Key-words:
Cadaver dissection - microsurgical anatomy - middle cerebral artery
Introduction
The initial descriptions of cerebral vasculature were given by anatomists, such as
Thomas Willis in the 16th century, who laid the foundation for neurosurgeons, neurologists,
and neuro-radiologists. The middle cerebral artery (MCA), is one of the branches of
the circle of Willis that supplies a significant part of the cerebral hemispheres.
Saccular aneurysms commonly arise from MCA and most of the arterio-venous malformations
(AVM's) receive arterial supply from MCA. Branches of MCA are encountered by neurosurgeons
in most supratentorial approaches. Hence a thorough knowledge of microsurgical neuroanatomy
with respect to its branching and variation patterns would help the treating neurosurgeon
in surgical or endovascular management. The introduction of cadaveric dissection of
cerebral vasculature as a part of the neurosurgical training module would help the
neurosurgical residents to understand the complex neuroanatomy of the brain vasculature
and help gain confidence during the surgical procedure.[[1]],[[2]],[[3]],[[4]]
To the best of our knowledge microsurgical anatomical studies of the MCA have not
been done among the Northwest Indian population. Anatomical variations of MCA that
have not been described before may come in as a surprise during any surgical intervention.
Hence, we intend to record the anatomical variations of the MCA anatomy and its implications
in contemporary vascular surgery and neurosurgical practice. The objective of this
work was to study and compare the microsurgical anatomy and variations of MCA in northwest
Indian cadavers with the available literature.
Methods
Fifteen cadaveric brains (5 cadavers and 10 retrieved formalin preserved brains),
that is 30 MCA vessels were dissected using an operating microscope (Carl Zeiss) with
an optical zoom of × 3 and × 20. The Sylvian fissure was split from lateral to medial,
origin of MCA identified, and M1 segment (MCA segment from the origin to genu)[[5]] was studied with respect to the outer diameter, length, and the pattern of division
of the main trunk and classified into, Type 1-bifurcation, Type 2-single trunk, Type
3-trifurcation, and Type 4-others [[Table 1]]. The outer diameter of each trunk and their respective lengths were measured. The
early cortical branches, which arise before the actual division of the main trunk,
were studied with respect to point of origin from MCA, outer diameter, the pattern
of origin (single branch/stem), and area of supply. The lenticulostriate artery as
defined as the branches arising from the medial and inferior aspect of the M1 segment
and directed towards anterior perforated substance (APS) were identified under high
magnification, their number, pattern of origin, and distance of origin from MCA were
studied and classified into, medial, intermediate and lateral groups. At the limen
insula where the MCA forms genu and continues into the Sylvian fissure is referred
to as the M2 segment (insular segment) up to the circular sulcus of the insula. M2
studied with respect to the outer diameter, length, pattern of division, and the origin
of cortical branches, similarly opercular segment (M3) and cortical segment (M4 and
M5) were studied. Schematic hand drawings of the MCA segments were done for each vessel,
relevant photographs taken and the cortical branches were studied up to the cerebral
convexity. The measurements were taken with the help of digital micro calipers and
the measurements were compared and confirmed by 2 independent observers.
Table 1: Branching pattern of main trunk of middle cerebral artery (M1 Segment)
Observation and Results
The MCA originates at the bifurcation of the internal carotid artery (ICA), lateral
to the optic chiasm, and courses laterally and slightly forward under the APS to reach
the medial end of the Sylvian fissure. At this point, the artery turns, crosses over
the limen insula, and enters the insular area. The main division of the MCA is usually
seen before or at the limen insula. The secondary trunks resulting from this division
will course over the surface of the insular cortex, giving rise to cortical branches
while turning over the opercular cleft, these cortical branches spread out over the
cerebral convexity.
Main trunk
The length of the main trunk (M1) from origin to genu, was commonly 16 ± 3 mm, with
no significant difference between either side. The shortest length of M1 measured
was 8 mm in one cadaver on one side and the longest being 23 mm in one cadaver with
Type 3 division. The outer diameter was 3 ± 0.5 mm bilaterally.
Early branches
The cortical branches arising from the main trunk proximal to the division of M1 segment
are described as early branches. Among the early branches studied 58% were destined
to the temporal lobe and 29% to the frontal lobe. The temporopolar and the anterior
temporal artery (ATA), which supply the temporal pole and the anterior portion of
the lateral aspect of the temporal lobe, respectively, were the early branches commonly
seen [[Table 2]]. The distance between MCA origin and the first early branch origin was 4 ± 2 mm
on the right and 4.4 ± 2.5 mm on the left side. The temporopolar artery, frequently,
the first cortical branch seen when the Sylvian fissure is dissected, was seen in
28 of the hemispheres studied (98%). In the 2 hemispheres, where it was absent, the
vascular supply to the temporal pole was provided by the collateral branches of the
ATA. The uncal artery was seen in 5 hemispheres.
Table 2: Classification based on division of M1 into Secondary trunks. Length, Outer diameter
and Number of Cortical Branches from Secondary trunks
Perforating branches
The medial group was seen in 20 of 30 hemispheres. Predominantly, it arose directly
from the M1 segment as 2–5 single twigs, at a distance of 2–4 mm from the MCA origin,
and pursued a direct course almost 90° to the APS [[Figure 1]]a and [[Figure 1]]b. The intermediate group, most consistently seen (26 out of 30 hemispheres), originated
from the M1 trunk as a single stem artery which later divided into multiple branches
(2–3 branches), at a distance of 5–7 mm from the MCA origin [[Figure 2]] and took an oblique course to the APS. The lateral group originated from either
the main trunk or secondary trunks (mostly superior trunk), was seen in 22 out of
30 hemispheres, at a distance of 7–15 mm from the MCA origin, and took an “S” shape
course to the APS.
Figure 1: (a) Perforator (b) Schematic sketch diagram: Perforator. MP - Medial perforator;
IP - Intermediate perforator; LP - Lateral perforator; ACA - Anterior cerebral artery;
FL - Frontal lobe; TL - Temporal lobe; ACP - Anterior clinoid process
Figure 2: IP - Single stem branching into multiple branches. IP - Intermediate perforator
Main division and secondary trunks
The main trunk of the MCA was classified based on its pattern of division into secondary
branches [[Table 1]]. The trunks arising from the division of MCA's main trunk were called “Secondary
trunks.” Bifurcation (Type 1): the most common type, seen in 24 of 30 hemispheres
(80%) where the main trunk is divided into a superior trunk (frontal) and inferior
trunk (temporal) [[Figure 3]]a and [[Figure 3]]b. Single trunk (Type 2) in 3 out of 30 hemispheres (10%), the cortical branches
arose as collateral vessels from a single trunk that ended in the angular artery [[Figure 4]]a and [[Figure 4]]b. Trifurcation (Type 3) in 3 out of 30 hemispheres (10%), the main trunk divided
into, superior, middle, and inferior trunks [[Figure 5]]a and [[Figure 5]]b. Type 4 (Others), >3 trunks-none in this study. Among the 24 cases in type 1,
5 hemispheres had equal dominance of trunks (20.8%), 12 had inferior trunk dominance
(50%) [[Figure 6]]a and [[Figure 6]]b and 7 had superior trunk dominance (29.1%). The length, outer diameter and division
pattern, and number of cortical branches from secondary trunks were studies [[Table 2]].{Figure 3}{Figure 4}{Figure 5}{Figure 6}
Figure 3: (a): Bifurcation pattern (b) Schematic sketch diagram - Bifurcation pattern. ICA
- Internal cerebral artery; MCA - Middle cerebral artery; ACA - Anterior cerebral
artery; ST - Superior trunk; MT - Middle trunk; IT - Inferior trunk; ACP - Anterior
clinoid process; FL - Frontal lobe; TL - Temporal lobe; OFA - Orbitofrontal artery,
PCA - Precentral artery, UA - Uncal artery, TpO - Temperopolar artery, ATA - Anterior
temporal artery, MTA - Middle temporal artery
Figure 4: (a) Single trunk. (b) Schematic sketch diagram - Single trunk. ATA - Anterior temporal
artery; PTA - Posterior temporal artery, PCA - Precentral artery, CA - Central artery,
AP - Anterior parietal artery, PP - Posterior parietal artery, AA - Angular artery;
ICA - Internal cerebral artery, MCA - Middle cerebral artery, ACA - Anterior cerebral
artery, ACP - Anterior clinoid process, FL - Frontal lobe, TL - Temporal lobe; PTA
- Posterior temporal artery
Figure 5: (a) Trifurcation pattern (b) Schematic sketch diagram - Trifurcation pattern. ICA
- Internal cerebral artery; MCA - Middle cerebral artery; ACA - Anterior cerebral
artery; EB - Early branch; ST - Superior trunk; MT - Middle trunk; IT - Inferior trunk;
ACP - Anterior clinoid process; FL - Frontal lobe; TL - Temporal lobe; PCA - Precentral
artery; CA - Central artery; ATA - Anterior temporal artery; MTA - Middle temporal
artery
Figure 6: (a) Inferior dominant (b) Pseudotrifurcation. IT - Inferior trunk; MTA - Middle temporal
artery; PTA - Posterior temporal artery; PPA - Posterior parietal artery; AA - Angular
artery; ST - Superior trunk
Cortical branches
The distribution of the cortical branches of the MCA has been extensively described.
In this study, 10 cortical branches were studied near their origin from M1 and M2
segments of the MCA.[[6]] The cortical branches studied were, temporopolar, anterior, middle, posterior temporal,
angular, orbitofrontal, precentral, central, anterior parietal, and posterior parietal
arteries. The pattern of origin of cortical branches from M2 [[Table 3]]. The outer diameter of the cortical branches at their origin and also the distance
of origin from the MCA origin was measured [[Table 4]]. The temporopolar, anterior temporal and orbitofrontal arteries originated relatively
close to MCA origin and the angular artery, posterior parietal, and posterior temporal
arise distally in the posterior half of the insular area. In Type 1, the cortical
branches from the secondary trunks were as follows-the superior trunk gave rise to
orbitofrontal, prefrontal, precentral, and central arteries, and the inferior trunk
gave rise to anterior temporal, middle temporal, posterior temporal, and angular arteries
while the anterior and posterior parietal was seen to arise from the dominant trunk.
In Type 3, the superior trunk gave rise to the orbitofrontal, prefrontal, precentral,
and central artery. The middle trunk gave rise to anterior parietal, posterior parietal,
and angular artery, and the inferior trunk gave rise to the anterior, middle, and
posterior temporal arteries. The unusual origin of cortical arteries was not observed.
Table 3: Origin of early branches and cortical branches
Table 4: Outer diameter of cortical vessels and distance of their origin from middle cerebral
artery origin
Stem arteries
The temporopolar and the ATA were the most common vessels arising from a common stem,
seen in 90% of hemispheres. Less frequent associations, the anterior temporal, middle
temporal and posterior temporal arteries in 5%; anterior temporal and posterior temporal
arteries in 5%; posterior temporal, posterior parietal, and central arteries in 2%;
central, anterior parietal, and precentral arteries in 4%; precentral, central, and
orbitofrontal arteries in 3%; posterior parietal and central arteries in 3%; and orbitofrontal
and central arteries in 1%. While commonly 2 stem pattern was observed in the frontal
lobe, temporal lobe had 4 stem pattern and the parietal lobe had 2 stem pattern [[Table 5]].
Table 5: Stem arteries
Cortical arteries
The cortical arteries arose from the stem arteries and supplied the individual cortical
areas. Generally, one or less commonly, two cortical arteries passed to each of the
12 cortical areas, the smallest cortical arteries arose at the anterior end of the
Sylvian fissure and the largest ones at the posterior limits of the fissure. The cortical
branches to the frontal, anterior temporal, and anterior parietal areas were smaller
than those supplying the posterior parietal, posterior temporal, temporo-occipital,
and angular areas. The smallest arteries supplied the orbitofrontal and temporopolar
areas, and the largest ones supplied the temporo-occipital and the angular areas.
Discussion
The main trunk of MCA takes origin from ICA (B), lateral to the optic chiasm, and
travels toward the medial end of Sylvian fissure below the APS.[[5]],[[7]],[[8]],[[9]] Bifurcation was seen in 80% of cases in our study similar to other studies[[7]],[[9]],[[10]] single trunk in 6% and trifurcation in 10%. In a North Indian study,[[11]] bifurcation was seen in 64%, single trunk in 6%, and trifurcation in 29%. In a
South Indian study,[[12]],[[13]] bifurcation was seen in 90%, trifurcation in 10%, and no single trunk. The mean
distance between the origin of the MCA and its main division was 18 ± 2.4 mm (right
hemisphere) and 18 ± 2.2 mm (left hemisphere), with no significant difference between
the two. In other studies, the mean length of M1 was measured to be 15 ± 1.3 mm,[[9]] 14–16 mm,[[14]] and 20 mm.[[12]] The diameter of M1 at origin was 2–3.5 mm with no significant difference between
both sides, in our study. In other studies, the mean diameter of M1 was 3 ± 0.1 mm[[9]] and 2–4 mm.[[12]]
The most proximal division (early bifurcation) was seen at 8 mm and the most distal
division (late bifurcation) at 25 mm. The more proximal the division, the more likely
that the perforating branches would arise from the secondary trunks.[[5]],[[7]],[[9]] Most saccular aneurysms of the MCA are located near the main division of the artery.[[15]],[[16]] Thus, while dissecting the aneurysm, the surgeon should be aware of the possibility
of finding perforating branches that run in a recurrent course from one of the secondary
trunks toward the APS.
Perforators arose M1 in 79%, 15.3% from M2 (superior - 8.5%, middle - 0.9%, inferior
- 5.9%); and the remaining 5.7% originated from early branches (early temporal branches,
5.3%, early frontal branches, 0.4%),[[9]] from M1 79.6% and from M2 in 20.3%.[[11]],[[17]] In our study, 90% perforating arteries were seen to arise before bifurcation and
10% from secondary trunks (superior trunk 8%, inferior trunk 2%) and 3% from early
branches. The number of perforators ranges from 3 to 15 in number.[[14]],[[18]] In our study, the number varied from 3 to 12. Four patterns of origin of perforators
were seen,[[14]] the most frequent being a single stem artery that then divides into many branches
(seen in 40%), two large parallel arteries that immediately divide into numerous branches
(30%), and numerous small twigs which arise directly from the inferio-medial side
of M1 (30%). The perforators can be divided into medial, intermediate, and lateral
groups.[[14]] The most consistent of the groups was the intermediate group in the current study,
seen in 93.3% with the commonest pattern being a single large stem which divided early
into multiple small arteries in its course to APS. The medial group was seen in 80%,
commonly arose as 2–4 parallel arteries at an obtuse angle from the parent artery
(the angle was however not measured). The lateral group was seen in 88.7%, and arose
as multiple small twigs at an acute angle from the parent vessel and took an S shape
course to APS. Perforators originated from MCA origin at a distance of 1 ± 0.2 mm
(medial group), 4 ± 1 mm (intermediate group), and 10 ± 2 mm (lateral group).
The knowledge of anatomy and the possibility of an early branch is important for the
surgical aspect, which would give a pseudo bifurcation appearance and result in misinterpretation
of true bifurcation and branches. The commonest early branch seen in our study was
the temporopolar artery (73.4%) as compared to 92% in other studies.[[9]] The uncal artery was seen to arise as an early branch in 5 cases (16%) in our study.
It is reported that the uncal artery takes origin mostly from ICA.[[14]] The commonest vessels arising as a common stem pattern in our study were the temporopolar
and ATA (43.3%), similar to other studies.[[7]],[[9]]
The MCA is one of the most common sites of saccular aneurysms,[[15]],[[16]],[[19]],[[20]] mostly located on the distal part of the M1 segment at the bifurcation of MCA.
Saccular aneurysms rarely arise distal to the proximal portion of the M2 segment.
Traumatic aneurysms or bacterial aneurysms are located most commonly in the M4 segment.[[21]],[[22]],[[23]] The majority of intracranial AVM's receive part of their blood supply from branches
of the MCA.[[24]] Clinical syndromes associated with occlusion of the individual cortical branches
of MCA are rare.[[25]],[[26]],[[27]],[[28]] Embolisms frequently cause occlusion of the MCA than thrombosis.[[26]],[[27]],[[28]] EC-MCA anastomosis is a treatment option for distal MCA occlusions and moya-moya
disease.[[29]] The external diameter of 1 mm is the minimum requirement for long-term anastomosis
patency.[[30]] In the temporal zone, an artery with a diameter >1.0 mm was present in 70% of the
hemispheres. Chater et al.[[30]] recommended small craniotomy for exposing the cortical branches of the MCA and
that it be centered 6 cm above the external auditory canal. The distance between the
ear canal and the posterior end of the Sylvian fissure was recorded to be 6.6 cm in
length,[[9]] similar to our study. The outer diameter of the vessels in the insular area was
larger than 1 mm, and in the case of the secondary trunks, it was usually >2 ± 0.2
mm in our study, similar to other studies.[[7]],[[8]],[[9]] The angular artery, the vessel most appropriate for external carotid-ICA anastomosis,
was the largest among cortical branches, 1.4 ± 1 mm in our study, and 1.5 ± 0.2 mm
in another study.[[7]] Anomalies of the MCA are less common.[[11]],[[31]],[[32]] The anomalies reported are duplication and accessory MCA.[[12]],[[17]],[[19]] Aneurysm of the accessory MCA has been reported.[[33]],[[34]] There were no anomalies observed in our study.
Several authors have used different contrast media, which helps in delineating vascular
microanatomy better.[[5]],[[35]],[[36]] In the current study, though initially contrast media (CSD granules) was injected,
due to technical reasons, the uptake was not acceptable. Hence, most brains dissected
were without prior contrast administration.
Conclusion
Good knowledge of the microsurgical anatomy of MCA and its variations is a prerequisite
for a neurosurgeon operating in this area, the frequent mistake of misinterpreting
early branch for division of the main branch, can be avoided with knowledge of its
occurrence of the same. Cadaveric microsurgical dissection and practice if included
as an integral part of neurosurgical training, as in our institute, will improve the
neuroanatomical knowledge and understanding during live surgical or endovascular procedures.
All neurosurgical training institutes should have a fully equipped microsurgical cadaveric
lab and microsurgical dissection should be included as part of the neurosurgical training
curriculum.
