Analysis of single-staged resection of a fourth ventricular tumor via a combined infratentorial-supracerebellar and telovelar approach: Case report and review of the literature

Abstract

INTRODUCTION

The authors explore a combined infratentorial-supracerebellar and telovelar approach in an adult, while avoiding vermian-splitting methods for a large, midline, fourth-ventricular tumor, unapproachable though a single traditional route. Experience with a combined surgical approach for pediatric patients has been published, but the authors believe that describing this combined method in an adult will provide a preliminary experience for further exploration of this approach in other adult patients.

PRESENTATION OF CASE

The authors present a review of the literature along with the case of a 60-year-old man with slight ataxia who presented with a 1-month history of gait difficulty and memory lapse. His MRI of the brain showed mild hydrocephalus and a large tumor of the fourth ventricle. Surgical removal through a suboccipital craniotomy was attempted, and part of the tumor overlying the tectum and the superior cerebellar velum was removed without difficulty. However, despite inferior retraction of the vermis, which allowed further resection of the tumor from the fourth ventricle, residual tumor in the caudal surgical resection cavity was present. Partial transection of the vermis was considered, but avoided because of potential neurological deficits. Instead, the authors redirected their approach and exposed the residual tumor by transecting the inferior medullary velum and removed additional tumor while avoiding the floor of the fourth ventricle. The infratentorial-supracerebellar and telovelar approach resulted in total gross resection of the tumor.

DISCUSSION

For patients with large midline tumors that arise from the superior vermis or the quadrigeminal plate and fill the upper third of the fourth ventricular space, this combined approach may offer a unique possibility of safe tumor removal.

CONCLUSION

This case demonstrates the benefit of a combined approach for a select group of patients.

1. Introduction

Approaching the fourth ventricle surgically is particularly challenging due to the limited working space provided by the important surrounding cerebrovascular structures. Its close relationship to the surrounding neural structures, including the brainstem and cerebellum, is the major limitation for surgical access. Various surgical routes to the fourth ventricular space have been described in the literature, including the conventional transvermian approach. Recent clinical and anatomical studies have suggested that the telovelar approach through dissection of the cerebellomedullary fissure and incision of the tela choroidea and the inferior medullary velum (two thin layers of tissue forming the lower half of the roof of the fourth ventricle) will maximize the extent of surgical exposure and working angle while minimizing operative morbidity.^1–3 In addition, transforaminal and subtonsillar approaches provide additional access routes by dissection along natural avascular planes. Retrosigmoid or far-lateral transcondylar routes may also permit entry into the fourth ventricle under special circumstances when the tumor has already created the surgical pathway (“transtumoral” corridor) through the lateral brainstem parenchyma.^1,3

Recently, Hermann et al.⁴ published a case series of 4 pediatric patients with giant midline posterior fossa tumors involving the fourth ventricle and tectal region. These authors achieved complete tumor resection in two patients and near-total tumor removal in the other two through a combined transventricular telovelar and supracerebellar-infratentorial approach. No new neurologic deficit occurred postoperatively. Adult patients do not typically present with giant tumors, but large tumors in this patient population present significant technical challenges. To explore such a combined surgical approach in an adult while avoiding vermian-splitting methods for a large, midline, fourth-ventricular tumor that is unapproachable though a single traditional route, we present the case of a large fourth ventricle tumor with associated hydrocephalus. Gross total tumor resection was achieved in one stage through an infratentorial-supracerebellar approach for the superior and a subsequent telovelar approach for the inferior portions of the tumor.

2. Illustrative case

A 60-year-old man presented with a 1-month history of gait difficulty and memory lapse. Except for slight ataxia, his neurologic examination was otherwise unremarkable. An MRI of the brain demonstrated a relatively large fourth ventricular tumor and mild hydrocephalus (Fig. 1a–c). Differential diagnosis for this lesion included a choroid plexus papilloma, a meningioma, and a metastatic lesion. Diagnostic tests for brain metastasis, including a chest, abdominal, and pelvic CT scan, were unremarkable.

Fig. 1.

The preoperative brain MRI of our patient with a 1-month history of gait difficulty and memory lapse demonstrates an inhomogenously enhancing fourth ventricular tumor with mild hydrocephalus. (a) Gadolinium-enhanced midline sagittal T1-weighted image. (b) Gadolinium-enhanced axial T1-weighted image at the level of the upper pons. (c) Gadolinium-enhanced axial T1-weighted image at the level of the lower pons.

Surgical removal through a suboccipital craniotomy was attempted while the patient was in a lateral position on his right side with his head turned away from the surgeon. A wide bilateral suboccipital bony removal extended from the transverse sinus through the foramen magnum was performed. C1 laminectomy was not deemed necessary (Fig. 2a–e). After opening of the dura over the cerebellum, a bridging vein underneath the tentorium and the central vein traveling over the cerebellum were identified, cauterized, and transected. Dissection over the superior portion of the cerebellum in the midline and slightly to the right side allowed identification of the tumor that was protruding through the anterior portion of the vermis; the tumor did not significantly invade the surrounding brain parenchyma (Fig. 2b). Due to the somewhat fibrous nature of the tumor, its excision through the suction apparatus was not readily possible. Portions of the tumor overlying the tectum and the superior cerebellar velum were removed without difficulty in piecemeal fashion.

Fig. 2.

Intraoperative microscopic images obtained during the procedure while the patient was placed in a lateral position with his right side down. A suboccipital craniotomy was performed and the dura of the posterior fossa was reflected over the dural sinus (star in panel a). A supracerebellar-infratentorial approach allowed exposure of tentorium (star) and tumor at the edge of the retractor (b). Despite inferior retraction on the vermis, there was residual tumor (star) in the caudal surgical resection cavity (c). Via a telovelar approach, the floor of the fourth ventricle (star) and the inferior edge of the residual tumor were identified (d). The floor of the fourth ventricle (star) was preserved after completion of tumor resection (e).

Further inspection and gentle inferior retraction of the vermis allowed resection of additional tumor into the fourth ventricle. Despite this maneuver, residual tumor in the caudal surgical resection cavity was present (Fig. 2c). Partial transection of the vermis was contemplated to increase further exposure of the inferior aspect of the tumor into the fourth ventricle. Due to the possible neurologic deficits associated with transecting the normal vermis, we avoided such a maneuver and instead changed and redirected the surgical corridor to approach the residual tumor through an inferior trajectory. The inferior medullary velum was transected and the floor of the fourth ventricle identified. This additional exposure, with gentle retraction of the vermis and cerebellum superiorly, readily allowed identification of the inferior edge of the residual tumor in the fourth ventricle (Fig. 2d). Additional tumor removal was possible and the floor of the fourth ventricle was carefully avoided. Return of clear fluid from the superior resection cavity into the inferior resection cavity assured communication of both resection routes (Fig. 2e).

This combined infratentorial-supracerebellar and telovelar approach accomplished gross total resection of the tumor (Fig. 3a–c). The patient tolerated the procedure well with no neurologic complications. The final pathological diagnosis was consistent with a metastatic prostate adenocarcinoma. He underwent additional staging imaging studies and ultimately adjuvant therapies.

Fig. 3.

Postoperative MRI of the brain demonstrating complete resection of the fourth ventricular tumor. (a) Gadolinium-enhanced midline sagittal T1-weighted image. (b) Gadolinium-enhanced axial T1-weighted image at the level of the midbrain. (c) Gadolinium-enhanced axial T1-weighted image at the level of the pons.

3. Discussion

The combination of infratentorial-supracerebellar and telovelar approaches for the resection of tumors affecting the fourth ventricle and related neuronal structures carries its associated risks. Approach-related complications include venous infarction due to sacrifice of subtentorial bridging veins and retraction injury of the cerebellum. Nevertheless, for patients with large midline tumors that arise from the superior vermis or the quadrigeminal plate and fill the upper third of the fourth ventricular space, this combined approach may offer a unique possibility of safe tumor removal.

As mentioned above, Hermann et al.⁴ recently published their experience with the combined approach for a series of four pediatric patients with giant posterior fossa midline tumors. We attempted a similar method in an adult. Since neurosurgical procedures in adults and children present challenges that are unique to each group, we believe description of this combined method in an adult will provide a preliminary experience for further exploration of this approach in other adult patients.

Piatt and Kellogg⁵ presented two pediatric patients who had tumors involving the superior vermis and filling the fourth ventricle. Both patients underwent combined infratentorial-supracerebellar and cerebellomedullary fissure approaches. The first patient died on the sixth postoperative day due to a massive cerebellar hemorrhagic infarction after a bilateral cerebellar exposure. In the second patient, a unilateral exposure resulted in a protracted postoperative course characterized by suboccipital pain, torticollis, feeding difficulties, and persisting hydrocephalus.

The cerebellum has three major classes of bridging veins, namely Galenic, tentorial, and petrosal. According to Piatt and Kellogg,⁵ simultaneous compromise of different bridging veins provoked by their surgical procedure resulted in venous insufficiency and infarction. In a supracerebellar approach, petrosal bridging veins most commonly compensate for sacrificed Galenic and tentorial systems. Addition of the telovelar approach risks this collateral venous drainage through the petrosal system and may lead to serious venous insufficiency.⁵ Koziarski et al.⁶ presented a somewhat similar case of an adult women suffering from a tectal and periaqueductal glioma. Her tumor was removed in one stage, partially via an infratentorial supracerebellar approach. The remainder was removed through access to the fourth ventricle and cerebral aqueduct. Postoperatively, the patient had bilateral ptosis and ocular disturbances which improved within 1 year.

Although the etiology and exact location of the tumors differ in all the presented cases, they all offer insight into risks and benefits of combined surgical approaches in this particular region. Indications for the infratentorial supracerebellar approach are numerous; it is a popular surgical technique for exposure of lesions in the pineal region or the superior vermis, the posterior third ventricle, and other regional structures.^5,7,8

The dissection of the cerebellomedullary fissure and incision of the tela choroidea and inferior medullary velum, commonly referred to as the telovelar approach, has recently gained attention as the preferred route for accessing lesions of the inferior fourth ventricle. Microsurgically, the major advantage of this access over the transvermian approach is the lack of necessity of splitting the vermis or removing parts of the cerebellum.^9–11 Preoperative identification of the cerebellomedullary fissure on MRI imaging as a landmark for fourth ventricular surgery aids in planning the telovelar approach and predicting pathological tumor anatomy.¹²

Clinical and anatomical cadaver studies have both demonstrated the superiority of the telovelar over the transvermian approach. In terms of morbidity, El-Bahy² presented 16 cases of different fourth ventricular tumors removed via the telovelar approach with no patient suffering from cerebellar mutism postoperatively. In all cases, the telovelar approach provided sufficient access for resection, limited only by the pathological nature of the tumor and infiltration of the surrounding neural structures.² Extensive aqueductal opening, consisting of dissection of the uvulotonsillar and medullotonsillar spaces bilaterally and incisions of teniae and the posterior margins of the lateral recesses, as reported by Matsushima et al.¹² for 19 cases, was not necessary. Kumabe et al.¹³ operated on five choroid plexus tumors of the fourth ventricle through the telovelar approach. In their experience, the major limiting factor for respectability was tumor infiltration and not the chosen route of access.

Rajesh et al.³ also reported removal of large fourth ventricular tumors. Fifteen patients were treated via the telovelar approach. Based on their experience, due to distortion of the normal anatomy by large adherent tumors and consequential difficulties in dissecting the normal avascular planes, initial decompression should precede aggressive resection. Comparably, these authors had a relatively high incidence of neurological deficits postoperatively. These deficits were attributed to the extent by which the tumor stretched the uvulotonsillar cleft, retraction injury to the dentate nucleus, and ischemic vascular injury.³

Unfortunately, neither El-Bahy² nor Rajesh et al.³ gave clear criteria of what they considered to be a large fourth ventricular tumor; this factor prevents a reasonable comparison of their results. In addition to the above clinical reports, Deshmukh et al.¹ published a well-designed cadaveric study quantifying and comparing telovelar and transvermian approaches. According to their investigation, the telovelar approach, augmented by additional C1 arch removal, provided a significantly larger working area. Horizontal working angles at all levels of the fourth ventricle, including at the obex and the lateral and rostral portions of this ventricle, were significantly greater in comparison to those of the transvermian approach. The unique advantage of the transvermian over the telovelar approach was the fact that the transvermian approach provided a greater vertical working angle for the rostral part of the ventricle. This advantage was nullified when C1 laminectomy was added to the telovelar approach.^1,3

Although the above mentioned approaches facilitate removal of the tumors in the lower portions of the fourth ventricle, the tumors located in the upper portions of this ventricle remain difficult to reach without transecting at least a portion of the vermis. Because of the reported neurologic risks associated with transecting an intact vermis, the literature advises against injury to this structure to gain exposure, if possible. Complications resulting from transection of the vermis include caudal vermis syndrome and transient cerebellar mutism. Caudal vermis syndrome is linked to disturbances of equilibrium and balance manifesting as truncal ataxia, gait disturbances, oscillation of the head and neck, and nystagmus.¹ Transient cerebellar mutism in conjunction with oral apraxia may occur.^1,2

4. Conclusions

A small select group of patients with surgical pathologies that may not be safely approached through a single exposure, either the telovelar or the supracerebellar-infratentorial approach, might benefit from the combined approach reported herein. The location of the lesion will dictate which approach will be first attempted.

Conflict of interest statement

None.

Funding

None.

Ethical approval

Written informed consent was obtained from the patient for publication of this case report and accompanying images. A copy of the written consent is available for review by the Editor-in-Chief of this journal on request.

Authors’ contributions

All authors participated in gathering and interpretation of data, study design, drafting and revising the article, approval of final manuscript for submission.