Discussion
Anatomical Description and its Variations
The meningeal arteries comprise arterial branches that rise up between the dura mater
and the bone, supplying both structures. There are three meningeal arteries: posterior
(PMA), middle (MMA), and anterior (AMA) ([Fig. 1], [Fig. 2]). The AMA originates from the anterior ethmoidal artery and supplies a short region
on the Galli crest[13]
[14]
[15] ([Fig. 2C]). The PMA starts from the vertebral, ascending occipital or pharyngeal arteries,[15] and supplies the medial portions of the dura of the posterior fossa, the cerebellar
sickle, the posterior segment of the brain scythe, and the adjacent tentorium. The
MMA, in turn, irrigates a greater surface of the occipital, parietal, frontal, and
temporal regions ([Fig. 2B]).
Fig. 1 Skull lateral view highlighting the temporal fossa. The frontal, occipital, parietal
and temporal bones were omitted, and the dura mater is represented by the gray shading
in figure A. (A) - representative 3D cranial image obtained from an oblique view showing vascularization
(in red) by the middle meningeal artery (MM) and its branches, as well as by the external
carotid artery (CE) ramifications. The MM is a branch of the maxillary artery (AM),
and the posterior meningeal artery (MP) is a branch of the FA (ascending pharyngeal
artery); (B) - representative 2D drawing of the MM and its branches, from a coronal view. CC:
common carotid artery; CI: internal carotid artery; CE: external carotid artery; FA:
ascending pharyngeal artery; AM: maxillary artery; MM: middle meningeal artery; FA:
posterior meningeal artery.
Fig. 2 Represents the anterior, middle and posterior meningeal artery. (A) - Side view. Middle meningeal artery and its frontal and parietal branches. (B) - Lateral-inferior view. Posterior meningeal artery and its vascular territory.
The MP artery is a branch of the FA. (C) - Front view. Evidence of ethmoid bone (anterior ethmoidal cells). Anterior meningeal
artery. which is a branch of the EA.CC: common carotid artery; CI: internal carotid
artery; CE: external carotid artery; AM: maxillary artery; MM: middle meningeal artery;
MMF: middle meningeal frontal branch; MMP: middle meningeal artery parietal branch.
AF: ascending pharyngeal artery; MP: posterior meningeal artery; AO: ophthalmic artery;
EA: anterior ethmoidal artery; MP: anterior meningeal artery.
The maxillary artery consists of a primary terminal branch of the external carotid
artery[16] and originates posteriorly to the mandibular branch. The MMA is the most common
branch of the mandibular segment of the maxillary artery and originates at a variable
distance from the external carotid artery and the superficial temporal artery[17] ([Fig. 2A], [Fig. 3A]). The MMA then irrigates the cranial dura mater and, via its perforating branches,
provides blood supply to the periosteum of the inner lamina of the cranial bones.[18] After entering the middle cranial fossa, the MMA performs a right-angled curve to
assume a horizontal course, and then runs forward and laterally through the floor
of the lateral piece of the middle cranial fossa, the dura, and the inner part of
the cranial vault[17]
[19]
[20] ([Fig. 3A], [Fig. 3B]).
Fig. 3 Middle meningeal artery pathway without anatomical variation. Figure shows contact
with bone projections. (A) - Bottom view. (B) - penetration of the middle meningeal artery into the skull by the spinous shape
(FS), extracranial, intraosseous and intracranial portion. The MM issues two branches,
MMP and MMF. TS is a branch of AM. (C) - relationship between the middle meningeal artery and the pterio (PT). CC: common
carotid artery; CI: internal carotid artery; CE: external carotid artery; AM: maxillary
artery; MM: middle meningeal artery; TS: superficial temporal artery; MMP: middle
meningeal artery parietal branch; MMF: middle meningeal artery frontal branch.
The MMA then changes its path after reaching the pterion mark, extending by the inner
area of the frontal and parietal bones ([Fig. 3C]). The second change in its course may occur at the bone canal or groove on the pterion
of the cerebral surface.[17] Therefore, the MMA can be divided into interosseous, extracranial, and intracranial
segments ([Fig. 3B]). The extracranial portion of the MMA runs superiorly from its origin and reaches
medially the external face of the skull base, following a right course in most cases.
It is worth reminding that the dura mater does not attach to this segment ([Fig. 4], [Fig. 5]). The intraosseous portion of the MMA extends by the outer and inner orifices of
the foramen spinosum of the higher wing of the sphenoid bone, crossing it. Finally,
the intracranial segment of the MMA is observed after the artery enters the skull.
This portion is characterized as the origin for most MMA branches, and arises in the
surface of the middle cranial fossa, opposite to the pterion[8] ([Fig. 3C], [Fig. 4], [Fig. 5], [Fig. 6]).
Fig. 4 Representation of the external carotid artery and its branches. (A) - Side view. (B) - Latero-posterior view. Evidence is MM, which is a branch of AM and MMRp, derived
from MM. CC: common carotid artery; CI: internal carotid artery; CE: external carotid
artery; Ts: superior thyroid artery; AL: lingual art; AF: facial artery; AF: ascending
pharyngeal artery; AP: posterior auricular artery; AOc: occipital artery; TS: superficial
temporal artery; AM: maxillary artery; MM: middle meningeal artery. B: Latero-posterior
view. MMA: accessory middle meningeal artery; MMRp: middle meningeal artery petrous
branch.
Fig. 5 Side view. (A) - arteriography showing branches of the external carotid artery. Evidence for MM
and MMP that are branches of AM. Topographic view of CI. (B) - 3D schematic drawing in the topography of the arteriography of figure A. CI: internal
carotid artery; CE: external carotid artery; AOc: occipital artery; AM: maxillary
artery; MM: middle meningeal artery. MMA: accessory middle meningeal artery; MMF:
middle meningeal artery frontal branch; MMP: middle meningeal artery parietal branch;
CA: anterior cerebral artery; CM: middle cerebral artery; CP: posterior cerebral artery.
Fig. 6 Top view. (A) - bilateral middle cranial fossa, with folded parietal bone, representing the MM
ascending the FS and following the middle fossa. (B) - 2D schematic drawing showing the anterior, middle and posterior fossa of the skull.
FS: spinous foramen; MM: middle meningeal artery.
This anatomical description is important to identify variations that affect the extracranial
([Fig. 7A], [7B]) and intracranial MMA branches portions ([Fig. 8A], [8B], [8C]). After MMA extension through the foramen spinosum, the petrous branch goes through
the canal of the greater petrous nerve, being basically divided into two branches:
1) the medial or cavernous branch, which contributes to irrigate the Gasser ganglion,
the third portion of the trigeminal nerve and the dura mater around the foramen ovale,
thus having an essential involvement in the origin of dural fistulas in cavernous
sinus region[18]; and 2) the basal tentorial branch, which irrigates the cerebellum tent and may
underlie dural fistulas of the lateral sinus, even irrigating tumors located in the
pontocerebellar angle, through branches that run under the upper petrosal sinus to
achieve that angle.
Fig. 7 Side view. Anatomical variations of the middle meningeal artery in the extracranial
segment. A - branching distal to the maxillary artery (AM). B - schematic representation
of MMA variation.
Fig. 8 Representation of common anatomical variations of the middle meningeal artery (MM)
after penetrating the skull through the spinous foramen (intracranial segment). A
- bifurcation in the ore, 25% of the cases; B - bifurcation when leaving the spinous
foramen (FS), 50% of the cases (most common); C- association of the bifurcation in
the ore with the exit of the FS, 13% of cases.
The petrosquamous branch, through its basal tentorial branches, runs posterolaterally
along the petrosquamous sulcus of the temporal bone and gives blood supply for the
basal ⅔ of the cerebellar tent. Besides, it come up with branches to the posterior
fossa and may even irrigate lateral sinus fistulas.[21]
Finally, it divides into two terminal branches: 1) the frontal branch, which irrigates
the bones that constitute the anterior cranial fossa and the anterior part of the
middle cranial fossa. Nevertheless, this branch may also originate the marginal artery
of the cerebellum tent, which is responsible for the irrigation of the anterosuperior
third of the cerebellum tent, contributing to supply the trochlear and oculomotor
in the cavernous sinus roof; and 2) the posterior branch, which runs away more horizontally
towards the posterior segment, supplying the supratentorial portion of the posterior
cranial fossa and the posterior region of the middle cranial fossa. Perforating branches,
belonging to the posterior and anterior branches, cross the arterial sulcus and originate
abundant lateral pathways that also reach the dipole and, eventually, the outer skull
layers.[18]
[20]
[21]
[22]
There are also 1) the ganglion branches or the trigeminal ganglion branch, which provide
blood to the trigeminal ganglion and associated roots; 2) the upper tympanic artery,
which runs through the semicanal to the tensor tympani muscle, supplying the muscle
itself as well as the mucosa lining the semicanal; 3) temporal branches, which traverse
tiny foramens in the greater wing of the sphenoid bone, anastomosing with the deep
temporal arteries; and, finally, 4) an orbital branch, which anastomoses with the
recurrent meningeal branch of the lacrimal artery.[18]
[19]
[23]
The accessory meningeal artery is a branch that can comes from the extracranial MMA
segment or from the internal maxillary artery[22] ([Fig. 4B], [Fig. 5B]). It promotes the vascularization of the pterygoid, veli palatine tensor muscle,
as well as to the auditory chanel.[19] It exhibits an endocranial branch, namely cavernous branch, which crosses over the
foramen ovale or the Versalius foramen, and contributes to the irrigation of the mandibular
branch of the trigeminal nerve, the dura adjacent to the thallus saddle and the semilunar
ganglion.[24]
[25] Their extracranial branches are also valuable, since they are involved in skull
base diseases such as angiofibromas, dural fistulas, and meningiomas, originated from
anastomoses with the ascending, mandibular, pterygovian arteries and ascending and
descending palatine arteries.[21]
The posterior superior alveolar artery commonly appears just before the maxillary
artery entry in the pterygopalatine fossa, and often shares a communal trunk with
the infraorbital artery, but it may also arise from the MMA. The reason for that phenomenon
could be the altered return of the plexiform anastomoses between the stapedial artery
and the maxillary artery, resulting in the fusion of the posterior superior alveolar
artery with the medial meningeal artery.[7] This feature bring severe surgical implications to the procedures involving intransantral
radical maxillectomy, lateral approach of the infratemporal fossa and pterygopalatine,
manipulations of the medial and anterior parts of the skull base (including the management
of oropharynx and nasopharynx lesions), as well as to the dorsocaudal management of
the medial skull base.[2]
[26]
[27]
It has been established that the Krönlein method, the surgical procedure based on
the orbit approach through the temporal fossa, mobilizing the malar bone, may constitute
the simplest way to localize the main trunk of the MMA, since there is lack of accurate
topographic information defining its pathway.[22]
[27]
[28] To localize the frontal branch, two imaginary lines should be used: an upper horizontal
line, guided by the top edge of the orbit, and an anterior vertical line, which crosses
the middle of the zygomatic arch. To establish the location of the parietal branch,
one must find the intersection of two lines: an upper horizontal line and a posterior
and vertical line, the latter running immediately beside the back of the mastoid process.[20]
Furthermore, several authors have shown that the anterior branch of the MMA, or the
pterion segment, which passes by the pterion and arises along the coronal suture,
may be surrounded by a canal-like bone structure.[5]
[29]
[30]
[31] This canal, which is found in between 49 and 75% of the skulls,[4]
[32] is formed mainly when the anterior MMA branch, which runs through the dura of the
sphenoidal fontanelle, is surrounded by bone in the closure of the fontanelle during
bone formation. It is always located around the pterion, posterior to the coronal
suture, at a lower level of the superior temporal bounder, but never below the frontal
bone. In cases where the anterior MMA branch is located in a bone canal, the MMA may
be damaged during removal of the bone flap during neurosurgical surgeries. Therefore,
to preserve its integrity during frontotemporal craniotomy, it must be exposed by
a perforation around the pterion.[30]
In this regard, Kornieieva et al. demonstrated that the morphological features of
the MMA may be related to the individual characteristics of the skull. Patients showing
a mesocephalic skull shape provide the most favorable anatomical conditions for the
endovascular approach of MMA-associated pathologies, whereas the brachycephalic skull
shape is characterized by a more negative anatomical prognosis. This makes this latter
kind of formation undesirable for MMA interventional manipulations, being the conventional
surgery the preferred method in these cases.[8]
The embryogenic MMA origin consists of the stapedial artery, the main trunk derived
from the hyoid artery at the level of the stapes, which is divided into maxillofacial
and supraorbital divisions. Together, these branches supply the orbit and provide
the intracranial MMA portion.[19]
[33] After the ophthalmic artery assimilates the intraorbital branches of the stapedial
artery, its proximal and retro-orbital branches evolve and are assimilated by the
intracranial MMA portion. Subsequently, the branches belonging to the maxillofacial
division of the stapedial artery are absorbed by the developing external carotid artery
and originate the internal maxillary artery (including the extracranial MMA segment).
At this step, the proximal (trunk) segment of the stapedial artery involutes around
the 3rd month of gestation, and the remaining structure becomes the tympanic MMA branch.[3]
[33]
[34]
[35]
[36]
[37]
[38] Accordingly, there are anatomical variations that can be explained by this particular
embryology. Among the anomalous origins of the MMA is the posteroinferior cerebellar
artery.[39] The embryological basis for this variation is still unknown, but, from a neurosurgical
point of view, this knowledge will certainly avoid destruction of blood supply to
structures located at the posterior cranial fossa during MMA embolization.[19] Another rare origin comprises the basilar artery or one of its branches.[23] The precise origin location is always speculative, but it can be associated with
persistent anastomosis around the trigeminal ganglion, as well as between the intracranial
elements of the stapedial artery and of the lateral pontine artery.[19]
A more common variant is the MMA originated from the internal carotid artery, which
occurs close to the lacerated foramen[19] ([Fig. 9]). The MMA may be generated from the extradural portion of the carotid siphon, a
feature that is possibly explained, under the embryological point of view, as an aberrant
origin (more distal or more caudal) of the hyoid artery from the internal carotid
artery. In this case, the union between the hyoid artery with the remaining parts
of the first branchial arch, to form the stapedial artery, does not occur, or occurs
unrelated to the stapes level. This abnormality is characterized, therefore, by the
absence of an undeveloped extracranial MMA. Another possible origin for the MMA is
the petrous segment of the internal carotid artery. The basis of this anomaly is the
persistence (defective involution) of the embryonic stapedial artery.[40] In this case, the internal carotid artery runs inside the carotid canal along with
the internal carotid artery, and then enters the lacerated foramen, without going
through the middle ear cavity or perforating the stapes. When it reaches the lacerated
foramen, it crosses the cavernous sinus just below the trigeminal ganglion. Subsequently,
it follows a regular course, being divided into posterior and anterior branches.[41]
Fig. 9 Side view. Parietal, occipital, zygomatic and temporal bone folded. Evidence of the
internal carotid artery. Anatomical variation of the middle meningeal artery (MM).
Branch adjacent to the lacerated foramen (FL). CC: common carotid artery; CE: external
carotid artery; CI: internal carotid artery; AO: ophthalmic artery.
Finally, the MMA may also originate from the ophthalmic artery, which comes, after
the assimilation of branches from the supraorbital segment of stapedial artery (that
is, the extraocular and intraorbital branches), by the early ophthalmic artery, which
initially only fills the eyeball. This feature occurs due to a development failure
of the intraorbital proximal branches and of the retro-orbital stapedius, so the intracranial
segment of the MMA remains connected to the intraorbital branches of the stapes. Besides
the involution failure of the maxillofacial portion of the stapedial artery, the extracranial
MMA portion is not formed.[40]
The remaining anatomical variations reported in the literature account for cases in
which the MMA enters the middle cranial fossa through the foramen ovale, close to
the mandibular nerve (as long as the spine foramen is absent),[41]
[42] being originated at the third part of the maxillary artery (pterygopalatine).[43] In this case, the MMA reaches the median cranial fossa by the lateral extremity
of the superior orbital cleft. The MMA can also be generated from the ascending pharyngeal
artery, crossing the lateral margin of the superior orbital fissure or through the
meningo-orbitary foramen of the greater wing of the sphenoid bone, as a branch of
the persistent stapedial artery.[44]
[45]
[46]
The persistent stapedial artery generally originates from the petrous segment of the
internal carotid artery.[47]
[48] It enters anteromedially into the hypotympanum, running next to the promontory.
Then, it goes cranially through the stapes obturator foramen, reaching the facial
canal by dehiscence, just behind the cochleariform process, going subsequently to
the middle cranial fossa.[49].[50]
[51]
[52] Their anastomotic branches enter the orbit through the superior orbital fissure
(meningo-ophthalmic artery) or through a foramen on the greater wing of the sphenoid
bone, called meningo-orbital foramen,[50] Hyrtl canal, or cranio-orbital foramen.[50]
[52] The branch that goes through the foramen is known as the meningolacrimal artery.
Furthermore, it is worth mentioning that the vascular system of the MMA is commonly
confounded with the anterior vascular network that goes by the superior orbital fissure
(sphenoidal artery) and through the meningo-orbital foramen (meningolacrimal artery).[50]
Clinical Considerations
The MMA that comes from the dura mater is incorporated in the groove or drip of the
internal surface of the skull and presents a straight, direct path.[8] Pseudoaneurysm can be formed when a hematoma or a secondary connective tissue formation
occurs following an injury to the temporal area. According to Kawaguchi et al.,[53] ∼ 70% of the MMA traumatic pseudoaneurysm cases are related to trauma fractures
affecting the temporal region. Post-traumatic MMA pseudoaneurysms can suddenly rupture
after repair of the brain lesion, and the time elapsed between the initial lesion
and the aneurysm development varies from 4 to 30 days.[53]
[54]
[55]
Therefore, the mortality can be notably reduced when the postpseudoaneurysm is promptly
diagnosed and treated.[56] The MMA may, therefore, be important for postsurgical revascularization, except
for indirect shunt, such as the encephalo-dura-arterio-synagiosis. It stimulates collateral
circulation between the temporal muscle and the dura mater, leading to angiogenesis.[1] The MMA is also frequently used as an endovascular embolization for conditions such
as FAVD, pseudoaneurysm, true aneurysm, and meningioma.[57]
[58] Suzuky et al.[59] reported that MMA endovascular embolization is currently the most effective method
to acute bleeding. To avoid complications in open cranial surgeries, endovascular
access is the choice procedure due to the extracranial origin and to the direct course
of the MMA to the cranial cavity.[60]
The rate of acute epidural hematomas and posttraumatic pseudoaneurysms of the MMA
subjected to nonconventional endovascular therapies is increasing in emergency room
settings.[58]
[59] As in post-traumatic MMA pseudoaneurysm, cranial fracture is commonly associated
to fistulas communicating the parallel middle meningeal vein and the diploic vein.[54]
[55] The MMA FAVD represents the second most frequent traumatic arteriovenous dural fistula
originated from posttraumatic carotid-cavernous sinus fistula. The clinical symptoms
include consciousness changes and headache, and resection by craniotomy and embolization
are the alternatives therapies.[61]
Migraine is generally considered a neurovascular disorder characterized by unilateral,
pulsatile headache pain, associated with photophobia, nausea, vomiting, and dizziness.
According to the described pathophysiology, vasodilatation lead by vasodilator agents,
such as the peptide related to the gene of calcitonin, nitric oxide and serotonin,
may constitute the mechanism underlying the stimulation of the cerebral and middle
meningeal arteries.[62]
Furthermore, during cranial surgery, to avoid visible damage to a possible anastomosis
between the MMA and the ophthalmic artery pathway to the ethmoidal artery, the MMA
needs to be preserved. Meningeal vessels attach to the inner part of the bony vault
of the skull and, in case they are fractured, the MMA can be damaged, causing epidural
hematoma in up to 85% of the cases.[63] Patients with cranial fractures that affect the meningeal vessels are more commonly
affected by epidural hematomas and recurrent episodes of hematoma-related bleeding,
so damage to the MMA may also be involved in recidivated chronic subdural hematoma.[31] Finally, the MMA also has an important impact in the treatment and prognosis of
MMD. As already known, MMD consists of an unusual cerebrovascular disorder featuring
progressive obstruction of the last portion of the internal carotid artery and its
main branches within the Willis circle (mainly middle and anterior cerebral arteries),
resulting in the development of a vascular network (Moya-Moya vessels) in the brain.[31]
[64]
[65]
[66]
[67] It is therefore crucial to know the surgical anatomy of the MMA around the pterion,
to keep intact its anterior branch during the surgical MMD management surgery. Not
surprisingly, in MMD patients, the anterior branch may potentially originate essential
collateral branches that provide blood supply to the anterior cerebral artery area.[31] In fact, the MMA plays an essential role in the progress and compensation of collateral
circulation in MMD. In the case of recurrent chronic subdural hematoma, when conventional
surgery and drainage fail, MMA embolization may constitute an alternative. Finally,
we consider that every neurosurgeon must know the anatomy of the MMA sufficiently
to correlate it with the diagnosed pathology, thus obtaining treatment effectiveness
and preventing iatrogenies.
