Surgical Management of Aneurysms of the Middle Cerebral Artery

Ruptured and Unruptured Middle Cerebral Artery Aneurysms

Of the 3005 patients, 2365 (79%) had a primary SAH from a ruptured IA. MCAAs were the cause of SAH in 802 (34%) of the 2365 patients. Once again, the MbifAs were the most frequent, comprising 87% of all ruptured MCAAs. M1As represented 9% of the ruptured MCAAs. There were only 18 patients with ruptured MdistAs, which represents less than 1% of all ruptured IAs and only 2% of all ruptured MCAAs. The median size for ruptured MbifAs was 10 mm (range 1 to 80 mm). Both the M1As and MdistAs were generally smaller than MbifAs, with median diameters of 4 mm (range 1 to 54 mm). Interestingly, 29% of the ruptured MbifAs and as many as 51% of the ruptured M1As were smaller than 7 mm in diameter. This would indicate that, at least in the Finnish population, even small MCAAs are dangerous, and the International Study of Unruptured Intracranial Aneurysms (ISUIA) results are controversial. Of the 1704 MCAAs, 69 (4%) were giant, with most of those (80%) located at the MCA bifurcation. Of the 69 giant MCAAs, 72% were ruptured. There were only 18 fusiform MCAAs (1%) among the 1704. Unlike the giant aneurysms, fusiform aneurysms were distributed rather evenly along the entire course of the MCA. The total number of unruptured IAs in this series was 1888. Among unruptured IAs, MCAAs were even more frequent than among ruptured IAs ( n = 902, 48%). MbifAs were again the most common (75% of all unruptured MCAAs). The unruptured MCAAs were smaller in general than their ruptured counterparts, with median size ranging from 3 to 5 mm depending on the aneurysm’s location.

Intracerebral Hematomas, Intraventricular Hemorrhage, and Preoperative Hydrocephalus

Ruptured MCAAs often bleed into the adjacent brain, and as many as 347 (43%) of the 802 patients with ruptured MCAAs presented with a space-occupying ICH. ICHs were most often seen in MbifAs and MdistAs, at 44% and 50%, respectively, and were less frequently present in ruptured M1As (36%). The higher risk for ICH in more distal MCAAs is probably due to a tighter cistern, with the aneurysm more closely surrounded by the adjacent brain. The ICH was usually located in the temporal lobe (80%) and less frequently in the frontal lobe (20%). In the entire series, there was only one patient with a ruptured MCAA and parietal ICH. Intraventricular hemorrhage (IVH) was associated with the ICH in 15% of those cases, and isolated IVH without ICH was seen in only 5% of patients. Rarely, ruptured MCAAs can also present with a subdural hematoma, adding to the mass effect of an ICH (0.5% in our series). Preoperative hydrocephalus was detected in 29% of ruptured MCAAs.

Associated Aneurysms

MCA aneurysms are often associated with other aneurysms, accounting for 40% of cases in our series. Of the 579 patients who had at least one associated aneurysm, 313 (54%) had an MCAA as an associated aneurysm, with the remaining 46% having associated aneurysms at locations other than the MCA. The most common associated aneurysm was MbifA. The associated MCAAs were more often seen at the opposite MCA than within the same MCA as the primary aneurysm (58% vs. 29%); 13% of patients with multiple MCAAs had the associated MCAAs on both MCAs (“mirror aneurysms”). MbifA was also the most frequently associated aneurysm among all 2365 patients with ruptured IAs in this series, and 12% had at least one associated MbifA.

Middle Cerebral Artery

The MCA is the major terminal branch of the ICA; it supplies a large part of the cerebral hemisphere along with the insula, lentiform nucleus, and internal capsule. The MCA is the most complex major cerebral artery owing to its anatomic and hemodynamic features. Details of the microneurosurgical anatomy of the MCA have been described by Yaşargil ^, and others.

The MCA is generally divided into four segments: M1 (sphenoidal, horizontal), M2 (insular), M3 (opercular), and M4 (cortical). The M1 segment, the most proximal segment of the MCA, begins at the carotid bifurcation and extends to the bifurcation of the MCA, which is usually at the level of the limen insula, where it splits into two and sometimes three major M2 branches. The M2s give rise to 8 to 12 branches before becoming the M3s at the peri-insular sulcus. The M3s continue to the surface of the sylvian fissure at the lateral surface of the brain. The M4 segments are located on the parasylvian surface of the brain and supply the lateral cortical surface of the cerebral hemisphere. ^{, , , ,}

M1 Segment

The M1 starts in the sylvian cistern at the carotid bifurcation, supralateral to the optic chiasm, inferior to the anterior perforated substance, and posterior to the division of the olfactory tract. Thick arachnoid covers the M1 origin and bridging arachnoid fibers surround its proximal part. M1 travels laterally in the sylvian fissure to its bifurcation at the insular apex. At the MCA bifurcation, the M1 splits into typically two (bifurcation) branches (M2s), the superior (frontal) and the inferior (temporal) branches. ^, Türe et al. divided the M1 branches into (1) the cortical branches (often called the temporopolar, frontotemporal, and orbitofrontal branches) and (2) the lateral lenticulostriate branches. In the surgical trajectory to the sylvian cistern, the cortical branches (up to three) mainly project toward the temporal lobe (75%) and less often toward the frontal lobe (25%). Variations include temporal only, temporal and frontal, frontal only, and no major cortical branches. ^, Lateral lenticulostriate arteries (LLAs) originate mainly from the M1 trunk (see further on), and identification of their origin should help to distinguish the true MCA bifurcation. The preservation of M1 branches is of paramount importance in the occlusive therapy for M1As.

Lateral Lenticulostriate Arteries

The LLAs are quite variable in their number (up to 20) and sites of origin. ^{, , , , ,} LLAs mainly arise from the frontal aspect or cortical branches of the M1. However, in up to 23% of cases, LLAs may also arise from the MCA bifurcation, the M2s, or an accessory M2. ^, The more proximal the bifurcation, the greater the number of postbifurcational LLA branches. In the surgical trajectory, LLAs mainly arise from the frontal aspect of the M1 and mainly turn toward the frontal lobe. LLAs enter the brain via central and lateral parts of the anterior perforating substance and supply the substantia innominata, putamen, globus pallidus, head and body of the caudate nucleus, internal capsule and adjacent corona radiata, and the central portion of the anterior commissure. M1As and MbifAs may more or less involve LLAs at their branching sites, ^{, ,} and LLAs may be displaced, compressed, distorted, or stretched by M1As. During dissection and clipping of M1As, the site and pattern of origin of the LLAs are of special concern. LLAs may arise from a single-stem branch of the M1, and severing the stem branch causes infarction of the entire LLA supply area. The arachnoid adhesions together with cortical and lateral lenticulostriate branches as well as very small pial branches also originating from M1 limit the mobilization of M1 in the sylvian fissure. ^{, ,}

Middle Cerebral Artery Bifurcation and M2 Segments

The location of the bifurcational complex in the sylvian fissure varies considerably depending on the length of the M1 as well as the angioarchitecture of the bifurcation complex. ^{, , ,} Occasionally a thick frontal or temporal cortical branch of the M1 trunk creates a “false bifurcation” more proximally. After their origin at the MCA bifurcation, the M2s run somewhat parallel and supply the insula. ^{, ,} The M2s are seldom of equal diameter (15%); usually the inferior (temporal) trunk is dominant (50%) among the two to four M2 branches. In 55% of the hemispheres studied by Türe et al., the dominant M2 trunk bifurcated soon after the main bifurcation. This gave an impression of trifurcation in 12.5%, and quadrifurcation was seen in 2.5% when both M2s bifurcated immediately. Umansky et al. reported bifurcation in 66%, trifurcation in 26%, and quadrifurcation in 4%; Gibo et al. reported bifurcation in 78%, trifurcation in 12%, and multiple trunks in 10%.

The M2s give rise to 8 to 12 branches, mainly arising from the superior trunk, before becoming the M3s. The superior (frontal) M2 is the origin of the prefrontal, precentral, and central arteries. Furthermore, 23% the anterior and posterior parietal arteries have their origin from the superior M2. They mainly supply the inferior frontal cortex, the frontal opercular cortex, and also the cortex in the parietal and central sulcus areas. ^{, , ,} The inferior (temporal) M2 is the main origin of the posterior and middle temporal arteries, supplying mainly the middle and posterior temporal cortex and temporo-occipital, angular, and posterior parietal regions. ^{, , ,}

Distal Middle Cerebral Artery Branches (M3 and M4)

The M3 (opercular) segments start at the peri-insular sulci, from where they rise toward the lateral surface of the brain at the surface of the sylvian fissure. The M3 branches run on either side (temporal or frontal) of the sylvian fissure; they do not generally cross over. The M3s mainly supply the medial opercular surface and, to a lesser extent (25%), the superior or inferior peri-insular sulcus. The M4 segments are located on the cerebral cortex, arising from inside the sylvian fissure. ^{, , ,} They supply the 12 previously documented arterial territories of the lateral surface of the cerebral hemisphere. These are the (1) lateral orbitofrontal, (2) prefrontal, (3) precentral, (4) central, (5) anterior parietal, (6) posterior parietal, (7) angular, (8) temporo-occipital, (9) posterotemporal, (10) middle temporal, (11) anterotemporal, and (12) temporopolar areas. ^{, , ,}

Cisternal Anatomy

The MCA (M1 to M3) travels inside the sylvian fissure for most of its course. Only the proximal portion of the M1 segment is found inside the carotid cistern, which is limited by the proximal sylvian membrane from its lateral border. After passing the proximal sylvian membrane, the M1 enters into the anterior compartment of the sylvian cistern. Most of the LLAs can usually be found in the anterior compartment of the sylvian cistern. The borderline between the anterior and posterior compartments of the sylvian cistern is the limen insula. The posterior compartment of the sylvian cistern is located behind the limen insulae, where the MCA, before or after bifurcating, makes a relatively sharp, almost 90-degree turn (“the genu of the MCA”). The posterior compartment is further divided into the medial and lateral compartments by the intermediate sylvian membrane. The medial compartment contains the M2 trunks, whereas the M3 segments passing toward the cortical surface run for most of their course in the lateral compartment. The width, depth, and folding of the sylvian fissure vary considerably. ^, In general, the portions of the MCA that are most difficult to reach are on the M1 segment once it has entered the sylvian cistern, as the cisternal space here is very deep and narrow and there is a high risk of injuring the LLAs.1 The other challenging region is the very distal part of the sylvian fissure, which is also narrow and carries the risk of damaging cortical MCA branches. Fortunately, most MCA aneurysms are located at the MCA bifurcation, which can be found in most cases at the border of the anterior and posterior compartments of the sylvian cistern, where the cistern is wider.

When the sylvian fissure for MCA aneurysms is being opened, the posterior compartment of the sylvian cistern is typically entered first. To enter the sylvian fissure, the frontotemporal arachnoid membrane covering the cortical surface above the sylvian fissure must be opened. Below that lies the lateral sylvian membrane, which must be opened as well. The superficial sylvian veins course between these two membranes. Entering still deeper into the sylvian fissure, another arachnoid membrane is encountered: the intermediate sylvian membrane. Distal portions of the M3 trunks can already be found above the intermediate sylvian membrane, but the M2 trunks are deeper, below this level.

Venous Anatomy

The most important vein encountered during surgery for MCA aneurysms is the superficial sylvian vein. It usually arises at the posterior end of the sylvian fissure as one or several trunks, and courses anteriorly and inferiorly along the fissure. The separate trunks often merge into a single large channel before emptying into the venous sinuses along the sphenoid ridge. The superficial sylvian vein receives the frontosylvian, parietosylvian, and temporosylvian veins and commonly anastomoses with the veins of Trolard and Labbé. It penetrates the arachnoid covering of the anterior portion of the sylvian fissure and joins the sphenoparietal sinus as it courses just below the medial part of the sphenoid ridge, or it may pass directly to the cavernous sinus. Anomalies of the venous configuration are common; sometimes the superficial sylvian vein may be absent altogether. ^, Most of the time the superficial sylvian vein courses mainly on the temporal side of the sylvian fissure; therefore arachnoid opening of the frontotemporal arachnoid membrane should be planned on the frontal lobe side of the sylvian fissure. Venous crossover branches from one side of the sylvian fissure to the other are more frequent than in arteries. The main trunk of the superficial sylvian vein should always be left intact to prevent postoperative venous infarcts. Small crossover branches may need to be coagulated and cut to provide sufficient exposure of the deeper parts of the sylvian fissure. Deeper inside the sylvian fissure, the deep middle sylvian vein can be encountered. This collects venous outflow mainly from veins of the insular cortex and it terminates in the basal vein of Rosenthal.

Kazumata et al. described a classification of sylvian veins with subclassification into superficial, intermediate, and basal veins. Superficial sylvian veins usually have a single main trunk with tributaries from the frontal or temporal lobe or two main trunks with drainage from the frontal lobe or the temporal lobe. The insular veins with a common stem that drains into the basal vein or into the sphenoparietal sinus are the intermediate sylvian veins. The olfactory vein, posterior fronto-orbital vein, anterior cerebral vein, and branches from the optic chiasm are the basal veins.

Location and Orientation of Middle Cerebral Artery Aneurysms

M1As can be found along the entire M1 segment, most often at its distal portion at the origin of one of the cortical branches. On angiograms, the M1As are oriented with their dome pointing in an anterior, inferior, superior, or posterior direction. The superior or posterior projecting M1As, also called frontally projecting, protrude toward the frontal lobe. They are considered the most challenging M1As for three main reasons: (1) they are heavily involved with LLAs; (2) in the surgical view, the M1 trunk partially or completely obstructs the view toward the aneurysm’s base and the origin of the cortical branch or branches; and (3) the dome is buried inside the inferior portion of the frontal lobe in the deepest and narrowest part of the proximal sylvian fissure. The M1As with anterior or inferior projection, also called temporally projecting, protrude toward the temporal lobe. They are usually easier to expose during dissection than the frontally projecting M1As.

The orientation of MbifAs in the sylvian fissure depends on the depth of the fissure, the length and course of the M1, and the projection of the MbifA dome. We classify MbifAs into five groups based on their orientation, as follows:

• Intertruncal MbifA: The dome projects superiorly in the coronal anteroposterior (AP) plane and posteriorly in the axial plane. Intertruncal MbifAs lie between the M2s, the base often more on the thicker M2, and the M2s are more or less involved in the base.

• Inferior MbifA: The dome projects inferiorly in the coronal AP plane and anteriorly (toward the sphenoid ridge) in the axial plane.

• Lateral MbifA: The dome projects laterally in the coronal AP plane and laterally in the axial plane, in the same direction as M1.

• Insular MbifA: The dome projects medially (toward the insula) in the coronal AP plane and medially in the axial plane.

• Complex MbifA: In some dysmorphic and large or giant aneurysms, the growth of the dome may be multidirectional and the relation with M1 and M2s may be a combination of the aforementioned types. Types 2, 3, and 4 are not intertruncal and do not principally involve the M2s. The orientation may be distorted by a space-occupying ICH.

We divide MdistAs into aneurysms of the M2 trunk or at the M2–M3 junction, and those distal to the M2–M3 junction or of peripheral (M3) branches. Location is more important than the dome orientation in MdistAs.