Fourth ventricle stent placement for treatment of type I Chiari malformation in children

Type I Chiari malformation (CM-I) is a common congenital malformation, often accompanied by syringomyelia. Obstruction of CSF circulation in the foramen magnum is the reason for the formation of the syringomyelia. Fourth ventricle stenting (FVS) could ensure the CSF flow from the fourth ventricle, which might represent an effective approach to achieve syringomyelia relief. We have reviewed four cases of CM-I children who received FVS implantation from November 2021 to July 2022. Each of the patients underwent FMD. The ventricular catheter of an Ommaya reservoir (Medtronic, Inc.) was used as a stent. Duraplasty was performed with autologous fascia. Cervical MRI rechecks were routinely done 3 months later, and the clinical symptoms were followed up. Four children received FVS, including one boy and three girls, aged from 12 months to 10 years, with a mean age of 6.8 years. No major complication occurred. The syringomyelia or hydrocephalus in each patient were all attenuated, as observed on the reexamination MRI images. During the follow-up time with a mean of 10.8 months, no patient had new symptoms. FVS is an effective and safe method for operation of CM-1 in children. The indications of FVS include redo-FMD, difficulties to ensure post-FMD CSF circulation patency at the foramen magnum and with obstructive hydrocephalus. A long-term follow-up duration is necessary.


Introduction
Type I Chiari malformation (CM-I) is a common congenital malformation with a prevalence of 0.6-0.9% in the general population and 0.6-1% in children [1]. Syringomyelia complication occurs in 30-85% of CM-I patients [1].
Most studies suggesting that the cause of syringomyelia is altered CSF dynamics at the level of the craniocervical junction [2].
Foramen magnum decompression (FMD) with or without duraplasty remains the recommended primary surgical treatment in such cases. The key factor for the success of this operation is to ensure patency of the foramen of Magendie. The implantation of a stent from the fourth ventricle to the cervical subarachnoid space could provide direct drainage of cerebral spinal fluid (CSF). This technique for Chiari malformation treatment was reported as early as in 1976 [3]. In 1986, Venes et al. [4] reported that 14 type 2 Chiari malformation patients received FMD and fourth ventricle stenting (FVS) with a good effect, including 13 children under 15 years of age. Additionally, in 1997, Park et al. [5] reported that 32 Chiari malformation children received FVS with 93% of patients' symptoms improved and 80% of syringomyelia remission. FVS is not a routine technique. In recent two decades, there are not much literatures reported on this. Here, we report four cases of CM-1 children who received FVS for different reasons. We have also discussed FVS indications.

Methods
In this study, we included the cases of four CM-I children (one boy and three girls) who received FVS implantation from November 2021 to July 2022. Their age was from 12 months to 10 years, with average of 6.8 years of age.
Each of the patients underwent FMD, including removal of the foramen magnum and C1 laminectomy. Subpial resection of the herniated tonsil was performed. Intradural exploration and sharp separation of adhesions were conducted to ensure no significant occlusion of the foramen of Magendie had occurred. The ventricular catheter of an Ommaya reservoir (Medtronic, Inc.) was used as a stent. The length of the stent was measured on the sagittal CT from middle of the fourth ventricle to the upper edge of C2. Approximately 3 cm of the catheter was inserted within the fourth ventricle along its floor, and the distal end was placed under carefully preserved arachnoid over the dorsal upper cervical spinal cord. The catheter was then secured to the dura using a 6-0 Prolene suture. Duraplasty was performed with autologous fascia. Cervical MRI rechecks were routinely done 3 months later, and the clinical symptoms were followed up.

Case 1
The first case was of a 10-year-old girl, who had suffered from scoliosis for 7 years. MRI indicated CM-I with syringomyelia from T4 to T10. Foramen magnum decompression with duraplasty (FMDD) was performed. The MRI recheck results 8 months later showed persistence of syringomyelia. Then, a second operation was performed with tonsillar resection (TR) and FVS. Further, the MRI recheck 3 months after the second operation revealed remission of syringomyelia ( Fig. 1).

Case 2
The second case was of a 12-month-old boy, who had an abnormal posture of walking for 1 month. MRI indicated hydrocephalus and subdural effusion of posterior fossa. Foramen of Magendie occlusion was considered on Cine MRI. Then, FMDD and FVS was performed. The MRI recheck 3 months later showed remission of hydrocephalus and subdural effusion (Fig. 2).

Case 3
The third case was of a 7-year-old girl, who had scoliosis for 1 month. MRI indicated CM-I with syringomyelia from C2 to T11. During the FMD operation, very prominent occipital and marginal sinuses were found. The dura opening was insufficient, and post-TR examination of the fourth ventricle could not be performed. Furthermore, the patency of the CSF flow at the foramen magnum cannot be ensured. Next, FVS was implanted. The MRI recheck 3 months later showed remission of syringomyelia (Fig. 3).

Case 4
The fourth case was of a 9-year-old girl, who had right leg weakness for 1 year. MRI indicated CM-I with syringomyelia from C4 to T11. Arachnoid adhesion was found during the exploration of the fourth ventricle, and sharp separation was performed. The foramen magnum was still crowded after TR, and the patency of CSF flow was Detail of the four cases was showed in Table 1. No complications occurred in the four patients, and no patient had new symptoms, with a mean follow-up time of 10.8 months.

Discussion
CM-I is a common congenital malformation in children, characterized by an obstruction of the CSF circulation and often accompanied by syringomyelia. One of the views on the etiology of syringomyelia is that the obstruction of CSF circulation in the foramen magnum is the reason for its development [6].
Currently, the treatment of CM-I is FMD surgery with or without duraplasty and with or without excision of the tonsil. A good effect was achieved with a clinical improvement rate from approximately 80 to 100%; stabilization or improvement of syringomyelia was observed in nearly all subjects [7]. But some patients had persistent, recurrent, or enlarging syringomyelia after an initial decompression operation.
Some studies found that obstruction of the foramen of Magendie was associated with persistent syringomyelia after FMD [2].Yuan et al. [8] reported that eight CM-I cases had persistent syringomyelia after FMD. During the secondary decompression operation, a structural cause was identified for the failed primary Chiari decompression in each case, including a thickened arachnoid veil, PICA adherence, pseudomeningocele, cerebellar tonsil descent, or intertonsillar adhesions. In an earlier study, John [9] reported 16 cases of persistent syringomyelia. Cine phase-contrast MR imaging and Queckenstedt test were used to evaluate the patency of CSF circulation at the foramen magnum in this previous research. Its findings showed that the previous surgical intervention had not relieved the obstruction of the CSF pathways at the foramen magnum. It was believed that enhancing the CSF outflow from the fourth ventricle by stent placement would aid in decompressing syringomyelia [10]. Park et al. [5] reported the case of a patient who developed recurrent syringomyelia  At re-operation, the stent was found to be dislodged, and the foramen of Magendie was re-occluded by arachnoid adhesions. Second FVS relieved syringomyelia 1 year later. Riordan and Scott [10] reported that 14 CM-1 patients received FVS as a secondary operation for persistent syringomyelia with remission in 13 patients. He proposed that stent placement was an effective technique to treat recurrent syringomyelia when scarring or partial occlusion of the foramen of Magendie was believed to recur if simply lysis was applied. Lou et al. [11] reported 15 CM-1 patients received FVS as a secondary operation for persistent syringomyelia. He found that both systolic and diastolic peak flow velocities significantly decreased on phase-contrast MRI, suggesting better CSF circulation after FVS than before.
We think FVS is proper as a second operation for persistent or recurrent syringomyelia, especially after the foramen of Magendie had been re-occluded by arachnoid adhesions or a scar. Simply redoing FMD without stenting increases the possibility of syringomyelia recurrence.
Besides re-operation, there is indication for FVS at initial operation if the decompression was not sufficient, and the patency of the CSF circulation at the foramen magnum could not be ensured. We met such situation during the operation of cases 3 and 4. The MRI post operation showed crowed at foramen magnum. However, FVS relieved the syringomyelia of both patients.
CM-I with hydrocephalus may also have indication for FVS. The MRI of case 2 indicated hydrocephalus with subdural effusion of posterior fossa. We considered that the foramen of Magendie was occluded, and the CSF outflow through the foramen of Luschka to the subdural space. After the occlusion was relieved by FMD with FVS, the hydrocephalus was attenuated as well as the subdural effusion.
Hydrocephalus is described in approximately 7-10% of CM-I patients [12,13]. The association between CM-I and hydrocephalus probably results from different, multifactorial, and not yet completely understood, mechanisms. Some authors postulated that the dissociation of CSF circulation at the level of the foramen magnum would stop the pressure transmission from the pulsating vessels to the CSF, with a subsequent decrease in the CSF flow compliance of both the brain (hydrocephalus) and the spinal cord (syringomyelia) [13].
Currently, most of the neurosurgeons agree on the need to operate hydrocephalus as a first step, although the reduction of the ventricular dilatation is followed by the persistence of the clinical signs and symptoms of CM-I in a certain number of cases [13]. Sharma et al. [14] proposed that if hydrocephalus arises from the fourth ventricle outflow obstruction from the malformation itself, then surgical decompression should result in resolution of hydrocephalus without additional unnecessary CSF diversion procedures.
Here, we report 4 representative cases and propose several indications for FVS, including redo-FMD after failure of the first operation, especially if the foramen of Magendie was re-occluded by arachnoid adhesions or a scar, the patency of the CSF circulation at the foramen magnum cannot be ensured after initial FMD due to predominant dura sinus or other reasons and with obstructive hydrocephalus.
FVS complications include dislodgement of the stent, which may result in syringomyelia recurrence, after which reoperation is needed [5,10]. Another was that the stent was either too long or firm to compress the extraocular nuclei or tracts in the upper fourth ventricle which led to fourth cranial nerve palsy and diplopia [5,15]. Nevertheless, no complication occurred in our study. Further follow is necessary.

Conclusion
FMD surgery with or without duraplasty and with or without excision of the tonsil remains the preferred treatment of CM-I. FVS is an effective and safe operation method for CM-1 in children. The indications of FVS include redo-FMD after failure of the first operation, especially after the foramen of Magendie had been re-occluded by arachnoid adhesions or a scar, the patency of the CSF circulation at the foramen magnum could not be ensured after FMD and with obstructive hydrocephalus. The complication of FVS including dislodgement of the stent and compression of fourth ventricle. FVS may not be the routine method and the indications should be taken seriously. A long-term follow-up duration is necessary.
Author contribution Peng Sun: conceptualization, methodology, investigation, writing original draft preparation, writing review and editing. Mading Zhou: data curation.Yutong Liu: investigation. Jianxin Du: supervision. Gao Zeng: conceptualization, writing review and editing, supervision. All authors have read and agreed to the published version of the manuscript.

Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Declarations
Ethics approval The present study was approved by the Ethics Committee of Xuanwu Hospital, Capital Medical University. All procedures were performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.
Consent to participate Written informed consent was obtained from the patients and their parents.