Syringohydromyelia in Patients with Chiari I Malformation: A Retrospective Analysis

Prevalence of Syringohydromyelia

Identifying syrinx formation in patients with symptomatic CMI is critical in working up their management plan. In our descriptive study of 108 symptomatic patients who were clinically diagnosed with CMI, syringohydromyelia was present in 39 (36.1%) patients. We believe that our prevalence is not affected by any selection bias that may falsely overestimate or underestimate the true figures because our patients were identified by MR imaging as well as clinical criteria in a specific 2014–2016 timeframe, including all referred individuals based on MR imaging findings and clinical assessment. They were not selected from neurosurgical archives or data bases in a trial, to avoid commonly encountered overestimation of syringohydromyelia in studies in which patients were surgical candidates. Our sample also included those patients who were incidentally diagnosed while undergoing MR brain imaging for any other reason and then referred for clinical consultation and diagnosed as having CMI based on confirming clinical signs and symptoms. Patients with secondary CMI such as those with an intracranial space-occupying lesion were also excluded.

Several studies have been attempted, with different criteria, to explore the imaging prevalence of syringohydromyelia among patients with CMI. In a study by Strahle et al,³ most patients underwent MR imaging of the cervical spine and almost half of them underwent full spine imaging, resulting in 22.9% of patients with CMI having a syrinx detected. Aitken et al¹¹ identified spinal syringes in 12% of children with CMI in their study; the authors relied on reviewing only radiology reports in many patients without having access to their images.

Craniocervical Bony Anomalies

In our study, the presence of craniocervical bony anomalies was statistically associated with syringohydromyelia. A retroverted odontoid with an angle of <70° was found to be the most common developmental osseous anomaly (n = 23) of the craniocervical junction among our series, while basilar invagination was present in only 6 cases. With logistic regression, craniocervical junction osseous anomalies and a skull base angle of >135° were most predictive of syrinx formation. Since 1896, when Arnold Chiari highlighted insufficient bone growth and insufficient enlargement of portions of the skull during development as additional mechanisms that cause increased intracranial pressure and subsequent tonsillar herniation, it has been accepted that developmental morphometric anomalies of the posterior fossa are linked to CMI.

In the classic study on 364 patients with CMI by Milhorat et al,¹ in which syringohydromyelia was found in 65% of patients, the authors highlighted commonly associated problems, including scoliosis (42%), a retroflexed odontoid process (26%), basilar invagination (12%), and varying degrees of bony dysplasia of the posterior cranial fossa based on volumetric calculations. Vega et al¹² studied 42 patients with CMI compared with 46 controls and found that patients with CMI had shorter clivus lengths and a shorter Chamberlain line. The concept of complex Chiari malformation is being widely accepted in the neurosurgery literature. A complex severe craniocervical anomaly would add more burden to the disease.¹³ We believe that a complex Chiari malformation might represent a separate entity of the disease that requires a different surgical approach. Brockmeyer¹⁴ defined the complex Chiari malformation as “cerebellar tonsil herniation combined with one or more of the following radiographic findings: brain stem herniation through the foramen magnum (Chiari 1.5 malformation), medullary kink, retroflexed odontoid, abnormal clival-cervical angle, occipitalization of the atlas, basilar invagination, syringohydromyelia or scoliosis.” The authors differentiated patients with complex Chiari malformation from those with typical CMI as being more likely to require advanced surgical interventions other than standard suboccipital decompression.

In another study by Moore and Moore,¹⁵ odontoid retroflexion, craniovertebral junction osseous anomalies, and syringohydromyelia were more often observed in patients with complex Chiari malformation than in those with typical CMI. These observations are in parallel with our findings. Our odds ratios were 4.8 and 4.3 for craniocervical anomalies and a skull base angle of >135°, respectively, in the prediction of syringohydromyelia. These findings might give importance to the variant of complex Chiari malformation as a special research entity and should be a point of emphasis in the radiology report when these findings are present. The position of the obex was described in the same study by Moore and Moore¹⁵ as a characteristic imaging feature that was present in all complex cases. However, we did not evaluate the obex level in our study due to interobserver variability.

CSF flow studies indicated that the tonsils in CMI partially obstruct the free movement of CSF across the foramen magnum. Normally, the cardiac systole delivers blood to the brain; most of the new volume is absorbed by the venous system of the brain, however, during systole; and about 0.75–1.0 mL of CSF gets rapidly moved from the cisterna magna across the subarachnoid space and into the spinal subarachnoid space at the level of the foramen magnum. This extra amount of spinal CSF should move back to the cranial space during diastole. Blocking this backward rapid movement of CSF partially entraps the spinal intrathecal space, resulting in reduced compliance in the spinal CSF space. The tonsillar movement is against a partially entrapped CSF space with reduced compliance and increased intrathecal pressure. It is the complex interplay between clivus inclination and odontoid angulation that can create a point of mechanical stress and tension leading to anterior brain stem compression.

The presence of associated skull base anomalies makes CMI defined by neurosurgeons a “complex” Chiari malformation, which requires more advanced surgical decompressive approaches. According to Bollo et al,¹³ the presence of basilar invagination puts the patient at risk of craniocervical fusion. In our study, we evaluated the presence of craniocervical kyphosis by identifying platybasia and odontoid retroversion and by measuring the skull base angle (intersecting lines from the nasion to the sella and from the sella to the anterior margin of the foramen magnum). A normal angle lies between 125° and 143°. Although an angle of >143° is required to quantitatively diagnose platybasia, we found that higher angles are more commonly associated with syrinx formation using logistic regression among our cases of CMI. Our findings are in full support of the suggested pathophysiology of CMI, in which an obtuse angle results in an upward tilt of the clivus with a relatively higher location of the opisthion. This aberrant osseous configuration is associated with 2 abnormal morphometric changes: 1) narrowing or ventral compromise to the foramen magnum with corresponding downstream CSF flow resulting in syrinx formation, and 2) a smaller posterior fossa volumetric capacity with corresponding cerebellar herniation and crowding of structures at the already compromised foramen magnum, leading to more blockage.

A cutoff point of 135° was statistically significant, showing a relatively high specificity of 82.6% in predicting an associated syringohydromyelia. Although its sensitivity was not high (50%), there were only 12/69 (17.4%) patients without syrinx who showed a skull base angle above 135°. Sgouros et al¹⁶ noted that skull base angles were larger in 30 patients with CMI compared with controls. The authors used a modified angle with the dorsum sella as a reference midpoint for intersecting lines. Their angle was slightly higher than ours where lines intersect more inferiorly in the pituitary center; however, in their results, the presence of syringohydromyelia was also associated with a larger angle (151°) compared with CMI without syringohydromyelia (145°). We believe that measuring the skull base angle in CMI can help identify those patients at risk of developing syrinx (OR = 4.8, P = .0006).

Impaired CSF Flow by Tonsillar Herniation

Disturbed CSF flow dynamics remain a standard phenomenon by which patients with CMI can develop syringohydromyelia. Bunck et al¹⁷ revealed pronounced alteration of CSF flow dynamics with 4D phase-contrast quantitative MR imaging in 12 patients with CMI with syringohydromyelia compared with 8 without it. In our study, we could not establish a statistically significant association between impaired CSF flow in cine phase-contrast MR imaging and syrinx formation. The association between the degree of mechanical blockage and the formation of syrinx has been debatable in the literature. Our finding of the lack of association may shed light on a noncompressive etiology of syringohydromyelia.

Schuster et al¹⁸ presented a systematic review of residual syringohydromyelia after decompressive surgery, in which the rate of postoperative persistent syrinx ranged between 0% and 22%, raising the possibility of a noncompressive etiology in the development of syrinx. We believe that CSF flow dynamics at the foramen magnum is a complicated process that would have been more accurately evaluated if quantitative indicators were considered. Due to this technical limitation of our study besides the relatively small number of cases with available technically acceptable phase-contrast MR images (69/108), a clear interpretation of these findings was not possible.

Clarke et al¹⁹ presented a computational model in CMI, in which the presence and absence of syringohydromyelia were compared. This study introduced an advanced understanding of the pressure gradient and peak pressure timing differences between CMI with or without syringohydromyelia. The authors found that the dynamic profile of subarachnoid spinal pressure relative to the cardiac cycle (in which intraspinal arteriolar pressure varies) is more critical in regard to the chance of fluid accumulation and the development of a presyrinx or syrinx state.¹⁹

The association between the degree of mechanical blockage and the formation of syrinx has been debatable in the literature. Although the degree of tonsillar herniation in our results gives an insight into the mechanical perspective of CSF flow compromise at the foramen magnum, it is still insufficient to predict syringohydromyelia on the basis of how far cerebellar tonsils have descended, possibly because of the complex mechanical-versus-nonmechanical algorithms determining the pathogenesis of the condition.

Study Limitations

Our study had a few technical limitations related to the partial inhomogeneity of the data (such as fewer CSF flow studies) as well as the cross-sectional design with a lack of longitudinal follow-up. The development of syringohydromyelia in CMI is a dynamic process. Further longitudinal studies are needed to follow up patients with CMI, trying to identify different trends in relation to syrinx formation in those patients and how these trends could be affected by the degree of mechanical blockage and the age of the patient. Quantitative assessment of CSF flow would also represent a valid parameter compared with the qualitative method we used. Assessment of the obex level by quantitative measurement of its position relative to the foramen magnum would have been an important variable that we recommend in future studies because it might be linked to the diagnosis of complex Chiari malformation besides other craniocervical anomalies.