Department of Orthopaedic Surgery, Kitasato University School of Medicine 2. Department of Anesthesiology, Kitasato University School of Medicine 3

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1 Original Contribution Kitasato Med J 2010;40:56-63 Posterior spinal fusion for scoliosis in Duchenne muscular dystrophy (DMD): short-term correction effect of instrumentation surgery using the pedicle screw system and local autogenous bone graft alone Takayuki Imura, 1 Masashi Takaso, 1 Toshiyuki Nakazawa, 1 Takamitsu Okada, 1 Masaki Ueno, 1 Kensuke Fukushima, 1 Wataru Saito, 1 Atsushi Minatani, 1 Ryousuke Shintani, 1 Gennyo Miyajima, 1 Naonobu Takahira, 1 Moritoshi Itoman, 1 Hirotsugu Okamoto, 2 Toshiyuki Okutomi, 2 Makihito Okamoto, 3 Takashi Masaki, 3 Eijyu Uchinuma 4 1 Department of Orthopaedic Surgery, Kitasato University School of Medicine 2 Department of Anesthesiology, Kitasato University School of Medicine 3 Department of Otolaryngology, Kitasato University School of Medicine 4 Department of Plastic Surgery, Kitasato University School of Medicine Objective: To determine the efficacy of local autograft bone in scoliosis surgery performed by posterior spinal fusion and segmental pedicle screw instrumentation in patients with Duchenne muscular dystrophy (DMD). Materials and Methods: Twenty patients with DMD scoliosis, years of age, were treated with posterior spinal fusion using local allograft bone alone and segmental pedicle screw instrumentation. Patients were reviewed clinically and with radiologic measurements. Results: Minimum follow-up was 2 years, and average operating time was 271 minutes. Average estimated blood loss was 890 ml. On a coronal plane, the average pre- and postoperative coronal curve measured 70 degrees and 15 degrees, respectively, and 17 degrees at the last follow-up. On a sagittal plane, the average pre- and postoperative sagittal thoracic curve (T3-T12) measured 7 degrees and 19 degrees, respectively, and 20 degrees at the last follow-up. The average pre- and postoperative sagittal lumbar curve (L1-L5) measured 20 degrees and 35 degrees, respectively, and 36 degrees at the last follow-up. There was no significant loss of correction in the coronal or sagittal planes. No patients complained of pain. And there was no pseudarthrosis clinically or radiographically. Conclusion: Local autograft bone is effective for scoliosis surgery in patients with DMD. Key words: Duchenne muscular dystrophy, local autograft bone, scoliosis surgery, segmental pedicle screw instrumentation Introduction D uchenne muscular dystrophy (DMD) is the most common form of muscular dystrophies and is often accompanied by deterioration of cardiopulmonary function and spinal deformity such as scoliosis. The natural history of scoliosis as well as the rapid deterioration of pulmonary function in DMD patients has been well established. 1,2 Usually, non-operative curves progress relentlessly to levels as great as 100 degrees. In DMD scoliosis, progression occurs much more frequently and quicker than in idiopathic scoliosis; therefore, early surgical correction of scoliosis has been recommended. 3,4 However, loss of correction of scoliosis in patients with DMD was described by some authors with hook and wire instrumentation. Despite the magnitude of this surgery, most patients and their principal care providers believe that scoliosis surgery improves function, cosmesis, sitting balance, and quality of life. 3,4 Harvesting autogenic or allogenic bone graft to increase the rate of arthrodesis during segmental instrumentation in any scoliosis surgery has been a standard procedure. Many authors have already reported their experiences with different types of bone grafting and the use of allograft bone has been reported to give Received 2 December 2009, accepted 5 January 2010 Correspondence to: Takayuki Imura, Department of Orthopaedic Surgery, Kitasato University School of Medicine Kitasato , Sagamihara, Kanagawa , Japan tk2003@kitasato-u.ac.jp 56

2 Posterior spinal fusion for scoliosis in DMD comparable results to those with autograft bone. 5-7 However, in many countries, banked allograft bone is often not available for scoliosis surgery. Harvesting autogenous bone grafts from the iliac crest is a standard procedure in spine surgery. A large quantity and good quality of corticocancellous bone can be obtained from the iliac crest. However, donor site morbidity caused by bone harvest remains a concern. 8 This procedure may have complications because of the longer operative time, increased blood loss, and a higher incidence of symptoms associated with the donor sites, including pain, fracture, hematoma, false aneurysm, neurovascular injuries, and gait disturbances. 8 Successful fusion has been reported using only local bone for long posterolateral fusion in adolescent idiopathic scoliosis. 9 To our knowledge, there have been no reports on the use of local autograft bone alone in scoliosis surgery in DMD patients. The purpose of this study was to document the efficacy and safety of local autograft bone alone and segmental pedicle screw instrumentation in scoliosis surgery in patients with DMD. Materials and Methods From May 2005 to June 2007, a total of 20 patients (nonambulatory boys) underwent posterior spinal fusion and segmental pedicle screw instrumentation for scoliosis secondary to DMD. Age at operation averaged 13 years (range, years). All the operations were performed by the same surgeon (MT). A minimum 2-year followup was required for inclusion in this study. All scoliosis curves were single curves (17 right and 3 left thoracolumbar curves). Institutional review board approval of Kitasato University was obtained for this study and informed consent was obtained from all the patients. Surgical techniques The primary aim of the surgery was to obtain a solid fusion, level pelvis, and a balanced spine in the coronal and sagittal planes. The incision was midline and extended over. The posterior elements of the spine were exposed from the upper thoracic spine to the sacrum by stripping the muscles subperiosteally. The spinous process, the lamina, and the base of the transverse process of the vertebrae are stripped of periosteum. After removal of all soft tissue, local autograft bone was harvested from the spinous process, laminae and transverse process of all the vertebrae that would not support instrumentation as bone graft sources (Figure 1). The bone grafts were cleaned of all the attached soft tissues. A bone mill morselized the grafts and further separated the soft tissue from the bone (Figure 2). Spinal cord function was monitored throughout the procedure. Autotransfusion via preoperative storage and intraoperative collection was used. The spine was instrumented by Expedium (DePuy Spine, Inc., Raynham, MA, USA). Correction of the curves was maintained by segmental pedicle screw and rod instrumentation. All curves were instrumented and fused from T3 or T4 to L5. For the all-screw constructs, A B Figure 1. The gross appearance of the exposed posterior column before bone grafting The posterior elements of the spine were exposed from the upper thoracic spine to the sacrum by stripping the muscles subperiosteally. The spinous process, the lamina, and the base of the transverse process of the vertebrae are stripped of periosteum. After removal of all soft tissue, local autograft bone was obtained from the spinous process, laminae, and transverse process of all the vertebrae that did not support instrumentation as bone graft sources. 57

3 Imura, et al. every level was instrumented on at least one side. Apical and proximal fixation was comprised of 4.3-mm pedicle screws in the thoracic spine, and distal fixation was of 5.5 pedicle screws in the lumbar spine. An image-guided spinal navigation system was not used. Screws were placed under fluoroscopic control. The segmental pedicle screw correction was performed with rod insertion, rotation, and translation, and appropriate distraction and compression to level the proximal and distal end vertebra. Decortication of extensive posterior elements for local bone graft was performed using a motorized gouge. The local bone graft was packed onto the prepared surfaces and placed in each facet (Figure 3). The wound was sutured in 3 layers with 2 drainage tubes. Clinical and radiologic assessment Assessment was performed both clinically and with radiologic measurements. Patients were reviewed clinically and questioned about whether they felt back pain during hospitalization and at the 3-month interval after the surgery, as described by Violas et al. 9 Sitting posterior-anterior and lateral radiographs were taken the day before surgery, and at a 3-month interval after surgery. On the coronal plane, the Cobb angles of the curves were measured. On the sagittal plane, thoracic kyphosis between T3 and T12 and lumbar lordosis between L1 and L5 were measured. We evaluated the efficacy of local autograft bone for spine fusion by radiographic assessments. Fusion was defined as: stable coronal and sagittal alignment over the follow-up period, no clinical complaints, no evidence of nonunion, and stable hardware as described by Shufflebarger et al. 10 All four of these criteria must be met to indicate fusion. Figure 2. The preparation of moresellized bone chips Bone grafts were cleaned off of all the attached soft tissues. The bone mill morselized the grafts and further separated the soft tissue from the bone. Results Twenty patients were prospectively enrolled into this study. No patients were lost to follow-up. Details of the patients and operative parameters are shown in Table 1. Radiographic measurements are given in Table 2. The average age at surgery was 13 years and 4 months (range, 11 years 8 months to 17 years 2 months). The average number of levels fused was 14.2 (range, 14-15). The average operating time was 271 minutes (range, A B Figure 3. The posterior column during bone grafting Bone grafts for the fusion were placed on the decorticated bed along the length of the instrumentation. 58

4 Posterior spinal fusion for scoliosis in DMD Table 1. Details of the patients and operative parameters in the study group Patient Follow-up Operative time Intraoperative blood Total blood Age No. (months) (min) loss (ml) loss (ml) , , , , , , , , , ,260 2, , , , , ,120 2, , , , , Mean ,100 Table 2. Radiolographic measurements in the study group Scoliotic curvature (*) Thoracic kyphosis (*) Lumbar lordosis (*) Pelvic obliquity (*) Patient No. Immediate 2-year Immediate 2-year Immediate 2-year Immediate 2-year Preop Last FU Preop Last FU Preop Last FU Preop Last FU postop postop postop postop postop postop postop postop Mean (77%) (62%) 6 6 FU, follow-up 59

5 Imura, et al. minutes). The average estimated blood loss was 890 ml (range, ml). The follow-up period averaged 37 months (range, months). During hospitalization, most patients reported back pain. At 3 months after surgery, no patients reported back pain or clinical complaints. On the coronal plane, the average preoperative coronal curve measured 70 degrees (range, degrees), and the average immediate postoperative curve measured 15 degrees (range, 8-25 degrees). At last follow-up, this average curve measured 17 degrees (range, 9-27 degrees), and we noticed less than 5 degrees in loss of correction in all patients. On the sagittal plane, the average pre- and postoperative sagittal thoracic curve (T3-T12) measured 7 degrees (range, degrees) and 19 degrees (range, degrees), respectively, and 20 degrees (range, degrees) at the last follow-up. The average pre- and postoperative sagittal lumbar curve (L1- L5) measured 20 degrees (range, degrees), including kyphotic patients, and 35 degrees (range, 8-46 degrees), respectively, and 36 degrees (range, 7-44 degrees) at the last follow-up. There was no significant loss of correction in the coronal or sagittal planes. Only pedicle screws were used as vertebral anchors in the thoracic and lumbar spine. In all patients, all convex vertebrae received screws. On the concave side, the most proximal and 3-9 thoracic vertebrae of the curve and all lumbar vertebrae received screws. In 20 patients, a total of 465 screws were placed safely with no reoperations for screw malposition. Fluoroscopy was used to confirm acceptable screw position. Clinically, there were no neurologic deficits or radicular symptoms. Figure 4 shows a radiographic example of a typical case. There were 7 postoperative complications. The most common complications were paralytic ileus, occurring in 5 patients, which resolved with observation and nothing by mouth within 48 hours. There were no neurologic complications, instrumentation failures, pull-outs of fixations, or infections. There were no reoperations for any reason or any second hospitalizations related to scoliosis surgery. Radiograph of 13-year-old boy. Sitting anteroposterior preoperative radiograph demonstrates a significant thoracolumbar curve of 92 from T5 to L4. Thoracic hypokyphosis and lumbar hyperlordosis are present. At the time of surgery, local allograft bone was used. Postoperative radiograph at 1 week after surgery. Significant initial coronal curve correction was obtained and lateral radiographs indicate the contouring of the rods allow for the creation of a corrected sagittal profile. Radiograph at a long-term follow-up of 3 years 2 months after surgery reveals the cessation of deformity progression and successful instrumentation, indicated by the absence of pseudoarthrosis. Figure 4 60

6 Posterior spinal fusion for scoliosis in DMD Discussion To our knowledge, the present study is the only reported study of consecutive patients with scoliosis secondary to DMD treated with segmental pedicle screw instrumentation and local autograft bone. Excellent minimum 2-year results are shown in this study, with no reoperations required for nonunion, infection, or instrumentation failure. Loss of correction was minimal. In the literature, some authors have emphasized an interest in allograft versus auto graft. 5-7 Allograft seems to provide good results. Fabry 11 compared 2 groups of scoliosis patients who had scoliosis surgery with a Harrington device. The first group consisted of 83 patients in whom autograft (iliac crest bone graft) was used and the second group of 99 patients in whom allograft (femoral heads bone graft) was used. After a short 1-year follow-up, Fabry recommended the use of allograft bone to prevent the problems of discomfort at the donor site. He also concluded hat there was no significant difference between the 2 groups (loss of correction or complications). Nakazawa et al. 12 also compared 2 groups of scoliosis patients undergoing surgery (iliac crest vs. femoral head). They found no significant difference in the radiographic fusion rate or clinical outcomes between the 2 groups but there were some specific complications that could be attributed to the donor site in the iliac crest bone graft group. Dodd et al. 13 concluded that even in the presence of adequate iliac crest, the use of bank bone is superior for grafting in idiopathic scoliosis surgery. Grogan et al. 14 attempted to show the ability of allograft bone to produce reliable results in comparison with autograft bone. However, banked allograft bone is not often available in many countries for spinal surgery and is ultimately inferior to autogenous bone. Potential risks of bacterial contamination and viral transmission using allograft bone have been recognized, although those risks are very small. 15,16 The posterior iliac crest has been the most common donor site for autogenic bone graft in scoliosis surgery. A large quantity and good quality of bone may be harvested from the iliac crest in idiopathic scoliosis surgery; however, donor site morbidity caused by bone harvest remains a concern. Moreover, the pelvis in patients with DMD is frequently relatively small and osteoporotic, and consequently inadequate for bone harvest. 12 The potential advantages of using autogenous bone graft from the iliac crest must be weighed against the potential disadvantages. Harvesting iliac crest bone graft 61 involves additional surgical procedures and may be accompanied by complications because of the longer operating time, increased blood loss, and the higher incidence of problems associated with the donor sites. Complications of harvesting iliac crest bone graft have been well recognized in the literature. 17 The complication rate reported in the literature varies widely, ranging from 0.76% to 25% for major and 9.4% to 39% for minor complications. 9,17-21 The minor complications are superficial infection, minor wound problems, and mild pain. The major complications are infection, prolonged wound drainage, large hematomas, reoperation, and longterm pain. Additionally, hemorrhage, blood loss, fracture, healing problems, and neurovascular injuries are complications that are unquestionable, even if variable ways of obtaining autogenous bone graft from the iliac crest have been described between the outer table and intracortical of the ilium. 17,20,22 In a review of 225 patients with long-term follow-up, Banwart et al. 18 reported major complications in 10%, which included hematoma, wound infection, reoperation, unsightly scar, and chronic pain limiting physical function. Minor complications were more frequent (39%) and included dysesthesia, prolonged wound drainage, broken drain, and superficial infection. Donor site pain after harvesting from iliac crest is common, and Lehmann et al. 19 reported this complication in 55% of patients followed up on average for 33 years after spinal fusion. More recently, Skaggs et al. 23 reported that the perioperative rate of complications in iliac crest bone grafting in children was low (2%), but complications of pain (24%) and pain severe enough to interfere with daily activity (15%) was significant at a mean follow-up of more than 4 years. There have been few reports on the use of local autograft bone alone in spinal fusion surgery. Sengupta et al. 24 compared the local autograft bone and iliac crest bone graft in posterolateral spinal fusion in the degenerative disease and reported a comparable overall radiologic fusion rate and clinical outcome using either local bone or iliac crest bone graft but reduced morbidity and hospital stay in the local bone group. Violas et al. 9 reported posterior spinal fusion with Cotrel-Dubousset instrumentation (all-hook constructs) for adolescent idiopathic scoliosis in 25 patients using only local allograft bone and found no incidence of instrumentation failure, loss of correction, or pseudarthroses after longterm follow-up of minimum 5 years. They evaluated the efficacy of local allograft bone for spinal fusion only by radiographs. In the present study, even though it is often difficult to accurately determine the grade of bone grafting by

7 Imura, et al. radiography, particularly in situations where there is massive hardware, as in segmental pedicle screw instrumentation with titanium rods, the lack of progression of deformity, the lack of loss of correction, and the absence of instrument failure with a minimum follow-up of 2 years indicate the probability of the absence of pseudarthrosis. Also, no patients reported back pain at 3 months after surgery or made any clinical complaints. These results indicate that using only local bone provides similar results to using allograft bone and iliac crest bone grafts. Also, segmental pedicle screw fixation enhances correction and stabilization of spinal deformity. Pedicle screws offer a better vertebral grip with a 3- column purchase and longer moment arm compared with other forms of spinal bone-implant interfaces such as hook placement or sublaminar wires on the lamina. The screws are immediately stable in all directions after insertion. Segmental pedicle screw instrumentation has also been reported to offer a significant coronal curve correction without neurologic or visceral complications and maintenance of correction. 25 Better correction and maintenance of correction in sagittal plane alignment has also been reported with the use of segmental pedicle screw instrumentation compared with other instrumentations such as hooks, wires, and hybrid constructs. 26,27 Although pedicle screws were thought to have a higher complication risk, some investigators have reported that there is no increased neurologic risk with pedicle screw fixation and confirmed that pedicle screw placement in the thoracic and lumbar spine can be performed accurately and safely However, because segmental pedicle screw instrumentation is so stable and rigid, it could mask pseudarthroses during the first few years. Therefore, a longer-term observation must be performed to determine the final fate of this method. We suggest a diligent procedure during the exposure of the spinal posterior element enhance an excellent arthrodesis. The combination of intraperiosteal dissection, extensive posterior element decortications, removal of as much of the soft tissue and articular facets as possible, and stable segmental pedicle screw instrumentation associated with local autograft bone allows a rigid segmental instrumentation with excellent maintenance of correction in young patients in a time of life that highly favors amelioration and good healing. In conclusion, this study has shown the efficacy of using only local autograft bone rigid segmental instrumentation for scoliosis surgery in patients with DMD. We recommend this technique for patients who must undergo scoliosis surgery. 62 Study limitations There are several limitations in this study, first, due to the relatively small number of cases. Also, there was no randomized control group. Radiologic assessment of fusion is never perfect. Determination of fusion has been difficult with no reliable methods. The definition of combined minimum radiologic loss of correction with no clinical complaints was selected for this study. Ideally, a CT scan with 2-mm slices and sagittal reconstructions would provide a better tool to assess fusion status. CT scans were not performed for every patient. Fusion was assessed from plain radiographs. All consecutive 20 patients had DMD scoliosis of less than 85 degrees and pelvic obliquity of less than 15 degrees, preoperatively. Therefore, it remains to be elucidated whether or not the same conclusions apply to DMD patients with higher degrees of scoliosis and pelvic obliquity. Longer-term observation must be performed to determine the final fate of this method. References 1. Hsu JD. The natural history of spine curvature progression in the nonambulatory Duchenne muscular dystrophy patient. Spine 1983;8: Smith AD, Koreska J, Mosley CF. Progression of scoliosis in Duchenne muscular dystrophy. J Bone Joint Surg Am 1989;71: Galasko CS, Williamson JB, Delaney CM. Lung function in Duchenne muscular dystrophy. Eur Spine J 1995;4: Galasko CS, Delaney C, Morris P. Spinal stabilization in Duchenne muscular dystrophy. J Bone Joint Surg Br 1992;74: Blanco JS, Sears CJ. Allograft bone use during instrumentation and fusion in the treatment of adolescent idiopathic scoliosis. Spine 1997;22: Chugh S, Marks DS, Mangham DC, et al. Autologous bone grafting in staged scoliosis surgery. The patient as bone bank. Spine 1998;23: Stricker SJ, Sher JS. Freeze-dried cortical allograft in posterior spinal arthrodesis: use with segmental instrumentation for idiopathic adolescent scoliosis. Orthopedics 1997;20: Kurz LT, Garfin SR, Booth RE Jr. Harvesting autogenous iliac bone grafts: a review of complications and techniques. Spine 1989;14: Violas P, Chapuis M, Bracq H. Local autograft bone in the surgical management of adolescent idiopathic scoliosis. Spine 2004;29:

8 Posterior spinal fusion for scoliosis in DMD 10. Shufflebarger HL, Geck MJ, Clark CE. The posterior approach for lumbar and thoracolumbar adolescent idiopathic scoliosis: posterior shortening and pedicle screws. Spine 2004;29: Fabry G. Allograft versus autograft bone in idiopathic scoliosis surgery: a multivariate statistical analysis. J Pediatr Orthop 1991;11: Nakazawa T, Takaso M, Imura T, et al. Autogenous iliac crest bone graft versus banked allograft bone in scoliosis surgery in patients with Duchenne muscular dystrophy. Int Orthop Dodd CA, Fergusson CM, Freedman L, et al. Allograft versus autograft bone in scoliosis surgery. J Bone Joint Surg Br 1988;70: Grogan DP, Kalen V, Ross TI, et al. Use of allograft bone for posterior spinal fusion in idiopathic scoliosis. Clin Orthop Relat Res 1999;369: Campbell DG, Li P, Oakeshott RD. HIV infection of human cartilage. J Bone Joint Surg Br 1996;78: Tomford WW, Starkweather RJ, Goldman MH. A study of the clinical incidence of infection in the use of banked allograft bone. J Bone Joint Surg Am 1981;63: Arrington ED, Smith WJ, Chambers HG, et al. Complications of iliac crest bone graft harvesting. Clin Orthop Relat Res 1996;329: Banwart JC, Asher MA, Hassanein RS. Iliac crest bone graft harvest donor site morbidity. A statistical evaluation. Spine 1995;20: Lehmann TR, Spratt KF, Tozzi JE, et al. Long-term follow-up of lower lumbar fusion in patients. Spine 1987;12: Summers BN, Eisenstein SM. Donor site pain from the ilium: a complication of lumbar spine fusion. J Bone Joint Surg Br 1989;71: Turner JA, Ersek M, Herron L, et al. Patient outcomes after lumbar spinal fusions. JAMA 1992;268: Catinella FP, De Laria GA, De Wald RL. False aneurysm of the superior gluteal artery. A complication of iliac crest bone grafting. Spine 1990;15: Skaggs DL, Samuelson MA, Hale JM, et al. Complications of posterior iliac crest bone grafting in spine surgery in children. Spine 2000;25: Sengupta DK, Truumees E, Patel C K, et al. Outcome of local bone versus autogenous iliac crest bone graft in the instrumented posterolateral fusion of the lumbar spine. Spine 2006;31: Kim YJ, Lenke LG, Cho SK, et al. Comparative analysis of pedicle screw versus hook instrumentation in posterior spinal fusion of adolescent idiopathic scoliosis. Spine 2004;29: Suk SI, Kim WJ, Kim JH, et al. Restoration of thoracic kyphosis in the hypokyphotic spine: a comparison between multiple-hook and segmental pedicle screw fixation in adolescent idiopathic scoliosis. J Spinal Disord 1999;12: Suk SI, Lee CK, Kim WJ, et al. Segmental pedicle screw fixation in the treatment of thoracic idiopathic scoliosis. Spine 1995;20:

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