Abstract
Objective
Knowledge of the location of tumor-feeding arteries is necessary for the safe surgery of intracranial meningiomas. Hence, this retrospective study aimed to comprehensively analyze the distribution of tumor-feeding arteries.
Methods
Patients who underwent intracranial meningioma surgery at our institution between 2015 and 2023 were included in this study. The tumor attachment sites and tumor-feeding arteries were evaluated based on the results of preoperative examinations. The tumor attachment sites were classified as non-skull bases (convexity, parasagittal, and falx) or skull bases (anterior skull base, sphenoid ridge, sphenopetroclival, petrous, tentorial, cerebellar convexity, and foramen magnum). These tumors were further subdivided according to their attachment areas.
Results
Among the 180 patients included, the tumor-feeding arteries were identified in 177 patients (98.3%). In 67 patients with non-skull base meningiomas, the middle meningeal artery primarily functioned as a tumor-feeding artery in the anterior and middle regions (78 of 108 feeding arteries, 72.2%), while the extracranial artery served as a tumor-feeding artery in the posterior region (20 of 37 feeding arteries, 54.1%). Conversely, skull base meningiomas exhibited a higher frequency of having tumor-feeding arteries derived from the internal carotid artery (132 of 278 feeding arteries; 47.5%); these tumor-feeding arteries are often found at the deepest part of the surgical field during tumor resection and require careful intraoperative handling.
Conclusions
Tumor-feeding arteries originate from different dural arteries depending on the tumor attachment site. These findings could help enhance surgical safety, especially in patients with meningiomas who have not undergone preoperative angiography.
Keywords: Meningioma, Tumor-feeding artery, Tumor attachment, Skull base
Introduction
Intracranial meningiomas are blood-rich tumors, and ensuring safe surgical removal entails proper handling of the tumor-feeding arteries [4, 6, 8, 17, 18, 21, 22, 26]. As most meningiomas originate in the dura mater, most of their feeding arteries are derived from the dural arteries [2–4, 6, 8, 9, 13, 17, 18, 21, 22, 26]. The normal dura mater has various trophic arteries depending on its location, with many branches of the external carotid artery (ECA), internal carotid artery (ICA), and vertebral artery (VA) forming a complex dural arterial network [13]. Although the feeding arteries of meningiomas commonly originate from the dural arteries that supply the site of tumor origin [4, 13], tumor-feeding arteries sometimes originate from dural arteries at distant sites [8]. Previous studies also reported the overlapping distributions of various dural arteries originating from the ECA, ICA, and VA [13]. To date, comprehensive reports delineating which dural arteries tend to develop into tumor-feeding arteries in intracranial meningiomas are lacking. Preoperative knowledge of the origin, location, and distribution of the tumor-feeding arteries is essential to determine the indications for preoperative embolization and the appropriate craniotomy area for tumor devascularization. This retrospective study aimed to evaluate the origin of meningiomas and the distribution of tumor-feeding arteries in the entire intracranial dura mater to enhance the safety and efficacy of tumor resection.
Materials and methods
Study design and patient population
We retrospectively evaluated the relationship between tumor attachment sites and tumor-feeding arteries in patients who underwent an initial craniotomy for the removal of intracranial meningiomas at Fujita Health University between January 2015 and December 2023. To evaluate the relationship between meningiomas and tumor-feeding arteries, patients with a history of craniotomy, multiple meningiomas, and concurrent intracranial tumors other than meningiomas were excluded. Patients who did not undergo contrast-enhanced magnetic resonance imaging (MRI), three-dimensional computed tomography angiography (3DCTA), or digital subtraction angiography (DSA) within 6 months before surgery were also excluded.
Data collection
Patient data, such as age, sex, and tumor pathology, were collected from the medical records.
We retrospectively evaluated the preoperative contrast-enhanced MRI, 3DCTA, and DSA scans of all patients to determine the tumor attachment sites and tumor-feeding arteries. All imaging studies were performed following the protocols outlined in previous studies [23, 24].
Evaluation of tumor attachment
The tumor attachment sites were evaluated using contrast-enhanced MRI, and the surface where the tumor and dura mater were connected was determined as the attachment site. Non-skull base meningiomas were classified into convexity, parasagittal, and flax meningiomas according to their attachment sites. These non-skull base meningiomas were subdivided into anterior, middle, and posterior meningiomas, and their feeding arteries were evaluated. Meanwhile, skull base meningiomas were classified into anterior skull base, sphenoid ridge, sphenopetroclival, petrous, tentorial, cerebellar convexity, and foramen magnum meningiomas, according to their attachment sites. Moreover, anterior skull base meningiomas were subdivided into olfactory groove, orbital roof, tuberculum sellae, and diffuse types; the sphenoid ridge into anterior clinoid process (ACP) and middle-to-lateral sphenoid ridge types; and petrous meningioma into petroclival, petrous apex, posterior petrous, and diffuse types. Anterior skull base and petrous meningiomas that showed attachment site expansion to two or more areas were classified as the diffuse type. These tumor attachment sites were classified based on the reports of previous studies and the distribution of dural arteries [4, 10, 14].
Evaluation of the feeders
Tumor-feeding arteries were identified using DSA and CTA. DSA was used to identify the tumor stain, and the artery leading to the tumor stain was referred to as the tumor-feeding artery. The location of the tumor-feeding arteries was identified based on the DSA, three-dimensional rotational angiography (3DDSA), and 3DCTA images. The location of the tumor-feeding artery was identified based on the findings of maximum intensity projection images obtained using 3DDSA (Fig. 1). However, if 3DDSA was not performed, it was determined based on the images captured from the frontal and lateral views on DSA and 3DCTA. The tumor-feeding arteries originating from the tumor and non-tumor sides were evaluated. If the tumor attachment extended bilaterally, the tumor-feeding arteries originating from both sides were counted as tumor-feeding arteries on the tumor side.
Fig. 1.
Identifying tumor-feeding arteries from the findings of the maximum intensity projection images derived from rotational angiography. Preoperative contrast-enhanced magnetic resonance imaging shows a foramen magnum meningioma (a), and left-side vertebral artery angiography shows a tumor stain (b). Coronal view of maximum intensity projection images obtained from rotational angiography shows a tumor-feeding artery derived from the anterior meningeal artery (c, d). Asterisk (b): tumor stain; arrowhead (c, d): anterior meningeal artery
The classification of tumor-feeding arteries followed the criteria established in previous studies, which extensively detailed the subdivision of the dural arteries [12, 13]. In the ECA system, dural branches originating from the ascending pharyngeal artery, occipital artery (OA), middle meningeal artery (MMA), superficial temporal artery (STA), and internal maxillary artery, and in the ICA system, dural branches originating from the meningohypophyseal trunk (MHT), inferolateral trunk (ILT), capsular artery, ophthalmic artery, and anterior cerebral artery were identified and classified. Similarly, the dural branches of the vertebral, anterior inferior cerebellar, and posterior cerebral arteries were identified and classified, and the presence of pial arterial supply was also evaluated. In the above reports [12, 13], the superior hypophyseal artery and posterior spinal artery are not described as supplying the dura mater. Therefore, they were not classified as dural arteries in this study.
Evaluating imaging studies
A board-certified neurosurgeon and a board-certified neurointerventionalist evaluated all imaging findings.
Results
Patient characteristics
A total of 180 patients (48 men and 132 women) were included in this study. The median ages were 58 years in men (range, 21–89 years; interquartile range, 49–69.5 years) and 61 years in women (range, 16–85 years; interquartile range, 47–67 years). Anaplastic meningioma (3 patients), atypical meningioma (19 patients), chordoid meningioma (2 patients), meningothelial meningioma (57 patients), transitional meningioma (42 patients), fibrous meningioma (16 patients), angiomatous meningioma (27 patients), secretory meningioma (8 patients), and microcystic meningioma (2 patients) were identified. Three other patients were diagnosed with Word Health Organization (WHO) grade 1 equivalent meningiomas, while one was diagnosed with WHO grade 2 equivalent meningioma.
The non-skull base meningioma group included 67 patients: 19 with falx meningiomas, 14 with parasagittal meningiomas, and 34 with convexity meningiomas (Table 1). The skull base meningioma group included 113 patients: 17 with anterior skull base meningioma, 35 with sphenoid ridge meningioma, 6 with sphenopetroclival meningioma, 37 with petrous meningioma, 10 with tentorial meningioma, 4 with cerebellar convexity meningioma, and 4 with foramen magnum meningioma (Tables 2, 3, 4 and 5).
Table 1.
Number of feeders identified in non-skull base meningiomas
| Tumor attachment | Falx | Parasagittal | Convexity | All | ||||
|---|---|---|---|---|---|---|---|---|
| The number of patients (with bilateral tumor attachment) | 19 (1) | 14 (1) | 34 (0) | 67 (2) | ||||
| Laterality | T | NT | T | NT | T | NT | T | NT |
| ECA | 21 | 16 | 17 | 14 | 45 | 17 | 83 | 47 |
| APhA, hypoglossal branch | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 0 |
| OA, jugular branch | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 1 |
| OA, mastoid branch | 0 | 1 | 0 | 1 | 2 | 0 | 2 | 2 |
| OA, parietal emissary branch | 2 | 1 | 3 | 3 | 3 | 0 | 8 | 4 |
| MMA, anterior division, lateral branch | 13 | 10 | 10 | 6 | 23 | 9 | 46 | 25 |
| MMA, posterior division, petrosquamosal branch | 0 | 0 | 0 | 0 | 1 | 0 | 1 | 0 |
| MMA, posterior division, parieto-occipital branch | 3 | 3 | 1 | 0 | 8 | 5 | 12 | 8 |
| Superficial temporal artery | 2 | 1 | 3 | 4 | 5 | 2 | 10 | 7 |
| Angular artery | 0 | 0 | 0 | 0 | 1 | 0 | 1 | 0 |
| Middle deep temporal artery | 0 | 0 | 0 | 0 | 2 | 0 | 2 | 0 |
| ICA | 3 | 2 | 0 | 0 | 2 | 4 | 5 | 6 |
| OphA, AEA, anterior falcine artery | 2 | 2 | 0 | 0 | 2 | 4 | 4 | 6 |
| OphA, posterior ethmoidal artery | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 0 |
| VA: posterior meningeal artery | 0 | 0 | 0 | 0 | 1 | 0 | 1 | 0 |
| PCA: tentorial branch | 1 | 2 | 0 | 0 | 0 | 0 | 1 | 2 |
T tumor side, NT non-tumor side, ECA external carotid artery, APhA ascending pharyngeal artery, OA occipital artery, MMA middle meningeal artery, ICA internal carotid artery, OphA ophthalmic artery, AEA anterior ethmoidal artery, VA vertebral artery, PCA posterior cerebral artery
Table 2.
Number of feeders derived from the external carotid artery in the anterior skull base, sphenoid ridge, sphenopetroclival, and petrous meningiomas
| Tumor attachment | Anterior skull base | Sphenoid ridge | Sphenopetroclival | Petrous | ||||
|---|---|---|---|---|---|---|---|---|
| The number of patients (with bilateral tumor attachment) | 17 (8) | 35 (0) | 6 (0) | 37 (0) | ||||
| Laterality | T | NT | T | NT | T | NT | T | NT |
| ECA | 10 | 2 | 56 | 0 | 11 | 0 | 38 | 1 |
| APhA, carotid branch | 0 | 0 | 0 | 0 | 0 | 0 | 2 | 0 |
| APhA, jugular branch | 0 | 0 | 0 | 0 | 0 | 0 | 5 | 0 |
| APhA, hypoglossal branch | 0 | 0 | 0 | 0 | 0 | 0 | 5 | 1 |
| OA, mastoid branch | 0 | 0 | 0 | 0 | 0 | 0 | 2 | 0 |
| MMA, anterior division, lateral branch | 1 | 0 | 9 | 0 | 0 | 0 | 0 | 0 |
| MMA, anterior division, medial branch | 4 | 1 | 20 | 0 | 3 | 0 | 1 | 0 |
| MMA, posterior division, petrosquamosal branch | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 |
| MMA, petrosal branch | 0 | 0 | 0 | 0 | 2 | 0 | 16 | 0 |
| Accessory meningeal artery | 0 | 0 | 7 | 0 | 2 | 0 | 6 | 0 |
| Artery of the foramen rotundum | 0 | 0 | 13 | 0 | 4 | 0 | 0 | 0 |
| Superficial temporal artery | 0 | 0 | 1 | 0 | 0 | 0 | 0 | 0 |
| Sphenopalatine artery | 4 | 1 | 0 | 0 | 0 | 0 | 0 | 0 |
| Middle deep temporal artery | 1 | 0 | 6 | 0 | 0 | 0 | 0 | 0 |
T tumor side, NT non-tumor side, ECA external carotid artery, APhA ascending pharyngeal artery, OA occipital artery, MMA middle meningeal artery
Table 3.
Number of feeders derived from the external carotid artery in the tentorial, cerebellar convexity, foramen magnum, and entire skull base meningiomas
| Tumor attachment | Tentorial | Cerebellar convexity | Foramen magnum | All | ||||
|---|---|---|---|---|---|---|---|---|
| The number of patients (with bilateral tumor attachment) | 10 (1) | 4 (0) | 4 (0) | 113 (9) | ||||
| Laterality | T | NT | T | NT | T | NT | T | NT |
| ECA | 9 | 2 | 6 | 0 | 0 | 2 | 130 | 7 |
| APhA, carotid branch | 0 | 0 | 0 | 0 | 0 | 0 | 2 | 0 |
| APhA, jugular branch | 0 | 0 | 0 | 0 | 0 | 0 | 5 | 0 |
| APhA, hypoglossal branch | 1 | 0 | 0 | 0 | 0 | 1 | 6 | 2 |
| OA, jugular branch | 0 | 0 | 1 | 0 | 0 | 1 | 1 | 1 |
| OA, mastoid branch | 2 | 1 | 2 | 0 | 0 | 0 | 6 | 1 |
| OA, parietal emissary branch | 0 | 0 | 1 | 0 | 0 | 0 | 1 | 0 |
| MMA, anterior division, lateral branch | 0 | 0 | 0 | 0 | 0 | 0 | 10 | 0 |
| MMA, anterior division, medial branch | 0 | 0 | 0 | 0 | 0 | 0 | 28 | 1 |
| MMA, posterior division, petrosquamosal branch | 2 | 0 | 0 | 0 | 0 | 0 | 3 | 0 |
| MMA, posterior division, parieto-occipital branch | 2 | 1 | 2 | 0 | 0 | 0 | 4 | 1 |
| MMA, petrosal branch | 1 | 0 | 0 | 0 | 0 | 0 | 19 | 0 |
| Accessory meningeal artery | 1 | 0 | 0 | 0 | 0 | 0 | 16 | 0 |
| Artery of the foramen rotundum | 0 | 0 | 0 | 0 | 0 | 0 | 17 | 0 |
| Superficial temporal artery | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 |
| Sphenopalatine artery | 0 | 0 | 0 | 0 | 0 | 0 | 4 | 1 |
| Middle deep temporal artery | 0 | 0 | 0 | 0 | 0 | 0 | 7 | 0 |
T tumor side, NT non-tumor side, ECA external carotid artery, APhA ascending pharyngeal artery, OA occipital artery, MMA middle meningeal artery
Table 4.
Number of feeders derived from the internal carotid, vertebral, anterior inferior cerebellar, and posterior cerebral artery in the anterior skull base, sphenoid ridge, sphenopetroclival, and petrous meningiomas
| Tumor attachment | Anterior skull base | Sphenoid ridge | Sphenopetroclival | Petrous | ||||
|---|---|---|---|---|---|---|---|---|
| The number of patients (with bilateral tumor attachment) | 17 (0) | 35 (0) | 6 (0) | 37 (0) | ||||
| Laterality | T | NT | T | NT | T | NT | T | NT |
| ICA | 29 | 4 | 42 | 0 | 14 | 1 | 35 | 5 |
| MHT, tentorial trunk | 0 | 0 | 8 | 0 | 2 | 0 | 13 | 0 |
| MHT, dorsal meningeal artery | 0 | 0 | 1 | 0 | 1 | 1 | 11 | 5 |
| MHT, inferior hypophyseal artery | 1 | 0 | 1 | 0 | 4 | 0 | 0 | 0 |
| ILT, superior division, medial tentorial artery | 0 | 0 | 2 | 0 | 2 | 0 | 8 | 0 |
| ILT, anterior division, medial branch | 1 | 0 | 8 | 0 | 1 | 0 | 2 | 0 |
| ILT, anterior division, lateral branch | 0 | 0 | 1 | 0 | 2 | 0 | 0 | 0 |
| Capsular artery | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
| OphA, AEA, anterior meningeal artery | 5 | 1 | 0 | 0 | 0 | 0 | 0 | 0 |
| OphA, posterior ethmoidal artery | 15 | 2 | 3 | 0 | 0 | 0 | 0 | 0 |
| OphA, deep recurrent ophthalmic artery | 0 | 0 | 4 | 0 | 0 | 0 | 0 | 0 |
| OphA, superficial recurrent ophthalmic artery | 6 | 1 | 5 | 0 | 1 | 0 | 1 | 0 |
| OphA, lacrimal artery | 0 | 0 | 9 | 0 | 1 | 0 | 0 | 0 |
| VA: anterior meningeal artery | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 |
| AICA: subarcuate artery | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 |
T tumor side, NT non-tumor side, ICA internal carotid artery, MHT meningohypophyseal trunk, DMA dorsal meningeal artery, IHA inferior hypophyseal artery, ILT inferolateral trunk, OphA ophthalmic artery, AEA anterior ethmoidal artery, VA vertebral artery, AICA anterior inferior cerebellar artery
Table 5.
Number of feeders derived from the internal carotid, vertebral, anterior inferior cerebellar, and posterior cerebral arteries in the tentorial, cerebellar convexity, foramen magnum, and entire skull base meningiomas
| Tumor attachment | Tentorial | Cerebellar convexity | Foramen magnum | All | ||||
|---|---|---|---|---|---|---|---|---|
| The number of patients (with bilateral tumor attachment) | 10 (1) | 4 (0) | 4 (0) | 113 (9) | ||||
| Laterality | T | NT | T | NT | T | NT | T | NT |
| ICA | 2 | 0 | 0 | 0 | 0 | 0 | 122 | 10 |
| MHT, tentorial trunk | 1 | 0 | 0 | 0 | 0 | 0 | 24 | 0 |
| MHT, dorsal meningeal artery | 0 | 0 | 0 | 0 | 0 | 0 | 13 | 6 |
| MHT, inferior hypophyseal artery | 0 | 0 | 0 | 0 | 0 | 0 | 6 | 0 |
| ILT, superior division, medial tentorial artery | 1 | 0 | 0 | 0 | 0 | 0 | 13 | 0 |
| ILT, anterior division, medial branch | 0 | 0 | 0 | 0 | 0 | 0 | 12 | 0 |
| ILT, anterior division, lateral branch | 0 | 0 | 0 | 0 | 0 | 0 | 3 | 0 |
| Capsular artery | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 |
| OphA, AEA, anterior meningeal artery | 0 | 0 | 0 | 0 | 0 | 0 | 5 | 1 |
| OphA, posterior ethmoidal artery | 0 | 0 | 0 | 0 | 0 | 0 | 18 | 2 |
| OphA, deep recurrent ophthalmic artery | 0 | 0 | 0 | 0 | 0 | 0 | 4 | 0 |
| OphA, superficial recurrent ophthalmic artery | 0 | 0 | 0 | 0 | 0 | 0 | 13 | 1 |
| OphA, lacrimal artery | 0 | 0 | 0 | 0 | 0 | 0 | 10 | 0 |
| VA | 2 | 1 | 1 | 0 | 3 | 0 | 7 | 1 |
| Anterior meningeal artery | 0 | 0 | 0 | 0 | 1 | 0 | 2 | 0 |
| Posterior meningeal artery | 2 | 1 | 1 | 0 | 2 | 0 | 5 | 1 |
| AICA: subarcuate artery | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 |
T tumor side, NT non-tumor side, ICA internal carotid artery, MHT meningohypophyseal trunk, ILT inferolateral trunk, OphA ophthalmic artery, AEA anterior ethmoidal artery, VA vertebral artery, AICA anterior inferior cerebellar artery
Of the 180 patients who underwent DSA, the six-vessel study was performed in 58 patients, the five-vessel study in 96 patients, the four-vessel study in 20 patients, the three-vessel study in two patients, and the two-vessel study in four patients.
Feeding arteries of non-skull base meningiomas
Tumor-feeding arteries were identified in 66 of the 67 patients with non-skull base meningiomas (98.5%). Details of the tumor-feeding arteries of non-skull base meningiomas at each attachment site are shown in Table 1 and Fig. 2.
Fig. 2.
Schematic representation of the main tumor-feeding arteries in non-skull base meningiomas. MMA, middle meningeal artery; OA, occipital artery; STA, superficial temporal artery
In 34 patients with convexity meningiomas, 48 tumor-feeding arteries originated from the tumor side, while 21 tumor-feeding arteries originated from the non-tumor side (Table 1). Pial arterial supply was identified in 12 of the 34 patients (35.3%). The tumor-feeding artery most frequently identified throughout the convexity meningioma was the lateral branch that originated from the anterior division of the MMA on the tumor side (23 of 34 patients [67.6%] and 23 of 69 feeding arteries [33.3%]) (Table 1). Similar trends were observed in anterior and middle convexity meningiomas (22 of 26 patients [84.6%] and 22 of 53 feeding arteries [41.5%]); however, the parieto-occipital branch that originated from the posterior division of the MMA on the tumor side was frequently identified as the tumor-feeding artery in posterior convexity meningiomas (4 of 8 patients [50.0%] and 4 of 16 feeding arteries [25.0%]). Furthermore, the OA and STA frequently functioned as tumor-feeding arteries in posterior convexity meningiomas (5 of 8 patients [62.5%] and 7 of 16 feeding arteries [43.8%]).
In 14 patients with parasagittal meningiomas, 17 tumor-feeding arteries originating from the tumor side and 14 tumor-feeding arteries originating from the non-tumor side were identified (Table 1). The lateral branch derived from the anterior division of the MMA on the tumor side (10 of 14 patients [71.4%] and 10 of 31 feeding arteries [32.3%]) and the non-tumor side (6 of 14 patients [42.9%] and 6 of 31 feeding arteries [19.4%]) was frequently identified as the tumor-feeding artery in parasagittal meningiomas (Table 1). Similar trends were observed in anterior and middle parasagittal meningiomas (tumor side: 10 of 11 patients [90.9%] and 16 of 24 feeding arteries [66.7%]) (non-tumor side: 6 of 11 patients [54.5%] and 6 of 24 feeding arteries [25.0%]). By contrast, tumor-feeding arteries derived from the extracranial arteries were more frequently identified in posterior parasagittal meningiomas (2 of 3 patients [66.7%] and 6 of 7 feeding arteries [85.7%]). Anterior cerebral artery-derived pial arterial supply was identified in 2 of 14 patients (14.3%).
Among the 19 patients with falx meningiomas, 25 tumor-feeding arteries originating from the tumor side and 20 tumor-feeding arteries originating from the non-tumor side were identified (Table 1). Similar to parasagittal meningiomas, the lateral branch derived from the anterior division of the MMA on the tumor and non-tumor sides was frequently identified as the tumor-feeding artery in anterior and middle falx meningiomas (tumor side: 13 of 17 patients [76.5%] and 13 of 31 feeding arteries [41.9%]) (non-tumor side: 9 of 17 patients [52.9%] and 9 of 31 feeding arteries [29.0%]). Meanwhile, tumor-feeding arteries derived from extracranial arteries were frequently identified in posterior falx meningiomas (2 of 2 patients [100%] and 7 of 14 feeding arteries [50.0%]). Anterior cerebral artery-derived pial arterial supply was identified in 10 of 19 patients (52.6%) and common among those with anterior falx meningioma (7 of 10 patients [70.0%]).
Feeding arteries of skull base meningiomas
Tumor-feeding arteries were identified in 111 of the 113 patients with skull base meningiomas (98.2%). Details of the tumor-feeding arteries of skull base meningiomas at each attachment site are shown in Tables 2, 3, 4, 5, 6 and 7 and Fig. 3.
Table 6.
Number of feeders per subdivided attachment in the anterior skull base and sphenoid ridge meningioma
| Tumor attachment | OG | OR | TS | Diffuse | ACP | M to L | |||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| The number of patients (with bilateral tumor attachment) | 7 (0) | 4 (3) | 2 (2) | 4 (3) | 11 (0) | 24 (0) | |||||||
| Laterality | T | NT | T | NT | T | NT | T | NT | T | NT | T | NT | |
| ECA | MMA, anterior division, lateral branch | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 9 | 0 |
| MMA, anterior division, medial branch | 0 | 0 | 2 | 0 | 0 | 0 | 2 | 1 | 4 | 0 | 16 | 0 | |
| Accessory meningeal artery | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 6 | 0 | |
| Artery of the foramen rotundum | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 3 | 0 | 10 | 0 | |
| Superficial temporal artery | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | |
| Sphenoparatine artery | 3 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| Middle deep temporal artery | 0 | 0 | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 6 | 0 | |
| ICA | MHT, tentorial trunk | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 3 | 0 | 5 | 0 |
| MHT, dorsal meningeal artery | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | |
| MHT, inferior hypophyseal artery | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 0 | 1 | 0 | |
| ILT, superior division, medial tentorial artery | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 2 | 0 | 0 | 0 | |
| ILT, anterior division, medial branch | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 0 | 4 | 0 | 4 | 0 | |
| ILT, anterior division, lateral branch | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | |
| Capsular artery | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 0 | 0 | 0 | |
| OphA, AEA, anterior meningeal artery | 2 | 1 | 1 | 0 | 1 | 0 | 1 | 0 | 0 | 0 | 0 | 0 | |
| OphA, posterior ethmoidal artery | 3 | 2 | 4 | 0 | 2 | 0 | 6 | 0 | 0 | 0 | 3 | 0 | |
| OphA, deep recurrent ophthalmic artery | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 3 | 0 | |
| OphA, superficial recurrent ophthalmic artery | 0 | 0 | 1 | 0 | 2 | 0 | 3 | 1 | 4 | 0 | 1 | 0 | |
| OphA, lacrimal artery | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 8 | 0 | |
T tumor side, NT non-tumor side, OG olfactory groove, OR orbital roof, TS tuberculum sellae, ACP anterior clinoid process, M to L middle-to-lateral, MMA middle meningeal artery, MHT meningohypophyseal trunk, ILT inferolateral trunk, OphA ophthalmic artery, AEA anterior ethmoidal artery, ICA ECA external carotid artery
Table 7.
Number of feeders per subdivided attachment in the petrous meningioma
| Tumor attachment | Petroclival | Petrous apex | Posterior petrous | Diffuse | |||||
|---|---|---|---|---|---|---|---|---|---|
| The number of patients (with bilateral tumor attachment) | 20 (0) | 8 (0) | 5 (0) | 4 (0) | |||||
| Laterality | T | NT | T | NT | T | NT | T | NT | |
| ECA | APhA, carotid branch | 2 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
| APhA, jugular branch | 1 | 0 | 1 | 0 | 1 | 0 | 2 | 0 | |
| APhA, hypoglossal branch | 4 | 1 | 0 | 0 | 1 | 0 | 0 | 0 | |
| OA, mastoid branch | 0 | 0 | 0 | 0 | 2 | 0 | 0 | 0 | |
| MMA, anterior division, medial branch | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| MMA, posterior division, petrosquamosal branch | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| MMA, petrosal branch | 10 | 0 | 1 | 0 | 1 | 0 | 4 | 0 | |
| Accessory meningeal artery | 5 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | |
| ICA | MHT, tentorial trunk | 6 | 0 | 5 | 0 | 0 | 0 | 2 | 0 |
| MHT, dorsal meningeal artery | 9 | 5 | 2 | 0 | 0 | 0 | 0 | 0 | |
| ILT, superior division,medial tentorial artery | 7 | 0 | 1 | 0 | 0 | 0 | 0 | 0 | |
| ILT, anterior division, medial branch | 1 | 0 | 1 | 0 | 0 | 0 | 0 | 0 | |
| OphA, superficial recurrent ophthalmic artery | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| VA: anterior meningeal artery | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | |
| AICA: subarcuate artery | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | |
T tumor side, NT non-tumor side, APhA ascending pharyngeal artery, OA occipital artery, MMA middle meningeal artery, MHT meningohypophyseal trunk, ILT inferolateral trunk, OphA ophthalmic artery, ICA internal carotid artery, ECA external carotid artery, VA vertebral artery, AICA anterior inferior cerebellar artery
Fig. 3.
Schematic representation of the main tumor-feeding arteries in skull base meningiomas. TS, tuberculum sellae; MMA, middle meningeal artery; ACP, anterior clinoid process; M to L, middle-to-lateral; AFR, artery of the foramen rotundum; AccMA, accessory meningeal artery; IHA, inferior hypophyseal artery; OA, occipital artery; DMA, dorsal meningeal artery; MHT, meningohypophyseal trunk; ILT, inferolateral trunk; AphA, ascending pharyngeal artery
In 17 patients with anterior skull base meningiomas, 45 tumor-feeding arteries were identified (Tables 2, 4, and 6). The posterior ethmoidal artery originating from the ophthalmic artery was the most frequently identified tumor-feeding artery in anterior skull base meningiomas (13 of 17 patients [76.5%] and 17 of 45 feeding arteries [37.8%]). A similar trend was observed in the olfactory groove, orbital roof, tuberculum sellae, or diffuse type (Tables 4 and 6). When the tumor attachment extended to the tuberculum sellae, the superficial recurrent ophthalmic artery derived from the ophthalmic artery was identified as the tumor-feeding artery (4 of 6 patients [66.7%] and 6 of 22 feeding arteries [27.2%], including the tuberculum sellae and diffuse type) (Table 6).
Ninety-eight tumor-feeding arteries were identified in 35 patients with sphenoid ridge meningiomas (Tables 2, 4, and 6). The medial branch derived from the anterior division of the MMA was frequently identified as the tumor-feeding artery in sphenoid ridge meningiomas (20 of 35 patients [57.1%] and 20 of 98 feeding arteries [20.4%]) (Tables 2 and 6). Similar trends were observed in ACP and middle-to-lateral sphenoid ridge meningiomas (Table 6). In ACP meningiomas, the superficial recurrent ophthalmic artery (4 of 11 patients[36.4%] and 4 of 23 feeding arteries [17.4%]) and the medial branch derived from the anterior division of the ILT (deep recurrent ophthalmic artery) (4 of 11 patients[36.4%] and 4 of 23 feeding arteries [17.4%]) frequently functioned as the tumor-feeding arteries (Table 6). Furthermore, the tentorial trunk of the MHT and the medial tentorial artery derived from the superior division of the ILT frequently served as the tumor-feeding arteries (4 of 11 patients[36.4%] and 5 of 23 feeding arteries [21.7%]) (Table 6). In middle-to-lateral sphenoid ridge meningiomas, the arteries of the foramen rotundum (AFR) and accessory meningeal artery (AccMA), the two arteries located close to the skull base, frequently functioned as the tumor-feeding arteries (13 of 24 patients [54.2%] and 16 of 75 feeding arteries [21.3%]) (Table 6).
In six patients with sphenopetroclival meningiomas, 26 tumor-feeding arteries were identified (Tables 2 and 4). The inferior hypophyseal arteries derived from the MHT (4 of 6 patients [66.7%] and 4 of 26 feeding arteries [15.4%]) and AFR (4 of 6 patients [66.7%] and 4 of 26 feeding arteries [15.4%]) were more frequently identified as the tumor-feeding arteries in sphenopetroclival meningiomas (Tables 2 and 4). Other tumor-feeding arteries branched from various dural arteries originating from the AccMA, MMA, MHT, ILT, and ophthalmic arteries, with an average of 4.3 tumor-feeding arteries identified per case.
Eighty-one tumor-feeding arteries were identified in 37 patients with petrous meningiomas (Tables 2, 4, and 7). The petrosal branch of the MMA was the most common tumor-feeding artery identified in petrous meningiomas (16 of 37 patients [43.2%] and 16 of 81 feeding arteries [19.8%]) (Table 2). However, the prevalence of tumor-feeding arteries developing in petrous meningiomas differed according to their attachment sites. The dorsal meningeal artery derived from MHT was more common in petroclival meningiomas (11 of 20 patients [55.0%] and 14 of 55 feeding arteries [25.5%]), tentorial arteries derived from ILT and MHT in petrous apex meningiomas (6 of 8 patients [75.0%] and 6 of 11 arteries [54.5%]), and dural branches from the ascending phalyngeal artery (2 of 5 patients [40.0%] and 2 of 5 feeding arteries [40.0%]) and OA (2 of 5 patients [40.0%] and 2 of 5 feeding arteries [40.0%]) in posterior petrous meningiomas (Table 7). Furthermore, 7 of 28 patients (25.0%) with petroclival and petrous apex meningiomas had tumor-feeding arteries originating from the ascending pharyngeal artery (9 of 66 feeding arteries [13.6%]) (Table 7).
Sixteen tumor-feeding arteries were identified in ten patients with tentorial meningiomas (Tables 3 and 5). The dural branch of the MMA was the most common tumor-feeding artery identified in tentorial meningiomas (6 of 10 patients [60.0%] and 6 of 16 feeding arteries [37.5%]) (Table 3). Various tumor-feeding arteries derived from the ECA, ICA, and VA were observed in tentorial meningiomas.
Seven tumor-feeding arteries were identified in four patients with cerebellar convexity meningiomas (Tables 3 and 5). The dural branch of the OA was the most common tumor-feeding artery in cerebellar convexity meningiomas (4 of 4 patients [100%] and 4 of 7 feeding arteries [57.1%]) (Table 3).
Five tumor-feeding arteries were identified in four patients with foramen magnum meningiomas (Tables 3 and 5). The dural artery, derived from the anterior and posterior meningeal arteries, was the most common tumor-feeding artery identified in foramen magnum meningiomas (3 of 4 patients [75.0%] and 3 of 5 feeding arteries [60.0%]) (Table 5).
Discussion
This study comprehensively evaluated the feeding arteries of meningiomas in the entire intracranial dural region. Previous reports on feeders throughout intracranial meningiomas have not evaluated detailed branches of dural arteries (e.g., MMA, AphA, OphA, MHT, and ILT branches have not been classified) [4], and this is the most detailed report on the origin of feeders throughout intracranial meningiomas. A variety of tumor-feeding arteries were identified, reflecting the complex arterial network of the dura mater [13], with specific trends depending on the site of origin. Preoperative DSA is not usually performed in all patients undergoing meningioma surgery owing to the invasive nature of angiography [24], and the details of the tumor-feeding arteries are not always available preoperatively. Therefore, knowledge of the location of the tumor-feeding arteries is essential for proper hemostasis during surgery. This study's results provide a detailed map of meningioma feeders, which should lower complication rates and increase tumor removal rates. In addition, the findings of this study may serve as a useful reference for identifying which vessels should be carefully examined during preoperative angiography.
Characteristics of tumor-feeding arteries in non-skull base meningiomas
In non-skull base meningiomas, the MMA and extracranial arteries such as the STA and OA frequently function as the tumor-feeding arteries (Table 1). In non-skull base meningiomas, the MMA predominantly serves as the tumor-feeding artery in the anterior and middle regions. By contrast, the extracranial artery functions as the tumor-feeding artery in the posterior region. This pattern may be attributed to the posterior region’s distance from the MMA origin and its proximity to the extracranial arteries [13]. Moreover, parasagittal and falx meningiomas often have tumor-feeding arteries extending from the non-tumor side (Table 1). Additionally, a relatively high frequency of pial arterial supply was observed, particularly in the anterior falx meningiomas. In these tumor-feeding arteries, particular attention should be paid to the location of the MMA-derived tumor-feeding arteries extending from the non-tumor side, which is relatively common in falx meningiomas. Because the tumor-feeding artery, derived from the MMA on the non-tumor side, runs along the inferior wall of the superior sagittal sinus and is distributed to the falx [13], it cannot be severed until the tumor attachment site is cut if a unilateral craniotomy is performed on the tumor side. To devascularize this tumor-feeding artery early, preoperative embolization or bilateral craniotomy should be performed across the superior sagittal sinus to sever the non-tumor-side MMA in the convexity dura. In addition, surgeons should watch out for the presence of pial arterial feeders, as they often lie in close proximity to normal arteries, and should only sacrifice the arteries present in the epiarachnoid plane. In the present study, tumor-feeding arteries originating from the dural branch of the anterior cerebral artery could not be explicitly identified. This is likely because, when anterior cerebral artery-derived feeders are present, it is often challenging to distinguish between pial arterial feeders and the dural branch of the anterior cerebral artery.
Characteristics of tumor-feeding arteries in anterior skull base meningiomas
In anterior skull base meningiomas, tumor-feeding arteries originating from the posterior ethmoidal arteries were frequently observed, consistent with the distribution pattern of the dural arteries (Table 4) [9, 13]. Furthermore, in alignment with the distribution of the dural arteries, the prevalence of tumor-feeding arteries originating from superficial recurrent ophthalmic arteries increased as the tumor extended to the tuberculum sellae (Tables 4 and 6) [9, 13]. Anterior skull base meningiomas are usually resected using a basal interhemispheric or frontotemporal approach. The superficial recurrent ophthalmic artery branches from the ophthalmic artery in the optic canal, passes along the side of the optic nerve, and spreads from the ACP to the tuberculum sellae (Fig. 4) [13]. Therefore, it is difficult to sever this artery early during surgery owing to its deep-seated location in the surgical field and its proximity to critical structure, regardless of the approach used. If there is a tumor-feeding artery branching from the superficial recurrent ophthalmic artery, assuming that the area near the optic canal is prone to bleeding, it may be advisable to create space by internal decompression, and after confirming the location of the optic nerve, devascularization of the tumor by cutting the tumor attachment near the optic canal (Fig. 4).
Fig. 4.
Imaging and intraoperative findings of the superficial recurrent ophthalmic artery developed as a tumor-feeding artery in the tuberculum sellae meningioma. Contrast-enhanced magnetic resonance imaging shows a slightly right-sided tuberculum sellae meningioma (a). The preoperative lateral view of the right side internal carotid artery angiography shows a tumor stain (asterisk) (b), and the three-dimensional digital subtraction angiography shows a superficial recurrent ophthalmic artery that had developed as a tumor-feeding artery (arrowhead) (c). Intraoperatively, the tumor-feeding artery derived from the superficial recurrent ophthalmic artery (arrowhead) has migrated into the tumor from just inside the right optic nerve (d). After tumor resection and the opening of the superior wall of the optic canal, the severed end of the superficial recurrent ophthalmic artery (cauterized) is identified in the medial part of the optic canal (circle) (e). Asterisk (b): tumor staining; arrowhead (c and d): superficial recurrent ophthalmic artery; circle (e): severed end of the superficial recurrent ophthalmic artery. ACA, anterior cerebral artery; MCA, middle cerebral artery; OphA, ophthalmic artery; CNII, optic nerve; TS, tuberculum sellae
Characteristics of tumor-feeding arteries in sphenoid ridge meningiomas
Both ACP and middle-to-lateral sphenoid ridge meningiomas had a high frequency of developing tumor-feeding arteries originating from the MMA (Table 6). However, ACP meningiomas also had a high frequency of developing tumor-feeding arteries originating from the superficial recurrent ophthalmic arteries and arteries branching from the MHT or ILT, while middle-to-lateral sphenoid ridge meningiomas had a higher frequency of developing tumor-feeding arteries originating from the AFR or AccMA (Table 6). Sphenoid ridge meningiomas are often resected using the frontotemporal or orbitozygomatic approaches. During surgery for ACP meningiomas, the superficial recurrent ophthalmic artery should be severed after confirming the location of the optic nerve, similar to anterior skull base meningiomas. The devascularization of the tumor-feeding arteries derived from the MHT and ILT was achieved by cutting the tumor attachment site. However, as the oculomotor nerve runs near these tumor-feeding arteries [13], care must be taken to avoid damaging the oculomotor nerve during devascularization. During surgery for middle-to-lateral sphenoid ridge meningiomas, the tumor-feeding arteries that penetrate the temporal base, such as the AFR and AccMA, can be severed early by performing a craniotomy to expand access to the temporal base and the extradural middle fossa dural peeling technique [15]. However, if the superficial middle cerebral vein or uncal vein drains into the pterygoid plexus through the foramen ovale or foramen rotundum, cauterization of these arteries near the foramen ovale or foramen rotundum is challenging owing to the risk of venous infarction [1, 5, 7, 11, 16, 19, 25]. Therefore, preoperative embolization should be considered in these cases.
Characteristics of tumor-feeding arteries in petrous meningiomas
Although the prevalence of the petrosal branch of the MMA becoming a tumor-feeding artery was higher in all petrous meningiomas, the frequency of tumor-feeding arteries originating from the MHT and ILT was higher when the attachment site was closer to the midline, as in the petroclival and petrous apex meningiomas (Table 7). Petroclival and petrous apex meningiomas are usually resected using the anterior transpetrosal approach [1–3]. However, these feeders from the MHT and ILT are located deep in the surgical field and are difficult to detect early during surgery. Furtheremore, MHT and ILT are difficult to embolize preoperatively owing to their tortuous appearance, making it difficult to insert a microcatheter [26]. However, recent studies reported that the distal balloon protection technique (the para-para method) is more effective in the preoperative embolization of these arteries and may be advantageous when tumor blood flow is abundant [26]. Furthermore, tumor-feeding arteries originating from the ascending pharyngeal artery are difficult to sever, and the tumor removal rates are reportedly reduced when this artery develops as a tumor-feeding artery in petroclival and petrous apex meningiomas [2]. As shown in the present study, the proportion of ascending pharyngeal arteries developing as tumor-feeding arteries in petroclival and petrous apex meningiomas was not high (7 of 28 patients [25.0%]) but was non-negligible. As tumor-feeding arteries influence the tumor removal rates [2], preoperative DSA should be considered to determine the presence of any tumor-feeding arteries that may be an obstacle to tumor removal.
Characteristics of tumor-feeding arteries in sphenopetroclival meningiomas
The tumor-feeding arteries of sphenopetroclival meningiomas have the characteristics both sphenoid ridge and petroclival meningiomas. In addition to the tumor-feeding arteries from the MMA petrosal branch, tumor-feeding arteries that penetrated the skull base, such as the AFR and AccMA, and tumor-feeding arteries derived from the MHT and ILT were frequently observed (Tables 2 and 4). The extension of sphenopetroclival meningiomas across multiple dural arterial territories resulted in the highest number of tumor-feeding arteries identified among skull base meningiomas (4.3 per case). To achieve the devascularization of sphenopetroclival meningiomas, similar to sphenoid ridge meningioma and petrous meningioma, the early devascularization of the AFR, AccMA, MHT, or ILT must be considered during surgery along with the extradural middle fossa dural peeling technique and/or preoperative embolization.
Characteristics of tumor-feeding arteries in tentorial meningiomas
Tentorial meningiomas showed various tumor-feeding arteries derived from the ECA, ICA, and VA (Tables 3 and 5). This observation reflects the formation of a complex network of dural arteries in the cerebellar tent, which has a large area [13]. Tentorial meningiomas are usually resected using the posterior approach. Therefore, of the tumor-feeding arteries observed in this study, the most difficult to devascularize would be the tentorial arteries derived from MHT and ILT that are distributed to the tumor found in the deepest portion of the operative field [13]. Since these tentorial arteries are difficult to sever until most of the tumor has been removed, preoperative embolization using the distal balloon protection technique described above should be considered if tumor stains from these arteries are prominent [26].
Characteristics of tumor-feeding arteries in cerebellar convexity and foramen magnum meningiomas
In cerebellar convexity meningiomas, tumor-feeding arteries originating from the OA and MMA were more frequent (Table 3), and many tumor-feeding arteries were easily devascularized during surgery. Meanwhile, tumor-feeding arteries, such as the hypoglossal branches of the ascending pharyngeal artery and anterior meningeal artery, were observed in the foramen magnum meningioma (Tables 3 and 5). These arteries were difficult to sever early in surgery, especially when the tumor attachment area was located from the anterior to the lateral region of the foramen magnum. Hence, exposing the dura mater near the hypoglossal canal using a transcondylar fossa approach for the ascending pharyngeal artery or performing preoperative embolization of the anterior meningeal artery should be considered [20].
Limitation
In this study, the number of patients included in the six-vessel study was limited, suggesting that some tumor-feeding arteries may not have been recognized. As this was a retrospective study of patients who underwent preoperative DSA and considering the variability in the surgical difficulty among meningiomas, demonstrating the changes in clinical outcomes based on the preoperative identification of tumor-feeding arteries proves challenging. Furthermore, the number of cases per attachment site was limited, underscoring the need for further studies with larger sample sizes to substantiate findings.
Conclusions
This study evaluated the details of tumor-feeding arteries in meningiomas, revealing a consistent trend of such arteries at each tumor attachment site. Superficial recurrent ophthalmic arteries and MHT- or ILT-derived tumor-feeding arteries are often observed, especially in skull base meningiomas. Hence, appropriately severing these arteries during surgery is crucial. Identifying the tumor-feeding arteries that could impede tumor removal based on the anatomical findings presented in this study and determining the appropriate extent of craniotomy are advisable. The results of this study could help enhance the safety and efficacy of surgery, especially in patients with meningiomas who have not undergone preoperative angiography.
Acknowledgements
The authors would like to thank Editage (www.editage.com ) for providing excellent English language editing assistance.
Author contributions
KY contributed to the study conception and design. KY, SH, and EF performed the data collection. KY performed the data analysis. KY contributed to the writing of the article. All authors contributed to the revision of the article.
Funding
The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.
Data availability
No datasets were generated or analysed during the current study.
Declarations
Competing interests
The authors declare no competing interests.
Ethical approval
This study was approved by the Ethics Review Board of Fujita Health University (approval no. HM23 - 432). All examinations and treatments were performed after obtaining written informed consent from the patients. Participation in the study was retrospective, and an opt-out method was employed.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
References
- 1.Adachi K, Hayakawa M, Ishihara K, Ganaha T, Nagahisa S, Hasegawa M, Hirose Y (2016) Study of Changing Intracranial Venous Drainage Patterns in Petroclival Meningioma. World Neurosurg 92:339–348. 10.1016/j.wneu.2016.05.019 [DOI] [PubMed] [Google Scholar]
- 2.Adachi K, Hasegawa M, Tateyama S, Kawazoe Y, Hirose Y (2018) Surgical Strategy for and Anatomic Locations of Petroapex and Petroclival Meningiomas Based on Evaluation of the Feeding Artery. World Neurosurg 116:e611–e623. 10.1016/j.wneu.2018.05.052 [DOI] [PubMed] [Google Scholar]
- 3.Adachi K, Hasegawa M, Hirose Y (2021) Prediction of trigeminal nerve position based on the main feeding artery in petroclival meningioma. Neurosurg Rev 44:1173–1181. 10.1007/s10143-020-01313-3 [DOI] [PubMed] [Google Scholar]
- 4.Ahmed AK, Wilhelmy B Jr, Oliver J et al (2023) Variability in the Arterial Supply of Intracranial Meningiomas: An Anatomic Study. Neurosurgery 93:1346–1352. 10.1227/neu.0000000000002608 [DOI] [PubMed] [Google Scholar]
- 5.Almefty R, Dunn IF, Pravdenkova S, Abolfotoh M, Al-Mefty O (2014) True petroclival meningiomas: results of surgical management. J Neurosurg 120:40–51. 10.3171/2013.8.JNS13535 [DOI] [PubMed] [Google Scholar]
- 6.Chen L, Li DH, Lu YH, Hao B, Cao YQ (2019) Preoperative Embolization Versus Direct Surgery of Meningiomas: A Meta-Analysis. World Neurosurg 128:62–68. 10.1016/j.wneu.2019.02.223 [DOI] [PubMed] [Google Scholar]
- 7.Hafez A, Nader R, Al-Mefty O (2011) Preservation of the superior petrosal sinus during the petrosal approach. J Neurosurg 114:1294–1298. 10.3171/2010.6.JNS091461 [DOI] [PubMed] [Google Scholar]
- 8.Hattori K, Miyachi S, Kobayashi N et al (2005) Contralateral meningeal artery supply of paramedian meningiomas. Surg Neurol 64:242–248; discussion 248. 10.1016/j.surneu.2005.02.006 [DOI] [PubMed]
- 9.Hiramatsu M, Sugiu K, Hishikawa T et al (2020) Detailed Arterial Anatomy and Its Anastomoses of the Sphenoid Ridge and Olfactory Groove Meningiomas with Special Reference to the Recurrent Branches from the Ophthalmic Artery. AJNR Am J Neuroradiol 41:2082–2087. 10.3174/ajnr.A6790 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Ichimura S, Kawase T, Onozuka S, Yoshida K, Ohira T (2008) Four subtypes of petroclival meningiomas: differences in symptoms and operative findings using the anterior transpetrosal approach. Acta Neurochir (Wien) 150:637–645. 10.1007/s00701-008-1586-x [DOI] [PubMed] [Google Scholar]
- 11.Ichimura S, Yoshida K, Kagami H et al (2012) Epidural anterior petrosectomy with subdural visualization of sphenobasal vein via the anterior transpetrosal approach--technical case report. Neurosurg Rev 35:609–613; discussion 613–604. 10.1007/s10143-012-0405-2 [DOI] [PubMed]
- 12.Lasjaunias P, Moret J, Mink J (1977) The anatomy of the inferolateral trunk (ILT) of the internal carotid artery. Neuroradiology 13:215–220. 10.1007/BF00344216 [DOI] [PubMed] [Google Scholar]
- 13.Martins C, Yasuda A, Campero A, Ulm AJ, Tanriover N, Rhoton A, Jr. (2005) Microsurgical anatomy of the dural arteries. Neurosurgery 56:211–251; discussion 211–251. 10.1227/01.neu.0000144823.94402.3d [DOI] [PubMed]
- 14.Meling TR, Da Broi M, Scheie D, Helseth E (2019) Meningiomas: skull base versus non-skull base. Neurosurg Rev 42:163–173. 10.1007/s10143-018-0976-7 [DOI] [PubMed] [Google Scholar]
- 15.Muhsen BA, Najera E, Borghei-Razavi H, Adada B (2022) Extended Middle Fossa Approach for Trigeminal Schwannoma Resection. J Neurol Surg B Skull Base 83:e615. 10.1055/s-0041-1727108 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Nakase H, Shin Y, Nakagawa I, Kimura R, Sakaki T (2005) Clinical features of postoperative cerebral venous infarction. Acta Neurochir (Wien) 147:621–626; discussion 626. 10.1007/s00701-005-0501-y [DOI] [PubMed]
- 17.Raz E, Cavalcanti DD, Sen C et al (2022) Tumor embolization through meningohypophyseal and inferolateral trunks is safe and effective. AJNR Am J Neuroradiol 43:1142–1147. 10.3174/ajnr.A7579 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Robinson DH, Song JK, Eskridge JM (1999) Embolization of meningohypophyseal and inferolateral branches of the cavernous internal carotid artery. AJNR Am J Neuroradiol 20:1061–1067 [PMC free article] [PubMed] [Google Scholar]
- 19.Shibao S, Toda M, Orii M, Fujiwara H, Yoshida K (2016) Various patterns of the middle cerebral vein and preservation of venous drainage during the anterior transpetrosal approach. J Neurosurg 124:432–439. 10.3171/2015.1.JNS141854 [DOI] [PubMed] [Google Scholar]
- 20.Shimizu S, Garcia AS, Tanriover N, Fujii K (2004) The so-called anterior meningeal artery: an anatomic study for treatment modalities. Interv Neuroradiol 10:293–299. 10.1177/159101990401000402 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Waldron JS, Sughrue ME, Hetts SW et al (2011) Embolization of skull base meningiomas and feeding vessels arising from the internal carotid circulation. Neurosurgery 68:162–169. 10.1227/NEU.0b013e3181fe2de9 [DOI] [PubMed] [Google Scholar]
- 22.Yamaki T, Tanabe S, Sohma T, Uede T, Shinya T, Hashi K (1988) Feeding arteries of parasellar meningiomas–angiographic study of medial sphenoid ridge and tuberculum sellae meningiomas. Neurol Med Chir (Tokyo) 28:553–558. 10.2176/nmc.28.553 [DOI] [PubMed] [Google Scholar]
- 23.Yamashiro K, Muto J, Wakako A et al (2021) Diploic veins as collateral venous pathways in patients with dural venous sinus invasion by meningiomas. Acta Neurochir (Wien). 10.1007/s00701-021-04777-4 [DOI] [PubMed] [Google Scholar]
- 24.Yamashiro K, Wakako A, Omi T et al (2022) Evaluating diploic vein blood flow using time-resolved whole-head computed tomography angiography and determining the positional relationship between typical craniotomy approaches and diploic veins in patients with meningioma. Acta Neurochir (Wien). 10.1007/s00701-022-05349-w [DOI] [PubMed] [Google Scholar]
- 25.Yamashiro K, Aadchi K, Omi T, Hayakawa M, Sadato A, Hasegawa M, Hirose Y (2023) Anatomical variations and flow alterations of the uncal vein and its clinical implications in petroclival meningiomas. Acta Neurochir (Wien) 165:1727–1738. 10.1007/s00701-023-05590-x [DOI] [PubMed] [Google Scholar]
- 26.Yamashiro K, Hayakawa M, Adachi K, Hasegawa M, Hirose Y (2024) Tumor embolization via the meningohypophyseal and inferolateral trunk in patients with skull-based tumors by using the distal balloon protection technique. AJNR Am J Neuroradiol. 10.3174/ajnr.A8169 [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
No datasets were generated or analysed during the current study.