Chiari I Malformation

Many theories have been put forth to explain the development of Chiari malformations in the absence of hydrocephalus (Figs. 9.1 to 9.3). Currently, the most appealing theory emphasizes the difficulty in rapidly equilibrating the CSF pressure wave seen during the Valsalva maneuver.^8–10 During this delay in achieving equilibrium, there is a vector of force out of the intracranial cavity (Fig. 9.4). The prolonged intracranial hypertension relative to the intraspinal compartment may result in the downward migration of the cerebellar tonsils, resulting in obstruction of normal CSF flow between the posterior cranial fossa and the cervical subarachnoid space. Conditions that impede the physiological flow of CSF at the foramen of Magendie enhance the formation of the malformation. These could include arachnoid veils or septations in this region as well as adhesions.¹¹ Alternatively, conditions that artificially lower the intraspinal pressure relative to the intracranial pressure (lumboperitoneal shunts) have been observed to “cause” the CIM with the subsequent development of syringomyelia. Parenthetically, there is some evidence that the CIM may result from derailment on chromosomes 9 and 15.¹²

FIGURE 9.1 Postmortem view of the Chiari I malformation from an adult male cadaver. Note the right tonsil that is descended more inferiorly.

FIGURE 9.2 Sagittal T1-weighted magnetic resonance image of a child with swallowing difficulty and Chiari I malformation. Note the dilated ventricular system.

FIGURE 9.3 Sagittal magnetic resonance image noting a Chiari I malformation in an adolescent girl with Valsalva-induced headaches. Also, note the retroversion of the odontoid process resulting in simultaneous ventral compression.

FIGURE 9.4 A, When ventricular and lumbar subarachnoid pressures are simultaneously monitored in a patient with a Chiari I malformation the pressures are the same in the resting state when calibrated against a reference. B, With the Valsalva maneuver there is an abrupt rise of lumbar pressure exceeding that seen in the ventricular system. C, With relaxation the lumbar space has its pressure rapidly fall and return to the baseline. The ventricular pressure, on the other hand, cannot equilibrate, and sustained intracranial hypertension relative to the intraspinal compartment is maintained for several seconds to a few minutes. This vector of force is the pathophysiological mechanism for the development of progressive displacement of the cerebellar tonsils into the cervical spine and the development of syringomyelia.

(From Williams B. Cerebrospinal fluid pressure-gradients in spina bifida cystica, with special reference to the Arnold-Chiari malformation and aqueductal stenosis. Dev Med Child Neurol Suppl. 1975;17:138-150

Initially considered an “adult” disease, the CIM is reported more frequently now in the pediatric population as a result of the widespread availability of detailed MRI. The clinical presentation of CIM essentially falls into three categories (Fig. 9.5):

FIGURE 9.5 Symptoms and signs of patients with Chiari I malformation.

Most commonly, patients present with occipital or cervical pain that is nonradicular but frequently associated with dysesthesias in the C2 dermatome.¹³ The neck pain or headache is frequently brought on by exertion or by coughing or sneezing (Valsalva-induced). Nonverbal children may relate their pain via irritability, crying, failure to thrive, or the presence of opisthotonos.

The diagnosis of CIM can easily be confirmed with MRI. The presence and extent of syringomyelia, seen in 50% to 75% of patients,^5,14–16 should be determined with an MRI of the entire spinal cord. Computed tomography (CT) may further elucidate the bony abnormalities and plain films may assist in the evaluation of stability issues. Dynamic MRI (cine-MRI) has been used to evaluate CSF flow around the craniocervical junction. In a review of 800 MRI examinations, one study noted that “normal” or “asymptomatic” patients may have cerebellar tonsils that extend 3 mm below the foramen magnum.¹⁷ The tonsillar herniation was noted to be clearly pathological when it exceeded 5 mm. Similarly, Barkovich and associates¹⁸ studied 200 normal patients and 25 patients with a “firm” diagnosis of CIM. Tonsils 2 mm below the foramen magnum were considered as the lowest extent of the tonsils in normal patients (specificity of 98.5% [three false positive results] and a sensitivity of 100%). Tonsils 3 mm below the foramen magnum were considered the lowest extent in normal patients (sensitivity 96% and specificity 99.5%). An additional study has documented ascent of the tonsils with increasing age in some patients.¹⁹

No medical treatment exists for the Chiari malformations. Numerous therapeutic paradigms exist (Fig. 9.6). The first decision that must be made is whether the lesion is truly symptomatic. Observation is warranted in asymptomatic patients without an associated syrinx. In symptomatic patients or asymptomatic patients with syringomyelia, surgical intervention is recommended. The degree of brainstem compression and tonsillar herniation is taken into account as well. In about 10% of patients hydrocephalus is associated with the CIM, in which case a CSF diversionary shunt or endoscopic third ventriculostomy should be the initial form of therapy. Similarly, symptomatic ventral compression out of proportion to dorsal compression may require a ventral decompression (i.e., transoral odontoid resection), especially in cases of myelopathy. The most common surgical procedure for the treatment of CIM is posterior fossa decompression. The goal of the operation is to enlarge the posterior fossa and to re-create the cisterna magna, thereby permitting normal flow of CSF from the posterior fossa to the cervical subarachnoid space. In the majority of CIM patients with a syrinx, the syrinx decreases in size and does not require direct treatment because the posterior fossa decompression treats the underlying pathological process causing the syringomyelia.

FIGURE 9.6 Therapeutic options for treating Chiari I malformation.

For decompression, the patient should be prone and the neck flexed (Fig. 9.7). The incision extends from a point just below the inion to the spinous process of C2. An avascular plane (nuchal ligament) between the paraspinous muscles is followed down to bone, and a subperiosteal dissection is then performed. A moderate suboccipital craniectomy, the width of the foramen magnum, is followed by the removal of the posterior arch of C1. Some techniques advocate either stopping here or opening the outer layer of the dura and then closing.^20,21 We open all layers of the dura and clip the opened arachnoid to the dural edge. Any arachnoid adhesions potentially obstructing the outflow of CSF from the foramen of Magendie are removed and the floor of the fourth ventricle is examined (Fig. 9.8). A portion of the occipital pericranium is harvested through a separate incision and duraplasty performed. The wound is closed in anatomical layers.

FIGURE 9.7 Operative position for posterior fossa decompression. A, The operative field is maintained horizontally with the head flexed and held in a pin fixation device. B, Preparation is made for a midline linear incision 2 cm below the external occipital protuberance and extending to the spinous process of C2. A 3-cm incision is made above the inion to harvest pericranium for grafting material.

FIGURE 9.8 Intraoperative view following decompression of a Chiari I malformation. The left and right cerebellar tonsils are spread with forceps to observe the floor of the fourth ventricle.

The results of craniocervical decompression are encouraging in long-term follow-up. Postoperative outcome is not age-based and early treatment tends toward better outcomes. Nearly 85% of patients will have relief of their head and neck pain, especially if it was Valsalva-induced.^5,20 Associated syringes decrease in size or collapse in the majority, albeit not all, of the patients who undergo a well-performed posterior fossa decompression. If decompression fails to improve the symptoms or decrease the size of the syrinx in a 6-month period, consideration should be given to either a reexploration of the posterior fossa with coagulation or resection of a cerebellar tonsil. Placement of a syringosubarachnoid shunt may be indicated in recalcitrant cases of syringomyelia that do not respond to an adequate posterior fossa decompression, although this lack of response is rare. Advanced symptoms of medullary dysfunction, muscle wasting, or dysesthesias in the trunk or extremities are unlikely to resolve but should not progress. Mild to moderate scoliosis has a high likelihood of improvement.

Chiari II Malformation

The caudal displacement of the cerebellar vermis, lower brainstem, and fourth ventricle is seen almost exclusively in patients with myelomeningoceles (Fig. 9.9). Numerous other anomalies of the nervous system and its support structure are seen in various combinations (Fig. 9.10). Of particular note is the vertical straight sinus resulting from the low-lying tentorium cerebelli, as well as the possibility of large venous lakes in the tentorium. Fenestrations may also be seen in the falx cerebri, which is often not well formed, and on occasion allow the gyri of the left and right cerebral hemispheres to interdigitate, giving the appearance of “Chinese lettering” on axial MRI (Fig. 9.11). Hydrocephalus occurs in approximately 90% of patients with CIIM.²² Split cord malformation is seen in up to 6% of patients with CIIM and syringomyelia has been reported to occur in between 20% and 95% of patients.² Other associated anomalies include tectal beaking secondary to partial or complete fusion of the colliculi into a single backward pointed peak and kinking at the level of the cervicomedullary junction. The latter anomaly is caused by caudal displacement of a portion of the medulla in conjunction with a spinal cord that is held in relative immobility by the dentate ligaments. The tracts of the spinal cord then double back on themselves for a short distance.The cerebellum is smaller than usual; in addition, the vermis and adjacent medial cerebellar hemispheres are poorly differentiated from each other. The extent of the medial cerebellar protrusion and the character of tissues involved vary considerably from case to case. Abnormalities of the cerebral cortical pattern have frequently been described in Chiari II patients. Radiographic signs of CIIM evident on CT scans include lückenschädel (85% of cases), scalloping of the posterior surface of the petrous pyramid (80%), tentorial hypoplasia (95%) with a wide incisura and a small posterior fossa, enlargement of the foramen magnum (73%), and inversion (or transtentorial upward herniation) of the cerebellum. Most of these abnormalities may be observed with other conditions; however, their combination is highly suggestive of CIIM. In addition to hydrocephalus, the ventricular system displays multiple abnormalities: the third ventricle may be only mildly dilated and contains a large massa intermedia (75%); the fourth ventricle is typically small or nonvisualized (70%); it is often flattened and elongated, extending into the cervical canal; the lateral ventricles may be asymmetrically dilated, with prominence of the atria and occipital horns (colpocephaly), and the septum pellucidum is frequently absent. The frontal horns and the anterior portion of the third ventricle are frequently pointed and acutely angulated. This sharpness of the frontal horn (lemon sign) and the caudal displacement of the fourth ventricle (banana sign) are relatively easily seen on in utero ultrasound examinations. The upper cervical canal also displays several bony and spinal cord anomalies in association with the CMII. The C1 arch may be incomplete in up to 70% of these patients, with the missing bone being replaced by a fibrous band corresponding to the periosteal envelope. The dorsal arch of C2 is almost always intact. Klippel-Feil fusion anomalies of the cervical spine are present in a small group of patients.²³ Basilar impression and C1 assimilation are quite uncommon in CIIM as opposed to CIM. Significant shortening and scalloping of the clivus can be seen.

FIGURE 9.9 Sagittal T1-weighted magnetic resonance image of a child with the Chiari II malformation. Note the large massa intermedia, thin corpus callosum, beaked tectum, and cortical dysplasia.

FIGURE 9.10 Axial CT image noting the towering cerebellum seen in patients with Chiari II malformation.

FIGURE 9.11 Axial CT image demonstrating the Chinese lettering that occurs in the Chiari II malformation and the absence of the falx cerebri.

The pathophysiology of the malformation has been postulated to be similar to that of the CIM, that is, a difficulty in equilibrating the dynamic CSF pulse pressure induced by Valsalva.^10,24 In the case of CIIM, the presence of CSF pooling in or leaking from the myelomeningocele sac lowers the intraspinal pressure and the result is the ectopia of not only the cerebellar vermis but the abovementioned portions of the brainstem. In support of this theory is the observation of reduced hindbrain herniation observed in some children who undergo fetal myelomeningocele closure.²⁵

Similarly grouped as in the earlier section, the symptoms of CIIM are best considered according to the area demonstrating disturbed function: brainstem, cerebellar, or spinal cord dysfunction (Fig. 9.12). Approximately 33% of these patients will develop some symptom of hindbrain herniation prior to the age of 5 years and outcome significantly worsens for presentation of these symptoms before 3 months of age.^26,27 Symptoms that may result in death if left untreated include stridor, apnea, and dysphagia resulting in aspiration, and are the leading cause of death in myelodysplastic patients. Nystagmus may be the earliest sign of cerebellar dysfunction and the initial spinal cord symptoms (weakness, bowel and bladder dysfunction) are secondary to the inadequate formation of the lower spinal cord. It is important to note that spinal cord function can worsen during development and that CSF diversionary shunt malfunction, syringomyelia formation, or spinal cord tethering must be ruled out and surgically dealt with if present. Scoliosis may also be present in this population and may be related to syringomyelia.

FIGURE 9.12 Symptoms and signs of patients with Chiari II malformation.

MRI continues to be the imaging procedure of choice in these patients. Indeed, the advent of MRI technology enabled the identification of the associated developmental abnormalities mentioned previously. Plain dynamic cervical spine radiographs may assist with any question of instability, just as plain thoracic and lumbar radiographs would help to follow the degree of scoliosis. Spinal cord syringes are best identified and followed with spinal MRI.

It is important to stress that adequate shunt function must be established prior to pursuing decompression of a symptomatic CIIM (Fig. 9.13).²⁸ This examination includes surgical inspection of the shunt because the ventricular system may not change size in this group. The number of CIIM decompressions at our institution has decreased significantly following the establishment of this paradigm. Symptoms warranting intervention include inspiratory stridor, sleep apnea, recurrent aspiration pneumonia, opisthotonos, and progressive spasticity or ataxia.

FIGURE 9.13 Therapeutic options for treating patients with Chiari II malformation.

When surgical decompression is elected, patients are positioned prone with the neck flexed. Unlike surgical decompression of a CIM, decompression of a CIIM rarely includes removal of the foramen magnum. Removal of the posterior elements of the vertebrae overlying the displaced cerebellar vermis must be performed (Figs. 9.14 and 9.15). The dura is opened widely and the fourth ventricle is identified. The choroid plexus is often in its embryonic extraventricular position. Following this frequently ectopically placed choroid plexus through the dense arachnoidal scarring will usually lead to the foramen of Magendie and the fourth ventricle. This is the crucial goal of the procedure. If any question exists as to the patency of the foramen, then a stent should be placed. The medullary kink, if present, must not be mistaken for the vermis, or the surgeon will end up dissecting into the brainstem. An expansion duraplasty is performed and the remainder of the wound is closed in anatomical layers.

FIGURE 9.14 Operative exposure of the Chiari II malformation.

FIGURE 9.15 Operative view of the Chiari II malformation.

Outcome following surgery is dependent on the severity of symptoms prior to intervention. Infants presenting with brainstem symptoms are less likely to have a significant improvement in their symptoms following decompression. Few studies exist regarding outcome; however, earlier intervention and fewer symptoms are thought to predict success.²⁷

Syringohydromyelia

Syringohydromyelia is a secondary process with many causes. The term syringomyelia has been used to describe any longitudinal fluid collection within the spinal cord. This term, however, refers to fluid collections outside the central canal. Hydromyelia refers to fluid collections enlarging the central canal. A combination of these two words, syringohydromyelia better connotes this disease process. However, for the purposes of simplicity we have used the term syringomyelia or syrinx throughout this chapter to denote any fluid collection within the spinal cord. Known pathological situations in which a syrinx may form include post-traumatic circumstances or in association with Chiari malformations (Figs. 9.16 to 9.18), neoplasms, arteriovenous malformations, arachnoiditis, or occult spinal dysraphism. Idiopathic syringomyelia also exists. The mechanism by which the fluid accumulates varies significantly and a useful informal system to classify syringes divides them into either communicating (Chiari, occult spinal dysraphism) or noncommunicating (neoplasm, arteriovenous malformations, arachnoiditis, traumatic). A terminal syrinx (lower one third of the spinal cord) is normally not a result of hindbrain herniation.

FIGURE 9.16 Sagittal magnetic resonance imaging demonstrating small syringes.

FIGURE 9.17 Sagittal magnetic resonance imaging demonstrating large syringes.

FIGURE 9.18 Axial view of Figure 9.17 noting the distended syrinx.

Fluid collections that begin in the ependyma-lined central canal (hydromyelia) may cause an outpouching in weak areas that can grow into the white matter of the cord (Fig. 9.19). The absence of ependyma then enables the syrinx to enlarge with less constraint. Of note are the crossing fibers of the spinothalamic tract in the ventral white commissure that are particularly vulnerable to syrinx expansion.

FIGURE 9.19 Stages in the progressive expansion of an ependyma-lined hydromyelia to a larger cavity compressing the central canal. This large cavity has no ependymal lining and so could be termed a syrinx.

Symptoms include loss of pain and temperature sensation in the arm or chest, diminished or absent deep tendon reflexes, and spasticity of the lower extremities. Longer-term findings include wasting of the intrinsic muscles of the hand and scoliosis. Dysesthetic pain over the thorax and arms is a particularly poor prognostic indicator for postoperative relief of symptoms. Acute loss of neurological function may occur with coughing or straining. When the Valsalva maneuver causes the epidural venous complex to expand, the cavity may be forced to dissect through white matter within the cord (Fig. 9.20). This may result in symptomatic or asymptomatic enlargement of the syrinx.

FIGURE 9.20 Increased intra-abdominal pressure caused by the Valsalva maneuver forces blood into the epidural venous complex. When the epidural veins are forcefully expanded against the enlarged cystic cord they may force the cyst to be displaced (usually cephalad). This sudden displacement with forceful coughing or sneezing may actually be associated with a significant worsening of the patient’s neurological condition.

MRI is the diagnostic procedure of choice for syringohydromyelia. Up to 75% of patients with CIM will have an associated syrinx identified on MRI, and between 20% and 95% of patients with CIIM will have a syrinx seen on imaging.² An extreme form of syringomyelia, which has ruptured through the pia mater of the spinal cord and expanded, may be seen in this group and is referred to as an exophytic syrinx. These syringes may be confused with spinal arachnoid cysts in this population.

If symptoms are functionally significant (Fig. 9.21) or progressive, intervention should be considered, with the recommended procedure varying widely depending on the underlying condition (Fig. 9.22). No medical therapy exists for syringomyelia. If no alternative explanation for a surgically significant syrinx is identified, exploration of the craniocervical junction should be considered. Follow-up MRI can readily evaluate residual or recurrent fluid. In the setting of a residual syrinx following a decompressed CIM, the patient should return to the operating room and the posterior fossa should be explored for readhesion of the arachnoid at the outlet of the fourth ventricle.^29–31 There is no consensus as to how long to wait and at our institution, we wait at least 6 months in asymptomatic patients. It is common for a cerebellar tonsil to be either partially coagulated or resected subpially during the secondary procedure. When operative therapy turns to stenting or shunting the syrinx, note that the arachnoid flow tends to be compromised in certain pathological states (i.e., arachnoiditis, post-traumatic) and therefore the distal end of the shunt should be placed either in the pleural space or the peritoneum. If the distal end of a syrinx stent is placed in the intrathecal space, it is imperative that it be placed in the subarachnoid space for absorption to take place properly. Reestablishment of a patent spinal canal and subarachnoid space may be undertaken in the setting of traumatic disruption through removal of bone fragments or bony realignment. This is made more difficult in the setting of a previous surgical fusion. Occasionally, syringes are multicompartmental and will require drainage at multiple sites. If the syrinx is the result of either arteriovenous malformations or tumor, primary treatment is directed at the appropriate pathology. Outcome is dependent on the degree of disability prior to intervention and the cause of the syrinx. Evaluation for any tethering elements (e.g., fatty filum terminale) should be made in patients with terminal syringes. If tethering is found, the offending element is addressed. If no tethering pathology is found, these patients can be watched unless there is unequivocal evidence for neurological decline (e.g., bladder function).

FIGURE 9.21 Left hand from a patient with a large cervicothoracic syringomyelia and dysesthetic pain that resulted in her biting the nails off her fingers.

FIGURE 9.22 Therapeutic options for patients with symptomatic syringomyelia.

Summary

Time and, when necessary, surgical intervention are needed to better elucidate the natural history of the hindbrain herniation syndromes known as the Chiari malformations. Numerous abnormalities of the nervous system may also be associated with them, and a unified theory has yet to be fully discerned. To date, all studies aimed at the Chiari malformations are classified as levels II and III. Syringomyelia is most often due to these abnormalities at the craniocervical junction but also occurs in response to other pathological processes of the spinal cord.