J Oral Maxillofac Surg 68:756-761, 2010
Calvarial Reshaping Using Bifocal Bidirectional Transport Distraction Osteogenesis Muzaffer Durmus, MD,* Fatih Zor, MD,† Serdar Ozturk, MD,‡ Ugur Bozlar, MD,§ Murat Turegun, MD,储 and Mustafa Sengezer, MD¶ Purpose: The aim of this study is to assess 3-dimensional reconstruction of cranial defects by use of
bifocal bidirectional transport distraction osteogenesis (BBTDO). This study was performed on 8 sheep, divided into a control group (n ⫽ 3) and treatment group (n ⫽ 5). Full-thickness cranial defects (50 ⫻ 40 mm) were created on calvaria. In the control group only the skin was closed. In the treatment group BBTDO was performed. Distraction was performed with a custom-made distraction device with a transport segment of 40 ⫻ 20 mm. After a 5-day period of latency, distraction was applied to the transport segment. During the first 20 days of distraction, the transport segment was distracted 1 mm in the forward direction and 0.5 mm in the upward direction. After the next 20 days of distraction, the transport segment was distracted 1 mm forward and 0.5 downward. After a total of 40 days’ distraction, a 30-day consolidation period was applied. Macroscopic, radiologic (computed tomography with volume measurements), and histologic evaluations were done. Results: No major complications were seen during the whole study period. In the control group the bone defects remained unhealed at the end of the study period. The same-sized defects in the treatment group healed with a convexity like the calvaria. Preoperative and postoperative cranial volume measurements of the treatment group animals showed an increase in cranial volume (P ⬍ .05). Histologic evaluation showed inductive bone regeneration and mature bone structure development within the distraction zone. Conclusion: The BBTDO is an effective and safe technique for 3-dimensional closure of cranial defects. © 2010 American Association of Oral and Maxillofacial Surgeons J Oral Maxillofac Surg 68:756-761, 2010 Materials and Methods:
Treatment of cranial defects and deformities is still challenging for reconstructive surgeons. Most commonly used techniques include the use of autografts and allogeneic implants, but these techniques have
some disadvantages such as limited donor site, implant exposure, and infection. Therefore research into alternative techniques continues.1,2 Distraction osteogenesis has recently become popular in the craniofacial region.1-5 Although distraction of the facial skeleton is frequently performed, distraction of the cranial bones has had limited relevance in both experimental and clinical settings.6 Because the cranium is a convex structure rather than a smooth surface, 3-dimensional (3D) reconstruction is crucial in this area. The aim of this study is to assess 3D reconstruction of cranial defects by use of bifocal bidirectional transport distraction osteogenesis (BBTDO).
*Plastic Surgeon, Diyarbakir Military Hospital, Diyarbakir, Turkey. †Assistant Professor, Department of Plastic and Reconstructive Surgery, Gulhane Military Medical Academy, Ankara, Turkey. ‡Associate Professor, Department of Plastic and Reconstructive Surgery, Gulhane Military Medical Academy, Ankara, Turkey. §Assistant Professor, Department of Radiology, Gulhane Military Medical Academy, Ankara, Turkey. 储Professor, Department of Plastic and Reconstructive Surgery, Gulhane Military Medical Academy, Ankara, Turkey. ¶Professor, Department of Plastic and Reconstructive Surgery, Gulhane Military Medical Academy, Ankara, Turkey. Address correspondence and reprint requests to Dr Zor: Gulhane Askeri Tip Akademisi, Plastik Cerrahi, 06018, Etlik, Ankara, Turkey; e-mail:
[email protected]
Materials and Methods The study was performed at the Research and Development Center of Gulhane Military Medical Academy, Ankara, Turkey. Before the initiation of the study, approval of the Scientific Research Board and Ethics Board of Animal Experiments was procured. All
© 2010 American Association of Oral and Maxillofacial Surgeons
0278-2391/10/6804-0008$36.00/0 doi:10.1016/j.joms.2009.04.135
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Group II (Treatment Group) After the creation of cranial defects, a transport bone segment of 40 ⫻ 20 mm was prepared (Fig 2A). BBTDO was applied in this group. DISTRACTOR APPLICATION AND DISTRACTION PROCEDURE
FIGURE 1. Newly developed distractor, which is capable of performing distraction in vertical and horizontal directions. Durmus et al. Calvarial Reshaping. J Oral Maxillofac Surg 2010.
test subjects were obtained from the barn of the Research and Development Center and prepared for the study for a period of 2 weeks.
After the attachment of the transport bone segment to the distractor, the distractor was mounted onto the cranium with bicortical miniscrews (Fig 2B). The incision was then closed in 2 layers. Distraction was begun after 5 days of latency. During the distraction period, horizontal distraction of 0.50 ⫻ 2 mm/day and vertical distraction of 0.25 ⫻ 2 mm/day were applied to the transport segment for 40 days. The vertical distraction procedure was done in an upward direction for the first 20 days and in a downward direction for the remainder. Later, a consolidation period of 30 days was started (Fig 3). Postoperative care and follow-up of the animals were performed in the barn
DESIGN AND DEFINITION OF DISTRACTOR
In accordance with the objective of the study, a distractor that is capable of performing bifocal and bidirectional distraction was designed. The distractor was able to apply vertical and horizontal distractions to the transport segment. The lengths of the vertical bar, horizontal bar, transport segment pin, and pin stabilizer of the device were 72 mm, 30 mm, 50 mm, and 25 mm, respectively (Fig 1). After its design, the device was produced by Trimed Medical Equipment (Ankara, Turkey). EXPERIMENTAL PROTOCOL
For this study, we used 2-year-old sheep, whose mean weight was 54 kg. The experimental protocol included 2 groups: control group (n ⫽ 3) and treatment group (n ⫽ 5). Multislice computed tomography (CT) of the cranium was performed in all animals before the experimental study. All animals were operated on under general anesthesia. After the induction of anesthesia and endotracheal intubation, the scalp was transected through a sagittal incision and the calvaria was exposed. Critical-size full-thickness bone defects measuring 60 ⫻ 50 mm were created on the calvaria of the animals as described by Kramer et al.3 Extreme care was paid not to disturb the integrity of the dura. Group I (Control Group) After the creation of critical-size cranial defects, no further procedure was performed in the control group except for closure of the skin.
FIGURE 2. Surgical procedure. A, Distractor and transport segment. B, Fixation of distractor and transport segment to cranium. Durmus et al. Calvarial Reshaping. J Oral Maxillofac Surg 2010.
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paring the preoperative and postoperative cranial volume of the test subjects.
FIGURE 3. Distraction protocol. Durmus et al. Calvarial Reshaping. J Oral Maxillofac Surg 2010.
during the experiment. Antibiotic prophylaxis with 25 mg/kg of cefazolin continued for 5 days. EVALUATION
At the end of the experiment, all subjects were operated on and macroscopic evaluation of the transport segment, distraction gap, and new bone generation was performed. Quantitative CT The quantity and quality of the new bone, generated in the distraction gap, were measured with a GE Medical Systems (Milwaukee, WI) quantitative CT device (50 kV, 7 mA, 40-millisecond exposure time). The cross-section setting was between 1 and 2 mm. Calculations and image analyses were performed with a Sun Sparc-10 processor (Sun Microsystems, Santa Clara, CA). CT scans were obtained in the preoperative, distraction, and consolidation periods. The movement of the transport segment, the success of the distraction, and the new bone formation were all determined by coronal, axial, sagittal, and 3D images. Cranial Volume Measurement Cranial volume measurements were made by use of tomographic cross sections from the foramen magnum to the vertex (Fig 4). Sun Microsystems Software was used in the measurement of the cranial volume.7 Statistical evaluation of the results was made by com-
Histopathologic Analysis After the consolidation period, bone biopsy specimens were obtained from the normal bone, newly generated bone, and transport segment separately. The samples were fixed in 10% formalin for 48 hours and then decalcified in an ethylenediaminetetraacetic acid solution for the next 48 hours. Longitudinal sections were obtained, and hematoxylin-eosin staining was performed by use of standard protocols. Histopathologic analysis was performed with light microscope under 25⫻, 50⫻, and 100⫻ magnification. Cortical thickness, remodeling, and generation of new bone, as well as its quantity and quality, were evaluated. STATISTICAL ANALYSIS
SPSS for Windows, version 10.0 (SPSS, Chicago, IL), was used for statistical analysis. Preoperative and postoperative cranial volume measurement values of the treatment group were compared by use of the Wilcoxon matched-pairs test. Significance was set at P less than .05.
Results No serious complication was observed during the postoperative period. The defects in the control group remained unchanged. All subjects in the treatment group tolerated the active distraction successfully. Macroscopic evaluation showed new bone formation that generated convexity at the distraction gap mimicking the cranium (Fig 5). QUANTITATIVE CT
A quantitative CT scan obtained in the preoperative period is shown in Figure 6A. No new bone formation
FIGURE 4. Left, Cranial tomographic imaging. Right, Cranial volume measurement. The volume measurements were evaluated through the cross sections between the foramen magnum and vertex. Durmus et al. Calvarial Reshaping. J Oral Maxillofac Surg 2010.
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FIGURE 7. Results obtained from cranial volume measurements performed preoperatively and postoperatively. FIGURE 5. Macroscopic view of distracted cranium showing closed distraction gap.
Durmus et al. Calvarial Reshaping. J Oral Maxillofac Surg 2010.
Durmus et al. Calvarial Reshaping. J Oral Maxillofac Surg 2010.
was visible in the coronal and sagittal cross sections (Fig 6C).
was observed in the control group (Fig 6B). The subjects in the treatment group showed successful bidirectional (horizontal and vertical) movement of the transport segment. The defect was successfully closed with convex newly formed bone at the distraction gap. The convexity of the newly formed bone
EVALUATION OF CRANIAL VOLUME MEASUREMENT
Preoperative and postoperative cranial volume measurements of the treatment group are shown in Figure 7. The results obtained in the treatment group showed a mean increase of 11.25 cm3 in the cranial volume, which was statistically significant (P ⬍ .05).
FIGURE 6. Quantitative CT results. A, Preoperative sagittal and coronal views. B, The unclosed defect is seen in the control group. C, Postoperative sagittal and coronal views of the distracted cranium showing successful closure of the defect in a convex pattern. Durmus et al. Calvarial Reshaping. J Oral Maxillofac Surg 2010.
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FIGURE 8. Histopathologic evaluation (hematoxylin-eosin stain, original magnification ⫻100). A, Newly formed bony structure at distraction gap. B, Mature compact bone at transport segment. Durmus et al. Calvarial Reshaping. J Oral Maxillofac Surg 2010.
HISTOPATHOLOGIC EVALUATION
In the control group, histologic examination of the animals showed only a thin ingrowth of bone from the margins. In the treatment group, histologic evaluation of the distraction gap showed new formation of mature bone with osteoblasts, osteoclasts, and osteocytes. A series of osteoblastic cells, which is called an osteoblastic rim, was seen near the edge of the newly formed bone. This series of cells was observed to be moving in all directions. In places where adequate bony structure accumulation was achieved, the osteoblastic activity was observed to decrease with formation of osteocytes. Intramembranous ossification was clearly observed at the distraction gap (Fig 8A). The analysis of the transport bone segment showed protection of the compact mature bone structure. It was observed that the Haversian system and osteon structures had been maintained in good condition (Fig 8B).
Discussion In adults, defects of the calvaria of a certain size do not heal spontaneously. In particular, corrections of congenital craniofacial deformities, severe craniofacial trauma, and ablative tumor surgery can require an extended demand of osseous reconstruction. On the other hand, methods such as autograft and allogeneic implantation have their own drawbacks.3,6 Since the introduction of monofocal distraction osteogenesis in the mandibular area by McCarthy, it has gained popularity for maxillary and midfacial reconstruction.8 Cranial distraction is a relatively new method for reconstruction of cranial bone defects. There are a limited number of studies about cranial distraction osteogenesis, and most of these studies are experimental.1,2 Similarly, the potential of bifocal transport osteogenesis in the craniofacial skeleton has been increasingly investigated, and it has been found to have limited clinical and experimental applications.9,10 The major drawback of bifocal distraction
osteogenesis is that it only allows monodirectional reconstruction of the calvaria. The calvaria is convex in shape, and this must be kept in mind during reconstruction. To our knowledge, there are no reports about BBTDO to close calvarial defects. In this study we showed that BBTDO is an effective technique to facilitate the 3D closure of full-thickness adult calvarial defects in a sheep model. All 5 subjects tolerated the active distraction period, and the critical-size bone defects were closed successfully. Moreover, with the described technique, the newly formed calvarial bone mimics the convexity of the native calvaria. The CT images clearly showed successful closure of the defect 3-dimensionally. Cranial volume measurements showed an increase in the cranial volume as a result of bidirectional distraction, which proves the volumetric gain with the present technique. Finally, we observed fibrous tissue at the docking site of our transport disc. It is likely that this fibrous tissue represents a partial interposition of soft tissues during the distraction period. There has been a consensus of opinions on the application of distraction at a speed of 1 mm/day on the horizontal plane.1,2,6 We applied 0.5 mm/day of vertical distraction and 1 mm/day of horizontal distraction, and we did not encounter any problem. To our knowledge, there is no example of bifocal bidirectional distraction in the literature. In particular, the ideal speed of the distraction in the vertical direction is not known. We think that further studies on this issue are needed. Using a cat model of calvarial distraction, Fukuta et al11 observed reduced bone deposition when the transport segment was separated from the underlying dura. They suggest that separating the transport disc from the dura reduces the blood supply and osteogenic capacity of the transport segment.10,11 In our study, the transport segment was used as a bone graft and the dura mater was not attached to it. Moreover, the transport disc was moving away from the dura mater. However, the bone formation at the distraction
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gap was found to be good in quality and quantity, whereas the transport segment kept its natural appearance and histology. To clarify the importance of the relationship of the dura and periosteum during the BBTDO procedure, further studies are required. In most cases the aim of the reconstructive surgeon is not only to close a calvarial defect but to reshape the calvaria as well. In this regard, we believe that the current technique may allow both reshaping the calvaria and increasing the calvarial volume in craniosynostosis patients in the clinical setting. To our knowledge, this is the first study in the literature describing reconstruction of a calvarial defect with an increase in cranial volume. Finally, a custom-made distraction device that is capable of performing bidirectional distraction to a transport segment was designed. The device was simple, effective, and easy to activate. It was stable enough to meet the principal biomechanical goal of bone transportation. We think that more complex devices, such as remote-activated biodegradable distraction devices, can be designed for the same purpose. In conclusion, we believe that BBTDO may be used to close the calvarial defects. The main advantage of this technique is that it allows reshaping of the calvaria as well as volumetric gain when needed.
References 1. Swennen G, Schliephake H, Dempf R, et al: Craniofacial distraction osteogenesis: A review of the literature. Part I: Clinical studies. Int J Oral Maxillofac Surg 30:89, 2001 2. Swennen G, Dempf R, Schliephake H: Cranio-facial distraction osteogenesis: A review of the literature. Part II: Experimental studies. Int J Oral Maxillofac Surg 31:123, 2002 3. Kramer FJ, Mueller M, Rahmstorf M, et al: Craniofacial reconstruction by transport distraction osteogenesis: Corticotomy versus osteotomy—An experimental study. J Craniofac Surg 15:556, 2004 4. Ilizarov GA: The tension-stress effect on the genesis and growth of tissues: Part II. The influence of the rate and frequency of distraction. Clin Orthop Relat Res 263, 1989 5. Samchukov ML, Cope JB, Cherkashin AM: Craniofacial Distraction Osteogenesis (ed 1). St Louis, Mosby, 2001 6. Cedars MG, Linck DL, Chin M, et al: Advancement of the midface using distraction techniques. Plast Reconstr Surg 103: 429, 1999 7. Deveci M, Oztürk S, Sengezer M, et al: Measurement of orbital volume by a 3-dimensional software program: An experimental study. J Oral Maxillofac Surg 58:645, 2000 8. Cope JB, Samchukov ML, Cherkashin AM: Mandibular distraction osteogenesis: A historic perspective and future directions. Am J Orthod Dentofacial Orthop 115:448, 1999 9. Stucki-McCormick SU: Reconstruction of the mandibular condyle using transport distraction osteogenesis. J Craniofac Surg 8:48, 1997 10. Bouletreau PJ, Warren SM, Paccione MF, et al: Transport distraction osteogenesis: A new method to heal adult calvarial defects. Plast Reconstr Surg 109:1074, 2002 11. Fukuta K, Saito K, Potparic´ Z: A comparison of single-stage versus gradual fronto-parietal advancement in terms of extradural dead space and bone deposition. Br J Plast Surg 51:169, 1998
