Suboccipital decompression for Chiari malformation associated scoliosis: risk factors and time course of deformity progression
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1 J Neurosurg Pediatrics 1: , 2008 Suboccipital decompression for Chiari malformation associated scoliosis: risk factors and time course of deformity progression FRANK J. ATTENELLO, M.S., MATTHEW J. MCGIRT, M.D., APRIL ATIBA, B.S., MURAYA GATHINJI, M.S., GHAZALA DATOO, B.S., JON WEINGART, M.D., BENJAMIN CARSON, M.D., AND GEORGE I. JALLO, M.D. Department of Neurosurgery, The Johns Hopkins School of Medicine, Baltimore, Maryland Object. Chiari malformation Type I (CM-I) is often associated with scoliosis. It remains unclear which subgroups of patients are most likely to experience progression of spinal deformity after cervicomedullary decompression. The authors goal was to determine the time frame of curvature progression and assess which patient subgroups are at greatest risk for progression of spinal deformity after surgery. Methods. The authors retrospectively reviewed the records of all pediatric patients with significant scoliosis in whom suboccipital decompression was performed to treat for CM-I during a 10-year period at a single academic institution. Clinical, radiological, and operative variables were assessed as independent factors for failure (worsening of scoliosis) by using a univariate regression analysis. Results. Twenty-one children (mean age 9 3 years; 4 male) underwent hindbrain decompression for CM-I associated scoliosis and were followed for a mean of 39 months. All patients harbored a syrinx. Eight patients (38%) experienced improvement in scoliosis curvature, whereas 10 (48%) suffered a progression. Thoracolumbar junction scoliosis (p = 0.04) and failure of the syrinx to improve (p = 0.05) were associated with 5- and 4-fold respective increases in the likelihood of deformity progression. Each increasing degree of preoperative Cobb angle was associated with an 11% increase in the likelihood of scoliotic curve progression (p 0.05). Conclusions. Over one third of patients with CM-I associated scoliosis will improve after cervicomedullary decompression alone. Cervicomedullary decompression is a good first-line option, particularly in children with concordant posterior fossa symptoms. Patients presenting with more severe scoliosis (increasing Cobb angle) or scoliosis that crosses the thoracolumbar junction may benefit from earlier orthopedic involvement and should be monitored regularly for curvature progression after cervicomedullary decompression. In cases in which there is a failure of the syrinx to show improvement after suboccipital decompression, the patients are also more likely to develop curvature progression. (DOI: /PED/2008/1/6/456) KEY WORDS Chiari malformation outcome predictors scoliosis C Abbreviations used in this paper: CI = confidence interval; CM-I = Chiari malformation Type 1; HR = Hazard ratio. HIARI malformation Type I, defined as caudal displacement of the cerebellar tonsils into the cervical canal, was first documented by Hans Chiari 4 in Over the last century, multiple symptoms of cerebellar, brainstem, and spinal cord pathology have been attributed to this complex disease. 11,13,14 Standard surgical management for CM-I remains posterior fossa decompression. 2,5,10 Up to 30% of all patients with CM-I and 60% of patients with Chiari malformation associated syringomyelia will present with scoliosis. 1,3,6 9,12,13 The authors of previous studies have reported a wide range of outcomes after hindbrain decompression for Chiari malformation associated scoliosis with 20 70% of patients experiencing curve progression. 1,3,6 9,12 Reports of improvement in scoliosis after hindbrain decompression also range widely from 20 to 60%. 1,3,6 9,12 Hence, there is no consensus on the absolute risk and time frame of scoliosis progression after hindbrain decompression. Furthermore, it remains unclear which subgroups of patients are most likely to suffer progression of their spinal deformity after cervicomedullary decompression. We set out to determine the time frame of curvature progression and assess which patient subgroups are at greatest risk for progression of spinal deformity postoperatively. Clinical Materials and Methods In 21 consecutive patients undergoing posterior fossa decompression for CM-I associated scoliosis at The Johns Hopkins Hospital between 1995 and 2005, we reviewed presenting symptoms, neurological deficits, demographic data, 456 J. Neurosurg.: Pediatrics / Volume 1 / June 2008
2 Suboccipital decompression for CM-I associated scoliosis comorbidities, pre- and postoperative radiological studies, operative records, and follow-up clinical records. An electronic database was created by inputting patients demographic information and presenting symptoms. Additionally, we also identified and recorded the presence and location of syringomyelia and scoliosis on magnetic resonance images or plain radiographs. All patients in this group were offered surgical decompression if we documented the following: 1) cerebellar tonsillar herniation 5 mm below the foramen magnum and either 2) hindbrain symptoms consistent with CM-I (tussive headache, cervical pain, central apnea, dysphagia, aspiration, vertigo, vocal cord paralysis, motor/sensory deficits, nystagmus, ataxia, uncoordination, and syringomyelia) or 3) syringomyelia manifesting with a scoliosis curvature or Cobb angle 10 on standing radiographs. Patients with minimal ectopia ( 5 mm below the foramen magnum but rostral to C-1) underwent suboccipital decompression only if they experienced tussive, reproducible headache in the presence of a syrinx and scoliosis. All patients underwent suboccipital decompression of the foramen magnum and C-1 laminectomy. The majority of patients also underwent duraplasty. Duraplasty was not performed in patients with minimal tonsillar ectopia and evidence of physiological hindbrain cerebrospinal fluid flow and tonsillar pulsations on intraoperative ultrasonography after decompression. Coagulation of the tonsil was only performed when tonsillar herniation was observed intraoperatively to extend below C-2. Patients who underwent spinal fusion prior to or during the CM-I decompression were excluded from this analysis. As a result, no patients in our study had spinal fusion either before or at the same time as CM-I decompression. Hence, this series represents patients presenting with Chiari malformation associated syringomyelia whose treatment consisted solely of hindbrain decompression and observation. The location of the deformity was defined as the following: with the apex at T2 10 for thoracic scoliosis, at T10 L1 for thoracolumbar scoliosis, and at L1 4 for lumbar scoliosis. Improvement or worsening in spinal curvature was determined by assessing postoperative radiographs of standing plain radiographs, with a change in the Cobb angle of 10 regarded as a significant change in spinal curvature. Improvement or worsening in syringomyelia was also evaluated on postoperative MR images, with 20% change in syrinx size regarded as significant. This CM-I database was retrospectively analyzed to assess the independent association of presenting symptoms, physical examination findings, radiological variables, and operative details with the postoperative progression of scoliosis; this was done using Kaplan Meier curves and logrank analysis for stratified covariates as well as Cox proportional hazards analysis for continuous covariates. Mean data are presented the standard deviation. Patient Population Results J. Neurosurg.: Pediatrics / Volume 1 / June 2008 Among 258 pediatric patients undergoing first-time posterior fossa decompression for CM-I, 33 patients (13%) presented with CM-I associated scoliosis during the study period. Two patients (6%) underwent fusion planned at the time of CM-I decompression, 2 (6%) underwent planned fusion after posterior fossa decompression, and 7 (21%) underwent follow-up at an outside institution, with 1 case (3%) removed due to the presence of CM-I and scoliosis without a syrinx. Patients in whom fusion was planned during or after posterior fossa decompression had severe ( 40 Cobb angle) and progressive scoliosis in the previous year. The 21 remaining patients continued to undergo follow-up at our institution and were included in the present study. Mean age at time of surgery was 9 3 years, and 4 patients (19%) were male. Presenting symptoms included hindbrain headache in 5 patients (24%; mean duration 12 months) and symptoms of syrinx or scoliosis alone (no headache) in 16 (76%; mean duration 20 months). Presenting symptoms are summarized in Table 1. Tonsillar herniation was 5 mm below the foramen magnum but rostral to C-1 in 1 patient (5%; mild ectopia), between C-1 and C-2 in 19 patients (90%; moderate ectopia), and below C-2 in 1 patient (5%; severe ectopia). Syringomyelia was present in all patients, involving the cervical spine in 19 (90%), the thoracic spine in 20 (95%), and the conus medullaris in 4 (19%) patients. When a syrinx was present, it spanned a mean 9 4 spinal levels. One patient (5%) had cervical scoliosis, 10 (48%) had thoracic scoliosis, 7 (33%) had thoracolumbar scoliosis, and 3 (14%) had lumbar scoliosis. The mean Cobb angle of the scoliotic curves was Only 1 patient did not undergo duraplasty, and in this case scoliosis progression was observed by 9 months postoperatively and there was lack of syrinx improvement. Imaging Follow-Up All patients underwent preoperative radiography at an average of 2 1 months before surgery. Patients routinely underwent standing radiography 3 months after surgery, with repeated radiography every 6 months unless symptom change prompted earlier imaging. Fourteen patients (67%) underwent their first postoperative radiographic studies within 4 months of surgery, with the remaining patients undergoing their radiological studies between 4 and 6 months after surgery. Twelve patients (57%) underwent a second postoperative radiographic examination within 1 year of sur- TABLE 1 Summary of presenting symptoms and signs in 21 consecutive pediatric patients with scoliosis and syringomyelia undergoing surgical decompression for CM-I* Variable No. of Patients (%) male sex 4 (19) headache 5 (24) cranial nerve or scoliosis symptoms alone 16 (76) sensory deficiency 3 (14) motor deficiency 3 (14) scoliosis cervical 1 (5) thoracic 10 (48) lumbar 3 (14) curve crosses CTJ 0 (0) curve crosses TLJ 7 (33) syrinx cervical 19 (90) thoracic 20 (95) conus medullaris 4 (19) * CTJ = cervicothoracic junction; TLJ = thoracolumbar junction. 457
3 F. J. Attenello et al. TABLE 2 Summary of pre- and postoperative characteristics Case Scoliosis No. Age at Surgery (yrs) Preop Cobb Angle ( ) Curvature Outcome improvement improvement improvement improvement improvement improvement improvement improvement no change no change no change progression progression progression progression progression progression progression progression progression progression FIG. 1. Kaplan Meier plots of time of onset of curve improvement (upper) and time of onset of curve worsening (lower), indicated by Cobb angle on standing radiographs, as a function of time after hindbrain decompression in children with CM-I. Eight patients (38%) experienced improvement in their scoliosis curvature, and 10 (48%) experienced scoliosis progression postoperatively. Of those patients with improvement, 50% exhibited improvement by 6 months, 88% by 2 years, and all patients by 3 years. Of those patients in whom the deformity worsened, 60% exhibited worsening at 1 year, 80% by 2 years, and all patients by 4 years. gery, and in the remaining patients the studies were performed between 12 and 18 months postoperatively. In 6 patients (29%) standing radiography was conducted 2 years after surgery. The mean follow-up duration was months (range months). Only 1 patient underwent follow-up for 6 months (4 months). All other patients were followed up to 2 years. Fifteen patients (71%) were followed for 2 years. Nine patients (43%) were followed for at least 3 years. Outcome and Predictors of Treatment Failure In 8 patients (38%) the scoliotic curvature improved after surgery, whereas in 10 (48%) the deformity progressed postoperatively (Fig. 1, Table 2). In 3 patients (14%) there was no change in scoliotic curvature at last follow-up examination. Three (30%) of 10 patients with deformity progression did eventually require spinal fusion during the study period. Fourteen patients (67%) exhibited improved syringomyelia at an average of 8 months. Failure of the syrinx to decrease in size was associated with a 4-fold likelihood of scoliosis progression (HR 3.80 [95% CI ], p = 0.05) (Fig. 2, Table 3). Syrinx improvement preceded curvature improvement by an average of 7 months. Scoliosis with apex at the thoracolumbar junction was associated with a 5-fold increase in the likelihood of curve progression (HR 4.75 [95% CI ], p = 0.04) (Fig. 2, Table 3). In addition, each increasing degree of Cobb angle was associated with an 11% increase in the likelihood of curve progression (p 0.05). Duraplasty was not performed in 1 patient and was not assessed as a predictor of outcome based on sample size. Discussion In our experience of hindbrain decompression as the initial treatment for CM-I associated scoliosis, we observed that scoliosis improved radiographically in more than one third of patients after hindbrain decompression alone. Patients presenting with an increasing Cobb angle or scoliosis crossing the thoracolumbar junction were at significantly greater risk of curve progression. Failure of the syrinx to improve was also associated with curve progression. The relative risk of scoliosis progression was greatest between 6 and 12 months after surgery with 29% of the deformities progressing by 12 months. After the 1st year, the estimated annual risk of progression was decreased, with 10% of the cases developing curve progression over each of the next 2 years, reaching 49% by 36 months. Improvement in scoliosis was noted in one third of patients. The curvature improved within the first 36 months of hindbrain decompression in all patients. Curvature improvement occurred at a similar incidence within the 1st and 2nd year postoperatively. Reports on progression of scoliosis after hindbrain decompression for CM-I remain limited. Farley et al. 7 reported on 9 patients who underwent decompression, 8 of whom 458 J. Neurosurg.: Pediatrics / Volume 1 / June 2008
4 Suboccipital decompression for CM-I associated scoliosis FIG. 2. Kaplan Meier plots showing the incidence of curve progression onset as a function of time after hindbrain decompression for CM-I in children. Lack of syrinx improvement (p = 0.05) (upper) and presence of scoliosis at the thoracolumbar junction (p = 0.04) (lower) were associated with an increased risk of scoliosis curvature progression. T-L Jxn = thoracolumbar junction. were candidates for fusion by the end of the follow-up period. The study had a small sample size with a high mean preoperative thoracic deformity (46 18 ). In their study involving hindbrain decompression, Hida et al. 9 reported improvement of the curvature in 38%, stabilization in 38%, and progression in 23%. Brockmeyer et al. 3 found that patients who were male, under the age of 10 years, and with preoperative curves 40 were more likely to improve after decompressive surgery. Eule et al. 6 described a study in which the vast majority of patients 8 years of age undergoing decompression alone experienced improvement or stabilization of their curves. Bhangoo and Sgouros 1 reported that age 10 and preoperative curve 30 were associated with decreased need for additional scoliosis surgery. The mean age and the mean Cobb angle of patients not requiring further surgery were 10 years and 29, respectively, compared with 13 years and 76 in those in whom additional surgery was required for deformity progression. Ghanem and associates 8 found that preoperative curves 40 were indicative of a worse outcome, but they found no correlation with age. Although the authors of the aforementioned studies described age and greater preoperative Cobb angles as predictors of subsequent curve progression, there is not a strong consensus as to the multiple variables that can identify high-risk patients outside of age and initial curve angle. We found that an increased degree of scoliosis preoperatively was a predictor of scoliosis progression after hindbrain decompression. Our observations are similar to those previously reported that suggest that either a Cobb angle 30 1,3 or 40 8 is a predictor of curvature progression. Furthermore, we found that the spinal level involved in scoliosis was also indicative of postsurgical outcomes. Based on Kaplan Meier estimates, 60% of patients with thoracolumbar scoliosis had curve progression within the first 12 months, and this rose to 80% by 24 months. We also found a significant correlation between failure of the syrinx to resolve and progressive scoliosis curvature postoperatively. Of 7 patients with a decrease in syrinx size and scoliotic curve, 57% exhibited a decrease in syrinx size prior to scoliotic change and 43% exhibited this syrinx decrease concurrently with improvement in scoliosis. It is not surprising that the decrease in syrinx size correlates with scoliosis improvement, as the syrinx is likely to be the cause of the scoliotic curve, and previous studies have commonly noted the occurrence of scoliosis in up to 60% of patients with syrinx. 1,3,6 9,12 In our scoliosis cohort there was a predominance of females, constituting 80% of our series. This was a natural variant of our population, as we did not include or exclude patients on the basis of sex. In addition, our series demonstrates that, among patients undergoing primary decompression for CM-I, 13% present with concurrent scoliosis. Re- J. Neurosurg.: Pediatrics / Volume 1 / June
5 F. J. Attenello et al. TABLE 3 Univariate association of clinical, radiographic, and surgical variables with postoperative worsening of scoliosis curvature following decompression for CM-I* Variable HR (95% CI) p Value female sex 1.22 ( ) age 1.12 ( ) nausea/vomiting 3.16 ( ) incontinence 0.61 ( ) sensory deficiency 1.60 ( ) motor deficiency 3.07 ( ) tonsillar coagulation 0.89 ( ) no. of syrinx levels 1.02 ( ) ectopia below C ( ) no. of scoliosis levels 1.12 ( ) curve across TLJ 4.75 ( ) Cobb angle 1.11 ( ) lack of syrinx improvement 3.80 ( ) * Scoliosis crossing the thoracolumbar junction and failure of syrinx to decrease 20% at follow-up were associated with a 5- and 4-fold increase in the likelihood of curve progression. Each increasing degree of Cobb angle curvature was associated with an 11% increase in the likelihood of curve progression. Variables associated with 0 or 1 case are not cited in the table. ported rates of scoliosis vary in the literature. In a series of 130 patients, Tubbs et al. 13 demonstrated that 18% of those with CM-I presented with concurrent scoliosis. It is not clear why our series shows a lower percentage of patients with scoliosis, although it may be due to regional differences or our referral pattern. These differences may warrant further investigation. Several limitations of this study should be recognized. It is retrospect in design and with nonstandardized follow-up intervals. It also is composed of a small sample size (21 patients). Hence, the study is underpowered to draw definitive negative conclusions. However, despite this small sample size, the statistical significance noted for increasing Cobb angle, scoliosis crossing the thoracolumbar junction, and lack of syrinx resolution highlights the strong correlation of these variables with outcome. Conclusions Over one third of patients with Chiari malformation associated scoliosis will improve after cervicomedullary decompression alone. Cervicomedullary decompression is thus a good first-line option particularly in children with concordant posterior fossa symptoms. Patients presenting with more severe scoliosis (increasing Cobb angle), lack of syrinx improvement during follow-up, or scoliosis crossing the thoracolumbar junction may benefit from earlier orthopedic involvement and should be monitored regularly for curve progression after cervicomedullary decompression. Disclosure This study was supported by a grant from the Congress of Neurological Surgeons and the Syringomyelia Alliance Project. References 1. Bhangoo R, Sgouros S: Scoliosis in children with Chiari I-related syringomyelia. Childs Nerv Syst 22: , Bindal AK, Dunsker SB, Tew JM Jr: Chiari I malformation: classification and management. Neurosurgery 37: , Brockmeyer D, Gollogly S, Smith JT: Scoliosis associated with Chiari 1 malformations: the effect of suboccipital decompression on scoliosis curve progression: a preliminary study. Spine 28: , Chiari H: Über Veranderungen des Kleinhirns infolge von Hydrocephalie des Grosshirns. Dtsch Med Wochenshr 17: , Elster AD, Chen MY: Chiari I malformations: clinical and radiologic reappraisal. Radiology 183: , Eule JM, Erickson MA, O Brien MF, Handler M: Chiari I malformation associated with syringomyelia and scoliosis: a twentyyear review of surgical and nonsurgical treatment in a pediatric population. Spine 27: , Farley FA, Puryear A, Hall JM, Muraszko K: Curve progression in scoliosis associated with Chiari I malformation following suboccipital decompression. J Spinal Disord Tech 15: , Ghanem IB, Londono C, Delalande O, Dubousset JF: Chiari I malformation associated with syringomyelia and scoliosis. Spine 22: , Hida K, Iwasaki Y, Koyanagi I, Abe H: Pediatric syringomyelia with chiari malformation: its clinical characteristics and surgical outcomes. Surg Neurol 51: , Meadows J, Kraut M, Guarnieri M, Haroun RI, Carson BS: Asymptomatic Chiari Type I malformations identified on magnetic resonance imaging. J Neurosurg 92: , Milhorat TH, Chou MW, Trinidad EM, Kula RW, Mandell M, Wolpert C, et al: Chiari I malformation redefined: clinical and radiographic findings for 364 symptomatic patients. Neurosurgery 44: , Sengupta DK, Dorgan J, Findlay GF: Can hindbrain decompression for syringomyelia lead to regression of scoliosis? Eur Spine J 9: , Tubbs RS, McGirt MJ, Oakes WJ: Surgical experience in 130 pediatric patients with Chiari I malformations. J Neurosurg 99: , Weinberg JS, Freed DL, Sadock J, Handler M, Wisoff JH, Epstein FJ: Headache and Chiari I malformation in the pediatric population. Pediatr Neurosurg 29:14 18, 1998 Manuscript submitted August 14, Accepted February 29, Address correspondence to: Matthew J. McGirt, M.D., 3553 Newland Road, Baltimore, Maryland mmcgirt1@jhmi.edu. 460 J. Neurosurg.: Pediatrics / Volume 1 / June 2008
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