Abstract
Purpose
This study aimed to evaluate the topographic features and branches of the middle meningeal artery (MMA) by three-dimensional rotational angiography (3DRA) and describe its variations’ radiological classification based on previous clinical examples of cadaver studies and literature.
Methods
We consecutively evaluated 87 cerebral hemispheres, including 32 females and 49 right sides between May 2020 and December 2021 who had undergone unilateral or bilateral cerebral and carotid artery 3D rotational angiography imaging by CCA injection and between 18 and 76-years-old. Maximum intensity projection images with 10–30 mm slice thickness were used for the morphological evaluations and measurements of MMA and its foramen, canal, and branches.
Results
The diameters of the common carotid artery, internal carotid artery, and external carotid artery were significantly smaller in females than in men (p = 0.021, 0.021, and <0.001, respectively). According to the branching pattern, the most common pattern of the MMA was Type Ia (49.4%). The ophthalmic artery completely originated from MMA in the 1 (1.1%) cerebral hemisphere. The MMA arises from the ophthalmic artery in 2 cerebral hemispheres (2.3%), and the ophthalmic artery and maxillary artery in 2 cerebral hemispheres (2.3%).
Conclusion
It was observed that the branching pattern may show differences when compared to the cadaver studies with a radiologic evaluation with 3D-RA.
Keywords: middle meningeal artery, variation, rotational angiography, variation, cone-beam computer tomography
Introduction
The MMA, which feeds more than two-thirds of the cranial dura, is the most significant dural artery. 1 The MMA is among the biggest branches of the external carotid artery (ECA), originating primarily from the maxillary artery (MA) but sometimes from the basilar artery or the internal carotid artery (ICA). 1 The foramen spinosum is crossed by MMA, which follows the temporal fossa anteriorly and laterally and acquires its characteristic appearance on DSA. In English literature, two studies described intracranial segments of the MMA.1,2 Merland et al. described branches based on cerebral angiographies as temporobasal segment, temporopterional segment, and coronal segment. 2 Martins et al. described branches based on cadaveric dissections as petrosal branches, cavernous branches, and anterior and posterior divisions. 1 In the posterior fossa, the front medial area, and the peri- and cavernous regions, the MMA has several anastomoses with branches originating from the ICA, ECA, and vertebrobasilar system. Another aspect that makes MMA different is its embryological development and numerous anatomical variations. 3
Three-dimensional rotational angiography (3D-RA) is an x-ray based medical imaging technique that provides an assessment of the arterial system via injected contrast material through a catheter using a fixed C-arm angiography device and acquires three-dimensional images like computed tomography. 4 Nowadays, 3D-RA is regarded as the best technique of catheter angiography to assess the intracranial and extracranial carotid artery and its branches.4–6 3D-RA makes an additional contribution to the detection and evaluation of intracranial structures. After the post-processing stages of the 3D dataset, it allows for obtaining high-resolution images in any projection without bone subtraction. These images provide flexible viewing angles, which is an advantage of 3D-RA, compared to Digital Subtraction Angiography (DSA). 6 Furthermore, 3DRA allows for the assessment of submillimeter arteries and their interactions with the surrounding tissues. 5 In addition, all of these, the evaluation of in vivo anatomy is among the most significant advantages of radiology compared to cadaver study. 6 Radiological examinations reveal organs and tissues in their natural state, but it is important to note that this study examined arteries with CCA injection. Fundamentally, radiological studies would be able to better evaluate medical records and patient comorbidities. To our knowledge, no radiologic research has been identified in the current literature that evaluates the MMA with the advantages of this imaging technique.
The focus of this research was to use three-dimensional rotational angiography to examine the topographic features and branches of the middle meningeal artery (MMA) and to describe the radiological classification of its variations based on previous clinical examples from cadaver studies and literature.
Materials and methods
51 adult cases who underwent unilateral or bilateral cerebral and carotid artery 3D rotational angiography imaging by CCA injection were included in the study. Common carotid artery, ICA, ECA, maxillary artery, middle meningeal artery diameters, foramen spinosum diameter and length, bony canal diameter, and length were measured and evaluated according to age, side, and gender. The origin and branching pattern of the middle meningeal artery were evaluated according to age, side, and gender. The relationship between the middle meningeal artery bifurcation and the pterion, the temporal fossa course of the middle meningeal artery regarding the sphenosquamosal suture were evaluated according to age, side, gender, and branching pattern.
Population
Patients examined with unilateral or bilateral cerebral and carotid artery DSA with 3D-RA via common carotid artery injection were evaluated for inclusion between May 2020 and December 2021. Exclusion criteria are defined as dento-facial deformities and occlusion or severe stenosis (more than 70%) of the ECA. Of the fifty-one adult patients (mean age: 50.06 ± 12.96 years) 19 males and 32 females were included according to the criteria. Thirty-six patients were bilaterally imaged, and in total 87 cerebral hemispheres were examined with 3D-RA images. All procedures performed in the studies involving human participants were by the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants included in the study.
3DRA And CBCT image protocols
The 3D-RA and flat-panel CBCT data were acquired using a monoplane flat-panel angiography system (Allura Xper FD20, Philips Medical Systems, the Netherlands). The “Cerebral Prop Scan” acquisition protocol was used. Raw data were acquired with a diagnostic catheter located in the common carotid artery. The contrast medium (300 mg I/mL) was infused with a rate of 4 mL/s for 6 s (total volume of 24 mL) with a 2-s imaging delay. After post-processing of raw data, very high spatial resolution CBCT reconstructions with 0.14–0.36 mm slice thickness were obtained and evaluated with Digital Imaging and Communications in Medicine (DICOM) viewing software (Medixant. RadiAnt DICOM Viewer [Software]. Version 2021.1. Jun 27, 2021. URL: https://www.radiantviewer.com). 6
Image analysis
For each patient, Cone Beam Computer Tomography (CBCT) image analysis was completed by two radiologists with consensus using Allura 3D-RA 6.4.6 on a workstation. 6 The reviewers could manipulate the images to optimize the visualization of vascular structures for the evaluation of morphological findings. The measurements were made using the same anatomical landmarks for standardization on the multiplanar reconstruction screen. The CCA was measured in the distal segment, proximal to the CCA bifurcation, perpendicular to the vessel wall. The ICA and ECA were measured in the proximal segment, distal to the CCA bifurcation, perpendicular to the vessel wall. The bony canal length measurement was measured by obtaining the long axis with MPR images.
The morphological evaluations and measurements of MMA were made on maximum intensity projection images with 10–30 mm slice thickness.
First of all, MMA was evaluated according to whether the origin is MMA or not, secondly, the branching pattern in the segment before the bone canal was evaluated. The morphological evaluation of branching pattern was classified according to the previous cadaver and radiology studies.
Statistical analysis
SPSS software (ver. 21.0 for Windows; SPSS Inc., Chicago, IL, USA) was used for statistical analysis. Descriptive statistics are given with mean, standard deviation, median, minimum, and maximum values or with frequency and percent for continuous or qualitative variables respectively. The Shapiro–Wilk test was used for the test of normality. The independent samples t-test was used for two-group comparisons of normally distributed variables. For non-normally distributed variables, the Kruskal–Wallis test was performed for independent group comparisons. The Bonferroni-corrected Mann–Whitney U test was used for post-hoc analysis. A p-value below 0.05 was assumed to be statistically significant for all statistical comparisons.
Results
A total of 87 adult cerebral hemispheres were examined, containing 32 females (62.7%) and 44 left sides (50.6%).
The mean diameter of the CCA was 6.53 ± 0.87 mm in women and 7.20 ± 0.99 mm in men, the mean diameter of the ICA was 5.04 ± 1.00 mm (min-max: 3.22–7.60 mm) in women and 5.56 ± 0.91 mm in men, the mean diameter of the ECA was 3.91 ± 0.59 mm in women and 4.62 ± 0.66 mm in men. Females had significantly smaller the common carotid artery, ICA, and ECA diameters than men (p = 0.021, 0.021, and <0.001, respectively). Age, gender, or the sizes of other arteries had no significant relationship (p > 0.05). The diameters of the CCA, ECA, MA, and MMA are given in Table 1.
Table 1.
The diameters of the common carotid artery, internal carotid artery, external carotid artery, maxillary artery and middle meningeal artery.
| Artery | Gender | Mean ± SD (diameter) (mm) | Median (diameter) (mm) | Minimum-Maximum (diameter) (mm) | p value |
|---|---|---|---|---|---|
| Common carotid artery | Female | 6.53 ± 0.87 | 6.35 | 5.00–8.60 | 0.021 |
| Male | 7.20 ± 0.99 | 7.05 | 5.60–8.64 | ||
| Internal carotid artery | Female | 5.04 ± 1.00 | 5.10 | 3.22–7.60 | 0.021 |
| Male | 5.56 ± 0.91 | 5.60 | 3.80–7.50 | ||
| External carotid artery | Female | 3.91 ± 0.59 | 3.90 | 2.70–5.20 | <0.001 |
| Male | 4.62 ± 0.66 | 4.60 | 3.40–6.80 | ||
| Maxillary artery | Female | 2.34 ± 0.32 | 2.20 | 1.70–3.10 | 0.656 |
| Male | 2.40 ± 0.35 | 2.40 | 1.60–3.10 | ||
| Middle meningeal artery | Female | 1.27 ± 0.37 | 1.20 | 0.70–2.80 | 0.367 |
| Male | 1.24 ± 0.29 | 1.30 | 0.30–1.80 |
Foramen spinosum (FS) was present in 85 cerebral hemispheres (97.7%). The FS's diameter was measured as 2.22 ± 0.45 mm. There was no significant gender, age, or side difference (p = 0.841, 0.484, and 0.580, respectively). The FS was measured at 6.44 ± 1.97 mm in length. There was no significant gender, age, or side difference (p = 0.053, 0.198, and 0.689, respectively).
Bony canal (BC) was present in 47 cerebral hemispheres (54%). The BC was measured to be 1.65 ± 0.41 mm in diameter. There was no significant gender, age, or side difference (p = 0.524, 0.677, and 0.524, respectively). The BC was measured at 12.29 ± 6.54 mm in length. The right bony canal was 11.00 ± 6.28 mm in length, while the left bony canal measured 13.96 ± 6.70 mm in length. There was no significant gender, age, or side difference (p = 0.221, 0.739, and 0288, respectively).
The maxillary artery gives rise to the MMA in 83 cerebral hemispheres (95.4%). The MMA arises from the ophthalmic artery in 2 cerebral hemispheres (2.3%), and the ophthalmic artery and maxillary artery in 2 cerebral hemispheres (2.3%).
In our study, we evaluate the MMA by three-dimensional rotational angiography (3DRA) and describe the radiological classification of its variations as a new classification based on the classification of Martins et al. which was defined in the cadaver study. Branches originating from the maxillary artery were evaluated as type 1 according to the origin of the artery. The presence of petrosal branch, anterior division, and posterior division was accepted as type 1a (49.4%) (Figure 1(a) and (b)). It was classified as type 1b (31.0%) only in the absence of the petrosal branch (Figure 2(a) and (b)). It was classified as type 1c (9.2%) only in the absence of posterior division (Figure 3(a) and (b)). In the absence of petrosal branch and posterior division, it was classified as type 1d (3.4%) (Figure 4(a) and (b)). It was classified as type 1e (2.3%) only in the absence of anterior division (Figure 5(a) and (b)). Branches originating from other than the maxillary artery were classified as type 2 (4.6%) (Figures 6(a), (b), 7 and 8). There was no significant difference between branching pattern and gender, age, or side (p = 0.981, 0.965, and 0137, respectively). The branching pattern of the MMA is given in Table 2.
Figure 1.
On 3D-RA maximum intensity projection image, the middle meningeal artery originates from the maxillary artery (a). The petrosal branch, anterior division, and posterior division were observed (b).
Figure 2.
On 3D-RA maximum intensity projection image, the middle meningeal artery originates from the maxillary artery (a). The anterior division and posterior division were observed (b). The petrosal branch was not observed.
Figure 3.
On 3D-RA maximum intensity projection image, the middle meningeal artery originates from the maxillary artery (a). The petrosal branch and anterior division were observed (b). The posterior division was not observed.
Figure 4.
On 3D-RA maximum intensity projection image, the middle meningeal artery originates from the maxillary artery (a). Only the anterior division was observed (b). The posterior division and petrosal branch were not observed.
Figure 5.
On 3D-RA maximum intensity projection image, the middle meningeal artery originates from the maxillary artery (a). The petrosal branch and posterior division were observed (b). The anterior division was not observed.
Figure 6.
On 3D-RA maximum intensity projection image, the middle meningeal artery originates from the maxillary artery and ophthalmic artery (a). Ophthalmic artery origin and the course were observed (b).
Figure 7.
On 3D-RA maximum intensity projection image, the middle meningeal artery originates from the ophthalmic artery.
Figure 8.
On 3D-RA maximum intensity projection image, the middle meningeal artery originates from the ophthalmic artery.
Table 2.
The middle meningeal artery was divided into 2 morphological classification according to the origin and their subgroups were defined according to the branching pattern by adaptation and modification of Martins et al. classification on maximum intensity projection image.
| Middle Meningeal Artery Types | Branches | Frequency | Percentage (%) |
|---|---|---|---|
| Type 1a | AD (+), PD (+), PB (+) | 43 | 49.4 |
| Type 1b | AD (+), PD (+), PB (−) | 27 | 31.5 |
| Type 1c | AD (+), PD (−), PB (+) | 8 | 9 |
| Type 1d | AD (+), PD (−), PB (−) | 3 | 3.4 |
| Type 1e | AD (−), PD (+), PB (+) | 2 | 2.2 |
| Type 2 | 4 | 4.5 |
Type 1: Originating from MA; Type 2: Originating from other arteries.
AD; Anterior Division, PD; Posterior Division, PB; Petrosal Branch.
The relationship between the MMA bifurcation point and the pterion was visually evaluated in 70 cases (80.5%). The bifurcation point was evaluated in three different groups pterion level (55.7%), below the pterion (34.3%), and above the pterion (10%). There was no significant gender, age, side, or the morphological pattern of the MMA difference (p = 0.874, 0.359, 0. 681, and 0.673, respectively).
The anteroposterior orientation of MMA was evaluated according to the sphenosquamosal suture. Orientation patterns were categorized into three types: Type 1, the MMA runs anterior to the sphenosquamosal suture (4.9%); Type 2, the MMA runs superposed with the sphenosquamosal suture (81.5%) and Type 3, the MMA runs posterior to the sphenosquamosal suture (13.6%). There was no significant gender, age, side, or the morphological pattern of the MMA difference (p = 0.777, 0.997, 0. 146, and 0.057, respectively).
The ophthalmic artery completely originated from MMA in 1 (1.1%) cerebral hemisphere. In 6 hemicrania (6.9%), it was determined that the ophthalmic artery had a common origin from the middle meningeal artery and ICA.
Discussion
The vascular anatomy of the meninges shows variations and has a complex structure. 3 There are detailed cadaveric dissection studies examining the branching and variational anatomy of MMA. 1 However, dissection studies provide less information about in vivo blood flow and vessel lumen diameter. The most significant differences between radiographic and cadaver studies are the ability to provide morphological details of the course, the ability to repeat all evaluations by different observers, in vivo evaluation, and ease of application.
The anatomy of MMA was evaluated with radiological modalities, especially DSA. In the study of Merland et al. in the 1970s with the angiographic imaging method, meningeal vascularization could be demonstrated in vivo, and the branching pattern was classified. 2 Compared to the early work of Merland et al., the identification and course of sub-millimetric vessels can now be studied in more detail through the development of high-resolution radiological techniques.
The MMA has increased importance in dural vascular anatomy due to the role of this artery in many diseases and treatments. For this reason, both interventional neuroradiologists and neurosurgeons are increasingly interested.
Understanding the function of MMA in the management of chronic subdural hematoma has increased the interest of neuroradiologists and neurosurgeons in MMA over the past 10 years. It mostly develops among patients over the age of 65 and receiving anticoagulant and antiplatelet therapy 7 Conventional treatment is evacuation via burr-hole opening which has a high recurrence risk (2–37%). 7 Link et al. and many investigators treat recurrent chronic subdural hematomas via endovascular MMA embolization. The main artery for bleeding membranes is the MMA. Several studies have demonstrated a significant increase in MMA diameter in patients with chronic subdural hematoma compared to healthy controls.8,9 This enlargement is attributed to the chronic inflammation and neovascularization associated with chronic subdural hematoma. Furthermore, the MMA may exhibit angiogenesis of fragile blood vessels, the formation of new membranes, and fragile capillaries within these and the outer subdural membrane in chronic subdural hematoma.10,11 When it is closed, the collection in the subdural region could be absorbed.7,10–12 Although the recurrence rate after this treatment is similar to surgical treatment, it is preferred because it is a less invasive procedure. 12
In addition to bleeding, MMA is also important in the treatment of tumors such as meningioma.13–15 Because the MMA is the main dural artery, most cranial meningiomas are vascularized by it. The formation of neoangiogenesis and elevated blood flow requirements in feeding arteries may be associated with tumors. 16 In meningiomas, the MMA exhibits elevated blood flow compared to normal physiological levels, augmenting the risk of aneurysm formation. 17 Although surgery is the most common treatment for symptomatic meningiomas, MMA embolization may be preferred before surgery to minimize bleeding during resection. 13 Depending on their location, meningiomas can be fed by ICA dural branches, ECA dural branches, or a combination of these. While the MMA and the anterior falcine artery branch of the OA usually supply anterior cranial fossa meningiomas, the MMA and the dural branches of the petrous and cavernous ICA usually provide middle cranial fossa meningiomas. The posterior meningeal artery branch of the vertebral artery and other ECA branches supply posterior fossa meningiomas, which are rarely fed by the MMA. Interventional neuroradiologists should carefully analyze the anatomy during embolization to minimize complications caused by probable anastomoses between the MMA and ICA branches.14,15
Based on this information, having an intimate knowledge of anatomy and variations of MMA, as well as vascular anastomoses provides increases the success of the treatments and prevents complications.
Since MRI and CT scans can’t provide detailed information about MMA branches, morphometric studies are insufficient through these modalities. The use of MPR and 3D-RA imaging methods allowed detailed evaluation of MMA branching and variation anatomy. To our knowledge, no radiologic research has been identified in the current literature that evaluates the MMA with 3D-RA. In this research, we investigated the morphometric evaluations of MMA and its branches in 51 cases, and the results were evaluated according to age and gender.
Gender differences in carotid artery diameter
Krejza et al. evaluated CCA and ICA diameters by ultrasound in 500 subjects. ICA (4.66 ± 0.78 mm) and CCA (6.10 ± 0.80 mm) mean diameters in women were considerably smaller than ICA (5.11 ± 0.87 mm) and CCA (6.52 ± 0.98 mm) mean diameters in males. 18
Baz et al. evaluated ICA diameters by computed tomography angiography in 70 subjects. They measured the length and width of the cervical and intracranial segments of the ICA. There was a significant difference in vessel diameters in all segments, and it was found to be thinner in female cases. In addition, there was a significant difference in vessel lengths in all segments, and it was found to be shorter in female cases. 19
In our study, females had significantly smaller the common carotid artery, ICA, and ECA diameters than men (p = 0.021, 0.021, and <0.001, respectively). Consistent with many studies in the literature, male and female cases had statistically significant diameter differences.
Morphological evaluation of foramen Spinosum
Yanagi evaluated the foramen spinosum and foramen ovale by investigating 111 fetal skulls, 25 pediatric skulls, and 220 adult skulls. The foramen spinosum measured 2.63 mm in diameter on average. In addition, there was no significant gender or side difference. 20
Lang et al. found that the length of the foramen spinosum is approximately 2.25 mm in neonates and 2.56 mm in adults in their study. In adults, the width varies from 1.05 mm to about 2.1 mm. 21
Worku et al. measured the mean foramen spinosum length of 64 adult skulls as 3.72 ± 1.33 mm on the right side and 3.37 ± 1.26 mm on the left. The mean foramen spinosum widths on the right and left sides are presented as 3.3 ± 1.19 mm and 2.97 ± 1.15 mm, respectively. 22
In our study, only two patients had no foramen spinosum and were unilateral. There was no significant gender or side difference in measurements. In comparison to the literature, we discovered that the foramen spinosum was longer in our study, and as noted in the previous paragraphs it is seen that all the existing studies were cadaveric. We think that we showed the length of the foramen spinosum along the entire axis in our evaluation with 3D-RA and MPR techniques may have affected and explained this difference from a technical point of view. Another reason why the measured anatomical lengths differ between populations is the difference in ethnicity, and we think that this may affect the results of our study. 23
Morphological evaluation of the bony canal
Honnegowda et al. examined 75 adult skulls for the bony canal and related features. The right bony canal's mean length was 12.8 ± 4.5 mm, whereas the left bony canal's mean length was 13.7 ± 9.3 mm, with a significant difference between them. 24
The average length of the bone canal was 9.2 mm, and there was no statistically significant difference between the right and left sides, according to Fujimoto et al. 25
According to CT scans, the incidence of the bone canal was 85.44% in Eberlova et al.'s study, and it was much higher in women than in males [8]. Although most canals are bilateral, the average canal length was 17.67 mm, and the average canal diameter was 1.33 mm. 26
The bone canal was found on 47 (54%) of the sides in our study. Between the sides, diameter, and length, there was no statistically significant difference (p: 0.524 and 0.288, respectively). In the comparison evaluation with gender, no significant differences were detected (p: 0.524 and 0.221, respectively).
Origin of the middle meningeal artery
The MA is usually the origin of MMA. It originates from the first segment of the MA in almost all cases. However, ICA, OA, and vertebrobasilar artery origins of MMA have also been reported. 27
Dilenge and Ascherl reported the incidence of MMA originating from OA as 0.5% based on a large angiographic series containing approximately 3500 cerebral angiograms 28 [6]. In addition, different MMA cases originating from OA have been defined as case reports in the literature. 29
In our study, the MMA origin of 87 hemicrania was evaluated. It was found to originate from MA on 83 sides (95.4%), OA on 2 sides (2.3%), and OA with MA on 2 sides (2.3%), and it was found to be in line with prior studies.
Branches of the middle meningeal artery
MMA branches were defined based on cerebral angiographies by Merland et al. and cadaver studies by Martins et al.1,2 Merland et al. described branches based on cerebral angiographies as temporobasal segment, temporopterional segment, and coronal segment. 2 Martins et al. examined 5 dry skulls and 20 adult cadavers and described branches as petrosal branches, cavernous branches, and anterior and posterior divisions. 1
In the evaluation of the branching pattern of MMA, the classification of Martins et al. was taken as a reference in our study. The classification of Martins et al. was based on the evaluation of microsurgery but the incidence of the branches they described in their studies was not expressed. In our study, radiological evaluation was performed, and it was found that not all branches were seen in all cases. Therefore, a modified classification was created based on the classification of Martins et al.
There are limited studies in the literature on the incidence of MMA branches. Chandler and Derezinski reported that anterior division was not seen at a rate of 0.7%. 30 In our study, anterior division 2 was not seen in the hemicrania, with a rate of 2.3%.
The most common MMA branching in our study was Type 1a and is consistent with the classical branching pattern. However, the second most common group is type 1b with a rate of 31% and the petrosal branch is not observed. The petrosal branch crosses the facial hiatus and the greater petrosal nerve to supply the facial nerve. It is important to know the presence of the petrosal branch in cases with the cavernous sinus, trigeminal nerve, or internal acoustic canal pathologies in which a subtemporal extradural surgical approach is applied. During this surgical approach, facial nerve deficits can be seen as a result of petrosal branch injury, and therefore, non-coagulation methods come to the fore in the approach to vascular hemorrhage control.
The different rates of variation among different populations may be due to ethnicity, and we think this has an impact on the findings of our research. 6
To our knowledge, no radiologic research has been identified in the current literature that evaluates the incidence of anterior division, posterior division, and petrosal branch of MMA in the current literature. Furthermore, our research is the first to use 3D-RA to examine the detailed anatomy of MMA.
Relationship between middle meningeal artery bifurcation and pterion
The pterion is formed as a result of calcification of the sphenoid fontanelle, which is the suture junction on the neurocranium's anterolateral side. 31 The pterion is one of the calvarium's components where it is particularly thin and is also used as a surgical reference, especially in the transylvian approach. 32 On the other hand, the pterion is also considered as a reference to the protection of the MMA's anterior branch during surgery in patients undergoing bypass surgery such as moyamoya disease. 33
The bifurcation of MMA is known to be in the Pterional region. 3 The position and morphology of the pterion have been evaluated in different studies, and the relationship between structures such as the frontozygomatic suture and MMA branches has been indicated. 34 However, to our knowledge, no radiologic research has been identified in the current literature that evaluates the frequency of the relationship between pterion and MMA bifurcation. In our study, the relationship between the bifurcation point and the pterion of 70 hemicrania (80.5%) was visually examined. In 24 (34.3%) of the hemicraniums, the bifurcation point was observed in the inferior of the pterion, in 39 (55.7%) pterion level, and in 7 (10%) pterion superior.
The course of the middle meningeal artery in the temporal Fossa
Salamon et al. evaluated the temporal fossa course of the MMA in arteriographic imaging of the meningeal arteries and divided it into three types according to its angulation acuity. 35 In our study, MMA was evaluated cross-sectionally, and for the evaluation of the anteroposterior course level, it was evaluated with reference to the sphenosquamous suture. A total of 81 MMAs arising from the maxillary artery and passing through the sphenosquamosal suture were studied. 4 (4.9%) MMAs were seen anterior to the sphenosquamosal suture, 66 (81.5%) superposed by the sphenosquamous suture, and 11 (13.6%) were observed posterior to the sphenosquamosal suture.
To our knowledge, no radiologic research has been identified in the current literature that evaluates the relationship and frequency of MMA by taking the sphenosquamous suture as a reference for the determination of the anteroposterior course. Furthermore, our research is the first to use 3D-RA to examine the detailed anatomy of MMA.
Ophthalmic artery of middle meningeal artery origin
Curnow published the first description of orbital branches originating from MMA in 1872. He claims that in the case of dissection, the MMA supplies all orbital branches except the central retinal artery, which originates from the supracavernous ICA. 36 In a study of 134 angiograms performed on children with intraocular retinoblastoma undergoing intra-arterial chemotherapy, Akdemir Aktaş et al. found that the ophthalmic artery originated from the middle meningeal artery in 2.2% of cases. 37 In 1 (1.1%) of 87 hemicrania evaluated in our study, OA was completely originating from MMA. In six cases (6.9%), OA was found to have a common origin with MMA and ICA. There is a relationship between MMA and OA in 8% of the cases. For this reason, there should be aware of the risk of visual loss due to retinal embolization through OA, especially in interventional procedures such as MMA embolization, and cases should be carefully evaluated in terms of the pre-embolization MMA-OA relationship.
Conclusion
It was observed that the branching pattern may show differences when compared to the cadaver studies with a radiologic evaluation with 3D-RA. Because 3D-RA imaging enables submillimetric evaluation and precise measurements, it is extremely useful in vascular anatomical studies. Radiological studies can contribute to this context by defining critical points before interventional and surgical operations. More research is needed to uncover topographical or radiological points that could reduce the number of complications associated with MMA and related anatomical structures.
Footnotes
Author contribution: L Sari: Project development, Data Collection, Manuscript writing. TF Yilmaz: Data analysis, Manuscript editing. II Oz: Data management, Manuscript editing
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Ethical approval: All procedures performed in the studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.
Funding: The author(s) received no financial support for the research, authorship, and/or publication of this article: No funding was received for this study.
Informed consent: Informed consent was obtained from all individual participants included in the study.
ORCID iD: Lutfullah Sari https://orcid.org/0000-0002-7482-1560
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