Lamina Osteotomy and Replantation With Miniplate Fixation for Thoracic Myelopathy Due to Ossification of the Ligamentum Flavum

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1 Lamina Osteotomy and Replantation With Miniplate Fixation for Thoracic Myelopathy Due to Ossification of the Ligamentum Flavum Zhi-Hong Nie, MD; Fa-Jing Liu, MD; Yong Shen, MD; Wen-Yuan Ding; Lin-Feng Wang, MD abstract Full article available online at Healio.com/Orthopedics. Search: Lamina osteotomy and replantation with miniplate fixation is often used to treat benign intradural tumors, effectively preventing nerve entrapment and postoperative spinal deformities. However, no studies report using this technique to treat thoracic myelopathy due to ossification of the ligamentum flavum (OLF). This article reports the clinical outcome of a series of 18 cases of contiguous multilevel OLF treated by lamina osteotomy and replantation with miniplate fixation. Eighteen consecutive patients at the authors institution were treated between 2008 and 2010 for contiguous multilevel OLF. Clinical efficacy, operative time, blood loss, sagittal alignment, and complications were investigated. Japanese Orthopaedic Association scale scores improved from preoperatively to three months postoperatively and at final follow-up (P,.01), with a mean recovery rate of 67.8%613.1%. No significant kyphotic deformity occurred postoperatively, and local kyphosis in the treated area increased by a mean of only at final follow-up. No patient required additional surgery due to spinal canal reobstruction and progressive spinal deformity. Cerebrospinal fluid leakage occurred in 4 patients and resolved after repair. Pulmonary infection and deep venous thrombosis occurred in 1 patient who was discharged with no complications after routine treatment. Figure: Preoperative lateral radiograph showing nodular projections in the canal around the dorsal of nerve root canal at the levels of T9-T10, T10- T11, and T11-T12. Lamina osteotomy and replantation with miniplate fixation is an effective therapeutic option for thoracic myelopathy due to contiguous multilevel OLF compression. The technique provides adequate decompression and stabilized sagittal alignment and avoids invasion of the spinal canal by scar tissue. The authors are from the Department of Spine Surgery, the Third Hospital of HeBei Medical University, Shijiazhuang, China. The authors have no relevant financial relationships to disclose. Dr Liu contributed equally to this study as first author. Correspondence should be addressed to: Yong Shen, MD, Department of Spine Surgery, the Third Hospital of HeBei Medical University, 139 Ziqiang Rd, Shijiazhuang , China (shenyongspine@ yahoo.com.cn). doi: / e353

2 Ossification of the ligamentum flavum (OLF), also called ossification of the yellow ligament, is a pathological condition that affects the ligament and causes insidiously progressive myeloradiculopathy. 1 Although it is considered a relatively rare entity that may cause thoracic myelopathy, 2-4 OLF is now easily detected using progressive imaging equipment, such as whole-spine magnetic resonance imaging (MRI) or computed tomography (CT). 5-7 Studies report that OLF accounts for 2% of all spinal disorders and 2.3% of all spinal surgery, 8 and the published cases of OLF are almost exclusively from patients in East Asian countries, particularly Japan and Korea. 1,4,6,9 Various surgical procedures have been developed for thoracic OLF. 2-4,10-12 Laminectomy may be the most common surgical procedure used to treat thoracic myelopathy, but postlaminectomy kyphosis and scar formation adjacent to the dura mater and nerve root may cause neurological deterioration. 5,13-15 The current study presents lamina osteotomy and replantation with miniplate fixation as a new surgical technique to address this disease. The efficacy and safety of this procedure were evaluated, with a special focus on complications occurring in the course of treatment. Materials and Methods Patients The study group comprised 18 patients (8 men and 10 women; 53 laminae) who underwent lamina osteotomy and replantation with titanium miniplate fixation due to contiguous multilevel thoracic OLF between January 2008 and March 2010 at the authors institution. Mean patient age was 56.3 years (range, years) at surgery. Mean duration of symptoms was months (range, months), and mean preoperative Japanese Orthopaedic Association (JOA) score was Patients with ossification of the posterior longitudinal ligament, space-occupying lesions, or cervical/lumbar myelopathy were excluded from this study because it Figure 1: Preoperative lateral radiograph showing nodular projections in the canal around the dorsal of nerve root canal at the levels of T9- T10, T10-T11, and T11-T12. could not be determined which factor was responsible for the myelopathy. All patients had an unremarkable medical history until the symptoms worsened and presented with dermatomal numbness, hyperreflexia, paraparesis, or sphincter dysfunction such as urinary incontinence. Patients chose to undergo surgical decompression mainly because of the failure of conservative treatment and recent neurological aggravation. 1 2A 2B Figure 2: Midsagittal (A) and axial (B) magnetic resonance images showing intramedullary signal intensity at the level of T10- T11 and the fused-type morphological features of the ossification of the ligamentum flavum. Radiological Evaluation Lateral radiographs of the thoracic spine revealed beaklike or nodular projections intruding into the dorsal foramen at the level of compression (Figure 1). Magnetic resonance imaging, especially whole-spine MRI, could clearly and comprehensively reveal the posterior compression of the spinal cord by the OLF (Figure 2). On T2- weighted MRI, 8 (44.4%) patients had increased intramedullary signal intensity at the compressed segments. All patients had continuous multisegmental lesions. The pathological ligamentum flavum involved 2 segments in 3 patients, 3 segments in 13 patients, and 4 segments in 2 patients. Of the 51 ossified segments (apart from 2 segments that were in the lumbar spine), 29 (56.9%) were located in the lower thoracic spine (T9-T12), 13 (25.5%) in the midthoracic spine (T5-T8), and 9 (17.6%) in the upper thoracic spine (T1-T4). Lateral radiographs were obtained with the patients in the neutral position pre- and postoperatively to compare the sagittal alignment changes at the surgically decompressed level. Local kyphosis in the surgical area was evaluated using the Cobb angle method (Figure 1). Postoperative neurological status and kyphosis change were assessed by 2 independent, experienced spinal surgeons (W.-Y.D., L.-F.W.) blinded to the surgical outcomes. Surgical Technique Under general anesthesia, patients were placed in the prone position with the abdomen suspended in midair. A straight longitudinal incision was made along the spinous processes centered over the level of the diseased segment. The junction of the articular process and lamina were clearly explored 1 lamina superior and 1 lamina inferior to this segment to facilitate the ensuing excision. Using a high-speed drill with a small blade (Midas Rex; Medtronic, Fort Worth, Texas), the laminae of the diseased segments were drilled away bilaterally to paper-thinness at the medial side of the facet joint. The supraspinous and interspinous ligaments at the inferior and superior margins of the diseased lamina were incised. e354 ORTHOPEDICS Healio.com/Orthopedics

3 Ossification of the Ligamentum Flavum Liu et al The spinous process and laminae of these segments were then elevated, and the dissection was performed from the caudal end using a nerve dissector and sharp-pointed knife so that the laminae along with the OLF could be removed gradually en bloc. The laminae were then prepared for reimplantation. The ossified flavum ligaments were extirpated, and the miniplates (Weigao Orthopaedic Device Co, Ltd, Weihai City, China) were attached to the spinous process and fixed with screws (4-6 mm in length). The laminae were then placed in the desired position. After the miniplates were adjusted and bent to achieve optimal realignment, they were secured to the base of the transverse process bilaterally with 8- to 10-mmlong screws. All decompression and reconstruction procedures were performed by the senior author (Y.S.) at a single institution. Neurological Assessment The dysfunction resulting from myelopathy was assessed using a modified JOA scoring system that excludes upperextremity function. A full score was 11 points. 16 The recovery rate after treatment was calculated using the Hirabayashi method: (postoperative JOA score2preoperative JOA score)/(112preoperative JOA score)3100%. 17 Statistical Analysis Continuous data are presented as mean6sd. Repeat analysis of variance tests were used to assess the statistical significance of any changes in parameters between the pre- and postoperative states. The Mann-Whitney U test did not conform to the normal distribution. A P value less than.05 was considered statistically significant. Statistical analysis was performed using SPSS version 16.0 software (SPSS, Inc, Chicago, Illinois). Results Clinical Results Mean operative time was minutes, and mean blood loss was ml. Mean follow-up was months (range, months) (Table 1). Mean JOA score improved to at 3 months postoperatively and at final follow-up, representing a significant increase compared with the preoperative score (F ; P,.001). Mean recovery rate at final follow-up was 67.8%613.1% (Table 2). Radiographic Analysis Mean Cobb angle of the surgical area increased from preoperatively to at 3 months postoperatively and at final follow-up. No statistical significance existed when compared with the preoperative level (F51.31; P..05). Mean local kyphosis in the treated area increased by (Table 2). Statistically, patients who had intramedullary intramedullary signal intensity on T2- weighted MRI showed a poorer recovery rate compared with patients with normal intensity (z ; P5.011). Postoperative MRI revealed that the spinal cord was smooth and the vertebral canal was unobstructed (Figure 3). During follow-up, no replanted laminae displacement was noted, and all patients showed complete bony healing within 3 to 6 months (mean, 4.6 months) (Figure 4). Complications Four patients experienced cerebrospinal fluid leakage intraoperatively. Dura ossification occurred in 2 patients, and the resection of the ossified tissue led to dural defects and cerebrospinal fluid leakage. High-speed drill injury and dural laceration occurred in 1 patient. Two patients were sutured with 6-0 Mersilk (Ethicon Ltd, Edinburgh, Scotland), and 2 were repaired with a piece of artificial dura. All 4 patients recovered in 2 weeks, and no cerebrospinal fluid cyst was found during follow-up. Pulmonary infection occurred in 1 elderly patient who smoked and remained in bed for more than 2 weeks due to weakness. The infection resolved after administration of the sensitive antibiotics sulbactam and cefoperazone based on the bacterial culture and drug susceptibility testing. One patient developed deep venous thrombosis in the left leg, and a dose of 4100 IU of low-molecular-weight heparin calcium was given subcutaneously. One month later, the thrombosis was decreased in size and the blocked vein recanalized. In addition, the swelling in the left leg completely disappeared. Aggravation of neurological symptoms, significant kyphosis, wound infection, and recurrence of ossification at the surgical segments were not noted (Figure 5). Discussion With the development of imaging techniques, especially high-resolution wholespine MRI, thoracic OLF is easy to detect and diagnose. Using large-scale crosssectional imaging studies, Guo et al 6 reported in a population study that 3.8% (66/1736) of patients were identified as having thoracic OLF. Among them, 31.8% (21/66) presented at multiple levels, and the continuous type accounted for 16.7% (11/66). In clinical practice, contiguous multilevel OLF is no longer a rare disease, and more attention should be given to this form of thoracic myelopathy. 1,6 A total of 18 patients with contiguous multilevel OLF were recruited for the current study. The lower thoracic spine (T9-T12) was the predominant lesion area, accounting for 56.9% of the total diseased segments, which is consistent with previous studies. 6,10,12,18 The reason why thoracic OLF has a predilection for the lower thoracic segments is puzzling, but a mechanical mechanism may play a key role in OLF development and distribution. 19,20 Okada et al 19 concluded that the lower thoracic spine had great mobility and vulnerability to flexion, extension, and rotation, undergoing local mechanical stress from tensile force due to frequent motion, and this may increase the prevalence of OLF. Otani et al 20 found that the incidence of OLF was higher in patients with kyphosis of the thoracic spine compared with individuals who had no kye355

4 Patient No./ Sex/Age, y Symptom Duration, mo OLF Levels ISI Change Table 1 Patient Clinical Data Operative Time, min Blood Loss, ml Follow-up, mo Complications 1/F/48 21 T11-L /F/57 30 T3-T5 Hyper T /M/52 25 T9-T11 Hyper T /F/59 31 T10-T CSFL 5/M/54 28 T11T12 Hyper T /F/41 16 T3-T /M/62 29 T10-T12 Hyper T /F/43 12 T4-T /M/68 36 T9-T Thrombosis 10/F/56 22 T3-T /F/70 34 T8-T10 Hyper T Pneumonia 12/M/51 10 T6-T /F/64 33 T8-T10 Hyper T CSFL 14/M/47 28 T11-L /F/66 16 T3-T4 Hyper T CSFL 16/M/58 20 T7-T /M/50 16 T10-T CSFL 18/F/67 39 T7-T9 Hyper T Mean Abbreviations: CSFL, cerebrospinal fluid leakage; Hyper T2, hyperintense on T2-weighted magnetic resonance image; ISI, intramedullary signal intensity; OLF, ossification of the ligamentum flavum. phosis of the thoracic spine and reported that local mechanical stress may be responsible for the development of ossification. Several posterior decompressive techniques have been developed to treat this disease. Apart from traditional laminectomy, 12,14 French-door laminectomy, 15 en bloc laminectomy, 10,15 fenestration, 9 and laminoplasty 11 have been applied clinically to treat thoracic OLF. Each procedure has its own advantages and disadvantages. Laminectomy and fenestration are relatively easy to perform, and no special tools are needed. French-door laminectomy and en bloc laminectomy can provide a more thorough decompression, but postoperative instability produced by wide laminectomy may affect the surgical outcome. In addition, these procedures do not prevent the invasion of hematoma and scar tissue, which can lead to late neurologic degeneration. 5,14 Transverse placement laminoplasty was reported by Hida et al, 11 in which laminae are cut using a surgical drill and then fixed using titanium miniplates after a 90 transverse rotation. The structural integrity of the spinal canal is preserved by the reconstruction of the posterior arch, but it is difficult to devise a suitable lamina to fill the gap. In the current study, the diseased segments were cut as a unit, and then the ossified ligamentum flavum was completely removed. Using titanium miniplates, the laminae were anchored at the base of the articular process bilaterally. This technique also provides adequate decompression and improves postoperative neurological function. In the current study, postoperative JOA scores improved significantly, and mean recovery rate was 67.8%, which is higher than the mean improvement rate in traditional laminectomy (48.4%) 12 and en bloc laminectomy (60.5%). 10 In addition, the current procedure had a shorter mean operative time than that of transverse placement laminoplasty (189 vs 234 minutes, respectively). 11 Most importantly, no patient had neural symptoms worsen, so the final result was satisfactory. The current technique has 4 additional advantages. First, it enables surgeons to obtain a sufficient operating field at the dissection of the dural adhesion to resect the ossified dura mater. Second, the posterior arch of the thoracic spine is reconstructed as a mechanical barrier, which can effectively prevent the invasion of scar tissue and avoid e356 ORTHOPEDICS Healio.com/Orthopedics

5 Ossification of the Ligamentum Flavum Liu et al failed back surgery syndrome. 13,14 Third, the retaining of the rear muscle attachment points can effectively avoid muscle atrophy and weakness. Fourth, it can decrease the incidence of postoperative instability, subluxation, and kyphotic deformity, to a certain extent. Some authors have suggested that a late onset increases the kyphotic deformity of the thoracic spine, which may minimize the possible beneficial effect of posterior decompression. 12,19,21 Aizawa et al 15,21 reported that an increased mean kyphotic angle was associated with laminectomy and ranged from 3.8 to 4. Chen et al 12 reported that after laminectomy, average kyphotic angle increased by 3 in a long-term follow-up. In the current study, the Cobb angle at the surgical area had a mean increased kyphotic angle of 1.9. Most (83.3%) of the current patients had a decompression level of 3 or more segments and more surgical levels involved than those in the study by Chen et al. 12 Therefore, the current technique was more effective at sustaining sagittal alignment than is laminectomy. Although laminectomy does not lead significantly to spinal instability, it cannot prevent hypermobility of the surgical segments, which can result in progression of kyphotic deformity in the long term. For these reasons, the authors chose lamina osteotomy and replantation combined with miniplate fixation to treat multilevel thoracic OLF. The postoperative images revealed no new compression, and the spinal cord remained smooth in all cases. It is still unknown whether intramedullary signal intensity on T2-weighted MRI can predict the surgical outcome. In most studies, the intramedullary signal change was considered to represent the presence of demyelination and microcavitation in the spinal cord, and it could not predict the outcome. 1,22 Other experts felt that intramedullary signal intensity had a negative effect on the surgical outcome. 9,23 In the current study, 44.4% (8/18) of patients showed intramedullary signal intensity on Table 2 Pre- and Postoperative Sagittal Alignment and Neurological Changes Patient No. Cobb Angle, deg JOA Score Pre 3 mo Post Final FU Pre 3 mo Post Final FU Recovery Rate, % Mean a a b b Abbreviations: deg, degrees; FU, follow-up; Post, postoperatively; Pre, preoperatively; JOA, Japanese Orthopaedic Association. a P..05 vs preoperatively by repeated measurement of analysis of variance. b P,.001 vs preoperatively by repeated measurement of analysis of variance. 3A Figure 3: Sagittal (A) and axial (B) magnetic resonance images showing that the spinal cord was unobstructed and the anteroposterior diameter of the canal had increased significantly. 3B e357

6 4A Figure 4: Anteroposterior (A) and lateral (B) radiographs showing the laminae fixed with a titanium miniplate bilaterally. No significant kyphotic deformity was noted in the surgical area 2 years postoperatively. 4B Figure 5: Lateral computed tomography scan (A) and anteroposterior 3- dimensional reconstruction (B) showing no new ossification and that the replanted laminae were stable with a firm bony fusion at final follow-up. 5A 5B T2-weighted MRI preoperatively, which was consistent with other studies. 12,23 The current study also found that patients who had intramedullary signal intensity on T2- weighted MRI showed a poorer neurological recovery compared with patients with a normal signal. Therefore, intramedullary signal intensity on T2-weighted MRI not only reflects the pathological condition of the spinal cord, but also can predict the prognosis of patients with thoracic OLF. Several perioperative complications have been reported in patients with thoracic OLF. Cerebrospinal fluid leakage after dural laceration is a major intraoperative complication, occurring especially in cases with dural adhesion and dural ossification. 2-4,9,12,18-24 Various methods and materials have been designed to repair dural laceration and defects, including lumbar subarachnoid drainage, sleeping in the prone position, silk suture, gelatin sponge, and artificial dura. 24 In the current study, cerebrospinal fluid leakage occurred in 4 patients; 6-0 silk suture was used for dural laceration, and artificial dura was used for dural defects. No cerebrospinal fluid pseudocyst, wound dehiscence, or meningitis occurred in the study. Conclusion Lamina osteotomy and replantation with miniplate fixation is an effective alternative surgical option for contiguous multilevel thoracic OLF, providing adequate decompression and stabilized sagittal alignment. In addition to the barrier effect, the laminae can effectively prevent the invasion of scar tissue toward the dura. References 1. Inamasu J, Guiot BH. A review of factors predictive of surgical outcome for ossification of the ligamentum flavum of the thoracic spine. J Neurosurg Spine.2006; 5(2): Ben Hamouda K, Jemel H, Haouet S, Khaldi M. Thoracic myelopathy caused by ossification of the ligamentum flavum: a report of 18 cases. J Neurosurg. 2003; 99(2 suppl): Miyakoshi N, Shimada Y, Suzuki T, et al. Factors related to long-term outcome after decompressive surgery for ossification of the ligamentum flavum of the thoracic spine. J Neurosurg. 2003; 99(3 suppl); Aizawa T, Sato T, Sasaki H, Kusakabe T, Morozumi N, Kokubun S. Thoracic myelopathy caused by ossification of the ligamentum flavum: clinical features and surgical results in the Japanese population. J Neurosurg Spine. 2006; 5(6): Yonenobu K, Ebara S, Fujiwara K, et al. Thoracic myelopathy secondary to ossification of the spinal ligament. J Neurosurg. 1987; 66(4): Guo JJ, Luk KD, Karppinen J, Yang H, Cheung KM. Prevalence, distribution, and morphology of ossification of the ligamentum flavum: a population study of one thousand seven hundred thirty-six magnetic resonance imaging scans. Spine (Phila Pa 1976). 2010; 35(1): Maiuri F, Iaconetta G, Gambardella A. Ossification of the yellow ligament causing thoracic cord compression. Arch Orthop Trauma Surg. 2000; 120(5-6): Hanakita J, Suwa H, Ohta F, Nishi S, Sakaida H, Iihara K. Neuroradiological examination of thoracic radiculomyelopathy due to ossification of the ligamentum flavum. Neuroradiology. 1990; 32(1): He S, Hussain N, Li S, Hou T. Clinical and prognostic analysis of ossified ligamentum flavum in a Chinese population. J Neurosurg Spine. 2005; 3(5): Jia LS, Chen XS, Zhou SY, Shao J, Zhu W. En bloc resection of lamina and ossified ligamentum flavum in the treatment of thoracic ossification of the ligamentum flavum. Neurosurgery. 2010; 66(6): Hida S, Naito M, Arimizu J, Morishita Y, Nakamura A. The transverse placement laminoplasty using titanium miniplates for the reconstruction of the laminae in thoracic and lumbar lesion. Eur Spine J. 2006; 15(8): Chen XQ, Yang HL, Wang GL, et al. Surgery for thoracic myelopathy caused by ossification of the ligamentum flavum. J Clin Neurosci. 2009; 16(10): Lawson KJ, Malycky JL, Berry JL, Steffee AD. Lamina repair and replacement to control laminectomy membrane formation in dogs. Spine (Phila Pa 1976). 1991; 16(6 suppl):s222-s Yücesoy K, Karci A, Kiliçalp A, Mertol T. The barrier effect of laminae: laminotomy versus laminectomy. Spinal Cord. 2000; 38(7): Aizawa T, Sato T, Ozawa H, et al. Sagittal alignment changes after thoracic laminectomy in adults. J Neurosurg Spine. 2008; 8(6): Li KK, Chung OM, Chang YP, So YC. Myelopathy caused by ossification of ligamentum flavum. Spine (Phila Pa 1976). 2002; 27(12):E308-E312. e358 ORTHOPEDICS Healio.com/Orthopedics

7 Ossification of the Ligamentum Flavum Liu et al 17. Hirabayashi K, Miyakawa J, Satomi K, Maruyama T, Wakano K. Operative results and postoperative progression of ossification among patients with ossification of cervical posterior longitudinal ligament. Spine (Phila Pa 1976). 1981; 6(4): Chang UK, Choe WJ, Chung CK, Kim HJ. Surgical treatment for thoracic spinal stenosis. Spinal Cord. 2001; 39(7): Okada K, Oka S, Tohge K, Ono K, Yonenobu K, Hosoya T. Thoracic myelopathy caused by ossification of the ligamentum flavum. Clinicopathologic study and surgical treatment. Spine (Phila Pa 1976). 1991; 16(3): Otani K, Aihara T, Tanaka A, Shibasaki K. Ossification of the ligamentum flavum of the thoracic spine in adult kyphosis. Int Orthop. 1986; 10(2): Aizawa T, Sato T, Sasaki H, et al. Results of surgical treatment for thoracic myelopathy: minimum 2-year follow-up study in 132 patients. J Neurosurg Spine. 2007; 7(1): Liao CC, Chen TY, Jung SM, Chen LR. Surgical experience with symptomatic thoracic ossification of the ligamentum flavum. J Neurosurg Spine. 2005; 2(1): Kuh SU, Kim YS, Cho YE, et al. Contributing factors affecting the prognosis surgical outcome for thoracic OLF. Eur Spine J. 2006; 15(4): Sun X, Sun C, Liu X, Liu Z, et al. The frequency and treatment of dural tears and cerebrospinal fluid leakage in 266 patients with thoracic myelopathy caused by ossification of the ligamentum flavum. Spine (Phila Pa 1976). 2012; 37(12):E702-E707. e359

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