Factors related to long-term outcome after decompressive surgery for ossification of the ligamentum flavum of the thoracic spine

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1 J Neurosurg (Spine 3) 99: , 2003 Factors related to long-term outcome after decompressive surgery for ossification of the ligamentum flavum of the thoracic spine NAOHISA MIYAKOSHI, M.D., YOICHI SHIMADA, M.D., TETSUYA SUZUKI, M.D., MICHIO HONGO, M.D., YUJI KASUKAWA, M.D., KYOJI OKADA, M.D., AND EIJI ITOI, M.D. Department of Orthopedic Surgery, Akita University School of Medicine, Akita, Japan Object. Factors related to long-term surgical outcome of thoracic myelopathy caused by ossification of the ligamentum flavum (OLF) have not been fully investigated. To evaluate these factors, the authors reviewed medical records obtained in patients who had undergone decompressive surgery for thoracic OLF. Methods. Thirty-four patients in whom decompressive surgery was performed for thoracic OLF (mean follow-up period 8 years) were recruited. Fourteen patients underwent simultaneous decompressive surgery for cervical or lumbar lesions. Patient age, duration of symptoms, OLF type, dural adhesion, neurological status classified by the Japanese Orthopaedic Association (JOA) scale before and after surgery (1 month postoperatively and at final follow up), and recovery rate were reviewed. The ossified ligamentum flavum was classified into five types according to Sato s classification by assessing preoperative computerized tomography scans. The mean preoperative JOA score (5) was significantly improved at 1 month after surgery (7.1) and at final follow up (7.9) (p 0.05). Recovery rates at 1 month and at final follow up were 34.6 and 44.2%, respectively. No significant correlations were found between age, OLF type, and neurological status before and after surgery. In patients with dural adhesion, which was observed in cases of larger-type OLF (p 0.02), lower JOA scores were observed compared with those in patients without dural adhesion both preoperatively and at 1 month after surgery (p 0.05) but not at the final follow-up examination. Higher JOA scores and recovery rates were demonstrated in patients who had undergone simultaneous surgery than in those who had not undergone simultaneous surgery at 1 month (p 0.05) but not at the final follow up. Using multiple regression analysis, the authors identified the duration of preoperative symptoms as the most important predictor of a high JOA score and recovery rate at the final follow up. Conclusions. Duration of preoperative symptoms represents the most important predictor of long-term surgeryrelated outcome in patients treated for thoracic OLF. The type of ossified ligamentum flavum, dural adhesion, and simultaneous surgery for coexistent cervical or lumbar lesions do not appear to influence the long-term postoperative prognosis. KEY WORDS ossification of the ligamentum flavum thoracic spine dural adhesion myelopathy decompression O SSIFICATION of the ligamentum flavum is often observed in the lower third of the thoracic spine 5,17,21 and frequently produces myelopathy. 5,13,15 Thoracic OLF-induced myelopathy has predominantly been reported in the Japanese population 5,7,11,13,14,16,17,19,22,26 and has rarely been reported in Caucasian individuals. 1,15,20,23,24 Even in Japan, however, thoracic myelopathy caused by OLF is far less common than cervical myelopathy. 7,17 The annual operation rate for thoracic myelopathy per one million people was 5.1 in Japan between 1988 and 1994; 64% of these cases were related to OLF. 17 This rate is only 9% of that reported for cervical myelopathy. 12 Because of the scarcity of cases, surgery-related outcome, particularly long-term outcome, and factors related to outcome in Abbreviations used in this paper: CT = computerized tomography; JOA = Japanese Orthopaedic Association; OLF = ossification of the ligamentum flavum; SD = standard deviation. J. Neurosurg: Spine / Volume 99 / October, 2003 patients with thoracic OLF-induced myelopathy have not been fully investigated. In this study, we retrospectively reviewed data obtained in patients with thoracic OLFinduced myelopathy who had undergone decompressive surgery to determine factors related to outcome. Cases of thoracic OLF are often complicated by the presence of multiple spinal lesions in the cervical and/or lumbar spine. 2,19,22 In the clinical setting, we cannot ignore these complicated cases because they are not small in number, and therefore clarification of their characteristics is important. In this study, we further compared data obtained in patients who had undergone simultaneous surgery for coexistent cervical or lumbar lesions with those in patients who had undergone surgery for thoracic OLF alone. Clinical Material and Methods Patient Population Since 1980, 45 consecutive patients with thoracic OLFinduced myelopathy have undergone decompressive sur- 251

2 N. Miyakoshi, et al. FIG. 1. Postmyelography CT scans demonstrating the OLF classification: Lateral type (upper left), extended type (upper center), enlarged type (upper right), fused type (lower left), and tuberous type (lower right). gery at our institution. Of these, 34 patients (22 men, 12 women) with follow-up data exceeding 5 years (mean 8 years, range 5 16 years) were included in the present study. The mean age of the population was 54 years (range years). Radiographs, preoperative CT studies, and clinical and operative records were available in all cases. Indication for surgery in all patients had been progressive and severe thoracic myelopathy. Decompressive laminectomy and resection of the ossified ligamentum flavum were performed in all cases. Fourteen patients underwent simultaneous decompressive surgery of the cervical or lumbar spine in addition to that for thoracic OLF, because coexisting cervical or lumbar lesions could not be excluded from causing their lower-extremity symptoms. Classification of OLF Ossification of the ligamentum flavum was classified into five types according to the range and morphological features of the ossification depicted on preoperative CT scans at the narrowest spinal level: lateral, extended, enlarged, fused, and tuberous 18 (Fig. 1). The lateral-type lesion showed ossification only at the facet joint capsule; the extended type showed ossification extending to the lamina; the enlarged type showed thickened ossification with anteromedial enlargement; the fused type showed thickened bilateral ossified ligaments fused at the midline; and the tuberous type showed fused ossified ligaments growing anteriorly. The more advanced the ossified ligamentum flavum from the lateral to the tuberous type, the more stenotic the spinal canal becomes. Clinical Evaluations For the assessment of neurological status, the JOA scoring system for cervical myelopathy 9,25 was modified for thoracic myelopathy. 17 Scores for manual dexterity (4 points) and sensory impairment of the upper extremities (2 points) were excluded from the original scoring system, creating a maximum (normal) score in the modified evaluation for thoracic myelopathy of 11 points (Table 1). The recovery rate 6 was calculated as: (postoperative JOA score preoperative JOA score)/(11 preoperative JOA score) 100. To clarify the effect of factors potentially affecting surgery-related outcome, we evaluated the relationships between JOA score/recovery rate and age, type of OLF, preoperative duration of symptoms, presence of dural adhesion observed intraoperatively, number of decompressed vertebrae, and performance of simultaneous decompressive surgery for coexisting cervical or lumbar lesions. Data Analysis All data are presented as the mean SD and were analyzed using the StatView statistical package (SAS Institute, Cary, NC). Statistical differences among groups were compared using the Fisher protected least significant difference method (post hoc test) for multiple comparisons in a one-way analysis of variance. The chi-square test was used for categorical variables. Correlations among variables were analyzed using the Pearson correlation coefficient or Spearman rank correlation, as appropriate. Using multiple regression, further analyses were conducted to determine the variables best correlating to surgical outcome. Probability values less than 0.05 were considered statistically significant. Results Outcome After Decompressive Surgery Table 2 provides a summary of overall outcome in the 34 patients treated for thoracic OLF. The JOA score was significantly improved both at 1 month and at final follow-up examination. Recovery rates at 1 month and at final follow up were 34.6 and 44.2%, respectively. Factors Related to Outcome of Thoracic OLF Based on CT scanning evidence, the OLF types were lateral in three cases, extended in two, enlarged in 15, fused in nine, and tuberous in five cases. No significant correlation was observed between the OLF type and the 252 J. Neurosurg: Spine / Volume 99 / October, 2003

3 Factors related to surgical outcome of thoracic OLF TABLE 1 Modified JOA scoring system for thoracic myelopathy* TABLE 2 Characteristics and outcomes in 34 patients with thoracic OLF* Function Score Description Variable Mean SD (range) motor lower extremity 0 unable to stand up & walk by any means 1 unable to walk w/o a cane or other support on level ground 2 walks independently but needs support on stairs 3 capable of fast but clumsy walking 4 normal sensory trunk 0 complete loss of touch & pain sensation 1 60% normal sensation &/or moderate pain or numbness 2 normal lower extremity 0 complete loss of touch & pain sensation 1 60% normal sensation &/or moderate pain or numbness 2 normal bladder 0 urinary retention &/or incontinence 1 sense of retention &/or dribbling &/or thin stream &/or incomplete continence 2 urinary retardation &/or pollakiuria 3 normal *Total score for a healthy patient is 11. preoperative JOA score or JOA score/recovery rate at 1 month and at final follow up (Table 3). Significant positive correlations were observed between the preoperative duration of symptoms and the preoperative JOA score (Table 4). The duration of symptoms showed significant negative correlations with the JOA score at final follow up, the recovery rate at 1 month, and the recovery rate at final follow up. Neither age nor the number of decompressed vertebrae showed significant correlations with the JOA score/recovery rate at any time point (data not shown). Dural adhesion was observed in zero (0%) of three lateral types, zero (0%) of two extended types, 11 (73%) of 15 enlarged types, five (56%) of nine fused types, and all five tuberous types (100%). The occurrence of dural adhesion increased substantially in conjunction with increased severity of OLF type (p = 0.02). The JOA scores preoperatively and at 1 month were significantly lower in patients with dural adhesion than in those without (Table 5). There were no significant differences, however, in JOA scores at final follow up and the recovery rates at 1 month and at final follow up observed between patients with and without dural adhesion. No other significant differences in demographic data were identified between the groups with and without dural adhesion. In patients who had undergone concomitant decompressive surgery of the cervical and/or lumbar spine in addition to treatment for ossified ligamentum flavum, higher JOA score and recovery rate were demonstrated at 1 month but not at final follow up, compared with scores in patients not undergoing comcomitant surgery (Table 6). Dural adhesion was observed in five (36%) of 14 patients with simultaneous surgery, and in 16 (80%) of 20 patients J. Neurosurg: Spine / Volume 99 / October, 2003 age at op (yrs) (22 78) preop duration of symptoms (mos) (2 60) follow-up period (yrs) (5 16) no. of decompressed thoracic vertebrae (1 11) JOA score preop (1 8) 1 mo (2 11) FFU (3 11) RR (%) 1 mo (0 100) FFU ( 50 to 100) * FFU = final follow up; RR = recovery rate. p 0.05 compared with preoperative JOA score. without simultaneous surgery, representing a significant difference between the groups (p 0.01). Multiple regression analysis identified the duration of symptoms is the most important predictor of the JOA score at final follow up, followed by the preoperative JOA score (Table 7). The duration of symptoms was also the most important predictor of recovery rate at final follow up. No other variables displayed significant associations with JOA score or the recovery rate at final follow up. Discussion Surgical Outcome of Thoracic OLF Thoracic OLF frequently develops in the lower thoracic region in middle-aged men. 19 Investigators of several studies have suggested that surgery is the most effective treatment for thoracic myelopathy. 4,7,15,26 In the present study, surgery-related outcome was evaluated using the JOA score and the recovery rate. The JOA score indicates the absolute status of the patient, whereas the recovery rate indicates relative improvement compared with preoperative status. The overall recovery rate at the final follow-up was 44.2%, which is comparable to the rates of 43.7 to 48% reported in the literature. 17,22 These recovery rates, however, remain lower than those for cervical myelopathy (50 70%) caused by cervical ossification of the posterior longitudinal ligament of the cervical spine. 6,8,10 Because the thoracic spine is least mobile, static compression rath- TABLE 3 Correlations between OLF type and JOA score or recovery rate Variable r Correlation* p Value OLF compared w/ preop JOA score mo JOA score FFU JOA score mo RR FFU RR * Correlation between variables as determined by Spearman rank correlation with OLF type was scored from small to large as: 1, lateral type; 2, extended type; 3, enlarged type; 4, fused type; and 5, tuberous type. 253

4 N. Miyakoshi, et al. TABLE 4 Correlations between preoperative symptom duration and JOA score or recovery rate Variable r Coefficient* p Value preop duration compared w/ preop JOA score mo JOA score FFU JOA score mo RR FFU RR * Data represent Pearson correlation coefficient. er than dynamic compression is the principal factor causing thoracic myelopathy. 22 Conservative treatments such as brace immobilization are not expected to improve thoracic myelopathy, and thus surgery is usually the treatment of choice. Conservative treatments, however, may be prescribed in some cases of thoracic myelopathy because the upper extremities are not involved and accordingly the activities of daily living are less impaired than in cases of cervical myelopathy. This may explain why the recovery rates in thoracic myelopathy are lower than those in cervical myelopathy. Factors Affecting Prognosis of Thoracic OLF Takei 22 has reported that factors leading to poor outcome after decompressive surgery for thoracic myelopathy caused by OLF and/or ossification f the posterior longitudinal ligament include preoperative lower-extremity function, length of illness, multiple ossification, level and progression of ossification, degree of thoracic kyphosis, and complications. After evaluating a variety of factors that might affect surgery-related outcomes in patients with thoracic OLF, Shiokawa, et al., 19 concluded that preoperative duration of symptoms was significantly shorter in patients with excellent outcomes. No significant differences were observed for prognosis and morbidity levels, presence of coexistent spinal lesions, presence of magnetic resonance imaging documented intramedullary changes, or operation for coexistent lesions. Sato, et al., 17 also reported that patients with thoracic myelopathy and longer preoperative duration of disease exhibited less improvement after surgery. We also found that the most important predictor of improved postoperative JOA score was a short duration of symptoms, followed by preoperative neurological status. A short duration of symptoms was also the only predictor of a good recovery rate. These results indicate that exacerbation of preoperative neurological status over a long period of time is largely irreversible. Therefore, to achieve the best results, surgical intervention should be undertaken as early as possible. Dural Adhesion Anticipation of dural adhesion is important to facilitate operative planning. The relationship between dural adhesion and surgical outcomes for thoracic OLF, however, has not been specifically evaluated. Dural adhesion was observed in 62% of the cases in our series. We found that dural adhesion was frequently observed in larger types of OLF. No correlation existed, however, between OLF type TABLE 5 Outcomes for thoracic OLF with or without dural adhesion* Dural Adhesion Variable No (13 cases) Yes (21 cases) age at op (yrs) preop symptom duration (mos) follow-up period (yrs) no. of decompressed thoracic vertebrae JOA score preop mo FFU RR 1 mo FFU *Values are expressed as the mean SD. p 0.05 compared with patients without dural adhesion. and preoperative neurological status or postoperative outcome. Dural adhesion represents a deleterious factor for preoperative and short-term postoperative neurological status, but not for long-term prognosis. Thoracic OLF and Coexistent Cervical or Lumbar Spine Lesions Many cases of thoracic OLF are complicated by the presence of multiple spinal lesions in the cervical and/or lumbar spine. 2,19,22 Careful judgment in determining the responsible lesion is therefore necessary. In patients with tandem lesions, neurological findings can play an important role in determining the responsible lesion. 5,22 Differentiating the nonresponsible lesions from the responsible lesion, however, is sometimes very difficult. 22 Therefore, in cases with tandem lesions of both the thoracic and the cervicolumbar spine, concomitant decompressive surgery should be considered unless the responsible lesion is obvious. In the present study, 14 patients (41%) underwent same-stage decompressive surgery for a cervical or lumbar lesion because TABLE 6 Outcomes after thoracic OLF treatment stratified by need/no need for concomitant decompression for coexistent cervical or lumbar lesions* Concomitant Op Variable No (20 cases) Yes (14 cases) age at op (yrs) preop symptom duration (mos) follow-up period (yrs) no. of decompressed thoracic vertebrae JOA score preop mo FFU RR (%) 1 mo FFU *Values are expressed as the mean SD. p 0.01 compared with group not requiring concomitant surgery. p 0.05 compared with group not requiring concomitant surgery. 254 J. Neurosurg: Spine / Volume 99 / October, 2003

5 Factors related to surgical outcome of thoracic OLF TABLE 7 Results of multiple regression analyses of surgical outcomes JOA Score at FFU RR at FFU Variable r Coefficient p Value r Coefficient p Value intercept age at op (yrs) preop symptom duration (mos) preop JOA score type of OLF* no. of decompressed vertebrae dural adhesion simultaneous op *Type of OLF was scored from small to large as: 1, lateral; 2, extended; 3, enlarged; 4, fused; and 5, tuberous. With dural adhesion = 1; without dural adhesion = 0. Simultaneous = 1; no simultaneous surgery = 0. these coexisting lesions could not be completely excluded from being the cause of the symptoms. Interestingly, in this study the presence of simultaneous surgery for coexisting cervical or lumbar lesion represented a positive prognostic factor for short-term results. A dural adhesion was observed significantly less often in patients who had undergone concomitant surgery than in those who had not. In other words, thoracic OLF requiring simultaneous decompressive surgery for coexistent spinal lesions is associated with a lower incidence of dural adhesion. These results might indicate that tandem lesions accelerate neurological deterioration and aggravate clinical symptoms before dural adhesions become evident. Abnormalities of spinal cord evoked potentials can reportedly indicate the spinal level involved in the development of a disorder. 2,3 Therefore, in cases with multiple lesions, electrophysiological monitoring such as the aforementioned modality should be considered in addition to comprehensive imaging-based diagnosis and neurological examination. Conclusions In the present study, factors related to long-term (mean follow-up period 8 years) surgical outcome of thoracic myelopathy caused by OLF were investigated. Factors such as the presence of dural adhesion and the need for concomitant surgery for coexistent cervical or lumbar lesions have not been investigated in other studies evaluating surgery-related outcomes of thoracic OLF. No correlations were observed between the types of OLF and preoperative neurological status or postoperative prognosis. Dural adhesion, which was frequently observed in larger types of OLF, represented a deteriorative factor for preoperative and short-term postoperative neurological status but not for long-term prognosis. Simultaneous decompressive surgery for coexistent cervical or lumbar lesions improves short-term results but not long-term prognosis. The most important predictor of long-term surgical outcome for thoracic OLF is duration of symptoms. J. Neurosurg: Spine / Volume 99 / October, 2003 References 1. Arafat QW, Jackowski A, Chavda SV, et al: Case report: ossification of the thoracic ligamenta flava in a Caucasian: a rare cause of myelopathy. Br J Radiol 66: , Baba H, Maezawa Y, Imura S: Spinal cord evoked potential monitoring for cervical and thoracic compressive myelopathy. Paraplegia 34: , Baba H, Tomita K, Kawahara N, et al: Spinal cord evoked potentials in thoracic myelopathy with multisegmental vertebral involvement. Spine 17: , Barnett GH, Hardy RW Jr, Little JR, et al: Thoracic spinal canal stenosis. J Neurosurg 66: , Hanakita J, Suwa H, Ohta F, et al: Neuroradiological examination of thoracic radiculomyelopathy due to ossification of the ligamentum flavum. Neuroradiology 32:38 42, Hirabayashi K, Miyakawa J, Satomi K, et al: Operative results and postoperative progression of ossification among patients with ossification of cervical posterior longitudinal ligament. Spine 6: , Ido K, Shimizu K, Iida H, et al: Surgical treatment for ossification of the posterior longitudinal ligament and the yellow ligament in the thoracic and cervico-thoracic spine. Spinal Cord 36: , Iwasaki M, Kawaguchi Y, Kimura T, et al: Long-term results of expansive laminoplasty for ossification of the posterior longitudinal ligament of the cervical spine: more than 10 years follow up. J Neurosurg (Spine 2) 96: , Japanese Orthopaedic Association: Scoring system (17 2) for cervical myelopathy. J Jpn Orthop Assoc 68: , Kawaguchi Y, Kanamori M, Ishihara H, et al: Progression of ossification of the posterior longitudinal ligament following en bloc cervical laminoplasty. J Bone Joint Surg Am 83: , Kojima T, Oonishi I, Kurokawa T: Ossification of the ligamentum flavum in the thoracolumbar spine of young adults report of two cases. Int Orthop 16:75 79, Kokubun S, Sato T, Ishii Y, et al: Cervical myelopathy in the Japanese. Clin Orthop 323: , Miyasaka K, Kaneda K, Ito T, et al: Ossification of spinal ligaments causing thoracic radiculomyelopathy. Radiology 143: , Okada K, Oka S, Tohge K, et al: Thoracic myelopathy caused by ossification of the ligamentum flavum. Clinicopathologic study and surgical treatment. Spine 16: , Omojola MF, Cardoso ER, Fox AJ, et al: Thoracic myelopathy secondary to ossified ligamentum flavum. J Neurosurg 56: , Otani K, Aihara T, Tanaka A, et al: Ossification of the ligamentum flavum of the thoracic spine in adult kyphosis. Int Orthop 10: , Sato T, Kokubun S, Tanaka Y, et al: Thoracic myelopathy in the 255

6 N. Miyakoshi, et al. Japanese: epidemiological and clinical observations on the cases in Miyagi Prefecture. Tohoku J Exp Med 184:1 11, Sato T, Tanaka Y, Aizawa T, et al: [Surgical treatment for ossification of ligamentum flavum in the thoracic spine and its complications.] Spine Spinal Cord 11: , 1998 (Jpn) 19. Shiokawa K, Hanakita J, Suwa H, et al: Clinical analysis and prognostic study of ossified ligamentum flavum of the thoracic spine. J Neurosurg (Spine 2) 94: , Shiraishi T, Crock HV, Lewis P: Thoracic myelopathy due to isolated ossification of the liamentum flavum. J Bone Joint Surg Br 77: , Smith DE, Godersky JC: Thoracic spondylosis: an unusual cause of myelopathy. Neurosurgery 20: , Takei Y: Posterior decompression surgery of thoracic myelopathy due to ossification of intraspinal canal ligaments. J Tokyo Med Coll 54: , van Oostenbrugge RJ, Herpers MJ, de Kruijk JR: Spinal cord compression caused by unusual location and extension of ossified ligamenta flava in a Caucasian male. A case report and literature review. Spine 24: , Vera CL, Cure JK, Naso WB, et al: Paraplegia due to ossification of ligamenta flava in X-linked hypophosphatemia. A case report. Spine 22: , Yonenobu K, Abumi K, Nagara K, et al: Interobserver and intraobserver reliability of the Japanese Orthopaedic Association Scoring System for evaluation of cervical compression myelopathy. Spine 26: , Yonenobu K, Ebara S, Fujiwara K, et al: Thoracic myelopathy secondary to ossification of the spinal ligament. J Neurosurg 66: , 1987 Manuscript received April 3, Accepted in final form July 22, Address reprint requests to: Naohisa Miyakoshi, M.D., Department of Orthopedic Surgery, Akita University School of Medicine, Hondo, Akita , Japan. miyakosh@doc.med. akita-u.ac.jp. 256 J. Neurosurg: Spine / Volume 99 / October, 2003

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