A Combined Transtemporal and High-parietal Approach for Large Intraventricular Trigone Meningioma: A Case Series and Review of the Literature

Abstract

The trigone of the lateral ventricle is deep and surrounded by eloquent gyri and subcortical fibers. Resection of intraventricular trigone tumors has therefore been challenging, and the optimal surgical approach to the trigone of the lateral ventricle remains controversial. Three patients with large intraventricular trigone meningioma (≥4 cm in diameter) underwent surgical excision using a combined transtemporal and high-parietal approach at Osaka City University Hospital between July 2016 and January 2021. Clinical and imaging studies, as well as surgical complications, were retrospectively reviewed based on medical records from our institution. We also reviewed 153 patients with intraventricular trigone meningioma from 11 reports in the literature and assessed pre- and postoperative symptoms. Gross total resection of the tumor was achieved in all cases. None of the patients showed deterioration of neurological symptoms at 3 months after tumor resection, although one patient experienced transient language dysfunction several weeks after surgery. No cases showed recurrence or required additional therapy. According to our literature review, postoperative visual field defects are more likely to persist than postoperative language dysfunction at 3 months postoperatively. In conclusion, combining the transtemporal and high-parietal approaches appears to be useful for treating large intraventricular trigone meningioma. Postoperative language dysfunction after resection of intraventricular trigone meningioma may tend to resolve more rapidly than postoperative visual field defect.

Introduction

Meningiomas are usually benign, slow-growing neoplasms that originate from meningothelial cells of the arachnoid layer, accounting for 13%-40% of primary brain tumors.^1-5) Intraventricular meningioma arises from the mesenchymal stroma of the choroid plexus, such as the arachnoid mater and tela choroidea, where meningothelial inclusion bodies are found.^1,6) Intraventricular meningiomas account for 0.5%-3.0% of all meningiomas and 9.8%-14% of all intraventricular tumors.^7,8) Twenty percent of intraventricular meningiomas are located in the lateral ventricle, of which 77.8% are in the trigone.^1,3,9)

Resection of a large intraventricular trigone meningioma is challenging because of its proximity to critical structures. However, the optimal approach to these lesions remains contentious. The transtemporal approach provides a short trajectory to access intraventricular trigone meningiomas and allows for the sacrifice of the main feeding vessel, particularly the anterior choroidal artery, at the initial stage of tumor resection. Conversely, this approach carries potential risks, including postoperative language dysfunction, visual field defects, and epilepsy. On the other hand, the high-parietal approach can avoid postoperative language dysfunction and visual field defects, but requires a long trajectory to access the intraventricular trigone meningioma and does not allow for the sacrifice of the feeding artery in the initial phase of tumor resection. We thus used both transtemporal and high-parietal approaches; the transtemporal approach was employed in the initial stage to sacrifice the feeding artery from the anterior choroidal artery, followed by the high-parietal approach for the actual tumor resection.

We describe herein 3 cases in which large intraventricular trigone meningiomas were surgically removed using combined transtemporal and high-parietal approaches. We assessed patient symptoms pre- and postoperatively. We also reviewed the literature on intraventricular trigone meningioma to assess the risk after tumor resection.

Materials and Methods

Three patients with large intraventricular trigone meningioma (≥4 cm in diameter)¹⁰⁾ underwent surgical excision via combined transtemporal and high-parietal approaches at Osaka City University Hospital between July 2016 and January 2021. Clinical and imaging studies, as well as surgical complications, were retrospectively reviewed based on the medical records at our institution.

The combined transtemporal and high-parietal approach

The patients were placed in the semi-prone park bench position. Tumor resection was performed via combined transtemporal and high-parietal approaches with the aid of a neuro-navigation system. A corticotomy approximately 1.5 cm in length was placed in the middle temporal gyrus about to reach the inferior horn of the lateral ventricle. After internal decompression of the tumor, the feeder from the choroidal artery was obliterated. Another corticotomy of about 1.5 cm was placed in the superior parietal lobule. Once access to the tumor was secured, the tumor was removed along the long axis of the surgical corridor. All patients achieved gross total resection of the tumor. Preoperative embolization of the lateral posterior choroidal artery was required in one patient.

Results

The 3 patients comprised 3 females, with a mean age of 59 years (range, 52-72 years). The tumor was recurrent in 2 cases, and 1 patient had a history of neurofibromatosis type 2.

Preoperative and postoperative symptoms and images

The characteristics of our 3 patients are shown in Table 1, and preoperative images are shown in Fig. 1. Our cohort included 2 patients with recurrence and another patient who had neurofibromatosis type 2. These 2 cases already showed neurological deficits after the previous surgery, including visual field defects. One patient experienced mild conduction aphasia postoperatively, but symptoms resolved within 3 months. No cases showed any new deficits at 3 months after surgery. Pathological diagnoses were fibrous meningioma, transitional meningioma, and meningothelial meningioma, respectively. No cases of recurrence were seen after tumor resection using the combined approach, and no patients needed additional therapy postoperatively.

Table 1

Demographic Characteristics of Patients Who Underwent Tumor Resection for Large Trigone Meningioma in Our Institution

Case	Age, sex	Pathology	Side	Maximum diameter (cm)/Volume (mL)	Virgin/recurrence	Preoperative embolization	Extent of resection	Blood loss (mL)/ Blood transfusion	Preoperative symptoms			Postoperative symptoms (1week/3months)			Follow-up (months)
									Visual	Language	Other symptoms	Visual	Verbal	Other symptoms
GTR: gross total resection
1	72 F	fibrous meningioma	left	5.6/66.1	recurrence	No	GTR	160/−	hemianopia	motor aphasia	hemiparesis	hemianopia/hemianopia	motor aphasia/motor aphasia	hemiparesis/hemiparesis	17.7
2	53 F	transitional meningioma	right	4.7/43.1	virgin	No	GTR	240/−	quadrant anopia	−	partial seizure	quadrantanopia/quadrantanopia	−/−	partial seizure/partial seizure	99.6
3	52 F	meningothelial meningioma	left	6.6/77.5	virgin	Yes	GTR	400/−	quadrant anopia	−	−	quadrantanopia/quadrantanopia	conduction aphasia/−	−/−	42.9

Fig. 1

Case 1. Preoperative and postoperative gadolinium-enhanced T1-weighted MRI and digital subtraction angiography. (A-C) Preoperatively, the tumor shows homogeneous enhancement (A, axial; B, coronal; C, sagittal). (D-F) Postoperative gadolinium-enhanced T1-weighted images after tumor resection via a combination of high parietal and transtemporal approaches did not show any residual tumor (D, axial; E, coronal). Preoperative digital subtraction angiography (F) reveals that the feeding arteries originate from the anterior choroidal artery.

Case 2. Pre and postoperative T2-weighted MRI and gadolinium-enhanced T1-weighted MRI. The tumor appears hyperintense on T2-weighted imaging (G, axial; I, sagittal). Coronal gadolinium-enhanced T1-weighted MRI shows slight heterogeneous enhancement (H, coronal). (J-L) Postoperative gadolinium-enhanced T1-weighted imaging after tumor resection via a combination of high parietal and transtemporal approaches did not show any residual tumor (J, axial; K, coronal; L, sagittal).

Case 3. Pre- and postoperative gadolinium-enhanced T1-weighted MRI (M-R) and digital subtraction angiography and skull X-ray photograph (S-X). M-O) Preoperatively, the tumor showed homogeneous enhancement (M, axial; N, coronal; O, sagittal). Postoperative gadolinium-enhanced T1-weighted imaging after tumor resection via a combination of high parietal and transtemporal approaches did not show any residual tumor (P, axial; Q, coronal; R, sagittal). Preoperative digital subtraction angiography (S-T), the feeding arteries were the anterior choroidal artery and the lateral posterior choroidal artery (white arrow). Digital subtraction angiography after endovascular treatment revealed that the feeding arteries had disappeared (U-V).

MRI: magnetic resonance imaging

Illustrative case

A left intraventricular trigone meningioma was discovered in a 52-year-old woman after she experienced headache and anomia (case 3, Fig. 1M-O). She showed homonymous quadrantanopia of the right lower quadrant and mild cognitive dysfunction. Scores for the revised Hasegawa Dementia Rating Scale, Mini-Mental State Examination, and Frontal Assessment Battery were 22, 20, and 13, respectively. The Wechsler Adult Intelligence Scale, 3rd edition (WAIS-III) and Wechsler Memory Scale-Revised (WMS-R) showed mild disturbance of working memory. WAIS-III results were as follows: Verbal Intelligence Quotient, 92; Performance Intelligence Quotient, 72; Full Intelligence Quotient, 81; Verbal Comprehension, 92; Working Memory, 72; Perceptual Organization, 75; and Processing Speed, 72. WMS-R results were as follows: Verbal Memory, 73; Visual Memory, 96; General Memory, 77; Attention / Concentration, 83; and Delayed Recall, 56. The Standard Language Test of Aphasia showed slight deteriorations in reading and calculation. The patient did not show unilateral spatial neglect.

The patient underwent feeder embolization 5 days prior to the surgical tumor removal. Because the anterior choroidal artery and lateral posterior choroidal artery supplied blood to the tumor (Fig. 1S and T), we performed coil embolization from the lateral posterior choroidal artery. Finally, the tumor stain from the lateral posterior choroidal artery had disappeared (Fig. 1U-X). Tumor resection was performed via combined transtemporal and high-parietal approaches, and we achieved gross total removal of the tumor (Fig. 1P-R). The pathological diagnosis was meningothelial meningioma. The patient experienced conduction aphasia for several weeks after tumor removal, but symptoms resolved within 3 months after surgery. The scores of WAIS-III and WMS-R evaluated about 13 months after tumor resection were improved, except for Verbal Intelligence Quotient and Verbal Comprehension. Postoperative WAIS-III results were as follows: Verbal Intelligence Quotient, 85; Performance Intelligence Quotient, 94; Full Intelligence Quotient, 88; Verbal Comprehension, 88; Working Memory, 88; Perceptual Organization, 91; and Processing Speed, 89. Postoperative WMS-R results were as follows: Verbal Memory, 97; Visual Memory, 98; General Memory, 96; Attention / Concentration, 92; and Delayed Recall, 94. The tumor has not recurred for 3.5 years.

Review of the literature on intraventricular trigone meningioma

We reviewed the literature between 2005 and 2021 using PubMed to clarify preoperative and postoperative symptoms after resection of intraventricular trigone meningioma by using the terms "trigone meningioma, trigonal meningioma, intraventricular meningioma, or ventricular meningioma". We excluded reports in which the tumor location could not be confirmed as the trigone, or in which both pre and postoperative symptoms were not clearly described. Finally, a total of 153 patients from 11 reports were reviewed.^11-21)

Table 2 shows pre and postoperative symptoms of patients with intraventricular trigone meningioma. The most common symptoms seen before tumor resection in patients with intraventricular trigone meningioma were increased intracranial pressure (ICP) (51.0%), followed by visual field defect (17.6%), language dysfunction (13.1%), and paralysis (12.4%). Preoperative ICP (51.0%), cognitive dysfunction (9.2%), and sensory disturbance (3.3%) all completely resolved after tumor resection. All but one patient (88.9%) showed resolution of preoperative epilepsy after tumor resection. Language dysfunction improved in 60.0% of patients compared to preoperatively, but remained the same or worsened in 40.0% of patients. Thirteen (48.1%) of the 27 patients who experienced visual field defect preoperatively showed postoperative improvement, whereas the remaining 14 (51.9%) did not. Preoperative paralysis (12.4%) tended to remain (57.9%) or worsen (10.5%) after tumor resection (Table 2). Among patients who experienced new symptoms after tumor resection, language dysfunction identified at 1 week after surgery tended to be transient (82.8%), whereas about 72.7% of visual field defects, about 66.7% of paralysis, and all cases of epilepsy seen at 1 week after tumor resection had not improved by 3 months after surgery (Table 3).

Table 2

Review of 153 Patients Identified from 11 Reports in the Literature Regarding Changes in Preoperative Symptoms after Tumor Resection

Symptoms	Preoperative symptoms	Postoperative symptoms
		Improved	Stable	Deteriorated
ICP: intracranial pressure
Language dysfunction	20 (13.1%)	12 (60.0%)	7 (35.0%)	1 (5.0%)
Cognitive dysfunction	14 (9.2%)	14 (100%)	0 (0%)	0 (0%)
Visual field defect	27 (17.6%)	13 (48.1%)	14 (51.9%)	0 (0%)
Paralysis	19 (12.4%)	6 (31.6%)	11 (57.9%)	2 (10.5%)
Epilepsy	9 (5.9%)	8 (88.9%)	1 (11.1%)	0 (0%)
Sensory dysfunction	5 (3.3%)	5 (100%)	0 (0%)	0 (0%)
Increased ICP	78 (51.0%)	78 (100%)	0 (0%)	0 (0%)

Table 3

Review of 153 Patients Identified from 11 Reports in the Literature Regarding Changes in New Postoperative Symptoms at 1 Week and 3 Months after Tumor Resection

Symptoms	New postoperative symptoms
	1 week after tumor resection	3 months after tumor resection
ICP: intracranial pressure
Language dysfunction	29 (19.0%)	5 (3.3%)
Cognitive dysfunction	2 (1.3%)	0 (0%)
Visual field defect	11 (7.2%)	8 (5.2%)
Paralysis	6 (3.9%)	4 (2.6%)
Epilepsy	3 (2.0%)	3 (2.0%)
Sensory dysfunction	0 (0%)	0 (0%)
Increased ICP	0 (0%)	0 (0%)

Discussion

Intraventricular trigone meningiomas may grow very large before being diagnosed.²²⁾ Gross total removal of the tumor is the gold standard of management for intraventricular meningiomas because the recurrence and mortality rates are lower than those seen in other locations.²³⁾ Intraventricular trigone meningiomas are mainly supplied by branches of the anterior and posterior choroidal arteries,^24,25) but the feeders are sometimes relatively difficult to manage because the trigone of the lateral ventricle is deeply seated and also surrounded by eloquent gyri and subcortical fibers. The optimal surgical approach to remove intraventricular trigone meningioma and the usefulness of preoperative embolization thus remain contentious issues.

Approaches to intraventricular trigone meningioma

To access intraventricular trigone meningioma, many approaches have been considered so far, such as the transtemporal approach,¹⁴⁾ high-parietal approach,¹⁷⁾ trans-sylvian approach, occipital interhemispheric approach,^15,18,19,26) and transcallosal approach.^{1,16,20,21,27-31)} The most popular are the high-parietal and transtemporal approaches,^1,10,16) although minimally invasive techniques using a transsulcal or transcortical approach with a tubular retractor system have recently been reported.^10,32)

The high-parietal approach offers good overall access to the tumor and carries a low risk of damage to subcortical fibers such as the arcuate fascicle,²⁴⁾ inferior fronto-occipital fascicle, and optic radiation, but encounters difficulty in accessing the feeder at the initial stage of tumor resection.^1,10,16) We performed the corticotomy at the superior parietal lobule, rather than the supramarginal or angular gyrus, to prevent postoperative language dysfunction and Gerstmann's syndrome in the dominant hemisphere, and spatial neglect in the non-dominant hemisphere. The transtemporal approach provides the shortest trajectory to the tumor and allows earlier obliteration of the feeding artery from the choroidal arteries,¹⁶⁾ but shows a much higher risk of direct damage to the inferior portion of the optic radiation. A look-up surgical corridor is also difficult to obtain without excessive retraction of normal brain tissue.³³⁾

The earlier sacrifice of the feeding artery from the choroidal artery could allow the safe removal of large intraventricular trigone meningioma.²⁵⁾ However, if we access the tumor only via a transtemporal approach, removing the superior part of the tumor becomes difficult. We have thus combined the transtemporal and high-parietal approaches for large intraventricular trigone meningiomas. After obliterating the feeding artery using the transtemporal approach, we safely removed the tumor using the high-parietal approach. For example, our patient (case 1) had not achieved gross total resection of the tumor at the previous hospital because it was difficult to control bleeding. According to preoperative digital subtraction angiography, tumor stain from the anterior choroidal artery was evident (Fig. 1F); thus, we chose to combine the transtemporal and high-parietal approaches. In the current study, no patients showed any postoperative deterioration of visual field defect, probably because our combined transtemporal and high-parietal approaches reduced retraction of the temporal lobe and optic radiation. To the best of our knowledge, only one previous case report has mentioned combining transtemporal and high-parietal approaches to remove an intraventricular trigone meningioma.³⁴⁾

Preoperative embolization of the choroidal artery and intraoperative blood loss

Postoperative mortality with intraventricular meningiomas appears mainly due to hematoma in the surgical bed.²³⁾ Two reports in the literature focused on blood loss during the removal of intraventricular trigone meningioma.^13,25) Yamao et al.²⁵⁾ performed preoperative obliteration of feeders, whereas Ma et al.¹³⁾ did not. Mean blood loss was 253 mL with the former,²⁵⁾ and 530 mL with the latter.¹³⁾ In our 3 cases, mean blood loss was 266 mL. These findings suggest that preoperative or earlier obliteration of the feeding artery could reduce intraoperative blood loss volume and lower the risk of postoperative hemorrhage.

Review of preoperative and postoperative symptoms of intraventricular trigone meningioma

Most (79.1%) preoperative symptoms improved at 3 months after tumor resection, while 19.2% were stable and 1.74% showed deterioration. Preoperatively increased ICP, cognitive dysfunction, and sensory disturbance tended to disappear after tumor removal, whereas visual field defects, paralysis, and language dysfunction tended to remain. On the other hand, 82.8% of language dysfunction symptoms evident at 1 week after tumor resection were transient, while about 72.7% of visual field defects, about 66.7% of paralysis symptoms, and all cases of epilepsy present at 1 week after tumor resection had not improved by 3 months postoperatively among patients who experienced new symptoms after tumor resection. Because newly occurring postoperative visual field defects tend to persist, selecting an appropriate surgical corridor using a transtemporal approach is important to prevent postoperative visual field defects, particularly homonymous hemianopia.

According to our review of the literature (Table 2), 9 (5.9%) of the 153 cases displayed preoperative epilepsy. In all but one case among these patients with preoperative seizures, epilepsy disappeared after tumor resection without the use of antiepileptic drugs. Three cases experienced a new onset of epilepsy postoperatively and required antiepileptic drugs. Although 2 reports suggested that more than 2 corticotomies in the same operation could increase the risk of postoperative epilepsy, one study specifically examined the relevance of corticotomy to postoperative epilepsy among children.³⁵⁾ They concluded that the size of the corticotomy did not represent a risk factor for postoperative epilepsy. Furthermore, to the best of our knowledge, no studies have reported on the risk of postoperative epilepsy after multiple corticotomies. Recently, Hoz et al.³⁶⁾ reviewed 2,604 patients who underwent transcortical approaches. They reported that the transcortical approach carried a potential risk of postoperative epilepsy, accounting for nearly 20%.³⁶⁾ It is important to recognize that multiple corticotomies may increase the rate of postoperative epilepsy, although 2 out of 3 patients did not experience postoperative epilepsy in the current study. Furthermore, we may need to evaluate the risk of bleeding during tumor resection and consider avoiding multiple corticotomies in the future.

Some limitations to this study need to be kept in mind when interpreting the results. First, we have reported on our experiences with 3 cases of large intraventricular trigone meningioma using combined transtemporal and high-parietal approaches. Further study with a larger cohort is clearly important to validate the extent of resection and pre- and postoperative neurological deficits of combined transtemporal and high-parietal approaches for large intraventricular trigone meningioma. Second, as meningioma usually occurs in adult cases, we need to consider the relationship between epilepsy and the use of multiple corticotomies in adult cases.

Conclusion

Combining high-parietal and transtemporal approaches appeared useful in the treatment of large intraventricular trigone meningioma. The advantages of this combined approach over other approaches include devascularization in the early stage of tumor removal, less retraction on the optic radiations, and safer achievement of gross total removal, although multiple corticotomies carry a potential risk of postoperative epilepsy.

In terms of pre and postoperative symptoms, language dysfunction tended to improve more than visual field defect.

Availability of Date and Materials

Data in support of the current study are available from the corresponding author on reasonable request.

Consent for Publication

All authors have approved the manuscript and agree with publication.

Ethics Approval

This study was approved by the institutional review board at the Graduate School of Medicine, Osaka City University (approval number 2020-296).

Conflicts of Interest Disclosure

All authors have no conflicts of interest.

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