Surgical Management of Aneurysms of the Middle Cerebral Artery

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Chapter 75 Surgical Management of Aneurysms of the Middle Cerebral Artery

The middle cerebral artery (MCA) is a very common site for aneurysm formation. In Finland, MCA aneurysms (MCAAs) represent 40% of all intracranial aneurysms.13 MCAAs are more frequent among unruptured aneurysms (48%) than among ruptured aneurysms (34%).4 Despite being so common, surprisingly few reports deal with MCA aneurysms, and especially the overall management outcome of this specific group of patients.517 Most MCAAs are located distal to the circle of Willis, and they are often broad based and one or several branches originate from a base.18 When ruptured, they present with intracerebral hematoma (ICH) in nearly half of all cases; many of these hematomas cause severe mass effect.13 In his pioneering work on surgery for intracranial aneurysms (IAs), Dandy considered MCAAs hazardous for surgical management, and even inoperable.19 Although currently only a few MCAAs are inoperable, they certainly still present striking problems as compared with other aneurysms in the anterior circulation. The main challenges when operating on MCA aneurysms is the lack of collateral circulation, so that inadvertent occlusion of the MCA or one of its branches can lead to calamitous infarctions and death, especially in acute subarachnoid hemorrhage (SAH). The MCAAs are less suitable for endovascular surgery than other anterior circulation aneurysms,2025 because of both their anatomy (broad neck with high recanalization rate) and their frequent association with expanding hematomas; thus neurosurgeons should focus on the safe treatment of these lesions.17,2632

The purpose of this chapter is to review practical anatomy, preoperative planning, and avoidance of complications in the microsurgical dissection and clipping of MCAAs. This review is mainly based on the experience of the senior author (JH) in two of the five Finnish University Hospital neurosurgical departments (Helsinki and Kuopio), which serve, without selection, the catchment area of the entire southern and eastern Finland regions (population 3 million). These two centers have treated nearly 10,000 aneurysm patients since the beginning of the microneurosurgical era in the mid 1970s. Our aim is to present a consecutive, population-based series with as little selection bias as possible. The data presented is not reflective of the senior author’s personal series alone. Most of the data is derived from the Kuopio Cerebral Aneurysm Database (1977–2005), which contains information on all 3005 consecutive patients harboring 4253 aneurysms who were treated at Kuopio University Hospital, Finland, from 1977 to 2005.13

Aneurysms of the MCA

Middle cerebral artery aneurysms can be classified into three groups: proximal (M1As), bifurcation (MbifAs), or distal type (MdistAs) aneurysms (Table 75-1). The proximal MCA aneurysms or M1As are located on the main trunk (M1) of the MCA, between the bifurcation of the internal carotid artery (ICA) and the main bifurcation of MCA.1 The MbifAs are located at the main bifurcation of the MCA.2 The MdistAs, originate from the branches of the MCA distal to the main bifurcation inside the sylvian fissure.3 Each of these aneurysms have special features due to anatomic location and general behavior that need to be taken into consideration when planning occlusive treatment. Assigning an MCAA into a particular group can sometimes be difficult since the length and caliber of the M1 segment often varies and there may be two or even three major branching sites along its course. Generally, we consider MCA bifurcation to be the first and major branching site of the MCA where two or more rather similarly sized arterial trunks divide at the limen insula level. Occasionally, a thick frontal or temporal cortical branch of the M1 trunk creates a more proximal “false bifurcation.”33

Table 75-1 Three Categories of MCA Aneurysms

Category Location
M1A Main trunk of MCA, between ICA bifurcation and main MCA bifurcation
MbifA Main MCA bifurcation
MdistA Branches distal to main MCA bifurcation

ICA, internal carotid artery; MCA, middle cerebral artery.

Incidence of MCA Aneurysms

The MCA aneurysms represented 40% of all IAs in a consecutive and population-based series of 3005 patients with 4253 IAs from 1977 to 2005 in the Kuopio Cerebral Aneurysm Data Base.14 Tables 75-2 through 75-5 present the clinical data on the 1456 patients with MCA aneurysms in this series. Of the 3005 patients, 1456 (48%) had 1704 MCA aneurysms (Table 75-2). The most frequent location for MCAAs was the MCA bifurcation, and 1166 patients had 1385 MbifAs (33% of all 4253 IAs and 81% of all MCAAs). This breakdown is similar to other MCAA series.6,1013,15,17,34,35 M1As comprised 14% of the MCAAs and MdistAs were the least frequent ones (5%) (Table 75-2). The right side dominated over the left side (55% vs. 45%) (Table 75-3).

Table 75-2 Patients with MCA Aneurysms in Consecutive and Population-Based Series of 3005 Patients with 4253 IAs from 1977 to 2005 in Kuopio Cerebral Aneurysm Database

  No. Patients No. Aneurysms
Whole series 3005 4253
 Patients with primary SAH 2365 (79%) 3325 (78%)
 Patients without primary SAH 640 (21%) 928 (22%)
MCA aneurysms 1456 1704
 M1As 221 (15%) 241 (14%)
 MbifAs 1166 (80%) 1385 (81%)
 MdistAs 69 (5%) 78 (5%)
Ruptured MCA aneurysms 802 802
 M1As 73 (9%) 73 (9%)
 MbifAs 711 (87%) 711 (87%)
 MdistAs 18 (2%) 18 (2%)
Fusiform MCA aneurysms 18 18
 Fusiform M1As 6 (33%) 6 (33%)
 Fusiform MbifAs 8 (44%) 8 (44%)
 Fusiform MdistAs 4 (22%) 4 (22%)

IA, intracranial aneurysm; MCA, middle cerebral artery; SAH, subarachnoid hemorrhage.

Ruptured and Unruptured MCA Aneurysms

Of the 3005 patients, 2365 (79%) had a primary subarachnoid hemorrhage (SAH) from a ruptured IA. MCAAs were the cause of SAH in 802 (34%) of the 2365 patients. Again the MbifAs were the most frequent, comprising 87% of all the ruptured MCAAs (Table 75-2). M1As represented 9% of the ruptured MCAAs. There were only 18 patients with ruptured MdistA, less than 1% of all the ruptured IAs, and 2% of all the ruptured MCAAs. The median size for ruptured MbifAs was 10 mm (range 1 to 80 mm) (Table 75-3). Both the M1As and MdistAs were smaller than MbifAs in general, with median diameters of 4 mm (range 1–54 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.36 Among the 1704 MCAAs, 69 (4%) were giant, most of them (80%) located at the MCA bifurcation. Of the 69 giant MCAAs, 72% were ruptured. There were 18 fusiform MCAAs, only 1% of all the 1704 MCAAs. Unlike the giant aneurysms, fusiform aneurysms were distributed rather evenly along the whole course of the MCA (Table 75-2). The total number of unruptured IAs in this series was 1888. Among the unruptured IAs, the MCAAs were even more frequent than among the ruptured ones (n = 902, 48%). MbifAs were again the most common (75% of all the 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 location (Table 75-3).

Intracerebral Hematoma, Intraventricular Hemorrhage, and Preoperative Hydrocephalus

Ruptured MCAAs bleed frequently into the adjacent brain, and as many as 347 (43%) of the 802 patients with ruptured MCAAs presented with a space-occupying ICH (Table 75-4). ICHs were most often seen in MbifAs and MdistAs, 44% and 50%, respectively, and it were less frequently present in ruptured M1As (36%) (Fig. 75-1A to C). 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%) (Table 75-3). 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%, and isolated IVH without ICH was seen in only 5% of patients (Table 75-4). Rarely, ruptured MCAAs can also present with a subdural hematoma adding to the mass effect of an ICH (0.5% in our series) (Fig. 75-1B). Preoperative hydrocephalus was detected in 29% of the ruptured MCAAs (Table 75-4).

Associated Aneurysms

Middle cerebral artery aneurysms are often associated with other aneurysms, accounting for 40% of cases in our series (Table 75-5). Of the 579 patients who had at least one associated aneurysm, 313 (54%) had an MCAA as an associated aneurysm and 46% had 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 at 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”) (Table 75-5) (Fig. 75-2). 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.

Microsurgically Relevant Anatomy

Middle Cerebral Artery

The middle cerebral artery (MCA) is the major terminal branch of the ICA supplying a large part of the cerebral hemisphere along with the insula, lentiform nucleus, and internal capsule.37 The MCA is the most complex major cerebral artery owing to its anatomic and hemodynamic features. Microneurosurgical anatomy details of the MCA have been described by Yaşargil13,33 and others.3742

The MCA is generally divided into four segments: M1 (sphenoidal), M2 (insular), M3 (opercular), and M4 (cortical).43 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 limen insula where it splits into two, sometimes three, major M2 branches. The M2s give rise to 8 to 12 branches before becoming the M3s at the peri-insular sulcus.37 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.13,33,37,38,43

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 olfactory tract. Thick arachnoid covers the M1 origin and bridging arachnoid fibers surround its proximal part. M1 travels laterally in the sylvian fissure until the bifurcation at the insular apex.37 At the MCA bifurcation, the M1 splits usually into two (bifurcation) branches (M2s), the superior (frontal) and the inferior (temporal).33,37 Türe et al. divided M1 branches into (1) the cortical branches (often named as temporopolar, frontotemporal, and orbitofrontal branches) and (2) the lateral lenticulostriate branches. In the surgical trajectory to the sylvian cistern, the cortical branches (one 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.37,43 Lateral lenticulostriate arteries originate mainly from the M1 trunk (see below), 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 lateral lenticulostriate arteries (LLAs) are quite variable in number (up to 20) and in sites of origin.33,37,38,40,41,44 Lateral lenticulostriate arteries mainly arise from the frontal aspect or cortical branches of the M1. However, LLAs may also arise, in up to 23%, from the MCA bifurcation, the M2s, or an accessory M2.37,40 The more proximal the bifurcation, the greater the number of postbifurcational LLA branches.43 In the surgical trajectory, LLAs mainly arise from the frontal aspect of the M1 and they 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.37 M1As and MbifAs may more or less involve LLAs at their branching sites,13,40,43 and LLAs may be displaced, compressed, distorted, or stretched by M1As.44 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 M1, and severing the stem branch causes infarct in the entire LLA supply area.44 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.33,37,41

MCA 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.33,37,38,43 Occasionally, a thick frontal or temporal cortical branch of the M1 trunk creates a “false bifurcation” more proximal.33 After their origin at the MCA bifurcation, the M2s run somewhat parallel and supply the insula.37,41,43 The M2s are seldom of equal diameter (15%), and usually, the inferior (temporal) trunk is dominating (50%). In 55% of the hemispheres studied by Türe et al., the dominant M2 trunk bifurcated soon after the main bifurcation.37 This gave an impression of trifurcation in 12.5%, and quadrifurcation was seen in 2.5% when both M2s bifurcated immediately. Umansky et al.40 reported bifurcation in 66%, trifurcation in 26%, and quadrifurcation in 4%, and Gibo et al.38 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.37 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 M2.37 They mainly supply the inferior frontal cortex, the frontal opercular cortex, and also the cortex in parietal and central sulcus areas.33,37,38,43 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.33,37,38,43

Distal MCA 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.37 The M4 segments are located on the cerebral cortex rising from inside the sylvian fissure.33,37,38,43 They supply the 12 previously documented arterial territories of the lateral surface of the cerebral hemisphere: (1) the lateral orbitofrontal, (2) the prefrontal, (3) the precentral, (4) the central, (5) the anterior parietal, (6) the posterior parietal, (7) the angular, (8) the temporo-occipital, (9) the posterior temporal, (10) the middle temporal, (11) the anterior temporal, and (12) the temporopolar areas.33,37,38,43

Cisternal Anatomy

The MCA (M1–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.45 After passing the proximal sylvian membrane the M1 enters into the anterior compartment of the sylvian cistern. It is usually in the anterior compartment of the sylvian cistern where most of the LLAs can be found.45 The borderline between the anterior and posterior compartment of the sylvian cistern is the limen insula. The posterior compartment of the sylvian cistern is located behind the limen insulae where MCA, before or after bifurcating, makes a relatively sharp, almost 90-degree turn (“the genu of MCA”).46 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.45 The width, depth, and folding of the sylvian fissure vary considerably.33,46 In general, the portions of MCA that are the 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 high risk of injuring the lateral lenticulostriate arteries.1 The other challenging region is the very distal part of sylvian fissure, which is also narrow and there is risk of damage to 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 opening the sylvian fissure for MCA aneurysms, the posterior compartment of the sylvian cistern is usually entered first. To enter the sylvian fissure, the frontotemporal arachnoid membrane covering the cortical surface above the sylvian fissure needs to be opened. Below that lies the lateral sylvian membrane, which needs to 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 portion of the M3 trunks can be found already 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.47 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.47 Anomalies of the venous configuration are common and sometimes the superficial sylvian vein may be absent altogether.33,47 Most of the time the superficial sylvian vein courses mainly on the temporal side of the sylvian fissure so that 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 branch 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.48

Location and Orientation of MCA Aneurysms

M1As can be found along the entire M1 segment, most often at the distal portion of the M1 segment at the origin of one of the cortical branches. On angiograms, the M1As are oriented with their dome pointing anterior, inferior, superior, or posterior (Fig. 75-3A to F). The superior or posterior projecting M1As, also called frontally projecting, project toward the frontal lobe. They are considered the most challenging M1As for three main reasons: (1) heavy involvement with LLAs, (2) in the surgical view the M1 trunk is partially or completely obstructing the view toward the aneurysm base and the origin of the cortical branch(s), 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, project toward the temporal lobe. They are usually easier to expose during dissection than the frontally projecting ones.

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 (Fig. 75-4A to H):

We divide MdistAs into aneurysms of the M2 trunk or at the M2–M3 junction (Fig. 75-6A and B), and those distal to the M2–M3 junction or of peripheral (M3) branches (Fig. 75-7). Location is more important than the dome orientation in MdistAs.

Imaging

In diagnostics, digital subtraction angiography (DSA) is still the “gold standard” in many centers. In our centers, multislice helical computed tomography (CT) angiography (CTA) is the primary modality for imaging of IAs for several reasons:

Some MCAAs may be difficult to visualize by routine 3D CTA,50,57 usually due to very small size, so that subsequent rotational 3D DSA is required.

For intraoperative navigation, 3D CTA and/or DSA reconstructions should be rotated to illustrate the length, depth, and course of the M1 in the sylvian fissure; projection of the MCAA dome and its relationship to the MCA bifurcation and M2 trunks, distance from the ICA bifurcation along the M1, and possible involvement with cortical branches; and the site of possible rupture. Other lesions of the MCA should be differentiated and vascular anomalies of the region should be looked for. In giant and fusiform MCA aneurysms, magnetic resonance imaging (MRI) with different sequences, along with 3D CTA, helps to distinguish the true wall of the aneurysm and the intraluminal thrombosis.

At the workstation, 3D CTA images can be rotated accordingly to evaluate the surgeon’s view to the MCA and the bifurcation, which is not standard but is tailored according to the aneurysm dome projection and relation to the MCA and its branches. The prime concern is to find a view that best helps to preserve the perforators around the base and the dome of the aneurysm.

Principles of Neuroanesthesia

A review of our neuroanesthesiologic principles in treatment of SAH patients has been published previously.59 Here we present only some key points.

In all SAH patients, arterial blood pressure is measured invasively. Before the ruptured aneurysm has been secured, systolic blood pressure must be controlled, and blood pressures above 160 mm Hg should be treated, such as with labetalol. At the same time, too-low a systolic blood pressure will not provide sufficient perfusion pressure and should be prevented as well. In patients with an intracranial space-occupying hematoma, higher blood pressure can be allowed to secure adequate cerebral perfusion pressure. The transmural pressure of the aneurysm sac is one of the determinants of the risk of rebleeding, but as this cannot be measured, the accepted blood pressure remains to be determined individually.

In conscious patients, spontaneous breathing is usually adequate but in patients with Glasgow Coma Scale (GCS) 8 or less, an artificial airway and controlled ventilation are indicated. Adequate anesthesia is required before intubation to prevent rebleeding, since laryngoscopy and intubation induces a stress response with an increase in blood pressure. Sedation using propofol should be considered in patients under controlled ventilation.

Tranexamic acid (1 g intravenously every 6 hours for 3 days) is administered to prevent rebleeding until clipping.60 Nimodipine (oral or intravenous) is given to all patients with ruptured aneurysms to prevent vasospasm.61,62

Postoperatively, all SAH patients are treated at the neurointensive care unit (NICU). Our general principles of postoperative treatment and monitoring are summarized in Table 75-6.

Table 75-6 Postoperative Care of Patients with Aneurysmal SAH at Neurosurgical ICU in Helsinki

Prevention/Treatment of Vasospasm
Nimodipine oral/I.V.
Magnesium: 60 mmol/day (only in detected vasospasm)
Hypertension: phenylephrine, norepinephrine, or dopamine/dobutamine
Hemodilution: Hct 0.3. Ringer’s acetate (+NaCl)/tetrastarch
Prevention of vasospasm:
HH: 1-2; Fischer: 1-2; sBP > 110–120 mm Hg, normovolemia
HH: 1-2; Fischer: 3-4; sBP > 140 mm Hg, normovolemia
HH: 3-5: Fischer: 3-4; sBP > 140–160 mm Hg, slight hypervolemia
Treatment of vasospasm:
“Triple H” (hypertension; hypervolemia; hemodilution): sBP > 160–180 mm Hg
Pulmonary/Airway Management
Oxygen/ventilatory support as needed: Normoventilation, SaO2 > 95%, PaO2 > 13 kPa
Pneumonia, aspiration: Antibiotics
Pulmonary edema: Noncardiogenic/cardiogenic, PEEP, furosemide, dobutamine
Seizures
Previous antiepileptic drugs (lorazepam or lavetiracetam)
No routine prophylaxis
Electrolytes and Glucose
Correct abnormalities
Hyponatremia: SIADH, CSW syndrome
B-gluc 5-8 mmol/L
Sedation, Postoperative Pain and Fever
Propofol and/or dexmedetomidine patients under mechanical ventilation
Benzodiatzepines
Opioids: Oxycodone
Paracetamol
Active cooling as needed
NSAIDs: 5–7 days post SAH
Thromboembolism
Antiembolic or pneumatic compression stockings
Individually LMWH 5–7 days postcraniotomy

CSW, cerebral salt wasting; HH, Hunt-Hess; LMWH, low molecular weight heparin; PEEP, positive end-expiratory pressure; SAH, subarachnoid hemorrhage; sBP, systolic blood pressure; SIADH, syndrome of inappropriate antidiuretic hormone hypersecretion.

Patient Positioning and Craniotomy

All except those rare distal MCAAs can be reached through a standard pterional approach as described by Yaşargil.13 At our institution we prefer the lateral supraorbital (LSO) approach, a more frontal and less invasive modification of the pterional approach.63

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