Transcranial resection of falcine meningiomas with the combination techniques of complete endoscope and intraoperative ultrasound

doi:10.21203/rs.3.rs-4826664/v1

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Transcranial resection of falcine meningiomas with the combination techniques of complete endoscope and intraoperative ultrasound

https://doi.org/10.21203/rs.3.rs-4826664/v1

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Transcranial neurosurgery with the assistance of endoscope and intraoperative ultrasound (IOUS) has emerged as a promising strategy for real-time visualization and guidance during tumor resection. In this study we aimed to explore the application of these techniques in the resection of falcine meningiomas (FM) and to investigate the feasibility and safety. In this report, combination techniques of transcranial endoscope and IOUS were used for the surgical resection in 11 patients with FM. Preoperative neuroimaging tests, including magnetic resonance imaging (MRI), computed tomography (CT), magnetic resonance angiography (MRA), and magnetic resonance venography (MRV) were utilized for the surgical planning. Real-time IOUS assisted the localization, visualization of tumor boundaries, assessment of adjacent structures, and guidance of the resection process. We found that tumors locating in the anterior, middle and posterior third of falx were found in 4, 5, and 2 patients, respectively. Tumors in unilateral falx were 8 cases, and in bilateral falx were 3 cases. Simpson grade I resection was carried out for all the patients. Benign tumor was present in 10 patients, and a patient was with WHO grade III for pathological finding. Postoperative complications occurred in two patients, a patient with temporary contralateral hemiplegia, and another patient with pulmonary infection. The average time of follow-up was 19.3 months. All patients had Karnofsky Performance Status (KPS) scores > 90 scores. In summary, the combination of endoscope and IOUS was feasible and safe for FM patients, especially for those with deep seated FMs.

falcine meningiomas

transcranial endoscope

intraoperative ultrasound

microneurosurgey

Falcine meningioma (FM), originating from the falx cerebri, is entirely covered with normal brain parenchyma but does not invade the superior sagittal sinus (SSS)[1]. It accounts for approximately 9% of all intracranial meningiomas[2, 3]. Al-Mefty et al. classified FM into three subtypes: anterior, middle, and posterior, on the basis of their relations to the coronal and lambdoid suture[4]. FM is attached to the cerebral falx, growing along the midline in a deep-seated position, and adjacent to the SSS. The cortical surface above the tumor often has some prominent drainage veins extending to the SSS. In the cases of affecting the middle to posterior third of falx, it may impact the sensory-motor cortex. Inappropriate surgical procedures usually cause various neurological impairments. Given that a subtotal resection predicts a higher rate of recurrence, the surgical resection of FM remains a challenge for neurosurgeons[5].

Initially, endoscopic technique was employed for pituitary adenomas resection with the transnasal approach. In recent years, with the evolution of equipment, transcranial endoscope has gradually arouse the interest among neurosurgeons. Compared with the microscope, endoscope offers the numerous advantages, including a wide angle viewing and a close-up observation, thus facilitating the removal of deep-seated lesions through a narrow surgical corridor[6] Meningioma is a kind highly vascularized tumor. An early disruption of the basal blood supply significantly promotes the surgical efficiency. Therefore, owing to the availability of deep-seated visual field, endoscopic technique may assist devascularization in the resection of meningioma without damaging normal brain tissue.

Intraoperative ultrasound (IOUS) has been widely applied in brain tumor resection, allowing for tumor localization and assessment with the advantages of non-ionizing radiation, ease of operation, and minimal interference to surgical process[7–12]. It plays a pivotal role in relocalization at the time of brain shift which is induced by the process of neuronavigation. In reviewing of previous studies, we found only 3 case reports depicting the removal of FM with complete endoscopic technique[13–15]. However combining the complete endoscopic with IOUS in the neurosurgical resection of FM is still scarce.

In this study, we reported a preliminary experience of resection of FM with the combining techniques of complete endoscope and IOUS. Two representative surgical videos were also presented. We will describe the surgical procedure and evaluate the feasibility as well as safety of the procedure.

Patients

A total of consecutive 11 patients (5 males and 6 females) were recruited from our department from December 2020 to June 2024. All patients were pathologically diagnosed as FMs and received endoscopic resection. Demographic and clinicopathological features were summarized at Table 1. This study was approved by the Institutional Ethics Committee of the First Affiliated Hospital of Anhui Medical University and was conducted according to the Declaration of Helsinki. Informed consents were obtained from all participants or immediate relatives.

Table 1

The demographic and clinicopathologica; features of the patients with falcine meningiomas. GTR: Gross total resection; KPS: Karnofsky Performance Status
No.	Age	Gender	Tumor location	Tumor size	Extent of resection	Simpson Grade	Postoperative complication	KPS
1	66	Female	Anterior 1/3	5.9	GTR	I	None	100
2	54	Female	Middle 1/3	3.3	GTR	I	None	100
3	68	Male	Middle 1/3	3.8	GTR	I	Pulmonary infection	100
4	36	Female	Anterior 1/3	6.6	GTR	I	None	100
5	63	Male	Middle 1/3	4.3	GTR	I	None	100
6	54	Female	Posterior 1/3	2.2	GTR	I	None	100
7	51	Male	Anterior 1/3	9.2	GTR	I	None	100
8	68	Female	Middle 1/3	2.4	GTR	I	Temporary contralateral hemiplegia	90
9	58	Male	Anterior 1/3	2.6	GTR	I	None	100
10	70	Male	Posterior 1/3	4.5	GTR	I	None	100
11	54	Female	Middle 1/3	1.1	GTR	II	None	100

FM classification and surgical design

Neuroimage tests, including computed tomography (CT) scan with thin bone window, magnetic resonance imaging (MRI), MR angiography (MRA), and MR venography (MRV) were performed for all the patients. Tumor located at unilateral side was found in 6 patients, while at bilateral sides was found in 5 cases. The median diameter of tumors was 4.2 ± 2.3 cm (ranging from 1 to 9 cm).We classified FMs into three subtypes based on the location of tumor relating to the falx. Tumors locating in the anterior, middle and posterior third of falx were found in 4, 5, and 2 patients, respectively.

Patient positioning and craniotomy

After general anesthesia, the patients were placed in a supine position, if tumor located in the anterior and middle third of falx. Alternatively, the patients were placed in a prone position, if tumor located in the posterior third of falx. An endoscopic pneumatic arm was installed on one side of the operating table. Based on the tumor size, straight incision parallel to the midline was adopted generally, and an arc-shaped incision perpendicular to the midline was used for large tumors across the falx. The maximum diameter of the bone window ranged from 2.5 to 6 cm, with a median diameter of 3×4 cm². Burr holes were drilled on the surface of the superior sagittal sinus before and after, and a milling cutter was used to remove the bone to expose the superior sagittal sinus (SSS) and adjacent dura mater. Then the dura mate was suspended. Gelatin sponge should be gently pressed on SSS for hemostasis, and then the head of the bed should be raised. All the tumors were surgically removed through interhemispheric transfalcine approach from the tumor side by a purely endoscope method with the assistance of the IOUS.

IOUS examination

After exposure of the dura mater, a sterile ultrasound probe (C251, 1-5MHZ, Hitachi, Japan) was connected to the ultrasound device (Hitachi, Japan). The IOUS was performed to identify the location, size, and relationships of the tumor with surrounding brain tissue and blood vessels. After the surgery, IOUS was also applied to detect whether the tumor was completely resected and whether there was any formation of oozing hematoma in the surgical area.

Endoscopic application

The neuroendoscope with 0-degree lens (4-mm diameter, 18-cm length, Karl Storz, Germany) was fixed with a pneumatic arm and introduced into the surgical field. Neurosurgeons can resect the tumor by a bimanual manipulation just as they operate under the microscope. Frequent intermittent irrigation kept the surgical field clean.

Tumor resection

Dura mater was incised in a reverse “C” form under the guidance of IOUS. The incision of dura should be as close as possible to the SSS and reflected to the midline medially. The arachnoid membrane between the cortical surface and SSS was dissected, and the bridging vein draining into SSS (the number is usually 1–3) should be carefully avoided. The interhemispheric fissure cistern was opened without retraction and then cerebral spinal fluid (CSF) was released. An enough cerebellar relaxation allows the full exposure and optical visualization of the tumor. The 4D principles (dedressing, devascularization, debulking, and dissection) were strictly followed during tumor resection: 1) dissecting the arachnoid membrane at the tumor-brain interface; 2) removing the tumor base with bipolar cautery; 3) intratumor decompression with ultrasonic aspiration; 4) complete removal of the tumor in a piecemeal fashion. The falx invaded by the tumor was resected thoroughly.

Surgical outcomes

Simpson grade I tumor resection was achieved in most of cases, except case 11 which achieved Simpson grade II tumor resection. As for case 11, the small sized tumor (with a diameter of 1 cm) located in the middle third of the SSS. It deeply seated with a soft consistency, grew inferiorly to the inferior sagittal sinus and intimately associated with deep venous plexus. The cerebral falx, which the tumor was attached to, remained intact. Therefore, in the process of surgical removal of tumor, the attached portion of the cerebral falx was reserved in order to prevent the injury of adjacent venous plexus and inferior sagittal sinus.

Pathological examination

All tumor tissues were were performed with pathological examinations to determine the characteristics. Among that, ten patients were found with WHO grade 1 meningiomas, and a patient was pathologically diagnosed with WHO grade 3 malignant meningioma. The patient received radiotherapy after operation.

Surgical complications and follow up for tumor relapse

Some surgery-related complications were reported. Postoperative pulmonary infection occurred in a patient. After a proper treatment in the intensive care unit, the patient recovered. Postoperatively hemiplegia on one side occurred in another patient with a tumor located in the middle third of the SSS, who recovered completely within one month of follow-up. Another patient were reported to be temporary contralateral hemiplegia. The remaining patients did not experience any complications or death. The follow-up period was 2 ∼ 42 months to assess the patients’ Karnofsky Performance Status (KPS) scores[16] and cranial MRI (with and without contrast). All the patients had KPS scores above 90 scores, and no tumor recurrence was observed in any patients. At a year follow up, no patient were reported to be relapse after the MRI scans.

Representative cases 1 (No. 8 patient)

A 68-year-old female presented to the hospital complaining with the weakness of left limb. Cranial MRI showed a medium-sized FM in left parietal lobe, locating deeply under the precentral gyrus. Preoperative neurological examination found normal muscle strength in all limbsl. Given the tumor was sized < 3 cm, we hypothesized that the patient’s symptoms might not be related to the mass effect of tumor. As requested by the patients and immediate family members, the patients received neurosurgical resection of tumor. The details of surgical processes were exhibited in Video 1,

A Simpson grade I tumor resection was achieved. On the first postoperative day, the patient was alert with a grade 4 muscle strength in the right limbs and a normal muscle strength at left limbs. Postoperative cranial CT scan showed no hemorrhage and residual tumor in the surgical area. However, the muscle strength of right limbs weakened to grade 1 at 3rd day postoperatively. Cranial CT scan found a mild edema around the surgical site. After dehydration therapy, the patient’s muscle strength improved to grade 3 when discharged. After one-month follow-up, the patient’s muscle strength recovered to a normal condition.. At a year follow up, we found no tumor relapse (Fig. 1), and the KPS score was > 90.

Representative case 2 (No. 7 patient)

A 51-year-old female presented with an alteration of personality for a year. Neurological examination revealed no abnormality. Enhanced cranial MRI scan found a huge occupying mass across the falx in the frontal lobe with a diameter of 9.2 cm. The patient received tumor resection with a purely endoscopic methods with an assitance of the IOUS. The patient was in a supine position and the head was fixed in a halo ring. A linear skin incision was designed perpendicular to the SSS and a bone window was created on the non-dominant right frontal hemisphere, through which the dura and SSS was exposed. IOUS was applied to localize the tumor and to detect adjacent structure. Tumor seating in the right falx was initially resected under full endoscope, followed by the contralateral tumor. A Simoson grade I tumor resection was achieved (Video 2). The patient had no discomfortableness and other complications after the operation. After a 20-month follow up, the patient had a KPS score of 100 and no tumor relapse (Fig. 2).

FM originates from the falcine with wide tumor base, growing along with cerebral longitudinal fissure cistern and being buried deeply below the cortex and SSS and there are a variety of numbers and types of cortical draining veins situated on the surface of the tumor, which drain into the SSS[17–19]. Therefore, the injury to any of the overlying cortical veins will lead to postoperative venous infarction, even a disastrous result[20]. Because of the above eloquent cortex, surgical removal of deep-seated FM, particularly in the mid-to-posterior third of the SSS poses a challenge. Even with a minimally invasive neurosurgery, a complete removal of tumor without comlications remains a challenge for neurosurgeons.

Numerous surgical approaches for FM have been reported, ranging from the transcortical approach with naked-eyes to the interhemispheric transfalcine approach with microneurosurgerical techniques[1, 3, 14, 15, 21]. However, the transcortical approach has largely been discarded due to the damages of brain tissue. The interhemispheric transfalcine approach can be further categorized into ipsilateral[3, 15] and contralateral[14, 21] approaches, each presenting its unique advantages. The fundamental principle guiding the selection of surgical approaches remains the safety in tumor resection. In our study, the ipsilateral interhemispheric transfalcine approach was chosen for unilateral localization in 6 out of 11 patients, while the contralateral approach via the non-dominant hemisphere was advocated for bilateral localization in the remaining 5 patients. The second representative case involved a giant FM with a diameter exceeding 9 cm. During surgery, the right non-dominant interhemispheric approach was adopted, enabling the resection of the bilaterally growing tumor through an unilateral approach.

endoscope offers a completely different view in comparison with that using traditional microscope. Complete endoscopic resection of FM offers greater flexibility in surgical approach selection due to the multi-angles and proximal observation capabilities, regardless of tumor size or location. Furthermore, with the development of auxiliary instruments, especially endoscopic holders such as a pneumatic arm, the operations of endoscope facilitate neurosurgeons has become handy. Lesions in regions of CPA, pineal and petrous clival have been reported to be operated with complete endoscope[22–26]. Furthermore, we can shift the lens of endoscope backward or forward freely to obtain an optical surgical vision. Sometimes, 30°, 45° of angled endoscope can be used to enlarge the exposure. Special position is not necessary for the patient.

Rigid endoscope with different lens offers a panoramic view which shows more detailed anatomical structures around the tumor, especially in a narrow and deeply surgical corridor[6]. Therefore, this panoramic view of the endoscope can confer significant advantages to the resection of FM via interhemispheric longitudinal fissure and transfalcine approach. Firstly, endoscope enables manipulation in the narrow corridor between the cortex and the SSS through a sparsely vascularized region. It facilitates the release of cerebrospinal fluid, brain relaxation and excision of the tumor base without traction, and thereby maximize the interruption of tumor blood supply as early as possible. Notably, the surgical corridor does not necessarily need to be established on the tumor's superior surface. It can be accessed obliquely, either anteriorly or posteriorly, a maneuver that is particularly challenging under the microscope. Except for a wide view field, endoscope facilitates close-up observation so that a clear surgical visual field can be achieved by adjusting the pneumatic arm. It can minimize the risk of the damage to adjacent blood vessels, nerves as well as brain tissue, and finally improves the rate of tumor resection.

IOUS has been shown to be a valuable imaging tool for localizing tumors and assessing the extent of resection[8, 27, 28]. In comparison with other intraoperative imaging techniques, such as MRI, CT, and neuronavigation systems, IOUS has the advantages of financial feasibility, ease of use, and availability without ionizing radiation exposure or major workflow interruption. In addition, IOUS also assesses the vascular architecture of tumoral and peritumoral tissues[29], and it plays a pivotal role in relocalization at the time of brain shift which is induced by the process of neuronavigation[10]. The experience of meningiomas showed hyperechogenic on IOUS with the 3rd grade[30]. Aside from localization of tumors,, we also used IOUS to measure tumor size and distance from the cortex and understand the relationships with surrounding structures. Furthermore, we tentatively located veins draining into the SSS and evaluated blood vessels adjacent to deep-seated tumors using this technique. This precision-guided approach facilitated the dural incision and tumor resection processes, thus expedite the surgical workflow, enhance the protection of surrounding tissue, and ultimately minimized the occurrence of complications.

Motor-sensatory deficit and seizure are the common postoperative complications for FM resection. Giombini et al.[31] reported that in the series containing 342 FM patients, the patient numbers with the complications of motor-sensatory and seizure were 30 and 42, respectively. Zuo et al.[21] observed 3 patients with motor-sensatory deficit and 2 patients with seizure in 20 FM patients. Murrone et al.[3] also found 4 patients had complications of motor-sensatory and seizure in the series of 95 FM patients. Interestingly, we found that the FM patients in these reported received the neurosurgery with the assistance of microscope, but the 6 cases receiving endoscope assistance showed no complications (Table 2). In our report, all patients also did not have any neurological deficit and approach-related complications postoperatively. We inferred that the less complications, which complete endoscope technique caused, might attributed to the minimization of brain retraction, perfect surgical field of vision and early devascularization. Beside, bridging veins to the SSS should be preserved. To prevent damage to crucial blood vessels on the cortical surface, we cut the dura away from tumor forwards or backwards and subsequently resected the tumor via an oblique surgical corridor which was much easily performed under endoscope than microscopy[32].

Table 2

Literature summary of resection of falcine meningiomas using complete endoscopic techniques. GTR: Gross total resection,
Year/Author	Case (n)	Tumor location (n)	Extent of resection	Simpson Grade
Spektor et al. 2016¹³	1	Anterior 1/3	GTR	Not available
2022, Sakaeyama et al. 2022¹⁴	4	Anterior 2/3 (3) Posterior 1/3 (1)	GTR	I
Zhang et al. 2023¹⁵	1	Middle 1/3	GTR	I
Present study	11	Anterior 2/3 (4) Middle 1/3 (5) Posterior 1/3 (2)	GTR	I

Generally, this technique using the combination of complete endoscope and IOUS offers numerous advantages, including precise dural incision, avoidance of draining veins, early tumor devascularization, minimal brain retraction, a wider surgical field of view, a higher rate of tumor resection, and fewer complications. However, this technique also has some limitations. Firstly, unlike microscope, endoscope offers a two-dimensional image that lacks depth perception, necessitating continuous training and adjustment for surgeons. It is crucial to follow the sequential learning process, progressing from anatomical research under a endoscope in the laboratory to clinical practice, from transnasal endoscope to transcranial endoscope, and from endoscopic-assisted minimally invasive neurosurgery to fully endoscopic minimally invasive neurosurgery. Additionally, the current study involved a relatively small number of cases. A research with an augmented sample size should be performed to further validate the effectiveness and safety of this technique.

We present a preliminary experience with complete endoscopic removal of FM with the assistance of IOUS, and the results were proved to be feasible and safe for FM patients by this resection strategy, especially for those with deep seated FMs.

Acknowledgement

None.

Author Contribution

Conception: JX and LY; data collection and operation: JX, CL and TZ; data interpretation: XC, QS, YL and XW; supervision: YZ and HC; manuscript drafting: TZ and JX; manuscript revision: LY

Funding

The study was supported by the Natural Science Research Project of Colleges and Universities in Anhui Province (KJ2021A0289); Open Research Project of the Key Laboratory of Reproductive Health and Genetics in Anhui Province (RHG-2021-3); Anhui Province Academic and Technical Leader Candidate Research Activities Funding Projects (2020H232).

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Conflict of interest

All authors declare no conflict of interest.

Ethical approval

The study was conducted according to the Declaration of Helsinki (as revised in 2013) and was approved by the Institutional Ethics Board of the First Affiliated Hospital of Anhui Medical University.

Consent to participate

Signed and informed consent was obtained from all individual participants or their relatives.

Financial interests

The authors declare they have no financial interests.

Disclosures

The authors have no further disclosures.

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No competing interests reported.

Video1.avi
Video 1: Resection of FM locating at the middle third of falx with the assistance of endoscope and IOUS (Case 8)
Video2.avi
Video 2. Resection of a giant FM by unilateral interhemispheric trans-falcine approach.

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You are reading this latest preprint version

Transcranial resection of falcine meningiomas with the combination techniques of complete endoscope and intraoperative ultrasound

Status:

Version 1

Abstract

Figures

Introduction

Methods

Patients

FM classification and surgical design

Patient positioning and craniotomy

IOUS examination

Endoscopic application

Tumor resection

Results

Surgical outcomes

Pathological examination

Surgical complications and follow up for tumor relapse

Representative cases 1 (No. 8 patient)

Representative case 2 (No. 7 patient)

Discussion

Conclusion

Declarations

References

Additional Declarations

Supplementary Files

Status:

Version 1