Skull base growth in children with Chiari malformation Type I
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1 See the corresponding editorial in this issue, pp 187. J Neurosurg (3 Suppl Pediatrics) 107: , 2007 Skull base growth in children with Chiari malformation Type I SPYROS SGOUROS, M.D., F.R.C.S.(SN), 1,2 MELPOMENI KOUNTOURI, B.SC., M.B.CH.B., 2 AND KAL NATARAJAN, PH.D. 2 1 Department of Neurosurgery and 2 Neuroscience Informatics Laboratory of the Institute of Child Health, Birmingham Children s Hospital, Birmingham, United Kingdom Object. The goal of this study was to establish whether children with Chiari malformation Type I (CM-I) have abnormal skull base geometry. Methods. Distances and angles between skull base landmarks were measured on preoperative magnetic resonance images obtained in 30 children (age range months) with symptomatic isolated CM-I; 16 of them (53%) had syringomyelia. Comparisons were made with 42 children of similar age who comprised the control group by using oneway analysis of variance. Results. The angle formed by the crista galli (CG), dorsum sellae (DS), and foramen magnum (FM) was larger than normal in individuals with CM-I than in those without (145 in patients with CM-I but no syringomyelia and 151 in those with CM-I and syringomyelia compared with 135 in controls; p = 0.000). The angle formed by the left internal auditory meatus (IAM), FM, and right IAM was also larger than normal in the patients (122 in patients with CM-I but no syringomyelia and 123 in those with CM-I and syringomyelia compared with 110 in controls; p = 0.001). The angle formed by the anterior clinoid process (ACP), CG, and right ACP was smaller than normal (29 in all patients with CM-I compared with 34 in controls; p = 0.000). The distance between the two IAMs was longer than normal (75 mm in patients with CM-I but no syringomyelia and 63 mm in those with CM-I and syringomyelia compared with 58 mm in controls; p = 0.000). The distance between the two ACPs was shorter than normal in the syringomyelia group (31 mm in patients with CM-I but no syringomyelia and 27 mm in those with CM-I and syrinx compared with 32 mm in controls; p = 0.001). Within the group of patients with CM-I, the DS FM and left ACP right ACP distances were smaller in the syringomyelia group (p = and p = 0.037, respectively). Conclusions. Children with CM-I have abnormal geometrical measurements of their entire skull base, not only the posterior fossa, irrespective of presence of syringomyelia. This may indicate a mesodermal defect as a possible cause of the malformation. (DOI: /PED-07/09/188) KEY WORDS Chiari malformation hindbrain hernia pediatric neurosurgery skull base syringomyelia A LTHOUGH the cause of hindbrain herniation in the context of CM-I has not been identified, there have been several suggestions for the possible mechanisms that can lead to the formation of hindbrain herniation, a term used to describe the prolapse of the cerebellar tonsils beyond the FM. It is widely believed that the small size of the posterior fossa is implicated or contributes to the formation of this condition, 1,3 6,10,13 following the concept of brain packing. Findings in a recent study conducted by our group showed that at least in children, this may be the case Abbreviations used in this paper: ACP = anterior choroidal process; ANOVA = analysis of variance; CG = crista galli; CM-I = Chiari malformation Type I; DS = dorsum sellae; FM = foramen magnum; IAM = internal auditory meatus; MR = magnetic resonance. only in those with CM-I and syringomyelia and may not be applicable to those without syringomyelia. 8 Malformation of the skull base often is seen on the MR images of children with CM-I, and indeed, such malformations are well known to be present in certain types of craniovertebral junction deformities. 4,15 Nevertheless, there is no detailed analysis of the development of the skull base geometry in children with CM-I. This study is in effect a continuation of our previous study on posterior fossa volume. Our aim is to identify whether there are measurable deformities of the skull base as well as to identify their potential role in the presence of syringomyelia. The possible presence of abnormal geometry of the skull base, even in patients with a normal posterior fossa volume, would imply the presence of a wider skull base abnormality. 188 J. Neurosurg: Pediatrics / Volume 107 / September, 2007
2 Skull base growth and CM-I Clinical Material and Methods Outline of the Study Using a segmentation technique already described, anatomical osseous landmarks of the skull base were identified on axial MR images, and distances and angles between them were calculated.9 The mean values were calculated for patient groups. The influence of syringomyelia was analyzed, and comparisons were made with control patients.9 Patient Population A total of 30 patients with isolated symptomatic CM-I were included in this study; 17 (57%) were boys. The study group included 14 children who presented with CM-I only (without syringomyelia), and 16 children with CM-I and syringomyelia (53% of all patients). All patients were treated with craniovertebral decompression at the Birmingham Children s Hospital, England, between 1998 and 2004 and are still undergoing clinical follow-up. A CM-I was considered the prolapse of the cerebellar tonsils at least 5 mm beyond the FM on midsagittal MR images. Patients with Chiari malformation Type 0 were not included in this analysis. Patients with any abnormality that could potentially interfere with skull base growth and hence possibly introduce a bias factor, such as a craniosynostosis-related hindbrain hernia (for example, Crouzon syndrome), or any other abnormalities or syndromes, or patients who received a ventricular shunt prior to craniovertebral decompression were excluded. The presence of a ventricular shunt at the time of presentation prior to imaging and surgical treatment potentially can influence skull growth in young children and for this reason it was considered an exclusion factor. All patients included in this study were included in the previous comparative study of posterior fossa volume.8 The control group included 42 children, 23 of whom were male (55%). Children in this group were included in the previous comparative study of posterior fossa volume.8 These children had presented to general pediatricians and pediatric neurologists between January 1995 and December 1997 with nonspecific symptoms such as headache (18 patients), dizziness (15 patients), migraine (two patients), strabismus (five patients), and a family history of cerebral hemorrhage (two patients). In all cases the MR imaging findings were entirely normal. No children with any medical or neurological disorder were included, regardless of how irrelevant to skull base growth the disorder might have been. All children in this group remained well 12 months after this study. For all patients the age at presentation used for statistical analysis was the age at the time the preoperative MR image was obtained. The mean age at presentation for all patients with CM-I was 128 months (range months). The age at presentation of the control volunteers ranged from 34 to 184 months (mean age 118 months, standard deviation 46.5 months, standard error of the mean 7.1 months). The ages of patients in the CM-I group were statistically not different from those the control group (p = 0.186, one-way ANOVA), thus making comparisons between the groups valid. There was no statistical difference in the mean age at presentation between the two subgroups of patients with CM-I; nevertheless, it is of note that patients with syringomyelia presentj. Neurosurg: Pediatrics / Volume 107 / September, 2007 ed at a younger age: CM-I alone, 144 months; CM-I and syringomyelia, 114 months (p = 0.119, one-way ANOVA). Computer-Aided Skull Base Analysis For this study, axial T2-weighted MR imaging examinations (5-mm slice thickness and a 1.5-mm interval) were used. The T2-weighted sequences were chosen as they show with better clarity and contrast the gray bone structures against the surrounding white cerebrospinal fluid signal. The technique of computer-aided analysis of the skull base has been previously described in detail.9 Briefly, certain landmarks of the skull base were identified in the neuroradiological examination of every patient, pertinent to the anterior and posterior fossae (Fig. 1). They included five true anatomical points (CG, left ACP, right ACP, left IAM, and right IAM) and two derived (virtual) midline points: the DS, which is the midpoint between the two posterior clinoid processes, and the FM, which is the midpoint between the two hypoglossal foramina. These points were used for calculations of geometric parameters and visualization of the anatomical arrangement of the skull base. The technique does not rely on the bilateral points (for example, both IAMs) being in the same axial MR imaging slice, as it is a 3D computer-aided analysis that is used to calculate angles and distances on the entire cube of MR imaging data. In practice, however, as most patients heads are aligned on the skull FIG. 1. Diagram showing the anatomical landmarks used for the computer-aided analysis of the skull base and the resulting angles (thin red lines) and distances (thick red lines) that were calculated. 189
3 S. Sgouros, M. Kountouri, and K. Natarajan base prior to obtaining the image, bilateral landmarks appear in the same axial slice on most MR images. The following angles were calculated: 1) CG-DS-FM, expressing the angle between the anterior fossa floor and the clivus; 2) left IAM FM right IAM, expressing the depth of the posterior fossa; 3) left IAM DS right IAM, expressing the width of the posterior fossa; and 4) left ACP CG right ACP, expressing the length of the anterior fossa. The following distances were calculated: 1) left IAM right IAM, expressing the width of the posterior fossa; 2) DS FM, expressing the depth of the posterior fossa; and 3) left ACP right ACP, expressing the width of the anterior fossa. Figure 2 shows these points identified on the MR image of a 14-year-old girl with hindbrain hernia due to CM-I. The posterior fossa is a true 3D structure, and attempts to analyze it with a series of geometric parameters is difficult, as the change in each one of them is reflected on all the others. This should be kept in mind during the interpretation of the results. Statistical Analysis A statistical analysis of the mean values for each measured parameter for each group was performed using oneway ANOVA with the aid of commercially available statistical software (SPSS Inc.). A probability value of less than 0.05 was considered to be statistically significant. Results Table 1 shows the mean values of the various parameters measured for the three groups of patients. Three of the four angles and two of the three distances showed statistically FIG. 2. Magnetic resonance images. A: Sagittal T1-weighted MR image obtained in a 14-year-old girl, showing significant hindbrain hernia. The tips of the cerebellar tonsils extend down to the inferior border of the arch of C-1. B D: Axial T2-weighted MR images identifying the anatomical landmarks shown in Fig. 1, indicated with red squares. 190 J. Neurosurg: Pediatrics / Volume 107 / September, 2007
4 Skull base growth and CM-I TABLE 1 Summary of mean values for the measured parameters* Parameter Group Control CM-I, CM-I & (42 No Syringo Syringo p p patients) (14 patients) (16 patients) Value Value angle ( ) CG-DS-FM lt IAM FM rt IAM lt IAM DS rt IAM lt ACP CG rt ACP distance (mm) lt IAM rt IAM DS-FM lt ACP rt ACP * Syringo = syringomyelia. Comparison of all three groups using ANOVA. Comparison of the two CM-I groups using ANOVA. significant differences between the CM-I groups and control group. The mean CG-DS-FM angle was similar in the two CM-I subgroups, but was larger than normal, indicating a greater slope of the clivus in relation to the floor of the anterior fossa in children with CM-I. The mean left IAM FM right IAM angle was similar in the two CM-I subgroups, but was also larger than normal, indicating a shallower posterior fossa in children with CM-I. The mean left ACP CG right ACP angle was the same for the two CM-I subgroups, but smaller than normal, indicating a longer anterior fossa in children with CM-I. The mean distance between the two IAMs was longer than normal, indicating a wider posterior fossa in children with CM-I. The mean distance between the two ACPs was similar between volunteers and children with CM-I only, but were smaller in children with CM-I and syringomyelia, indicating a narrower anterior fossa in the latter group. Comparing the two CM-I subgroups the differences in DS-FM and left ACP right ACP distances were statistically significant. It was difficult to assess the significance of the difference in the DS-FM distance as the values for the two CM-I subgroups were on either side of the normal value. There was a tendency for significance in the mean CG-DS-FM angle and the distance between the two IAMs. Discussion In a previously published study 8 we found that children with CM-I only have a normal posterior fossa volume, whereas children with CM-I and syringomyelia have a smaller than normal posterior fossa volume. This finding differed from many other studies, 4 6,10 in which the authors had concluded that all patients with CM-I have a small posterior fossa, and as it was explained, this transpired from studies with a large percentage of patients with syringomyelia, in which the authors did not analyze the two subgroups separately. The results of our posterior fossa volume study demonstrated that there was an obvious phenotypic difference between patients with syringomyelia and those without, although it was not obvious whether it was a matter of different degree of the same pathophysiological mechanism operating or whether there were two separate disease entities. J. Neurosurg: Pediatrics / Volume 107 / September, 2007 In this study we have attempted to further explore the differences between the two subgroups of CM-I by measuring anatomical parameters of the bone architecture of the skull base. We have demonstrated that children with CM-I overall have a wider and steeper posterior fossa, different clival angle, and longer anterior fossa in comparison with children without CM-I. Similarly, other geometric studies in the past showed abnormal measurements of the various parts of the posterior fossa. 2,6,10,11,14 Most of these studies were based on 2D lateral skull radiographs, and the authors did not take into account the 3D nature of the skull base and they did not investigate the anterior fossa. Nevertheless, it has been shown that in adult patients with CM-I the posterior fossa is shallower and shorter, 6,10,13 there is clival shortening, 7,14 and there are various degrees of occipital hypoplasia. 5,13 Our study is a computer-aided 3D analysis of the skull base, which depicts with a higher degree of reliability these geometric differences between children with and without CM-I. We have focused on children and analyzed the effect of syringomyelia. In addition to the posterior fossa, our analysis helped us investigate in some detail the geometry of the anterior fossa in patients with CM-I. The presence of a possible association between anterior fossa geometric abnormalities and hindbrain herniation has been pointed out already in a study in which the authors found a high incidence of CM-I among a group of children with simple metopic ridge, without synostosis, in whom the anterior fossa geometric measurements were abnormal (smaller than normal). 12 It was postulated that abnormal geometry may correlate with a smaller volume of anterior fossa and that it may have a correlation with caudal migration of intracranial contents and resultant hindbrain herniation. From our results it is difficult to support or refute this suggestion. In broad agreement with previously published studies, findings in our study indicate that in patients with CM-I there is deficient growth of the posterior skull base. They also show that the anterior skull base is affected as well, a feature not previously appreciated widely. It is difficult to assess whether the changes in the anterior fossa are secondary to the changes in the posterior fossa, or part of the primary defect. Certainly our findings indicate mesodermal deformity of at least the occipital bone, as previously demonstrated, but probably affecting primarily the entire skull base. Authors of other studies 10,14 have indicated that in CM-I there is presumed paraxial mesodermal insufficiency leading to underdevelopment of the basichondrocranium; this has also been supported by findings from animal models as well. 3 In this study we have demonstrated that there are anatomical geometric differences between children with syringomyelia and those without. Although some statistical differences were found in different parameters, it should be acknowledged that in practice all the measured parameters are interrelated and significant diversion of one of them from normal would almost certainly lead to diversion of most if not all of them. It has been shown that in patients with CM-I the development of the cerebral structures of the hindbrain is normal, 5 and it seems that the problem arises from the underdevelopment of the osseous enclosure which, in the concept of brain packing, is pushing the cerebellum to prolapse beyond the FM. This concept is not entirely satisfactory, as it cannot explain why children younger than 10 years of age with asymptomatic hindbrain herniation do not 191
5 S. Sgouros, M. Kountouri, and K. Natarajan exhibit imaging-documented deterioration of the hindbrain herniation as they grow (personal observations of the senior author [S.S.]). It will have to be assumed that the growth of the hypoplastic skull base is completed early, so there is no change, but this may not be true as the rest of the cranial skeleton is evolving, in particular the craniofacial skeleton that projects downward from the skull base. The one issue that remains unresolved is whether the presence of syringomyelia represents a completely different mesodermal deformity or more severe extent of affliction. In this study we identified differences between the two subgroups but we have not been able to explore this issue conclusively. Conclusions Children with CM-I have abnormal geometric measurements of the entire skull base not only the posterior fossa irrespective of the presence of syringomyelia. This may indicate a mesodermal defect affecting the growth of the entire skull base as a possible cause of the malformation. The cause for the observed differences according to the presence of syringomyelia is unclear. References 1. Badie B, Mendoza D, Batzdorf U: Posterior fossa volume and response to suboccipital decompression in patients with Chiari I malformation. J Neurosurgery 37: , Caetano De Barros M, Farias W, Ataíde L, Lins S: Basilar impression and Arnold-Chiari malformation. A study of 66 cases. J Neurol Neurosurg Psychiatry 31: , Marin-Padilla M, Marin-Padilla TM: Morphogenesis of experimentally induced Arnold Chiari malformation. J Neurol Sci 50:29 55, 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: , Nishikawa M, Sakamoto H, Hakuba A, Nakanishi N, Inoue Y: Pathogenesis of Chiari malformation: a morphometric study of the posterior cranial fossa. J Neurosurg 86:40 47, Nyland H, Krogness KG: Size of posterior fossa in Chiari type 1 malformation in adults. Acta Neurochir (Wien) 40: , Schady W, Metcalfe RA, Butler P: The incidence of craniocervical bony anomalies in the adult Chiari malformation. J Neurol Sci 82: , Sgouros S, Kountouri M, Natarajan K: Posterior fossa volume in children with Chiari malformation Type I. J Neurosurg 105 (2 Suppl): , Sgouros S, Natarajan K, Hockley AD, Goldin JH, Wake M: Skull base growth in childhood. Pediatr Neurosurg 31: , Stovner LJ, Bergan U, Nilsen G, Sjaastad O: Posterior cranial fossa dimensions in the Chiari I malformation: relation to pathogenesis and clinical presentation. Neuroradiology 35: , Thompson DNP, Harkness W, Jones BM, Hayward RD: Aetiology of herniation of the hindbrain in craniosynostosis. An investigation incorporating intracranial pressure monitoring and magnetic resonance imaging. Pediatr Neurosurg 26: , Tubbs RS, Elton S, Blount JP, Oakes WJ: Preliminary observations on the association between simple metopic ridging in children without trigonocephaly and the Chiari I malformation. Pediatr Neurosurg 35: , Tubbs RS, Wellons JC, Smyth MD, Bartolucci AA, Blount JP, Oakes WJ, et al: Children with growth hormone deficiency and Chiari I malformation: a morphometric analysis of the posterior cranial fossa. Pediatr Neurosurg 38: , Vega A, Quintana F, Berciano J: Basichondrocranium anomalies in adult Chiari type I malformation: a morphometric study. J Neurol Sci 99: , Williams B: Syringomyelia. Neurosurg Clin N Am 1: , 1990 Manuscript submitted March 21, Accepted June 1, Some of the material of this paper was presented at the 32nd Annual Meeting of the International Society of Pediatric Neurosurgery, September 1, 2004, Buenos Aires, Argentina. This work and the Neuroscience Informatics Laboratory of the Institute of Child Health at Birmingham Children s Hospital in general is supported by the Bernard Williams Syringomyelia Research Fund. Address reprint requests to: Spyros Sgouros, M.D., F.R.C.S.(SN), Department of Neurosurgery, Birmingham Children s Hospital, Steelhouse Lane, Birmingham, B4 6NH, United Kingdom. S.Sgouros@bham.ac.uk. 192 J. Neurosurg: Pediatrics / Volume 107 / September, 2007
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