Clinicoradiological study of adult Chiari malformation type 1 patients with emphasis on cerebrospinal fluid peak flow velocity at foramen magnum level
Correspondence Address: Source of Support: None, Conflict of Interest: None DOI: 10.4103/0028-3886.263214
Source of Support: None, Conflict of Interest: None
Keywords: Chiari 1 malformation, foramen magnum decompression, posterior fossa decompression, syringomyelia
Chiari malformation More Details generally describes an increasing degree of hindbrain herniation through the foramen magnum. Chiari type 1 malformation (CM1) is defined as herniation of cerebellar tonsils of at least 5 mm or more through the foramen magnum., Approximately one third of individuals with tonsillar herniation, revealed by magnetic resonance (MR) study, are asymptomatic. The degree of tonsillar herniation correlates poorly with the severity of signs and symptoms. Consequently, much research regarding the CM1 has been focused on CSF dynamics rather than the anatomic relationships of the tonsils and brainstem. The volume of fluid (in mL/min) moving through the foramen magnum during each cardiac cycle depends less on the shape and compliance of the foramen magnum and more on the changes in the cerebral blood volume with each cardiac cycle. The velocity of flow through the foramen magnum (in cm/s) depends, to a greater degree, on the dimensions and shape of the foramen magnum. Any process that restricts flow within the foramen magnum is more likely to increase the velocity of flow than to decrease the volume of flow. Hypothetically, tonsillar herniation, adhesions within the foramen magnum, or other processes that affect the capacity of the foramen magnum may increase the peak CSF velocity. The aim of this study was to investigate the clinicoradiological profile of CM1 patients, measure the peak CSF velocity at foramen magnum, and assess the changes after foramen magnum decompression.
Approval for this study was obtained from our institutional review board. The study was carried out between December 2014 and December 2016 in the Department of Neurosurgery. Only patients who met the criteria for CM1 (peg-shaped cerebellar tonsils herniating >5 mm below the foramen magnum), and were of age ≥18 years, were included in this study. The radiological study of a total of 32 patients of CM1 was done both preoperatively and postoperatively at 6 months by an magnetic resonance imaging (MRI) scan. The signs and symptoms in each patient were noted and compared to those present postoperatively. The mean follow-up period was 14 months.
MRI was performed using a 3 Tesla (MagnetomVerio, Siemens Healthcare, Erlangen, Germany) scanner. The imaging protocol included a T1-weighted (W) scan for the morphological assessment and two cine velocity encoded phase contrast scans, one with a high velocity encoding (70–80 cm/s) for imaging the arterial and venous blood flows to and from the cranium, and the second with a low velocity encoding (7–8 cm/s) for imaging the CSF flow at the foramen magnum region. The pixel size was 0.9 × 0.9 mm, with a slice thickness of 1 × 1.5 mm. The spatial resolution of the phase-contrast MR images was 0.694–0.977 mm. Other typical imaging parameters were flip angle 10°, matrix × 240 × 176, field of view 250 × 250, repetition time (TR) 21 msec, echo time (TE) 6.8 msec, and slice thickness of 5 mm. Flow analysis was conducted with commercially available software, installed on the image work station. Peak CSF velocity was measured preoperatively and after 6 months postoperatively to assess the changes in CSF flow.
A total of 30 patients underwent surgical decompression in the prone position. A standard suboccipital craniectomy was performed to ensure a wide decompression of the cerebellar hemispheres, brainstem, and midline structures. In all cases, a C-1 laminectomy was also performed to decompress the cervical spinal cord. The atlantooccipital ligament was divided and the underlying outer dural leaflet was incised and reflected radially while maintaining the integrity of the inner leaflet of the dura. Closure was then performed in a standard multilayered fashion, similar to that used in intradural procedures, to guard against any potential CSF leak not noted intraoperatively. Two patients underwent a ventriculo-peritoneal shunting procedure due to the preoperative presence of gross hydrocephalus.
Statistical analysis of data was done by the Statistical Package for the Social Science (SPSS) 20.0.1 and Graph Pad Prism version 5. The data was summarized as mean and standard deviation for numerical variables, and as counts and percentages for categorical variables. Unpaired proportions were compared by chi-square test or Fisher's exact test, as appropriate. Correlation was calculated by Pearson correlation analysis.
Once a t value was determined, a P value was found using a table of values from Student's t-test distribution. If the calculated P value was below the threshold chosen for statistical significance (usually the 0.10, the 0.05, or 0.01 level), then the null hypothesis was rejected in favor of the alternative hypothesis. A P value ≤ 0.05 was considered statistically significant.
The patients included 15 men and 17 women (53.1% women) with an age range of 18–45 years. 62.5% patients belonged to an age less than 30 years. Tonsillar herniation in the preoperative period ranged from 5 to 25 mm. All patients had symptoms and/or signs that were attributed to Chiari I malformation. The symptoms of 32 patients are presented in [Table 1]. Syrinx was present in 23 (71.8%) patients and its most common (43.8%) distribution was in the cervicodorsal region. Progressive scoliosis occurred in one patient with syringomyelia. The duration of symptoms ranged from 4 months to 20 years before the establishment of diagnosis.
8 (25.6%) of the 32 patients reported a complete resolution of their symptoms, 18 (56.25%) patients reported partial resolution, and 6 reported no improvement in their symptoms. The latency to begin seeing an improvement in symptoms ranged from 10 days to 4 months. 16 (88.9%) patients noted some improvement in their headache. Six patients had complete resolution of their headache, 5 had decreased frequency of headache, 2 were able to control their headache with over-the counter analgesics, and 4 (including one of the patients with decreased headache frequency) had resolution of some, but not all, headache subtypes. Other symptoms that were alleviated postoperatively included upper and lower extremity sensory changes (n = 7), neck pain (n = 4), dizziness/vertigo (n = 5), visual symptoms (n = 1), and dysphagia (n = 2). Two patients did not report any improvement in symptoms within 1 year of follow-up. Patients who did not report an immediate clinical improvement continued to experience headaches (n = 2), neck pain/stiffness (n = 2), dizziness (n = 1), and photophobia (n = 1). No patient had a worsening of symptomatology following surgery.
Following the decompression, tonsillar herniation ranged from 3 to 18 mm (mean 7.35 mm). 24 patients had an improvement in tonsillar herniation; in six patients, there was no difference; and, 2 patients had a 0.8 mm worsening of herniation. Of the 21 patients presenting with syringomyelia, the syrinx diameter reduced in 61% patients in the follow-up period. The syrinx diameter was minimally decreased (less than 30% compared with the preoperative values) in 28% patients and remained unchanged in 11% of patients. The mean CSF peak velocity at the foramen magnum region was 4.38 cm/s in the preoperative period, that reduced to a mean value of 3.16 cm/s after posterior fossa decompression. This is depicted in [Table 2] as well as [Figure 1], and the correlational analysis is shown in [Figure 2].
Chiari malformation leads to partial obstruction of CSF flow in proximity to the foramen magnum. Alterations in CSF flow resulting from a small posterior fossa and tonsillar obstruction lead to abnormalities in fluid pressures in the spinal canal. The presence of a small or abnormal posterior fossa may also contribute to the Chiari symptomatology and dynamics, probably contributing more to brain stem symptoms and abnormal brain stem motion than to CSF flow abnormalities. The role of adhesions in obstructing or redirecting flow may also be important, regardless of the amount of tonsillar descent present.
The clinical presentation is due to compression at the foramen magnum, paroxysmal intracranial hypertension, central cord disturbance, and cerebellar, or brainstem dysfunction. The predominant symptom in adults is pain; and, the reported incidence of pain is less in children since they have difficulty in localizing pain and may simply be more irritable, making the establishment of the diagnosis in them difficult. There is involvement of the pyramidal and posterior column tracts accordingly, due to the cervicomedullary compression at the level of foramen magnum.
The presence of syrinx leads to the classical presentation of dissociated and/or suspended sensory loss, albeit more often mentioned than it is actually present. Scoliosis is seen frequently in those cases of Chiari I malformation associated with syringomyelia. The interval from the clinical presentation to diagnosis can be only a few days but can be as long as 46 years. There is a tendency for a shorter interval in those patients with associated syringomyelia when compared to those without it. The incidence of autonomic disturbances and respiratory compromise is also common. The cranial nerve involvement is also frequent; in two (06%) of our patients such an occurrence was seen. Occurrence of associated syringomyelia has been reported in between 50 and 76% patients in various series. Klekamp et al., has described the results of his clinical series with clinical stabilization obtained in 86% patients and a decrease in the syrinx size in 87% of the cases, with a maximum follow-up of 8 years. In our series, the associated syrinx was present in 23 (71.87%) patients. The distribution of syrinx was cervicodorsal in 43.8% and only cervical in 21.9% patients. A total of 62% (20/32) of patients demonstrated radiographic improvement, 25% (8/32) remained stable, and 12.5% (4/32) developed an increased syrinx size or the development of a new syrinx. Of the 20 patients with an improved syrinx size, 7 (35%) demonstrated near-complete collapse of the syrinx, and in 4 (20%) patients, the syrinx was at least 50% smaller. The incidence of decrease in the syrinx size in our series was 62%, which is lower than that seen in the series by Klekamp et al.
Analysis of measurements obtained postoperatively at 6 months demonstrated a decrease in the peak systolic velocity at the foramen magnum. Unobstructed CSF flow across the enlarged foramen magnum and the progressive decrease of syrinx flow confirm that a craniocervical decompressive procedure can effectively correct this malformation. The cerebrospinal fluid flow dynamics data obtained in this study are consistent with the fact that removal of the junctional block re-establishes the normal communication between the cranial and spinal compartments. The resolution of the condition of increased spinal subarachnoid pressure interrupts the mechanisms of syrinx maintenance, leading to a progressive reduction in the cavity size and eventually to its collapse. It is of interest to note that the rate of syrinx disappearance in this series was 37.5% (12 of 32 patients). In the majority of cases, a residual syrinx was still visible on follow-up MR images. This data was not surprising and probably reflected the atrophic state of the spinal cord, induced by the increased preoperative syrinx pressure. This condition, however, does not necessarily correlate with clinical disturbances.
It is reasonable to consider that other factors are involved in the pathogenesis of syringomyelia. The first is another time-dependent variable. Chiari I malformation is an acquired, not a congenital, disorder. However, it is impossible to establish exactly at which point the cerebellar tonsilar descent occurs in each patient and how long it takes, once present, to become symptomatic. It is theoretically possible that in patients without a syrinx, the period of time it takes for the malformation to reach its final position may be shorter, and a patient becomes symptomatic earlier because of a brainstem conflict with the clivus. This period could not be sufficiently long enough to induce syrinx formation. Another possibility is that CSF flow blockage is not always present at the foramen magnum. We should consider the tonsillar descent as a dynamic phenomenon (as the cine MR imaging displays) that is potentially reversible. Intermittent spontaneous relief of the CSF block could temporarily resolve the pressure changes across the foramen magnum. The extent of tonsillar descent may not be considered crucial in this sense, as it has been demonstrated that there is no direct correlation between the tonsillar herniation and clinical symptoms.
One more factor that could influence the penetration of CSF into the spinal cord is the compliance of the spinal cord itself to pressure modifications. This factor is also unpredictable, and there is no known method with which its relevance in normal and pathological conditions could be determined.
Clinical results of this study also indicate that a craniocervical decompressive procedure adequately treats Chiari I malformation-related disturbances. Patients with signs and symptoms of brainstem compression were especially responsive to the posterior fossa enlargement, as were those with syrinx-related clinical disturbances. Although the results of this series were rewarding, it must be pointed out that improvement of syrinx-induced signs and symptoms of spinal cord dysfunction are not easily predictable. The clinical outcome depends on the degree of spinal cord damage induced by the syrinx.
CSF flow velocity
In the present study, we found diminished maximal velocities after craniocervical decompression in adult patients with Chiari I malformation. We got a significant P value when we compared the preoperative CSF velocity at the foramen magnum with postoperative values, and this is shown in [Table 2]. This study adds support to the theory that the Chiari I malformation is associated with abnormal CSF flow at the foramen magnum. The study did not show a correlation between the changes in maximal CSF velocities and the degree of clinical improvement. The physiologic significance of increased velocity and inhomogeneous flow of CSF in Chiari I patients requires more study.
Other measurements of CSF flow [Figure 3] and [Figure 4] in Chiari I patients before and after suboccipital decompression are not readily comparable to our data because of differences in methodology. In one study, the peak velocities during systole and diastole were measured at the foramen magnum and in the cervical spine before and after surgery. In that study, the flow measurements were averaged for the entire subarachnoid space, whereas we measured flow on a voxel-by-voxel basis. In another study of eight patients who underwent suboccipital decompression, peak velocities were measured in a sagittal rather than an axial section and were averaged for a region of interest. This is again unlike our study, in which the peak velocity was recorded in the foramen magnum voxel recording the highest velocity. In another study of ten Chiari I patients who had surgical treatment, the mean systolic and diastolic velocities were measured. Some investigators have employed axial sections, as we did. In one such study, postoperative measurements were not reported. In another study, CSF flow was measured at the C5–C6 level and at the foramen magnum, of 20 patients who underwent suboccipital decompression. Flow, reported as peak flow rate (in mL/s), increased as a result of surgery. CSF flow within the foramen magnum, especially in patients with a Chiari I malformation, is complex; a single flow measurement such as the extreme velocity or the average velocity may not serve well as an index of abnormality. We tested the hypothesis that peak velocities are affected by suboccipital decompression, because we expected that these measurements would be more sensitive to the presence of the regional high velocity jets; however, the methods we used are not optimized. Therefore, although a temporally and spatially resolved velocity measurement has potential importance in assessing the severity of the Chiari I malformation, much refinement in the analysis of the technique may be needed. Furthermore, the precision and accuracy of the MR methodology has limitations that have been noted previously. Finally, an independent observer did not assess the patients before and after surgery.
Studies of CSF flow at the foramen magnum with MRI have suggested that the Chiari I malformation produces an anatomic and physiologic block to the flow of CSF at the foramen magnum. In patients with Chiari I malformation, the arterial pressure wave in the cranial vault produces an enlarged cervical subarachnoid pressure wave that may contribute to the development of a syrinx and to clinical signs and symptoms. Our results are consistent with the theory of a physiologic block of CSF flow in patients with Chiari I malformation. A surgically produced decrease in physiological obstruction would likely reduce the maximal velocities. Additional studies and more sophisticated methods of flow analysis are probably required to determine which flow patterns are not physiologic, which criteria predict the development of a syrinx or symptoms, and what changes in flow characterize successful surgical treatment.
Although the selection criteria for surgery is based mainly on the degree of tonsillar herniation and presenting symptoms, the degree of CSF flow obstruction rather than the degree of tonsillar herniation can better select patients who are most responsive to surgery. Further studies are needed to ascertain a direct correlation between the change in maximal velocity and clinical improvement.
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Conflicts of interest
There are no conflicts of interest.
[Figure 1], [Figure 2], [Figure 3], [Figure 4]
[Table 1], [Table 2]