Minimally Invasive Approaches in the Surgical Treatment of Intracranial Meningiomas: An Analysis of 54 Cases

Abstract

Background

Intracranial meningiomas, being a fairly common disease in the population, often require surgical treatment, which, in turn, can completely heal the patient. The localization of meningiomas often influences treatment even if they are asymptomatic. By modernizing approaches to surgical treatment, it is possible to minimize intra- and postoperative risks, while achieving complete removal of the tumor. One of these methods is minimally invasive neurosurgery, the development of which in recent years allows it to compete with standard surgical methods. The purpose of this study was the objectification of minimally invasive approaches, such as the calculation of the craniotomy area and the ratio of craniotomy area to the resected tumor volume.

Methods

The retrospective study consisted of a group of 54 consecutive patients who were operated on in our neurosurgery clinic specialized on minimally invasive neurosurgery. Preoperative planning was carried out using the Surgical Theater visualization platform. Using this system, the tumor volume and craniotomy surface area were calculated. During the analysis, the symptoms before and after the surgery, classification of tumors, postoperative complications, further treatment and follow-up results were assessed.

Results

Twelve (22.2%) patients were men and 42 (77.8%) were women. The mean age of the group was 64.2 years (median 67.5). The craniotomy area ranged from 202 to 2,108 mm² (mean 631 mm²). Tumor volume ranged from 0.85 to 110.1 cm³ (mean 21.6 cm³). The craniotomy size of minimally invasive approaches to the skull base was 3–5 times smaller than standard approaches. Skull base meningiomas accounted for 19 cases (35.2%), convexity meningiomas for 26 cases (48.1%), and falx and tentorium meningiomas for 9 cases (16.7%). Three complications were reported: postoperative hemorrhage, CSF leakage, and ophthalmoplegia. Relapse was detected in 2 patients with a mean follow-up of 26.3 months (median 20).

Conclusion

Minimally invasive approaches in the surgical treatment of intracranial meningiomas reduce the possibility of operating trauma by several times; they are safe and sufficient for complete removal of the tumor.

INTRODUCTION

Meningiomas are often benign, slow-growing, and usually noninfiltrating tumors of derived from meningothelial cells, which account for about 37.6% of central nervous system tumors [1,2]. The incidence in the population, according to various sources, ranges from 1.5 to 9 per 100,000 population [3,4,5,6]. Most of them are intracranial meningiomas (about 80%) [7], which are the most common intracranial tumors (37.1%) [4,8]. Old age, genetic predisposition, and ionizing radiation are known to be risk factors for the development of meningiomas [4]. There is also evidence that female sex hormones can influence the pathogenesis, which explains the higher incidence in women compared to men: 2.3 to 1 [9,10].

Meningiomas are usually asymptomatic and manifest themselves in case of large size, contact with eloquent regions of the brain or surrounding edema. Therefore, symptomatic skull base meningiomas are much smaller than convexital meningiomas. Various studies show a prevalence of asymptomatic meningiomas of about 1% in the population [11,12,13].

The growth rate of meningiomas is usually slow, so they often remain asymptomatic [14,15]. This explains the fact that 50% of these tumors are found at autopsy [2], with most of them with a size of no more than 1 cm in diameter [15].

There are several classifications of meningiomas: by localization (skull base, convexital, falxial, parasagittal, and intraventricular meningiomas) [16,17], WHO classification (WHO I–III) [18], Simpson classification (Grade I–V) [19].

Intracranial meningiomas are often asymptomatic. With a certain volume and/or localization as well as surrounding edema, meningiomas manifest themselves symptomatically. The most common symptoms are headache [20,21], dizziness [21,22], cognitive disorders [23], focal neurological symptoms [22,24], and convulsive seizures [25,26,27].

When a meningioma is detected, the following questions should be answered [28]:

• · Does the location of meningioma correlate with clinical symptoms?

• · Can existing symptoms be reduced by surgical treatment?

• · Is there a preponderance of surgical treatment benefits in comparison with surgical risks?

If the answer to these questions is negative, observation is recommended [28].

Surgery is the treatment of choice for most meningiomas [28,29,30,31]. It has a dual role: removal of additional intracranial volume, reducing symptoms, and also providing material for histological examination. The tactics of further treatment is determined on the basis of histology.

Summarizing the available information, intracranial meningiomas, being a fairly common disease in the population, often require surgical treatment, which, in turn, can completely cure the patient. In the case of incomplete resection or malignancy of the tumor, radiation therapy has shown good results. Neurosurgical operation is the main method of treatment, and its implementation significantly affects both the quality and life time of the patient.

Thus, by modernizing approaches to surgical treatment, it is possible to minimize intra- and postoperative risks, while achieving complete tumor removal. One of these methods is minimally invasive neurosurgical tumor removal [32], the development which in recent years allows it to compete with standard neurosurgical methods.

To date, there are many studies on the surgical treatment of intracranial meningiomas. However, we have not found any studies that include measurements of the surgical approach size in relation to the volume of the operated tumor. Taking into account the fact that our clinic has accumulated extensive experience in the use of minimally invasive approaches, we have decided to perform a retrospective study and objectify the possibilities of “keyhole” approaches in order to clearly show the differences from standard craniotomies.

MATERIALS AND METHODS

The retrospective study consisted of a group of consecutive patients who were operated on in our neurosurgery clinic specialized on minimally invasive neurosurgery from 2015 to 2021 and who already had at least one postoperative 3 months follow-up MRI at the time of the study group analysis.

The exception was: 1) Tumors recurrences that have not been previously operated on in our clinic; 2) Multiple meningiomas. In this case, it is difficult to assess the effect of surgical treatment, which is often a part of a complex therapy, including radiation therapy and peptide receptor radionuclide therapy (PRRT) [28,33]; and 3) The en-plaque meningiomas, which also require a combined approach to treatment in some cases. This is the only exception where large accesses are required to remove the tumor. However, these meningiomas are rare [34].

All patients were operated using minimally invasive surgical approaches. This means that we used such small approaches that were not only smaller than the standard ones, but also sufficient for complete tumor resection. These are keyhole approaches for skull base meningiomas and smaller craniotomies compared to the dural base of the tumor.

Preoperative planning was carried out using the Surgical Theater visualization platform (Surgical Theater, Los Angeles, CA, USA). By using this system, the volume of the tumor and the surface area of the craniotomy were also calculated.

The main objective of this study was the objectification of minimally invasive approaches, such as the calculation of trepanation area and the trepanation area to the volume of the resected tumor ratio.

When we compared minimally invasive approaches to the skull base (pterional and retrosigmoid) with standard approaches, a standard approach was simulated in the Surgical Theater for the same patient and compared with a minimally invasive approach that we performed.

In the process of retrospective analysis, clinical symptoms before and after surgery, histological (WHO) and surgical (Simpson) classification, postoperative complications, further treatment, and follow-up were also assessed.

Statistical data processing was carried out using nonparametric methods in SPSS Statistics (Version 23.0; IBM Corp., Armonk, NY, USA).

The study was approved by the local ethics committee (IRB approval number 22-57-Br). Informed consent was obtained from all individual participants included in this study.

RESULTS

The study group consisted of 54 patients operated, 12 (22.2%) patients were men and 42 (77.8%) were women. The mean age of the group was 64.2 years. The predominant localization of meningiomas was the convexity (48.1%), more often in the frontal and parietal regions. Skull base meningiomas accounted for 35.2%, more often in the anterior cerebral fossa. In all cases, a total resection of the tumor was performed, with Simpson Grade I in 9 (16.7%) cases and Simpson Grade II in 45 (83.3%) cases. According to histological classification, most meningiomas were WHO I (75.9%), WHO II accounted for 22.2%, and 1 case (1.9%) was WHO III (Table 1).

Table 1. Summary of characteristics of the study group of patients.

Variable			Value (n=54)
Age (yr), mean/median			64.2/67.5
Sex
	Male		12 (22.2)
	Female		42 (77.8)
Clinical feature
	Headache		18 (33.3)
	Seizure		14 (25.9)
	Focal neurologic symptoms		17 (31.5)
		Paresis/hypoesthesia	4 (7.4)
		Cerebellar dysfunction	5 (9.3)
		Dysphasia/aphasia	5 (9.3)
		Vision imprairment	3 (5.6)
	Other (incidental findings)		5 (9.3)
		Tumor progression	2 (3.7)
		Localization	2 (3.7)
		Traumatic brain injury	1 (1.9)
Tumor location
	Skull base		19 (35.2)
		Anterior fossa	14 (25.9)
		Middle fossa	0 (0)
		Posterior fossa	5 (9.3)
	Convexity		26 (48.1)
		Frontal	12 (22.2)
		Parietal	8 (14.8)
		Temporal	1 (1.9)
		Occipital	4 (7.4)
		Cerebellum	1 (1.9)
	Falx		6 (11.1)
	Tentorium		3 (5.6)
WHO grade
	I		41 (75.9)
	II		12 (22.2)
	III		1 (1.9)
Simpson grade
	I		9 (16.7)
	II		45 (83.3)
Complication
	Postoperative hemorrhage		1 (1.9)
	CSF leakage		1 (1.9)
	Ophthalmoplegia		1 (1.9)

Values are presented as n (%). CSF, cerebrospinal fluid

The main symptoms were chronic headaches (33.3%). As a rule, these patients had sufficiently large tumors, so the indications for surgery were clear. Only in 2 patients, the tumor was observed for several years and then operated on due to progression. A fairly common acute symptom is epileptic seizures, which were reported in 14 (25.9%) patients. Of these, in 2 cases the seizures were focal and in 12 they were generalized. Focal neurological symptoms were present in 17 patients (31.5%), which corresponded to the localization of the tumor.

Minimally invasive approach

Carrying out the operation through a minimally invasive approach requires careful planning. The Surgical Theater visualization platform (Surgical Theater, Los Angeles, CA, USA) played a big role in this part preparation for surgery. It was possible to choose the optimal approach in terms of size, as well as to study the anatomical location of the tumor with it. The available MRI and CT scans were used. The mean craniotomy size was 631 mm² (Fig. 1, Supplementary Video 1 in the online-only Data Supplement). At the same time, the craniotomy size to skull base tumors (retromastoid, suboccipital, pterional [Fig. 2, Supplementary Video 2 in the online-only Data Supplement], supraorbital approaches) did not differ much from the size of the approach to convexity tumors (Table 2). The volume of the tumor averaged 21.6 cm³. Fig. 3 shows the ratio of the craniotomy size compared to the actual tumor volume.

Fig. 1. A 49-year-old female patient with headaches and homonymous hemianopsia on the right for several months. A: Preoperative T1 weighted image with contrast agent in the axial plane. B: Planning the minimally invasive approach. C: The actual size of the craniotomy (on postoperative images).

Fig. 2. A 74-year-old female patient who was diagnosed with a sphenoid wing tumor on the right after suffering a generalized epileptic seizure. A: Preoperative T1 weighted image with contrast agent in the axial plane. B: Standard pterional approach. C: Planned minimally invasive pterional approach. D: Postoperative MRI 3 months later.

Table 2. Tumor volume and craniotomy size in the study group.

Variable	Mean/Median
Tumor volume (cm3)	21.6/11.7
Craniotomy size (mm2)	631/491
Skull base tumor volume (cm3)	13.3/7.39
Skull base craniotomy size (mm2)	489/410
Skull base craniotomy size (standard) (mm2)	2,018/2,275
Convexity tumor volume (cm3)	26/16
Convexity craniotomy size (mm2)	708/503

Fig. 3. Ratio of tumor volume to craniotomy size. To visualize the craniotomy size, we used a 2 Euro coin (520.5 mm² surface area). Over 50% of surgeries were performed through a craniotomy smaller than this surface area. For 46 (85.2%) surgeries, the area is less than 2 coins, and for 52 (96.3%), it is less than three.

Since there are no standard approaches to convexity tumors, and craniotomy sizes can vary greatly, we compared standard approaches to skull base tumors (pterional and retrosigmoid) with approaches routinely performed in our clinic in order to visualize minimally invasive methods. The mean size of the minimally invasive approach was 489 mm², while the mean size of the standard approach was 2,018 mm², which is 4 times more than in the minimally invasive approach. It should also be taken into account that the size of the skin incision with standard accesses is also noticeably larger.

Fig. 4 shows the craniotomy area to tumor volume ratio using the example of pterional and retromastoid approaches. Minimally invasive approaches are marked in blue, and standard approaches orange. Fig. 4 shows that the minimally invasive pterional approach is approximately 5 times smaller than the standard one, and the retromastoid approach is approximately 2.5 times smaller.

Fig. 4. Ratio of tumor volume to the size of the minimally invasive craniotomy and to the size of the standard pterional (A) and retrosigmoid (B) approach. Minimally invasive approaches are marked in blue, and standard calculated approaches are orange.

Three postoperative complications were registered: postoperative hemorrhage, cerebrospinal fluid (CSF) leakage, and ophthalmoplegia. At the same time, the first two complications required reoperation, which were successfully performed.

Although the risk of bleeding is estimated at 2.6% [35], postoperative bleeding in the first case developed on the 3rd postoperative day against the background of arterial hypertension.

In the second case, CSF leakage occurred in the patient after Simpson Grade I resection (with the bone) in the region of the posterior cranial fossa. As it is known, the occurrence of liquor fistula during operations on the posterior cranial fossa is higher, due to the position of the patient lying on the back. The trepanation size and the dura mater removed part in this case were above average. After plastic surgery with a large amount of Lyoplant, no relapses were observed.

Another patient with a large sphenoid wing meningioma, developed ophthalmoplegia postoperatively. She was diagnosed with an anaplastic rapidly growing WHO III meningioma, which could not be removed without damage to the cranial nerves, and the operation was necessary for health reasons due to the large volume of the tumor.

The total follow-up period was in average 26.3 months (median 20). In the group of atypical meningiomas, 9 patients received radiation therapy at a dose of 50.4–60 Gy. All patients received a dose of more than 50 Gy, also recommended by current treatment protocols [28]. Two patients refused the proposed therapy.

In this group, only two recurrences were registered, which lies within the current data described in the literature. One of them underwent radiation therapy with a low dose (20 Gy), which subsequently stopped tumor growth. In the second case, WHO II atypical meningioma (originally WHO I) was diagnosed after reoperation.

DISCUSSION

Our study has both practical and theoretical implications. In practical terms, this means that minimally invasive approaches in surgery for most meningiomas can be considered a good alternative to standard approaches. Especially when it comes to approaches to the skull base. We did not set ourselves the task of operating through an approach as small as possible but rather not larger than absolutely necessary. We used an approach, sufficient to completely remove the tumor. This of course entails also a change in paradigm in the treatment of meningiomas. The commonly shared opinion, that the craniotomy has to be lager then the meningioma, especially in convexity meningiomas, in order to be able, resect the dura and remove the dural tail, we do not share. Using state of the art neurosurgical tube shaft instruments for microsurgery and performing the surgical removal endoscopy assisted, resection of the dura and the dural tail can also be achieved as we were able to show in our study. The surgical strategy used is to hollow out the tumor and the dissect it from the surrounding tissue with cotton patties being inserted between the cortex and the tumor. The dura resection and removal of the dural tail is then performed endoscopically.

Although we did not set ourselves the task of comparing the number of postoperative complications between minimally invasive and standard methods, the low number of complications in our group may indicate a high efficiency of these methods.

Thus, minimally invasive approaches can be considered safe, while allowing complete tumor resection to be achieved.

A separate topic of discussion is the duration of the operation. For many reasons, we have not studied the average operation time, but we can state that the extracranial part of the operation is faster than in case of standard approaches. This applies to both to the craniotomy and the completion of the operation, including the duroplasty, refixation of the bone or cranioplasty using alloplastic material and skin suturing.

Another important issue to consider is the cosmetic effect of small approaches which require only small and mostly straight skin incisions. Furthermore, we shave off hair only along a narrow corridor about 3–5 mm wide in the area of the planned skin incision and suture the skin intracutaneously closing and sealing the skin with Dermabond skin glue. The small incision and the good cosmetic results have also the positive effect that the patients are not stigmatized since they do not have a bandage wrapped round their head and can take a shower on the first day after surgery. After all, modern neurosurgery has already for a long time, provided not only the prolongation of lives of patients, but also the quality of life. We did not observe any cases of impaired wound healing and wound infections in our series, which can be largely attributed to the small approaches we used.

Based on both theoretical and practical data, we find the Simpson II resection to be the best choice whenever possible. That is, in cases where macroscopically the bone and dura mater look unchanged. This can reduce the occurrence of complications such as liquor fistula to a minimum.

Given that new studies show similar recurrence outcomes of benign meningiomas after different types of complete resection (Simpson I–III), the use of less traumatic surgical tactics (Simpson II–III) with minimally invasive approaches seems to be more reasonable. The rejection of Simpson I resection unambiguously strengthens the position of “keyhole” approaches in the surgical treatment of intracranial meningiomas [17].

The theoretical meaning of this work lies in the objectification and quantitative presentation of minimally invasive surgical approaches. In the review of current literature, we did not find any papers focusing and evaluating these issues. Thus, this work can lay the foundation for further similar studies. This, in turn, contributes to the standardization of minimal invasive approaches and the consolidation of minimally invasive methods in neurosurgery of both meningiomas and other neurosurgical pathologies.

Studying and comparing standard and minimally invasive approaches to the skull base, we showed that even a decrease of the average craniotomy size by 3–5 times does not affect either the risks of postoperative complications or the possibility of complete tumor removal. Thus, these approaches can be considered efficient and safe for the patient. Furthermore, results of this study even suggest that minimally invasive approaches can reduce operative associated risks for the patient. However, further studies on this topic have to be performed.

The recurrence rate, even with WHO I meningiomas after 10 years, is quite high and fluctuates around 47% [18,36]. In our study, relapse occurred only in 2 cases, in one of which WHO II atypical meningioma was diagnosed; however, our follow-up times did not reach 10 years yet.

The limitations of this study are a relatively small sample and a relatively short follow-up period. However, with this study, we are able to achieve a quantitative assessment of minimally invasive approaches in the surgical treatment of intracranial meningiomas and show that they are safe.

In conclusion, minimally invasive approaches in the surgical treatment of intracranial meningiomas reduce the surgical trauma by several times and are safe and sufficient for complete tumor removal.

Availability of Data and Material

The datasets generated or analyzed during the study are available from the corresponding author on reasonable request.

Supplementary Materials

The online-only Data Supplement is available with this article at https://doi.org/10.14791/btrt.2024.0005.

Video 1

First, preoperative MRI images in three projections, as well as preoperative planning using the Surgical Theater visualization platform are shown. Then the surgery is presented. A craniotomy is performed approximately 2×2 cm occipitally to the left. The dura mater is opened crosswise. Removal of the tumor occurs after its thorough preparation from the surrounding tissues with simultaneous coagulation of small vessels. After complete removal of the tumor, hemostasis and endoscopic inspection of the resection area are performed. Duroplasty is performed using the sandwich technique with Tachosil. At the end of the video, the size of the craniotomy is presented.

Video 2

Surgical Theater is used to plan a mini-pterional approach.