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Healing process after alveolar ridge distraction in sheep
Healing process after alveolar ridge distraction in sheep Alexander Gaggl, MD, DDS,a Günter Schultes, MD, DDS,a Siegrid Regauer, MD,b and Hans Kärcher, MD, DDS, PHD,c Graz, Austria UNIVERSITY HOSPITAL GRAZ
Objective. Mandibular augmentation by distraction of the alveolar ridge has been in use for several years. Since 1996, a distraction device that remains in the alveolar ridge after distraction has been used by the Department of Oral and Maxillofacial Surgery of Graz University. The distraction device is transformed into a dental implant after the end of the distraction process and can later be used for prosthetic purposes. We aimed to show the application of the device in this animal experiment and to follow the osseous healing process. Study design. Two distraction implants were inserted into the mandibles of 8 sheep. Distraction of 0.5 mm per day was carried out for 8 days. Two sheep were killed 1, 2, 3, and 6 months after distraction, and the dissected mandibles were examined clinically, radiologically, and histologically. Results. After the first month of distraction, only slight radiopacity of the distraction gap was found. This increased steadily up to the third month after distraction. The boundary between the distraction fragments and the gap disappeared gradually. Six months after distraction, a homogenous fine-meshed spongiosa structure was found in the area of distraction. Histologic examination showed desmoid ossification in the distraction gap and a continued increase in osteoid. After 6 months, mature bone was found. Only in the center was the rebuilding process not complete. Six months after distraction, osseointegration of the implants was shown in the region of the screw thread and distraction cylinder. Conclusions. The healing process corresponded to that found in long bones, but showed only desmal ossification. Osseous integration of the distraction implants was found 6 months after distraction, although the implants were stable 3 months after distraction. (Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000;90:420-9)
Callus distraction, first described by Codivilla1 in 1905, has long been used to provide autologous bone. Since standardization of the method by Ilizarov2,3 in the 1960s, the method has been used mainly in orthopedic surgery to lengthen long bones. However, not only long bones are capable of forming new bone. In recent years the method has been used to cover defects of the facial skeleton. Its main use in oral and maxillofacial surgery has been to correct severe growth defects in the mandible and maxilla. At the Second International Congress of Cranial and Facial Bone Distraction Processes in Paris in June 1999, callus distraction was advocated mainly for childhood syndromes and sleep apnea symptoms that require surgery because the results of osteotomy are rarely satisfactory.4-10 Distraction devices have been used to ventralize the hypoplastic maxilla and midface to correct congenital syndromes11,12 and for horizontal elongation of the mandible in patients with extensive mandibular microsomia.13-17 The advantage of callus aSenior
surgeon, Department of Oral and Maxillofacial Surgery. Institute of Pathology. cHead, Department of Oral and Maxillofacial Surgery. Received for publication Dec 3, 1999; returned for revision Feb 22, 2000; accepted for publication May 31, 2000. Copyright © 2000 by Mosby, Inc. 1079-2104/2000/$12.00 + 0 7/12/109159 doi:10.1067/moe.2000.109159 bPathologist,
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distraction is the slow but controlled correction of features, which can be improved by orthognathic surgical procedures but which, because of rigid fixation, does not allow long-term prospective correction. Callus distraction is a dynamic procedure with the possibility of overcorrection; thus it is important to take into consideration the later completion of correction by functional orthodontic treatment.18 By using intraoral callus distractors, ugly scars can be avoided.19 Callus distraction of the facial skeleton, as in orthopedic surgery, is usually done in young people whose bones have high potential for regeneration. A new possibility in the treatment of maxillofacial problems is the use of distractors in the reconstruction of defects of the mandible after tumor resection in adults. The use of osteo-transport-distractors enables reestablishment of mandibular continuity by using the method of callus distraction. Shvyrkov et al20 described the use of distractors in the closure of defects in the continuity of the mandible after tumor resection and the use of osteo-transport-distractors even in bones affected by radiotherapy, which might be expected to have less regenerative capacity. The reconstruction of missing bony structure is the first step in using this technique to reestablish structural qualities of the alveolar ridge and to enable further prosthetic treatment in elderly patients in whom poor regenerative powers are expected. The covering of
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defects in the mandible after tumor resection is an important therapeutic indication. However, defects in the mandible are rare compared with alveolar defects caused by trauma, periodontitis, or loss of bone as a result of atrophy of edentulous segments of the alveolar ridge. Block et al21 described a successful alveolar ridge augmentation with an intraorally placed distractor in preparation for later dental implantation in an experimental study in animals. The use of this method in humans was first described by Chin and Toth22 in 1996. They used alveolar ridge distraction to reconstruct a defect after loss of teeth from trauma. Both distraction methods, described by other authors as well, constituted a preparation for the later implant site.23-30 Thus the use of callus distraction for the augmentation of deficient mandibular segments, even in elderly patients with reduced osteogenic potential, and the possibility of improving the implant site by the technique of alveolar ridge distraction were shown. Until now the healing process has been verified only for callus distraction of the long bones and of the mandibular ramus and corpus.31-34 In the case of alveolar ridge distraction, however, other surgical and morphologic conditions must be considered regarding osseous healing. Extensive removal of the periosteum of the small distraction fragment is needed, which remains pedunculated to the soft tissue. Because of the need for gingival cover and perfusion, a different arrangement is required compared with other regions of the jaw. Total cover of the deficient alveolar ridge is the aim, to satisfy the esthetic demands of surgeons and patients. The methods of alveolar ridge distraction described above demand a 2-step or 3-step procedure: insertion and removal of the distractor and insertion of the implant.24,27 We aimed to simplify the operation and reduce the operative time and the inconvenience to patients by a system that unites the qualities of a distractor with those of a dental implant.35 This distraction implant has been evaluated in the Department of Oral and Maxillofacial Surgery of Graz University since 1996. Special conditions have to be met even after distraction has been completed. Among these is that the distraction implant must be fully integrated in the bone to ensure a good prosthetic result in the long term. The recommended time for initial loading by a prosthetic superstructure was based on empirical data, although the closure of the distraction gap with bone and osseous integration of the implant surface is of vital importance for any implant. We aimed to verify the time for loading these implants to ensure a successful long-term outcome. We studied the development of callus in the distraction gap and the osseointegration of distraction
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Fig 1. The 11-mm distraction implant, a self-cutting conical titanium screw implant.
implants in animals. We selected sheep, following the work of Sawaki et al,36 who successfully carried out horizontal distraction of the mandibular corpus with implant-based supported distractors in sheep.
DESCRIPTION OF THE DISTRACTION IMPLANT The distraction implant (SIS-Trade Inc, Klagenfurt, Austria) combines the qualities of a callus distraction device with those of a dental implant. It comprises a conical chemically pure titanium screw with a maximum diameter of 4.1 mm (Fig 1). At present it is available in lengths of 7, 9, 11, and 13 mm. In the undistracted state ready for insertion it has the qualities of a self-cutting conical screw with 0.2 mm screw thread profile depth and a pitch of 0.6 mm in the coronal and apical portion. The apical part contains the distraction
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Fig 3. Scheme of distraction implant after modification into definitive design. Now it is a combined screw and cylinder implant. Fixation screw fills center of implant. Head of implant can be used for later prosthetic superstructures.
Fig 2. The 11-mm distraction implant partly distracted. Distraction cylinder can be activated by central screw with coronal approach.
cylinder 6.5-mm long located in the coronal implant part telescopically (Fig 2). The distraction screw lies in the center of the distraction cylinder. It is 6 mm long and lies free in the distraction chamber in the coronal implant region. The distraction chamber lies in the distraction head of the implant. The roof of the distraction chamber allows adequate screw support on activation of the distractor. This takes place by a left turn of the distraction screw. The screw thread is synchronized so that a left turn of 360 degrees corresponds to a 0.25 mm movement in the implant transition region. Activation of the distraction screw and thus the head of the distractor is carried out through coronal access with the aid of a distraction screw driver. This may be placed on the hexagonal-shaped coronal screw head and turned to the left in 90-degree steps.
The distraction head is 4 mm in height and exceeds the implant neck by this length. After distraction, the head of the distractor can be replaced by a conventional implant head, and the distractor is thus transformed to an implant (Fig 3). All components of the implant are of titanium medical grade 4 and 5. Both implant heads are polished. The surface of the screw implant is roughened by laser treatment to achieve a greater surface. The surface structure is created in an atmosphere of inert gas by placing individual hollows with special optical devices in front in an exactly defined grid. The depth of primary roughness is 30 to 50 µm. Further roughness is created on the surface of the ridges and hollows through melting transformation of the lasered area. The depth of these secondary roughnesses is 2 to 10 µm. For functional reasons the surface of the distraction cylinder is smooth or machine roughened. The microroughness measures 2 µm. The coronal osseous part of the implant is also machine roughened over a length of 1.5 mm to enable cleaning of the neck part of an exposed implant during wound healing.
MATERIAL AND METHODS We used 8 adult sheep with a mean age of 3 years. The operations were carried out with the animals under balanced combination anesthesia.
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Fig 4. Intraoperative photograph after segmental osteotomy and insertion of 2 distraction devices.
The first step was the injection into an ear vein of 0.1 mg/kg Gewacalm and 0.1 mg/kg atropine sulfate; this was followed by orotracheal intubation. Initially, anesthesia was with 4 µg/kg fentanyl and 1.5 mg/kg Hypnomidate. Relaxation was achieved with 0.5 mg/kg Pavulon. Further anesthesia was by insufflation of nitrous oxide, 50%, and 0.8% to 1.2% Forane. After disinfection of the operation site, an incision was made in the edentulous left anterior portion of the mandibular alveolar ridge, and a mucoperiosteal flap was prepared. The alveolar process was then reduced by 4 mm with a milling machine, and a plane implant site of 3 cm mesiodistal length was created. A horizontal osteotomy was done 5 mm away from the implant plateau with an oscillating microsaw over the entire plateau length of 3 cm. Two distraction implants 11 mm in length were inserted into the alveolar ridge. The implant site was hollowed by core and pilot drilling preceded by parallel drilling. The osteotomy was completed in the lateral segment by vertical incisions (Fig 4). To ensure free mobility of the segments, the wound was closed with absorbable suture material after an intraoperative trial of distraction. After extubation and injection of analgesia (subcutaneously) (Tramal, 100 mg) and prophylactic antibiotics (intramuscularly) (Retarpen, 2.4 mg), the animals were returned to the stables and were given feed pellets soaked in water for 1 week. After this 7-day healing period, distraction was initiated. No further medication was given, and distraction was carried out in steps of 0.5 mm daily by activation of the distraction cylinder twice
a day (1 turn every 12 hours). Distraction was carried out for 8 days. After this, both implants were blocked by a bridge of polymethylmethacrylate to facilitate healing of the distraction implant. The implants were allowed to heal for 1, 2, 3, or 6 months before 2 sheep at each time were killed by an overdose of Ketalar, and the specimens were dissected. Initially, the condition around the implant was assessed by probing the gap with a periodontal probe. This was done mesially, distally, orally, and vestibularly in the 4 distinct regions of the implant. The greatest probing depth was noted. Further clinical assessment was made of the horizontal mobility of the implant. Measurements were made with the Periotest apparatus (Siemens, Erlangen, Germany) at right angles to the implant axis. This was repeated 5 times for each implant. The highest and lowest values were rejected, and the median of the 3 remaining values was recorded. Enoral radiographs of the distraction region were taken. The edentulous distracted alveolar process region and the nondistracted contralateral alveolar process (reference) were removed from the dissected skull. From the region between the distraction implants, a 5-mm–wide bone wedge was removed and examined histologically. After decalcification of the specimen, fixation in formalin, histologic preparation, and staining with hematoxylin-eosin, the specimens were examined under a light microscope (Wild M3Z; Leica, Hildesheim, Germany). The segments of alveolar process carrying the distraction implants that were obtained 6 months after distraction were treated differently. These specimens were treated by fixation in 5% formaldehyde solu-
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Fig 5. Radiograph 1 month after distraction.
Fig 6. Radiograph 3 months after distraction.
tion according to Lillie (pH 7.3) and dehydrated increasingly with ethanol; the fat was removed with ether-chloroform and they were soaked with MMA monomer before finally being polymerized into blocks. With the aid of an internal cleavage saw, 3 slices were cut out of the
middle of the bone implant complex, polished, and stained with Giemsa or by the method of Kossa and Paragon (fuscin and toluidine blue) and assessed morphometrically and histologically with a light microscope (Wild M3Z, Leica; and Metaval; Zeiss, Jena, Germany).
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Fig 7. Radiograph 6 months after distraction.
Fig 8. Histologic specimen (hematoxylin-eosin, original magnification ×22.5). Two months after distraction, granulation tissue decreases and osteoid increases.
RESULTS Radiologic examination 1 month after distraction showed slight opacity of the distraction gap. In the transitional zone of the distraction segments, a blurring of the zonal limits was seen (Fig 5). After 2 months, this effect was more pronounced with reduction in
radiotranslucence in the distraction gap. However, differences in radiotranslucence between the segments and the distraction gap were clearly visible. After 3 months, the distraction gap was more radiopaque, and its density was comparable with that of the distraction segments. Distraction gap and distraction segments
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Fig 9. Histologic specimen (hematoxylin-eosin, original magnification ×56). After 6 months, mature bone is seen in distraction gap. Remodeling still going on in center of distraction only.
were still clearly distinguishable (Fig 6). Only after 6 months was there a homogenous radiologic structure of the distracted alveolar process. The typical spongy bony structure was almost identical to that of the nondistracted opposite side (Fig 7). Histologic examination of the distraction gap showed the presence of callus in the gap; the ossification was mainly mesenchymal with large amounts of soft tissue and collagen fibers. Osteoid was seen in the region near the segments of distraction and small amounts of chondroid tissue in the central area. In the second month after distraction, a further increase in osteoid in the central distraction region was found, as was a reduction in the number of collagen fibers. There was extensive vascularization in the area close to the distraction segments. The chondroid tissue had completely disappeared. Signs of lamellar ossification were seen at this stage. Zones of calcification (cement lines) were seen occasionally (Fig 8). There were many more cement lines by the third postdistractional month, and the bone continued to mature. Lamellar bone was now seen in the central part of the bone, and connective tissue had become rare. In the region of distraction, the osteoid was increasingly calcified with lacunar resorption and restructuring of the mature bone. Six months after distraction, restructuring was also present at the edges of the distracted region (Fig 9). In the central region, single islands of mature restructured bone were seen. The tissue around the implant showed a bone apposi-
tion surface of 70% to 80% in the implant screw thread area in the sixth postdistractional month. The distraction cylinder had an apposition surface of 60% to 70%. Clinical results of peri-implant probing and Periotest values are shown in Table I.
DISCUSSION Since Sawaki et al36 described vertical distraction of the mandible by means of implant barred distractors, sheep have been accepted as suitable animals for combined distraction and implantation. In contrast to Sawaki et al, our experiment dealt with alveolar distraction of the mandible, which was first described by Block et al21 in 1996 in an animal model. Block et al examined beagle dogs treated in a 2-stage procedure by alveolar ridge distraction and later by insertion of an implant in the distracted bone. These authors, along with Nosaka et al,37 reported osseous integration of dental implants in distracted callus. They showed the typical radiologic and histologic healing process leading to an osseous integration of 70% of the surface of the implant as early as 12 weeks after insertion of the implant. Our experiments showed a similar result with distraction implants after 6 months. This value (similar to normal osseous integration of implants in bone) applied only to the laser-treated screw thread, whereas the total area of osseous integration in the smooth distraction cylinder area still lagged behind the implant—about 65%, 6 months after distraction. The
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Table I. Clinical results Sheep number
Implant number
Months after distraction
Probing depth (mm)
Periotest value
1
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16
1 1 1 1 2 2 2 2 3 3 3 3 6 6 6 6
3 4 2 3 3 2 3 3 3 3 4 3 2 2 2 3
+5 +5 +6 +7 +3 +4 +4 +4 +1 +1 +1 –2 –3 –1 0 –1
2 3 4 5 6 7 8
osseous integration was greater than that found after other augmentation techniques.37 The process of restructuring in the distraction gap containing the implant was not complete 6 months after distraction. With continual increase in mature bone structure in the other parts of the distraction gap, a further increase in bone is to be expected. Nocini et al32 reported that the restructuring process continued as late as 1 year after horizontal distraction of the mandible in spite of the homogeneous bony structure found on radiographic examination. This was also seen in our experiment 6 months after distraction. In spite of the distraction gap having completely disappeared and the homogeneous radiologic findings, incompletely calcified bony structures were in the center of the distraction. Only a few chondral cells were seen in the early postdistractional phase, and they were found mainly in the center of the distraction region, which appeared to be vascularized to a lesser extent than the peripheral parts. In the peripheral parts, laminar bone production with several osteoblasts and osteoid formation was seen. This phase of the distraction corresponded to the longitudinal polarization phase found by Wiedemann31 in the long bones from the tenth postoperative day to the second postoperative month. As early as the second postoperative month, in agreement with Wiedemann, we found continuous fading of the transition zone from local bone to the distraction region with an increase in characteristic changes from the third to the sixth postoperative month. Radiographs showed an increase in opacity in this region. Histologic examination showed fusion of the distraction fragments over the distraction gap with calcification of the osteoid already taking place and the appearance of numerous osteo-
clasts. This was the ossification period.31 It was only after 6 months that signs of the consolidation period were found with the formation of a neocortex and the appearance of mature local bony tissue in all areas of distraction. The question arises about the timing of stability sufficient for application of prostheses. It might be expected that enough stability would be achieved only after completion of the entire restructuring process. However, the tendency in implantology is for early loading of conventional implants,38 so that early application of prosthetic structures also seems appropriate for distraction implants. Sufficient implant stability is achieved 3 months after distraction (Periotest values <+3). Histologic findings suggest high implant stability at this time, so that it appears to be adequate for loading by prosthetic superstructures, particularly as the peri-implant gingiva has healed normally.
CONCLUSION Sheep are an adequate animal model for alveolar ridge distraction with distraction implants. The healing process of the distraction gap corresponds to that of other bones and is not completed by the sixth postoperative month. However, within 3 months after distraction, an adequate osseous basis has been created, providing implant stability and allowing further prosthetic treatment. Osseous integration within the distraction cylinder is delayed, which may be explained by the slow maturing of bone in the center of the distraction. Six months after distraction, good osseous integration is achieved with an implant bone surface area of about 70%. However, results from experiments with animals may not reflect the healing process in humans. Clinical studies are needed to evaluate the method further.
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REFERENCES 1. Codivilla A. On the means of lengthening, in the lower limbs, the muscles and tissue which are shortened through deformity. Am J Orthop Surg 1905;2:353-9. 2. Ilizarow G. Sammelband der orthopädischen Gesellschaft Kurgan 1954;1:146-54. 3. Ilizarow G. Sammelband der wissenschaftlichen Gesellschaft Kurgan. 1954;1:155-60. 4. Gellrich NC, Gutwald R, Lagreze W, Lauer G, Velthoven V, Schmelzeisen R. Orbital growth simulation in a rare case of M. Crouzon combined with a Kleeblattschädel. 2nd International Congress Cranial and Facial Bone Distraction Processes. Abstract book; 1999 June; Paris. Bologna, Italy: Monduzzi Editore; 1999. p. 66. 5. Kessler P, Wiltfang J, Erbe M, Merten HA, Neukam FW. Distraction osteogenesis in complex syndromal disease. International proceedings, 2nd International Congress Cranial and Facial Bone Distraction Processes. Abstract book; 1999 June; Paris. Bologna, Italy: Monduzzi Editore;1999. p. 107-11. 6. Kreusch T, Terheyden H, Fleiner B. The Silver Russel syndrome, a rare indication for bilateral mandibular distraction osteogenesis. 2nd International Congress Cranial and Facial Bone Distraction Processes. Abstract book; 1999 June; Paris. Bologna, Italy: Monduzzi Editore;1999. p. 80. 7. Ortitz Monasterio F, Molina F. DOG in Pierre Robin sequence and related respiratory problems in children. 2nd International Congress Cranial and Facial Bone Distraction Processes. Abstract book; 1999 June; Paris. Bologna, Italy: Monduzzi Editore; 1999. p. 70. 8. Vazquez MP, Soupre V, Karcenty B, Renault F, Garabedian EN, Bahuau M, et al. The Pierre Robin sequence—a non-indication of early mandibular distraction in our experience. 2nd International Congress Cranial and Facial Bone Distraction Processes. Abstract book; 1999 June; Paris. Bologna, Italy: Monduzzi Editore; 1999. p. 73. 9. Ouayoun MC, Levy C, Petelle B, Fleury B, Meyer B. Mandibular distraction osteogenesis for obstructive sleep apnea syndrome. 2nd International Congress Cranial and Facial Bone Distraction Processes. Abstract book; 1999 June; Paris. Bologna, Italy: Monduzzi Editore; 1999. p. 72. 10. Sorrel Dejerine E, Meulien P, Fleury B, Hausser-Hauw C. Mandibular distraction in the treatment of sleep apnea syndrome. 2nd International Congress Cranial and Facial Bone Distraction Processes. Abstract book; 1999 June; Paris. Bologna, Italy: Monduzzi Editore; 1999. p. 71. 11. Karp NS, Thorne CHM, McCarthy JG, Sisson HA. Bone lengthening in the craniofacial skeleton. Ann Plast Surg 1990;24: 231-4. 12. Yamamoto H, Sawaki Y, Ohkubo H, Ueda M. Maxillary advancement by distraction osteogenesis using osseointegrated implants. J Cranio Maxillofac Surg 1997;25:186-91. 13. McCarthy JG, Schreiber J, Karp NS. Lengthening of the human mandible by gradual distraction. Plast Reconstr Surg 1992;89:1-13. 14. McCarthy JG. The role of distraction osteogenesis in the reconstruction of the mandible in unilateral craniofacial microsomia. Clin Plast Surg 1994;21:625-31. 15. Bell WH, Harper RP, Gonzales M, Cherkashin AM, Samchukov ML. Distraction osteogenesis to widen the mandible. Br J Oral Maxillofac Surg 1997;35:11-6. 16. Klein C, Howaldt HP. Lengthening of the hypoplastic mandible by gradual distraction in childhood—a preliminary report. J Craniomaxillofac Surg 1995;23:68-73. 17. Molina F. Discussion. A CT scan technique for quantitative volumetric assessment of the mandible after distraction osteogenesis. Plast Reconstr Surg 1997;99:1248-50. 18. Breuning H, van Strijen PJ. Orthodontic treatment planning for mandibular distraction. International Proceedings, 2nd International Congress Cranial and Facial Bone Distraction Processes. Abstract book; 1999 June; Paris. Bologna, Italy: Monduzzi Editore; 1999. p. 259-63. 19. Diner PA, Viguier E, Tomat C, Franchi G, Accart G, Katz PH, et al. A new generation of submerged distraction devices: use of bidirectional intraoral mandibular distraction in children. International Proceedings, 2nd International Congress Cranial
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and Facial Bone Distraction Processes. Abstract book; 1999 June; Paris. Bologna, Italy: Monduzzi Editore; 1999. p. 113-22. Shvyrkov MB, Shamsudinov AG, Shvyrkova II. Lecture. The large human mandibular defect restitution by gradual distraction. International Congress on Cranial and Facial Bone Distraction Processes. Abstract book; 1999 June; Paris. Bologna, Italy: Monduzzi Editore; 1999. p. 93. Block MS, Chang A, Crawford C. Mandibular alveolar ridge augmentation in the dog using distraction osteogenesis. J Oral Maxillofac Surg 1996;54:309-14. Chin M, Toth BA. Distraction osteogenesis in maxillofacial surgery using internal devices: review of five cases. J Oral Maxillofac Surg 1996;54:45-53. Aldegheri A, Dubrana A. Maxillary alveolar process reconstruction using distraction osteogenesis: a case report. International Proceedings, 2nd International Congress Cranial and Facial Bone Distraction Processes. Abstract book; 1999 June; Paris. Bologna, Italy: Monduzzi Editore; 1999. p. 145-9. Lazar F, Hidding J, Zöller JE. Knöcherne Regeneration des Unterkieferalveolarfortsatzes mit Hilfe der vertikalen Kallusdistraktion. Dtsch Zahnärztl Z 1999;54:51-6. Bekisz O, Remy-Paquay P, Rompen E. Vertical bone distraction for the reconstruction of a posttraumatic atrophy of the alveolar ridge. 2nd International Congress Cranial and Facial Bone Distraction Processes. Abstract book; 1999 June; Paris. Bologna, Italy: Monduzzi Editore; 1999. p. 31. Fedotov S. Reconstruction of mandibular defects by lengthening of bone regenerate. 2nd International Congress Cranial and Facial Bone Distraction Processes. Abstract book; 1999 June; Paris. Bologna, Italy: Monduzzi Editore; 1999. p. 33. Hidding J, Lazar F, Zöller JE. The vertical distraction of dentulous alveolar segments. 2nd International Congress Cranial and Facial Bone Distraction Processes. Abstract book; 1999 June; Paris. Bologna, Italy: Monduzzi Editore; 1999. p. 45. Morton M, Al Aredy T, Brown P. A new unidirectional screw for intraoral distraction. 2nd International Congress Cranial and Facial Bone Distraction Processes. Abstract book; 1999 June; Paris. Bologna, Italy: Monduzzi Editore; 1999. p. 39. Perdyk FBD, van Strijen PJ. Correction of severe mandibular atrophy by means of distraction osteogenesis. 2nd International Congress Cranial and Facial Bone Distraction Processes. Abstract book; 1999 June; Paris. Bologna, Italy: Monduzzi Editore; 1999. p. 44. Zöller JE, Hidding J, Lazar F. The very atrophic mandible—Is distraction osteogenesis a solution of this problem? 2nd International Congress Cranial and Facial Bone Distraction Processes. Abstract book; 1999 June; Paris. Bologna, Italy: Monduzzi Editore; 1999. p. 43. Wiedemann M. Morphologische Grundlagen der Kallusdistraktion. Zentralbl Chir 1994;119:587-93. Nocini PF, Wangerin K, Albanese M. Histological examination of osteogenic tissue obtained one year after distraction of the mandible. 2nd International Congress Cranial and Facial Bone Distraction Processes. Abstract Book; 1999 June; Paris. Bologana, Italy: Monduzzi Editore; 1999. p. 29. Rachmiel A, Laufer D, Lewinson D. Bone formation and neovascularization during distraction osteogenesis. The influence of TGF-β. 2nd International Congress Cranial and Facial Bone Distraction Processes. Abstract book; 1999 June; Paris. Bologna, Italy: Monduzzi Editore; 1999. p. 7. Stewart K, Weyand B, van´t Hof R, Maffulli N, Poole M. A histomorphometric analysis of IGF-1 infusion during mandibular distraction osteogenesis in rabbits. 2nd International Congress Cranial and Facial Bone Distraction Processes. Abstract book; 1999 June; Paris. Bologna, Italy: Monduzzi Editore; 1999. p. 6. Gaggl A, Schultes G, Kärcher H. Distraction implants—a new operative technique for alveolar ridge augmentation. J Cranio Maxillofac Surg 1999; 27:214-21. Sawaki Y, Ohkubo H, Yamamoto H, Ueda M. Mandibular lengthening by intraoral distraction using osseointegrated implants. Int J Oral Maxillofac Implants 1996;11:186-93. Nosaka Y, Tsunokuma M, Hayasi H, Haeniwa H, Hamamoto K,
ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY Volume 90, Number 4 Nakajima M, et al. Placement of osseointegrated implants in distraction osteogenesis at the consolidation period. International Proceedings, 2nd International Congress Cranial and Facial Bone Distraction Processes. Abstract book; 1999 June; Paris. Bologna, Italy: Monduzzi Editore; 1999. p. 137-43. 38. Ducheyne P, DeMeester P, Abernoudt E. Influence of a functional dynamic loading on bone ingrowth into surface pores of orthopedic implants. J Biomed Mater Res 1977;11:811-38.
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Reprint requests: Dr Alexander Gaggl Klinische Abteilung für Mund-, Kiefer- und Gesichtschirurgie Universitätsklinik / LKH Graz Auenbruggerplatz 7 A-8036 Graz Austria / Europe [email protected]
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Objective. Mandibular augmentation by distraction of the alveolar ridge has been in use for several years. Since 1996, a distraction device that remains in the alveolar ridge after distraction has been used by the Department of Oral and Maxillofacial Surgery of Graz University. The distraction device is transformed into a dental implant after the end of the distraction process and can later be used for prosthetic purposes. We aimed to show the application of the device in this animal experiment and to follow the osseous healing process. Study design. Two distraction implants were inserted into the mandibles of 8 sheep. Distraction of 0.5 mm per day was carried out for 8 days. Two sheep were killed 1, 2, 3, and 6 months after distraction, and the dissected mandibles were examined clinically, radiologically, and histologically. Results. After the first month of distraction, only slight radiopacity of the distraction gap was found. This increased steadily up to the third month after distraction. The boundary between the distraction fragments and the gap disappeared gradually. Six months after distraction, a homogenous fine-meshed spongiosa structure was found in the area of distraction. Histologic examination showed desmoid ossification in the distraction gap and a continued increase in osteoid. After 6 months, mature bone was found. Only in the center was the rebuilding process not complete. Six months after distraction, osseointegration of the implants was shown in the region of the screw thread and distraction cylinder. Conclusions. The healing process corresponded to that found in long bones, but showed only desmal ossification. Osseous integration of the distraction implants was found 6 months after distraction, although the implants were stable 3 months after distraction. (Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000;90:420-9)
Callus distraction, first described by Codivilla1 in 1905, has long been used to provide autologous bone. Since standardization of the method by Ilizarov2,3 in the 1960s, the method has been used mainly in orthopedic surgery to lengthen long bones. However, not only long bones are capable of forming new bone. In recent years the method has been used to cover defects of the facial skeleton. Its main use in oral and maxillofacial surgery has been to correct severe growth defects in the mandible and maxilla. At the Second International Congress of Cranial and Facial Bone Distraction Processes in Paris in June 1999, callus distraction was advocated mainly for childhood syndromes and sleep apnea symptoms that require surgery because the results of osteotomy are rarely satisfactory.4-10 Distraction devices have been used to ventralize the hypoplastic maxilla and midface to correct congenital syndromes11,12 and for horizontal elongation of the mandible in patients with extensive mandibular microsomia.13-17 The advantage of callus aSenior
surgeon, Department of Oral and Maxillofacial Surgery. Institute of Pathology. cHead, Department of Oral and Maxillofacial Surgery. Received for publication Dec 3, 1999; returned for revision Feb 22, 2000; accepted for publication May 31, 2000. Copyright © 2000 by Mosby, Inc. 1079-2104/2000/$12.00 + 0 7/12/109159 doi:10.1067/moe.2000.109159 bPathologist,
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distraction is the slow but controlled correction of features, which can be improved by orthognathic surgical procedures but which, because of rigid fixation, does not allow long-term prospective correction. Callus distraction is a dynamic procedure with the possibility of overcorrection; thus it is important to take into consideration the later completion of correction by functional orthodontic treatment.18 By using intraoral callus distractors, ugly scars can be avoided.19 Callus distraction of the facial skeleton, as in orthopedic surgery, is usually done in young people whose bones have high potential for regeneration. A new possibility in the treatment of maxillofacial problems is the use of distractors in the reconstruction of defects of the mandible after tumor resection in adults. The use of osteo-transport-distractors enables reestablishment of mandibular continuity by using the method of callus distraction. Shvyrkov et al20 described the use of distractors in the closure of defects in the continuity of the mandible after tumor resection and the use of osteo-transport-distractors even in bones affected by radiotherapy, which might be expected to have less regenerative capacity. The reconstruction of missing bony structure is the first step in using this technique to reestablish structural qualities of the alveolar ridge and to enable further prosthetic treatment in elderly patients in whom poor regenerative powers are expected. The covering of
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defects in the mandible after tumor resection is an important therapeutic indication. However, defects in the mandible are rare compared with alveolar defects caused by trauma, periodontitis, or loss of bone as a result of atrophy of edentulous segments of the alveolar ridge. Block et al21 described a successful alveolar ridge augmentation with an intraorally placed distractor in preparation for later dental implantation in an experimental study in animals. The use of this method in humans was first described by Chin and Toth22 in 1996. They used alveolar ridge distraction to reconstruct a defect after loss of teeth from trauma. Both distraction methods, described by other authors as well, constituted a preparation for the later implant site.23-30 Thus the use of callus distraction for the augmentation of deficient mandibular segments, even in elderly patients with reduced osteogenic potential, and the possibility of improving the implant site by the technique of alveolar ridge distraction were shown. Until now the healing process has been verified only for callus distraction of the long bones and of the mandibular ramus and corpus.31-34 In the case of alveolar ridge distraction, however, other surgical and morphologic conditions must be considered regarding osseous healing. Extensive removal of the periosteum of the small distraction fragment is needed, which remains pedunculated to the soft tissue. Because of the need for gingival cover and perfusion, a different arrangement is required compared with other regions of the jaw. Total cover of the deficient alveolar ridge is the aim, to satisfy the esthetic demands of surgeons and patients. The methods of alveolar ridge distraction described above demand a 2-step or 3-step procedure: insertion and removal of the distractor and insertion of the implant.24,27 We aimed to simplify the operation and reduce the operative time and the inconvenience to patients by a system that unites the qualities of a distractor with those of a dental implant.35 This distraction implant has been evaluated in the Department of Oral and Maxillofacial Surgery of Graz University since 1996. Special conditions have to be met even after distraction has been completed. Among these is that the distraction implant must be fully integrated in the bone to ensure a good prosthetic result in the long term. The recommended time for initial loading by a prosthetic superstructure was based on empirical data, although the closure of the distraction gap with bone and osseous integration of the implant surface is of vital importance for any implant. We aimed to verify the time for loading these implants to ensure a successful long-term outcome. We studied the development of callus in the distraction gap and the osseointegration of distraction
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Fig 1. The 11-mm distraction implant, a self-cutting conical titanium screw implant.
implants in animals. We selected sheep, following the work of Sawaki et al,36 who successfully carried out horizontal distraction of the mandibular corpus with implant-based supported distractors in sheep.
DESCRIPTION OF THE DISTRACTION IMPLANT The distraction implant (SIS-Trade Inc, Klagenfurt, Austria) combines the qualities of a callus distraction device with those of a dental implant. It comprises a conical chemically pure titanium screw with a maximum diameter of 4.1 mm (Fig 1). At present it is available in lengths of 7, 9, 11, and 13 mm. In the undistracted state ready for insertion it has the qualities of a self-cutting conical screw with 0.2 mm screw thread profile depth and a pitch of 0.6 mm in the coronal and apical portion. The apical part contains the distraction
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Fig 3. Scheme of distraction implant after modification into definitive design. Now it is a combined screw and cylinder implant. Fixation screw fills center of implant. Head of implant can be used for later prosthetic superstructures.
Fig 2. The 11-mm distraction implant partly distracted. Distraction cylinder can be activated by central screw with coronal approach.
cylinder 6.5-mm long located in the coronal implant part telescopically (Fig 2). The distraction screw lies in the center of the distraction cylinder. It is 6 mm long and lies free in the distraction chamber in the coronal implant region. The distraction chamber lies in the distraction head of the implant. The roof of the distraction chamber allows adequate screw support on activation of the distractor. This takes place by a left turn of the distraction screw. The screw thread is synchronized so that a left turn of 360 degrees corresponds to a 0.25 mm movement in the implant transition region. Activation of the distraction screw and thus the head of the distractor is carried out through coronal access with the aid of a distraction screw driver. This may be placed on the hexagonal-shaped coronal screw head and turned to the left in 90-degree steps.
The distraction head is 4 mm in height and exceeds the implant neck by this length. After distraction, the head of the distractor can be replaced by a conventional implant head, and the distractor is thus transformed to an implant (Fig 3). All components of the implant are of titanium medical grade 4 and 5. Both implant heads are polished. The surface of the screw implant is roughened by laser treatment to achieve a greater surface. The surface structure is created in an atmosphere of inert gas by placing individual hollows with special optical devices in front in an exactly defined grid. The depth of primary roughness is 30 to 50 µm. Further roughness is created on the surface of the ridges and hollows through melting transformation of the lasered area. The depth of these secondary roughnesses is 2 to 10 µm. For functional reasons the surface of the distraction cylinder is smooth or machine roughened. The microroughness measures 2 µm. The coronal osseous part of the implant is also machine roughened over a length of 1.5 mm to enable cleaning of the neck part of an exposed implant during wound healing.
MATERIAL AND METHODS We used 8 adult sheep with a mean age of 3 years. The operations were carried out with the animals under balanced combination anesthesia.
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Fig 4. Intraoperative photograph after segmental osteotomy and insertion of 2 distraction devices.
The first step was the injection into an ear vein of 0.1 mg/kg Gewacalm and 0.1 mg/kg atropine sulfate; this was followed by orotracheal intubation. Initially, anesthesia was with 4 µg/kg fentanyl and 1.5 mg/kg Hypnomidate. Relaxation was achieved with 0.5 mg/kg Pavulon. Further anesthesia was by insufflation of nitrous oxide, 50%, and 0.8% to 1.2% Forane. After disinfection of the operation site, an incision was made in the edentulous left anterior portion of the mandibular alveolar ridge, and a mucoperiosteal flap was prepared. The alveolar process was then reduced by 4 mm with a milling machine, and a plane implant site of 3 cm mesiodistal length was created. A horizontal osteotomy was done 5 mm away from the implant plateau with an oscillating microsaw over the entire plateau length of 3 cm. Two distraction implants 11 mm in length were inserted into the alveolar ridge. The implant site was hollowed by core and pilot drilling preceded by parallel drilling. The osteotomy was completed in the lateral segment by vertical incisions (Fig 4). To ensure free mobility of the segments, the wound was closed with absorbable suture material after an intraoperative trial of distraction. After extubation and injection of analgesia (subcutaneously) (Tramal, 100 mg) and prophylactic antibiotics (intramuscularly) (Retarpen, 2.4 mg), the animals were returned to the stables and were given feed pellets soaked in water for 1 week. After this 7-day healing period, distraction was initiated. No further medication was given, and distraction was carried out in steps of 0.5 mm daily by activation of the distraction cylinder twice
a day (1 turn every 12 hours). Distraction was carried out for 8 days. After this, both implants were blocked by a bridge of polymethylmethacrylate to facilitate healing of the distraction implant. The implants were allowed to heal for 1, 2, 3, or 6 months before 2 sheep at each time were killed by an overdose of Ketalar, and the specimens were dissected. Initially, the condition around the implant was assessed by probing the gap with a periodontal probe. This was done mesially, distally, orally, and vestibularly in the 4 distinct regions of the implant. The greatest probing depth was noted. Further clinical assessment was made of the horizontal mobility of the implant. Measurements were made with the Periotest apparatus (Siemens, Erlangen, Germany) at right angles to the implant axis. This was repeated 5 times for each implant. The highest and lowest values were rejected, and the median of the 3 remaining values was recorded. Enoral radiographs of the distraction region were taken. The edentulous distracted alveolar process region and the nondistracted contralateral alveolar process (reference) were removed from the dissected skull. From the region between the distraction implants, a 5-mm–wide bone wedge was removed and examined histologically. After decalcification of the specimen, fixation in formalin, histologic preparation, and staining with hematoxylin-eosin, the specimens were examined under a light microscope (Wild M3Z; Leica, Hildesheim, Germany). The segments of alveolar process carrying the distraction implants that were obtained 6 months after distraction were treated differently. These specimens were treated by fixation in 5% formaldehyde solu-
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Fig 5. Radiograph 1 month after distraction.
Fig 6. Radiograph 3 months after distraction.
tion according to Lillie (pH 7.3) and dehydrated increasingly with ethanol; the fat was removed with ether-chloroform and they were soaked with MMA monomer before finally being polymerized into blocks. With the aid of an internal cleavage saw, 3 slices were cut out of the
middle of the bone implant complex, polished, and stained with Giemsa or by the method of Kossa and Paragon (fuscin and toluidine blue) and assessed morphometrically and histologically with a light microscope (Wild M3Z, Leica; and Metaval; Zeiss, Jena, Germany).
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Fig 7. Radiograph 6 months after distraction.
Fig 8. Histologic specimen (hematoxylin-eosin, original magnification ×22.5). Two months after distraction, granulation tissue decreases and osteoid increases.
RESULTS Radiologic examination 1 month after distraction showed slight opacity of the distraction gap. In the transitional zone of the distraction segments, a blurring of the zonal limits was seen (Fig 5). After 2 months, this effect was more pronounced with reduction in
radiotranslucence in the distraction gap. However, differences in radiotranslucence between the segments and the distraction gap were clearly visible. After 3 months, the distraction gap was more radiopaque, and its density was comparable with that of the distraction segments. Distraction gap and distraction segments
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Fig 9. Histologic specimen (hematoxylin-eosin, original magnification ×56). After 6 months, mature bone is seen in distraction gap. Remodeling still going on in center of distraction only.
were still clearly distinguishable (Fig 6). Only after 6 months was there a homogenous radiologic structure of the distracted alveolar process. The typical spongy bony structure was almost identical to that of the nondistracted opposite side (Fig 7). Histologic examination of the distraction gap showed the presence of callus in the gap; the ossification was mainly mesenchymal with large amounts of soft tissue and collagen fibers. Osteoid was seen in the region near the segments of distraction and small amounts of chondroid tissue in the central area. In the second month after distraction, a further increase in osteoid in the central distraction region was found, as was a reduction in the number of collagen fibers. There was extensive vascularization in the area close to the distraction segments. The chondroid tissue had completely disappeared. Signs of lamellar ossification were seen at this stage. Zones of calcification (cement lines) were seen occasionally (Fig 8). There were many more cement lines by the third postdistractional month, and the bone continued to mature. Lamellar bone was now seen in the central part of the bone, and connective tissue had become rare. In the region of distraction, the osteoid was increasingly calcified with lacunar resorption and restructuring of the mature bone. Six months after distraction, restructuring was also present at the edges of the distracted region (Fig 9). In the central region, single islands of mature restructured bone were seen. The tissue around the implant showed a bone apposi-
tion surface of 70% to 80% in the implant screw thread area in the sixth postdistractional month. The distraction cylinder had an apposition surface of 60% to 70%. Clinical results of peri-implant probing and Periotest values are shown in Table I.
DISCUSSION Since Sawaki et al36 described vertical distraction of the mandible by means of implant barred distractors, sheep have been accepted as suitable animals for combined distraction and implantation. In contrast to Sawaki et al, our experiment dealt with alveolar distraction of the mandible, which was first described by Block et al21 in 1996 in an animal model. Block et al examined beagle dogs treated in a 2-stage procedure by alveolar ridge distraction and later by insertion of an implant in the distracted bone. These authors, along with Nosaka et al,37 reported osseous integration of dental implants in distracted callus. They showed the typical radiologic and histologic healing process leading to an osseous integration of 70% of the surface of the implant as early as 12 weeks after insertion of the implant. Our experiments showed a similar result with distraction implants after 6 months. This value (similar to normal osseous integration of implants in bone) applied only to the laser-treated screw thread, whereas the total area of osseous integration in the smooth distraction cylinder area still lagged behind the implant—about 65%, 6 months after distraction. The
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Table I. Clinical results Sheep number
Implant number
Months after distraction
Probing depth (mm)
Periotest value
1
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16
1 1 1 1 2 2 2 2 3 3 3 3 6 6 6 6
3 4 2 3 3 2 3 3 3 3 4 3 2 2 2 3
+5 +5 +6 +7 +3 +4 +4 +4 +1 +1 +1 –2 –3 –1 0 –1
2 3 4 5 6 7 8
osseous integration was greater than that found after other augmentation techniques.37 The process of restructuring in the distraction gap containing the implant was not complete 6 months after distraction. With continual increase in mature bone structure in the other parts of the distraction gap, a further increase in bone is to be expected. Nocini et al32 reported that the restructuring process continued as late as 1 year after horizontal distraction of the mandible in spite of the homogeneous bony structure found on radiographic examination. This was also seen in our experiment 6 months after distraction. In spite of the distraction gap having completely disappeared and the homogeneous radiologic findings, incompletely calcified bony structures were in the center of the distraction. Only a few chondral cells were seen in the early postdistractional phase, and they were found mainly in the center of the distraction region, which appeared to be vascularized to a lesser extent than the peripheral parts. In the peripheral parts, laminar bone production with several osteoblasts and osteoid formation was seen. This phase of the distraction corresponded to the longitudinal polarization phase found by Wiedemann31 in the long bones from the tenth postoperative day to the second postoperative month. As early as the second postoperative month, in agreement with Wiedemann, we found continuous fading of the transition zone from local bone to the distraction region with an increase in characteristic changes from the third to the sixth postoperative month. Radiographs showed an increase in opacity in this region. Histologic examination showed fusion of the distraction fragments over the distraction gap with calcification of the osteoid already taking place and the appearance of numerous osteo-
clasts. This was the ossification period.31 It was only after 6 months that signs of the consolidation period were found with the formation of a neocortex and the appearance of mature local bony tissue in all areas of distraction. The question arises about the timing of stability sufficient for application of prostheses. It might be expected that enough stability would be achieved only after completion of the entire restructuring process. However, the tendency in implantology is for early loading of conventional implants,38 so that early application of prosthetic structures also seems appropriate for distraction implants. Sufficient implant stability is achieved 3 months after distraction (Periotest values <+3). Histologic findings suggest high implant stability at this time, so that it appears to be adequate for loading by prosthetic superstructures, particularly as the peri-implant gingiva has healed normally.
CONCLUSION Sheep are an adequate animal model for alveolar ridge distraction with distraction implants. The healing process of the distraction gap corresponds to that of other bones and is not completed by the sixth postoperative month. However, within 3 months after distraction, an adequate osseous basis has been created, providing implant stability and allowing further prosthetic treatment. Osseous integration within the distraction cylinder is delayed, which may be explained by the slow maturing of bone in the center of the distraction. Six months after distraction, good osseous integration is achieved with an implant bone surface area of about 70%. However, results from experiments with animals may not reflect the healing process in humans. Clinical studies are needed to evaluate the method further.
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ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY Volume 90, Number 4 Nakajima M, et al. Placement of osseointegrated implants in distraction osteogenesis at the consolidation period. International Proceedings, 2nd International Congress Cranial and Facial Bone Distraction Processes. Abstract book; 1999 June; Paris. Bologna, Italy: Monduzzi Editore; 1999. p. 137-43. 38. Ducheyne P, DeMeester P, Abernoudt E. Influence of a functional dynamic loading on bone ingrowth into surface pores of orthopedic implants. J Biomed Mater Res 1977;11:811-38.
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Reprint requests: Dr Alexander Gaggl Klinische Abteilung für Mund-, Kiefer- und Gesichtschirurgie Universitätsklinik / LKH Graz Auenbruggerplatz 7 A-8036 Graz Austria / Europe [email protected]
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