPa). While the specific histological structure of the varying zones in the distraction gap was similar after continuous and intermittent distraction, bone healing was accelerated after continuous distraction as shown by ultrasonography and scanning electron microscopy. © 2001 The British Association of Oral and Maxillofacial Surgeons
(Mandibular distraction with corticotomy: analysis of the bone elongation and soft tissue expansion. Paper presented at 63rd Annual Meeting of the American Society of Plastic and Reconstructive Surgery 1994), and Klein and Howaldt11 recognized the importance of this method and introduced it for the treatment of congenital craniomaxillofacial anomalies. The first craniomaxillofacial application was in the distraction of hypoplastic mandibles.12–17 The importance of the extent and frequency of distraction on bone healing was recognized by llizarov.18,19 The distraction rate of 1 mm/day proved to be optimal. Higher rates led to pseudarthrosis, and lower rates to rapid bone healing. On the other hand, llizarov18,19 found that increased frequency of distraction formed bone of a better quality. The devices available today for clinical use do not allow continuous distraction. The microhydraulic distraction cylinder used in the present study was invented and patented by Wiltfang et al. in 199620,21 and developed in cooperation with an engineering team from the University of Aachen, Germany.22 This microhydraulic cylinder allows continuous as well as intermittent distraction through a remote control device, which is fixed on the experimental animal’s back (with no moving elements in direct contact with skin or mucosa) and allows pressure monitoring during distraction. In contrast to motor driven devices described
INTRODUCTION Maxillomandibular hypoplasia, facial asymmetry, and congenital micrognathia are common abnormalities of the craniofacial skeleton. In adults, these deformities are usually treated by osteotomies and skeletal fixation.1–3 Despite the fact that orthognathic surgery has had widespread success, the treatment has several limitations,4 including the inability of the muscles to be stretched acutely. The soft tissues will not accommodate extended musculoskeletal movements, which are required for many congenital deformities, unless additional soft tissue procedures are performed.5 An alternative approach is callus distraction, which was first described by Codivilla6 and Abbot7 for long bones. New bone forms between the surfaces of bone segments, which are gradually separated by incremental traction. The distraction forces also create tension in the surrounding tissues. Adaptive changes – so-called distraction histiogenesis8 – subsequently occur in different tissues, including skin, fascia, nerves, blood vessels, ligaments, cartilage, and periosteum and allow larger skeletal movements. Distraction osteogenesis was rediscovered by Ilizarov and Smelyshev9 and introduced into clinical use. Nowadays it has become an established method in orthopaedics and traumatology with many skeletal applications. McCarthy et al.,10 Molina and Ortiz-Monasterio 2
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by Schmelzeisen et al.23 and Ploder et al.,24 which do not have a pressure monitoring, the hydraulic system is less complicated and, although it is small, it allows the generation of high pressures. We aimed to record pressure values in continuous and intermittent distraction osteogenesis, and to compare histological findings using light and scanning electron microscopy. The process of distraction was followed by ultrasonography. MATERIAL AND METHODS Description of the microhydraulic cylinder The hydraulic unit consists of a cylinder and a piston both made from medical grade steel. The cylinder has an external diameter of 9 mm and is small enough to be implanted subcutaneously (Fig. 1). The mechanical properties of the cylinder/piston unit are similar to those of a conventional reconstruction plate. Shearing forces (like bite forces) of up to 50 N are therefore well tolerated. Piston and cylinder are protected against rotational forces by a slot and key mechanism. The maximum piston extension is 25 mm. The distractor is fixed with four bicortical screws, and the integrated fixation plate of the piston is adjustable to allow adaptation to the underlying bone. All metal parts of the distractor can be steam sterilized. The seals and the hydraulic tube can be disinfected. The whole system is simple to assemble. The distraction device is connected to an extracorporal steering unit through a flexible hydraulic tube. The injector system can be activated manually once a day for intermittent distraction. To allow continuous distraction an automatic hydropneumatic injector system is attached to the microhydraulic cylinder and the hydropneumatic injector system is loaded with carbon dioxide once a day to ensure constant pressure on the hydraulic fluid.
Fig. 1 Protoype of the microhydraulic distractor.
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Saline is used as the hydraulic medium. Both injector systems can generate a maximum distraction force of 45N and are connected to a pressure receptor to allow pressure measurements during distraction. Animal experiment Six adult, female Göttingen miniature pigs were chosen as test animals. The minipig is particularly suitable for bone regeneration studies, but the bone apposition rates (1.2 m/dy) of the pig are slightly faster than the rate in humans (0.8 m/dy).25 A distraction rate of 1.5 mm was therefore used to achieve comparable results. Protocol and guidelines were approved by the Committee of Ethics of the University of Erlangen/ Nuremberg and the responsible administrative district (permission: 509.42502/01.11.98). After endotracheal intubation, the right mandibular angle was exposed by a submandibular approach and an osteotomy was made distal to the row of teeth. Importance was placed on the preservation of the inferior alveolar nerve and vessel bundle. The microhydraulic distraction cylinder was fixed with two 3.5-mm bicortical screws (Leibinger-Stryker, Freiburg, Germany) on each side of the osteotomy gap (Fig. 2). The hydraulic tube was connected to the cylinder and placed in a subcutaneous tunnel. The flexible tube punctured the animal’s skin in the dorsal neck region and was connected to the injector system, which was fixed on the animal’s back. Distraction started a week after the operation. We estimated to gain about 12–15 mm of bone. In three animals (group 1) the microhydraulic cylinder’s piston was extended at a rate of 1.5 mm/24 h by the automatic hydro-pneumatic injector system to achieve continuous distraction. In the other three animals (group 2), the piston was activated manually once a day to achieve intermittent distraction of the same extent. During the observation period, daily distraction pressure measurements were recorded by a connectable pressure receptor. Ultrasound examinations were made once a
Fig. 2 Microhydraulic distractor in situ on a pig’s mandible.
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week to follow the distraction process. After 10 days of active distraction one animal in each group was killed. After a further 20 days of a fixation period the other two animals from each group were killed. The distracted bone segment of the mandible was resected, and after conventional radiographs had been taken the bone was prepared for light- and scanning electron microscopy (EM). Histological examination During the intervals of observation, a polychrome sequence marking with tetracycline, calceine green, xylenol orange and alizarin-complex was done using the dosage mentioned by Rahn.26 An intra-arterial angiogram with a suspension of Berlin blue and barium sulphate was taken before the animals were killed. The specimens were fixed in 2.5% glutaraldehyde. Nondecalcified thin sliced sections of bone were examined by light- and fluorescence microscopy.27 Additional specimens were decalcified in solutions containing increasing concentrations of alcohol. They were then dried by the critical point drying method with liquid carbon dioxide and coated with gold/palladium. These probes were examined by scanning EM (Zeiss DSM 960).
RESULTS Insertion of the microhydraulic cylinder was easy. Bicortical screw fixation gave sufficient stability and the distraction devices were well tolerated by the animals. Even pressure peaks of more than 3000 kPa caused by masticatory action did not loose of the device. Feeding the animals orally during the observation period was no problem. One animal developed a local inflammation
where the hydraulic tube emerged from the skin, which resolved after local treatment with antibiotics (Tardomyocel™, Bayer, Leverkusen, Germany). In all animals, the intended amount of distraction of 14–15 mm was achieved. During distraction in the intermittent group, pressure monitoring showed a gradual increase in the pressure needed to activate the device during the first four days. Pressure peaks of up to 2400 kPa were reached immediately after activation of the device. Thirty minutes later the pressure had fallen substantially and reached a level of 800 to 900 kPa after 2 to 4 hours (Fig. 3). The high pressure peaks were seen only in intermittent distraction. With continuous distraction a mean pressure of 1200–1300 kPa was sufficient to move the piston a distance of 1.5 mm in a 24 hour period (Fig. 4). Ultrasonography was a valuable tool in monitoring the process of reossification in the distraction gap. After continuous distraction (group 2), ultrasonography showed accelerated consolidation of the bone in the osteotomy gap compared with group 1. The reduced penetration of ultrasonic waves in the distraction gap showed faster bony reorganization with continuous bone distraction. Histological examination showed a specific zonal structure in both groups. The central fibrous zone was poorly mineralized and consisted of longitudinally orientated bundles of collagenous fibre. At the periphery of this central area was a zone of extended bone formation. A zone of longitudinally orientated primary bone formation followed and ended adjacent to the former osteotomy. After active distraction the fibrous interzone ossified and woven bone regenerated to bridge the gap. Cartilage was rarely found. While the specific zonal structure was found following continuous as well as intermittent distraction, the newly formed bone was more mature after continuous distraction. Fluorescence microscopy of the central fibre zone 20 days after the end of active distraction showed that ossification in the
Fig. 3 Pressure monitoring diagram of intermittent manual distraction, 11.5 mm/day for 10 days.
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centre of the distraction zone was more mature after continuous (Fig. 5a) than intermittent distraction (Fig. 5b). This was also shown by scanning EM as spongy bone formation in the central distraction zone which seemed to be more mature after continuous distraction (Figs 6a,b).
DISCUSSION Distraction osteogenesis consists mainly of three sequential periods: latency, distraction, and consolidation. The histological findings in the distraction gap resemble the histological changes during healing of a fracture: inflammation, soft callus, hard callus, and remodelling.8 During distraction, the soft callus period is interrupted
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by the application of gradual traction. The fibrous tissue becomes longitudinally orientated along the axis of distraction, and the distraction gap is characterized by a specific zonal structure. A poorly mineralized fibrous zone is located in the centre and consists of longitudinally orientated bundles of collagenous fibres. At the periphery of the central area a zone of longitudinally orientated cylindrical primary osteons follows. This zone resembles a bone growth zone adjacent to the osteotomy. After the end of distraction, the fibrous interzone ossifies and woven bone regenerates to bridge the gap. After resorption of the primary osteons, further maturation and lamellar reorganization of the bone in the distraction zone continues for a year or more until the newly formed bone has the same structure as the pre-existing
Fig. 4 Pressure monitoring diagram of mean continuous distraction, 1.5 mm/day for 10 days.
Fig. 5 (a) Histological specimen showing a zonal structure, which was found in both groups. A central fibrous zone, a zone of extended bone formation, a zone of longitudinally orientated osteons, and the osteotomy zone. Fluorescence microscopy of the central fibre zone 20 days after end of active continuous distraction showed mature woven bone regenerates C: corticotomy zone, R: row of micropillars, W: woven bone regenerates (undecalcified thin sliced section, fluorescence microscopy, original magnification 4). (b) Fluorescence microscopy of the central fibre zone 20 days after end of active intermittent distraction showed that ossification of the centre of the distraction zone was not as mature as after continuous distraction C:corticotomy zone, R: row of micropillars, W: woven bone regenerates (undecalcified thin sliced section, fluorescence microscopy, original magnification 4).
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Fig. 6 (a) The woven bone regenerates looked mature after continuous distraction (scanning EM, original magnification 100). (b) The woven bone regenerates after intermittent, discontinuous distraction appeared to be not as advanced than after continuous distraction (7a) (scanning EM, original magnification 100).
bone.28–30 These histological changes were also found in distraction of long bones. In 1982 Panikarovski et al.31 were the first to present histological findings after mandibular (membranous bone) distraction in dogs. Their group also found a fibrous interzone in the centre of the distraction gap with collagenous fibres orientated parallel to the axis of distraction. Longitudinally orientated trabeculae originated from the osteotomy zone and progressed towards the fibrous zone. Karp et al.32 differentiated four zones: a central zone of fibrous tissue, a zone of extended bone formation, a zone of bone remodelling, and a zone of mature bone. In summary, the mechanism of bone formation after distraction of membranous bone are similar to those following distraction of long bones. While the specific histological zonal structures of the distraction gap in our study were similar in both distraction methods and in accordance with the results of Panikarovski et al.31 and Karp et al.,32 bone healing after continuous distraction was accelerated as shown by ultrasonography and scanning EM. The woven bone regenerates that bridged the gap were more mature at the comparable observation time. We did not find substantial formation of cartilage, as found by Kojimoto et al.33 and Delloye et al.34 in rabbits. This is an indicator of sufficient stability of the microhydraulic distraction system, as cartilage formation could be interpreted as a result of shear forces acting on the distraction zone.30 In continuous bone distraction, a smaller amount of pressure is sufficient and bony regeneration seems to be accelerated, which may reduce the fixation period. It is often impossible to measure the healing process with the monitoring techniques available today. On the other hand, the mechanical forces can be adjusted by monitoring the pressure during distraction and this may help to evaluate the progress of bone healing in the distraction gap.
The subcutaneous application of the distractor by an intraoral approach prevents external scar formation caused by pin fixation and reduces the risk of infection, as direct contact with the skin is avoided. The whole system can be sterilized and is easy to assemble. REFERENCES 01. Steinhäuser E, Janson I. Kieferorthopädische Chirurgie – Eine interdisziplinäre Aufgabe. Bd I, Berlin: Quintessenz, 1988. 02. Bell WH, Scheidemann GB. Correction of vertical maxillary deficiency: stability and soft tissue changes. J Oral Surg 1981; 39: 666–672. 03. Bell WH, Epker BN. Surgical orthodontic expansion of the maxilla. Am J Orthod 1976; 70: 517–524. 04. Cope JB, Samchukov ML, Cherkashin AM. Mandibular distraction osteogenesis: a historic perspective and future directions. Am J Orthod Dentofacial Orthop 1999; 115: 448–460. 05. Schendel SA, Epker BN. Results after mandibular advancement surgery: an analysis of 87 cases. J Oral Surg 1980; 38: 265–282. 06. 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. 07. Abbot LC. The operative lengthening of the tibia and tibula. J Bone Joint Surg 1927; 9A: 128–135. 08. Samchukov ML, Cherkashin AM, Cope JB. Distraction osteogenesis: origins and evolution. In: McNamara JA Jr, Trotman CA, eds. Advances in Craniofacial Orthopedics, Vol. 34, Craniofacial growth series. Ann Arbor: University of Michigan, Center for human growth and development, 1998: 1–35. 09. Ilizarov GA, Smelyshev NN. Lengthening of the femur with simultaneous closed arthrodesis of the hip joint. Ortop Traumatol Protez 1972; 33: 62–68. 10. McCarthy JG, Schreiber JS, Karp N. Lengthening the human mandible by gradual distraction. Plast Reconstr Surg 1992; 89: 1–8. 11. Klein C, Howaldt HP. Mandibular micrognathism as a sequela of early childhood capitulum fractures and their treatment using distraction osteogenesis. Fortschr Kiefer Gesichtschir 1996; 41: 147–151. 12. Guerrero C. Expansion mandibular quirurgica. Review Venezuela Ortodontica 1990; 1: 48. 13. McCarthy JG, Staffenberg DA, Wood RJ, Cutting CB, Grason BH, Throne CH. Introduction of an intraoral bone-lengthening device. Plast Reconstr Surg 1995; 96: 978–981. 14. Guerrero C, Bell WH, Flores A, Modugno VL, Contasti G, Rodriguez AM. Distraction osteogenica mandibular intraoral. Odontol al Dia 1995; 11: 116–132.
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Continuous and intermittent bone distraction using microhydraulic cylinder 15. Chin M, Toth BA. Distraction osteogenesis in maxillofacial surgery using internal devices: a review of five cases. J Oral Maxillofac Surg 1996; 54: 45–53. 16. Bell WH, Harper RP, Gonzales M, Cherkashin AM, Samchukow ML. Distraction osteogenesis to widen the mandible. Br J Oral Maxillofac Surg 1997; 35: 11–19. 17. Diner PA, Kollar EM, Viguier E, Maurin N, Vasquez MP. Intraoral submerged bidirectional device for mandibular distraction. In: Diner P, ed. Proceedings First International Congress on Cranial and Facial Bone Distraction Processes. Bologna: Monduzzi Editore 1997: 67–74. 18. Ilizarov GA. The tension-stress effect on the genesis and growth of tissues. 1. The influence of stability of fixation and soft-tissue preservation. Clin Orthop 1989; 238: 249–281. 19. Ilizarov GA. The tension-stress effect on the genesis and growth of tissues: II. The influence of the rate and frequency of distraction. Clin Orthop 1989b; 239: 263–285. 20. Wiltfang J, Merten HA. Knochendehnungsgerät: Mikrohydraulikzylinder zur Durchführung einer bidirektionalen, kontinuierlichen Kallusdistraktion. No. 19645392, IPC: A61B 17/68 (04.11.1996), München: Deutsches Patentamt 1998. 21. Wiltfang J, Kessler P, Schultze-Mosgau S, Merten HA, Günther G. Continuous bone distraction with the help of a microhydraulic cylinder. In: Diner P, ed. Proceedings Second International Congress on Cranial and Facial Bone Distraction Processes. Bologna: Monduzzi Editore 1999: 35–40. 22. Günther G. Konstruktion und Entwicklung eines miniaturhydraulischen Knochendistraktors zur Streckung eines Schweineunterkiefers. Fakultät für Maschinenwesen, Institut für Fluidtechnische Antriebe und Steuerungen. RheinischWestfälische Technische Hochschule Aachen. Studienarbeit 1998. 23. Schmelzeisen R, Neumann G, von der Fecht R. Distraction osteogenesis in the mandible with a motor driven plate: a preliminary animal study. Br J Oral Maxillofac Surg 1996; 34: 375–378. 24. Ploder O, Mayr W, Schmetz G, Unger E, Ewers R, Plenk H Jr. Mandibular lengthening with an implanted motor-driven device: preliminary study in sheep. Br J Oral Maxillofac Surg 1996; 37: 273–276. 25. Hönig JF, Merten HA. Das Göttinger Miniaturschwein (GMS) als Versuchstier in der humanmedizinischen osteologischen Grundlagenforschung. Zeitschrift für Zahnärztliche Implantologie 1993; 2: 237–243. 26. Rahn BA. Die polychrome Sequenzmarkierung des Knochens. Acta Nova Leopoldina 1976; 44: 249–253. 27. Donath K. Säge-Schliff-Technik. Fortschr Kiefer Gesichtschir 1983; 28: 97–101. 28. Schenk RK, Gachter A. Histology of distraction osteogenesis. In: Brighton CT, Friedlaender G, Lane JM, eds. Bone Formation and Repair. Rosemont: American Academy of Orthopedic Surgeons 1994: 387–294.
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29. Saleh M, Stubbs DA, Street RJ, Lang DM, Harris SC. Histologic analysis of human lenghtened bone. J Pediatr Orthop 1993; 2: 16–23. 30. Reichel H. Der diaphysauml;re Knochen nach Kallusdistraktion. Densitometrische, biomechanische und histologische Untersuchungen zur operativen Beinverlängerung. München. Zuckschwerdt-Verlag 1996. 31. Panikarovski VV, Grigorian AS Kaganovich SI, Osipian EM, Antipova ZP. Characteristics of mandibular reparative osteogenesis under compression-distraction osteosynthesis: an experimental study. Stomatologiia 1982; 61: 21–25. 32. Karp NS, JG McCarthy JS, Schreiber. Membranous bone lengthening: a serial histological study. Ann Plast Surg 1992; 29: 2–7. 33. Kojimoto H, Yasui H, Goto T. Bone lengthening in rabbits by callus distraction: the role ot periosteum and endosteum. J Bone Joint Surg 1988; 70A: 543–549. 34. Delloye C, Deletortrie G, Gautelier L. Bone regenerate formation in cortical bone during distraction lengthening: an experimental study. Clin Orthop 1990; 250: 34–42.
The Authors J. Wiltfang MD, DMD, PhD Associate Professor P. Keßler MD, DMD Senior Resident F. W. Neukam MD, DMD, PhD Professor and Chairman Department of Oral and Maxillofacial Surgery University of Erlangen-Nuremberg Erlangen, Germany H.-A. Merten MD, DMD, PhD Assistant Professor Department of Oral and Maxillofacial Surgery University of Göttingen Göttingen, Germany Correspondence and requests for offprints to: Jörg Wiltfang MD, DMD, PhD, Associate Professor, Department of Oral and Maxillofacial Surgery, University of Erlangen-Nuremberg, Glückstrasse 11, 91054 Erlangen, Germany. Tel:;49 9131 8533616; Fax:;49 9131 8534219; E-mail: [email protected] Paper received 25 January 2000 Accepted 22 September 2000 Published online 18 January 2001
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British Journal of Oral and Maxillofacial Surgery (2001) 39, 2–7 © 2001 The British Association of Oral and Maxillofacial Surgeons doi: 10.1054/bjom.2000.0564, available online at http://www.idealibrary.com on
BRITISH
Journal of Oral and Maxillofacial Surgery
Continuous and intermittent bone distraction using a microhydraulic cylinder: an experimental study in minipigs J. Wiltfang,* P. Keßler,* H.-A. Merten,† F. W. Neukam* *Department of Oral and Maxillofacial Surgery, University of Erlangen-Nuremberg; †Department of Oral and Maxillofacial Surgery, University of Göttingen, Germany SUMMARY. Distraction osteogenesis of the mandible is an option in the treatment of mandibular hypoplasia. Today, only intermittent distraction devices are available for clinical application. The aim of this study in minipigs was to evaluate continuous bone distraction using a microhydraulic cylinder. After a seven-day interval, continuous or intermittent distraction of 1.5 mm/day was established for 10 days. Immediately after active distraction, two animals and 20 days later the other four animals were killed and radiographs taken. The mandible was then removed en bloc and the distracted bone examined histologically. Intermittent distraction forces of up to 2500 kPa were necessary to move the cylinders’ piston. The pressure needed for continuous distraction was considerably lower (1200–1300 kPa). While the specific histological structure of the varying zones in the distraction gap was similar after continuous and intermittent distraction, bone healing was accelerated after continuous distraction as shown by ultrasonography and scanning electron microscopy. © 2001 The British Association of Oral and Maxillofacial Surgeons
(Mandibular distraction with corticotomy: analysis of the bone elongation and soft tissue expansion. Paper presented at 63rd Annual Meeting of the American Society of Plastic and Reconstructive Surgery 1994), and Klein and Howaldt11 recognized the importance of this method and introduced it for the treatment of congenital craniomaxillofacial anomalies. The first craniomaxillofacial application was in the distraction of hypoplastic mandibles.12–17 The importance of the extent and frequency of distraction on bone healing was recognized by llizarov.18,19 The distraction rate of 1 mm/day proved to be optimal. Higher rates led to pseudarthrosis, and lower rates to rapid bone healing. On the other hand, llizarov18,19 found that increased frequency of distraction formed bone of a better quality. The devices available today for clinical use do not allow continuous distraction. The microhydraulic distraction cylinder used in the present study was invented and patented by Wiltfang et al. in 199620,21 and developed in cooperation with an engineering team from the University of Aachen, Germany.22 This microhydraulic cylinder allows continuous as well as intermittent distraction through a remote control device, which is fixed on the experimental animal’s back (with no moving elements in direct contact with skin or mucosa) and allows pressure monitoring during distraction. In contrast to motor driven devices described
INTRODUCTION Maxillomandibular hypoplasia, facial asymmetry, and congenital micrognathia are common abnormalities of the craniofacial skeleton. In adults, these deformities are usually treated by osteotomies and skeletal fixation.1–3 Despite the fact that orthognathic surgery has had widespread success, the treatment has several limitations,4 including the inability of the muscles to be stretched acutely. The soft tissues will not accommodate extended musculoskeletal movements, which are required for many congenital deformities, unless additional soft tissue procedures are performed.5 An alternative approach is callus distraction, which was first described by Codivilla6 and Abbot7 for long bones. New bone forms between the surfaces of bone segments, which are gradually separated by incremental traction. The distraction forces also create tension in the surrounding tissues. Adaptive changes – so-called distraction histiogenesis8 – subsequently occur in different tissues, including skin, fascia, nerves, blood vessels, ligaments, cartilage, and periosteum and allow larger skeletal movements. Distraction osteogenesis was rediscovered by Ilizarov and Smelyshev9 and introduced into clinical use. Nowadays it has become an established method in orthopaedics and traumatology with many skeletal applications. McCarthy et al.,10 Molina and Ortiz-Monasterio 2
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by Schmelzeisen et al.23 and Ploder et al.,24 which do not have a pressure monitoring, the hydraulic system is less complicated and, although it is small, it allows the generation of high pressures. We aimed to record pressure values in continuous and intermittent distraction osteogenesis, and to compare histological findings using light and scanning electron microscopy. The process of distraction was followed by ultrasonography. MATERIAL AND METHODS Description of the microhydraulic cylinder The hydraulic unit consists of a cylinder and a piston both made from medical grade steel. The cylinder has an external diameter of 9 mm and is small enough to be implanted subcutaneously (Fig. 1). The mechanical properties of the cylinder/piston unit are similar to those of a conventional reconstruction plate. Shearing forces (like bite forces) of up to 50 N are therefore well tolerated. Piston and cylinder are protected against rotational forces by a slot and key mechanism. The maximum piston extension is 25 mm. The distractor is fixed with four bicortical screws, and the integrated fixation plate of the piston is adjustable to allow adaptation to the underlying bone. All metal parts of the distractor can be steam sterilized. The seals and the hydraulic tube can be disinfected. The whole system is simple to assemble. The distraction device is connected to an extracorporal steering unit through a flexible hydraulic tube. The injector system can be activated manually once a day for intermittent distraction. To allow continuous distraction an automatic hydropneumatic injector system is attached to the microhydraulic cylinder and the hydropneumatic injector system is loaded with carbon dioxide once a day to ensure constant pressure on the hydraulic fluid.
Fig. 1 Protoype of the microhydraulic distractor.
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Saline is used as the hydraulic medium. Both injector systems can generate a maximum distraction force of 45N and are connected to a pressure receptor to allow pressure measurements during distraction. Animal experiment Six adult, female Göttingen miniature pigs were chosen as test animals. The minipig is particularly suitable for bone regeneration studies, but the bone apposition rates (1.2 m/dy) of the pig are slightly faster than the rate in humans (0.8 m/dy).25 A distraction rate of 1.5 mm was therefore used to achieve comparable results. Protocol and guidelines were approved by the Committee of Ethics of the University of Erlangen/ Nuremberg and the responsible administrative district (permission: 509.42502/01.11.98). After endotracheal intubation, the right mandibular angle was exposed by a submandibular approach and an osteotomy was made distal to the row of teeth. Importance was placed on the preservation of the inferior alveolar nerve and vessel bundle. The microhydraulic distraction cylinder was fixed with two 3.5-mm bicortical screws (Leibinger-Stryker, Freiburg, Germany) on each side of the osteotomy gap (Fig. 2). The hydraulic tube was connected to the cylinder and placed in a subcutaneous tunnel. The flexible tube punctured the animal’s skin in the dorsal neck region and was connected to the injector system, which was fixed on the animal’s back. Distraction started a week after the operation. We estimated to gain about 12–15 mm of bone. In three animals (group 1) the microhydraulic cylinder’s piston was extended at a rate of 1.5 mm/24 h by the automatic hydro-pneumatic injector system to achieve continuous distraction. In the other three animals (group 2), the piston was activated manually once a day to achieve intermittent distraction of the same extent. During the observation period, daily distraction pressure measurements were recorded by a connectable pressure receptor. Ultrasound examinations were made once a
Fig. 2 Microhydraulic distractor in situ on a pig’s mandible.
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week to follow the distraction process. After 10 days of active distraction one animal in each group was killed. After a further 20 days of a fixation period the other two animals from each group were killed. The distracted bone segment of the mandible was resected, and after conventional radiographs had been taken the bone was prepared for light- and scanning electron microscopy (EM). Histological examination During the intervals of observation, a polychrome sequence marking with tetracycline, calceine green, xylenol orange and alizarin-complex was done using the dosage mentioned by Rahn.26 An intra-arterial angiogram with a suspension of Berlin blue and barium sulphate was taken before the animals were killed. The specimens were fixed in 2.5% glutaraldehyde. Nondecalcified thin sliced sections of bone were examined by light- and fluorescence microscopy.27 Additional specimens were decalcified in solutions containing increasing concentrations of alcohol. They were then dried by the critical point drying method with liquid carbon dioxide and coated with gold/palladium. These probes were examined by scanning EM (Zeiss DSM 960).
RESULTS Insertion of the microhydraulic cylinder was easy. Bicortical screw fixation gave sufficient stability and the distraction devices were well tolerated by the animals. Even pressure peaks of more than 3000 kPa caused by masticatory action did not loose of the device. Feeding the animals orally during the observation period was no problem. One animal developed a local inflammation
where the hydraulic tube emerged from the skin, which resolved after local treatment with antibiotics (Tardomyocel™, Bayer, Leverkusen, Germany). In all animals, the intended amount of distraction of 14–15 mm was achieved. During distraction in the intermittent group, pressure monitoring showed a gradual increase in the pressure needed to activate the device during the first four days. Pressure peaks of up to 2400 kPa were reached immediately after activation of the device. Thirty minutes later the pressure had fallen substantially and reached a level of 800 to 900 kPa after 2 to 4 hours (Fig. 3). The high pressure peaks were seen only in intermittent distraction. With continuous distraction a mean pressure of 1200–1300 kPa was sufficient to move the piston a distance of 1.5 mm in a 24 hour period (Fig. 4). Ultrasonography was a valuable tool in monitoring the process of reossification in the distraction gap. After continuous distraction (group 2), ultrasonography showed accelerated consolidation of the bone in the osteotomy gap compared with group 1. The reduced penetration of ultrasonic waves in the distraction gap showed faster bony reorganization with continuous bone distraction. Histological examination showed a specific zonal structure in both groups. The central fibrous zone was poorly mineralized and consisted of longitudinally orientated bundles of collagenous fibre. At the periphery of this central area was a zone of extended bone formation. A zone of longitudinally orientated primary bone formation followed and ended adjacent to the former osteotomy. After active distraction the fibrous interzone ossified and woven bone regenerated to bridge the gap. Cartilage was rarely found. While the specific zonal structure was found following continuous as well as intermittent distraction, the newly formed bone was more mature after continuous distraction. Fluorescence microscopy of the central fibre zone 20 days after the end of active distraction showed that ossification in the
Fig. 3 Pressure monitoring diagram of intermittent manual distraction, 11.5 mm/day for 10 days.
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centre of the distraction zone was more mature after continuous (Fig. 5a) than intermittent distraction (Fig. 5b). This was also shown by scanning EM as spongy bone formation in the central distraction zone which seemed to be more mature after continuous distraction (Figs 6a,b).
DISCUSSION Distraction osteogenesis consists mainly of three sequential periods: latency, distraction, and consolidation. The histological findings in the distraction gap resemble the histological changes during healing of a fracture: inflammation, soft callus, hard callus, and remodelling.8 During distraction, the soft callus period is interrupted
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by the application of gradual traction. The fibrous tissue becomes longitudinally orientated along the axis of distraction, and the distraction gap is characterized by a specific zonal structure. A poorly mineralized fibrous zone is located in the centre and consists of longitudinally orientated bundles of collagenous fibres. At the periphery of the central area a zone of longitudinally orientated cylindrical primary osteons follows. This zone resembles a bone growth zone adjacent to the osteotomy. After the end of distraction, the fibrous interzone ossifies and woven bone regenerates to bridge the gap. After resorption of the primary osteons, further maturation and lamellar reorganization of the bone in the distraction zone continues for a year or more until the newly formed bone has the same structure as the pre-existing
Fig. 4 Pressure monitoring diagram of mean continuous distraction, 1.5 mm/day for 10 days.
Fig. 5 (a) Histological specimen showing a zonal structure, which was found in both groups. A central fibrous zone, a zone of extended bone formation, a zone of longitudinally orientated osteons, and the osteotomy zone. Fluorescence microscopy of the central fibre zone 20 days after end of active continuous distraction showed mature woven bone regenerates C: corticotomy zone, R: row of micropillars, W: woven bone regenerates (undecalcified thin sliced section, fluorescence microscopy, original magnification 4). (b) Fluorescence microscopy of the central fibre zone 20 days after end of active intermittent distraction showed that ossification of the centre of the distraction zone was not as mature as after continuous distraction C:corticotomy zone, R: row of micropillars, W: woven bone regenerates (undecalcified thin sliced section, fluorescence microscopy, original magnification 4).
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Fig. 6 (a) The woven bone regenerates looked mature after continuous distraction (scanning EM, original magnification 100). (b) The woven bone regenerates after intermittent, discontinuous distraction appeared to be not as advanced than after continuous distraction (7a) (scanning EM, original magnification 100).
bone.28–30 These histological changes were also found in distraction of long bones. In 1982 Panikarovski et al.31 were the first to present histological findings after mandibular (membranous bone) distraction in dogs. Their group also found a fibrous interzone in the centre of the distraction gap with collagenous fibres orientated parallel to the axis of distraction. Longitudinally orientated trabeculae originated from the osteotomy zone and progressed towards the fibrous zone. Karp et al.32 differentiated four zones: a central zone of fibrous tissue, a zone of extended bone formation, a zone of bone remodelling, and a zone of mature bone. In summary, the mechanism of bone formation after distraction of membranous bone are similar to those following distraction of long bones. While the specific histological zonal structures of the distraction gap in our study were similar in both distraction methods and in accordance with the results of Panikarovski et al.31 and Karp et al.,32 bone healing after continuous distraction was accelerated as shown by ultrasonography and scanning EM. The woven bone regenerates that bridged the gap were more mature at the comparable observation time. We did not find substantial formation of cartilage, as found by Kojimoto et al.33 and Delloye et al.34 in rabbits. This is an indicator of sufficient stability of the microhydraulic distraction system, as cartilage formation could be interpreted as a result of shear forces acting on the distraction zone.30 In continuous bone distraction, a smaller amount of pressure is sufficient and bony regeneration seems to be accelerated, which may reduce the fixation period. It is often impossible to measure the healing process with the monitoring techniques available today. On the other hand, the mechanical forces can be adjusted by monitoring the pressure during distraction and this may help to evaluate the progress of bone healing in the distraction gap.
The subcutaneous application of the distractor by an intraoral approach prevents external scar formation caused by pin fixation and reduces the risk of infection, as direct contact with the skin is avoided. The whole system can be sterilized and is easy to assemble. REFERENCES 01. Steinhäuser E, Janson I. Kieferorthopädische Chirurgie – Eine interdisziplinäre Aufgabe. Bd I, Berlin: Quintessenz, 1988. 02. Bell WH, Scheidemann GB. Correction of vertical maxillary deficiency: stability and soft tissue changes. J Oral Surg 1981; 39: 666–672. 03. Bell WH, Epker BN. Surgical orthodontic expansion of the maxilla. Am J Orthod 1976; 70: 517–524. 04. Cope JB, Samchukov ML, Cherkashin AM. Mandibular distraction osteogenesis: a historic perspective and future directions. Am J Orthod Dentofacial Orthop 1999; 115: 448–460. 05. Schendel SA, Epker BN. Results after mandibular advancement surgery: an analysis of 87 cases. J Oral Surg 1980; 38: 265–282. 06. 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. 07. Abbot LC. The operative lengthening of the tibia and tibula. J Bone Joint Surg 1927; 9A: 128–135. 08. Samchukov ML, Cherkashin AM, Cope JB. Distraction osteogenesis: origins and evolution. In: McNamara JA Jr, Trotman CA, eds. Advances in Craniofacial Orthopedics, Vol. 34, Craniofacial growth series. Ann Arbor: University of Michigan, Center for human growth and development, 1998: 1–35. 09. Ilizarov GA, Smelyshev NN. Lengthening of the femur with simultaneous closed arthrodesis of the hip joint. Ortop Traumatol Protez 1972; 33: 62–68. 10. McCarthy JG, Schreiber JS, Karp N. Lengthening the human mandible by gradual distraction. Plast Reconstr Surg 1992; 89: 1–8. 11. Klein C, Howaldt HP. Mandibular micrognathism as a sequela of early childhood capitulum fractures and their treatment using distraction osteogenesis. Fortschr Kiefer Gesichtschir 1996; 41: 147–151. 12. Guerrero C. Expansion mandibular quirurgica. Review Venezuela Ortodontica 1990; 1: 48. 13. McCarthy JG, Staffenberg DA, Wood RJ, Cutting CB, Grason BH, Throne CH. Introduction of an intraoral bone-lengthening device. Plast Reconstr Surg 1995; 96: 978–981. 14. Guerrero C, Bell WH, Flores A, Modugno VL, Contasti G, Rodriguez AM. Distraction osteogenica mandibular intraoral. Odontol al Dia 1995; 11: 116–132.
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The Authors J. Wiltfang MD, DMD, PhD Associate Professor P. Keßler MD, DMD Senior Resident F. W. Neukam MD, DMD, PhD Professor and Chairman Department of Oral and Maxillofacial Surgery University of Erlangen-Nuremberg Erlangen, Germany H.-A. Merten MD, DMD, PhD Assistant Professor Department of Oral and Maxillofacial Surgery University of Göttingen Göttingen, Germany Correspondence and requests for offprints to: Jörg Wiltfang MD, DMD, PhD, Associate Professor, Department of Oral and Maxillofacial Surgery, University of Erlangen-Nuremberg, Glückstrasse 11, 91054 Erlangen, Germany. Tel:;49 9131 8533616; Fax:;49 9131 8534219; E-mail: [email protected] Paper received 25 January 2000 Accepted 22 September 2000 Published online 18 January 2001