15 M1 Anatomy and Role of Perforators in Outcome
15.1 Case Description
15.1.1 Clinical Presentation
A 76-year-old female presented with a 90-minute history of severe left-sided weakness, involving upper and lower limb, left facial droop, dysarthria, and gaze deviation. National Institutes of Health Stroke Scale (NIHSS) score was 18. Comorbidities included a previous history of unprovoked pulmonary embolus, hypercholesterolemia, and bipolar disorder. Although the patient denied a previous history of stroke, subsequent imaging showed an old lacunar infarct involving the right head of caudate nucleus. There were no other relevant comorbidities and no other cardiovascular risk factors.
15.1.2 Imaging Workup and Investigations
Noncontrast enhanced CT of the brain (Fig. 15.1a, b) demonstrated old lacunar infarct right basal ganglia, but no evidence of early infarction. There was no evidence of hemorrhage. CT angiography (CTA) demonstrated occlusion of the mid and distal M1 segment of the right middle cerebral artery (MCA), involving the very proximal M2 segments. There was, however, excellent collateralization to the MCA territory, with filling of MCA branches back to the level of the proximal M2 segments, showing the relatively short length of thrombus (Fig. 15.1c).
CT perfusion demonstrated significant mismatch with prolonged time to peak (TTP) within the right MCA territory (Fig. 15.2a), and preservation of relative cerebral blood volume (Fig. 15.2b).
15.1.3 Diagnosis
Right M1 segment of MCA occlusion.
15.1.4 Treatment
In view of the high NIHSS score, presentation clearly within the time window, lack of early change on CT, presence of large artery occlusion on CTA, and the excellent collateral supply to the occluded territory, decision was made to proceed with treatment and intervention.
Initial Management
Full-dose intravenous tissue plasminogen activator (tPA) was administered.
Endovascular Treatment
Material
8-Fr short angiographic sheath.
8-Fr MERCI balloon guide catheter.
5-Fr H1 slip catheter.
0.035 angled hydrophilic wire.
Trevo 18 microcatheter.
Synchro 14 microguidewire.
Trevo 4 × 20 mm stent retriever.
8-Fr Angio-Seal closure device.
Technique
Intervention was performed with conscious sedation and local anesthetic. A single-wall right common femoral artery puncture was performed, and the 8-Fr short vascular access sheath inserted. The 8-Fr balloon guide catheter was advanced to the right internal carotid artery (ICA) over a 5-Fr H1 slip catheter with the aid of an angled Terumo guidewire using roadmap guidance. Right ICA angiography confirmed the presence of occlusive thrombus in the M1 segment of the right MCA (Fig. 15.3a). There was good leptomeningeal collateralization to the right MCA territory from anterior cerebral artery (ACA; Fig. 15.3b) with retrograde filling of MCA to the M2 level in arterial phase of angiography. The presence of occlusive M1 thrombus resulted in occlusion of lenticulostriate perforators. There was some filling of the medial lenticulostriate territory through perforators arising from the very proximal patent right M1 segment and A1 segment.
A Trevo 18 microcatheter was navigated to the right MCA over Synchro 14 microwire. The M1 occlusion was traversed and the microcatheter placed in the proximal superior division of the right MCA. Microcatheter injection confirmed position distal to thrombus. A Trevo 4 × 20 mm stent retriever was then deployed from the M2 division of MCA, across the M1 thrombus to the level of supraclinoid ICA. The stent was left in situ for 5 minutes to allow incorporation of thrombus. Control angiography with the stent retriever deployed demonstrated some antegrade flow in the right MCA with filling defects consistent with thrombus in the stent (Fig. 15.3c, arrow depicts stent retriever distal tip). After 5 minutes, the guide catheter balloon was inflated in the proximal right ICA, and stent retrieval performed with flow arrest and continuous manual aspiration. Despite this, clot was not retrieved in the stent retriever, and control angiography showed unchanged appearance of the right M1 occlusion. In total, four passes of stent retriever were required to fully recanalize the right M1 occlusion, with thrombus retrieved in the stent on the third and fourth passes. Final angiography demonstrated complete restoration of flow through the right M1 segment, with normal filling of the territory beyond the occlusion (Fig. 15.3d, e). There was filling of the lenticulostriate perforators (Fig. 15.3d). No evidence of arterial narrowing or spasm was seen at the site of thrombectomy.
All devices were removed. Hemostasis of the femoral artery puncture site was achieved by insertion of an 8-Fr Angio-Seal.
Postprocedure Care/Outcome
The patient demonstrated on-table improvement following recanalization of the occluded artery, with improved power on the left side. She was transferred to the neuro high dependency unit in stable condition for further monitoring and care. Her subsequent course in hospital was uneventful. Noncontrast CT performed at 24 hours postprocedure (Fig. 15.4) showed infarction in the right putamen and in the posterior limb of internal capsule superiorly. There was no hemorrhagic transformation. Aspirin 81 mg once daily was commenced following the CT. She remained normotensive throughout her hospital stay. On day 5 postprocedure, the patient was discharged to rehabilitation center; her symptoms had almost completely resolved with just mild left-sided weakness remaining. On 3-month follow-up, she had further improved with complete resolution of the left-sided weakness.
15.2 Companion Case
15.2.1 Clinical Presentation
A 56-year-old woman presented with a 1-hour history of left facial droop, mild left upper limb weakness with pronator drift on examination, and left arm numbness with profound sensory deficit in the left arm. Examination also revealed mild dysarthria and left-sided neglect. NIHSS score was 7. Past medical history was significant for rheumatic heart disease with mitral stenosis and hypertension. There were no other cardiovascular risk factors, and family history was noncontributory.
15.2.2 Imaging Workup and Investigations
Noncontrast enhanced CT of the brain was performed at 70 minutes from symptom onset, with no evidence of early or established ischemic change and no hemorrhage (Fig. 15.5a–c). ASPECTS score was 10. Hyperdensity consistent with thrombus in an M2 branch was identified in the right sylvian fissure (Fig. 15.5b, c, arrow). CTA confirmed occlusion of a large caliber M2 branch of the right MCA (Fig. 15.5d, sagittal oblique reconstruction, arrow). The right M1 segment of MCA and lenticulostriate perforators from the M1 segment were patent.
CT perfusion demonstrated significant mismatch with a wedge-shaped area of prolonged TTP and mean transit time within the right MCA territory (Fig. 15.6a, b), as well as reduction in relative cerebral blood flow with preservation of relative cerebral blood volume (Fig. 15.6c, d).
15.2.3 Diagnosis
Right M2 branch occlusion.
15.2.4 Treatment
In view of the NIHSS score of 7, presentation clearly within the time window, lack of early change on CT, and the presence of large artery occlusion on CTA with mismatch on CT perfusion, decision was made to proceed with treatment and intervention.
Initial Management
Full-dose intravenous tPA was administered.
Endovascular Treatment
Material
8-Fr short angiographic sheath.
5-Fr Berenstein diagnostic catheter.
0.035 Angled hydrophilic wire.
0.035 Advantage exchange length guidewire.
8-Fr MERCI balloon guide catheter.
Rebar 18 microcatheter.
Synchro 14 microguidewire.
Solitaire AB 3 × 20 mm stent retriever.
8-Fr Angio-Seal closure device.
Technique
Intervention was performed with conscious sedation and local anesthetic. A single-wall right common femoral artery puncture was performed, and the 8-Fr short vascular access sheath inserted. A 5-Fr Berenstein diagnostic catheter was advanced to the right proximal ICA over a 0.035 angled Terumo glide wire. Angiography confirmed persistent right M2 branch occlusion (Fig. 15.7a, b, arrows). There was normal variant anatomy with right M1 segment trifurcation. The occluded branch gave supply to the central group, parietal and angular branches of MCA, with collateralization from ACA evident on late arterial to venous phase of angiography (not shown). The right M1 segment and lenticulostriate perforators were patent. A standard exchange maneuver was performed in the right ECA, with the Advantage exchange length guidewire, and the 8-Fr MERCI balloon occlusion guide catheter advanced to the right cervical ICA. Through this, a Rebar 18 microcatheter was navigated through the M1 segment, and across the M2 occlusion with the aid of a Synchro 14 guidewire. Microcatheter injection confirmed position distal to the thrombus. A 3 × 20 mm Solitaire was then deployed across the thrombus. Control angiography with the stent retriever in situ showed partial reopening of the occluded branch (Fig. 15.7 c, d, arrows), with filling of the central group but no filling of posterior parietal or angular arteries. It was presumed that the lesion constituted a “Y”-shaped thrombus, or else covered the origin of these branches. The stent was left in situ for 5 minutes to allow incorporation of thrombus, after which retrieval was performed with flow arrest and suction. Three large clot fragments were obtained from the stent and suction syringe. Control angiography showed complete recanalization of the occluded branch and reperfusion of the entire distal territory, including the posterior parietal and angular branches (Fig. 15.8a, b). There was mild spasm seen in the M2 branch at the site where stent retriever had been deployed (Fig. 15.8a, b, arrows).
The guide catheter was removed. The 8-Fr Angio-Seal device was placed at the puncture site for hemostasis.
Postprocedure Care/Outcome
The patient demonstrated on-table improvement, with improvement of the facial droop, left upper limb weakness, dysarthria, and neglect. Some residual sensory disturbance remained, which resolved over her hospital stay. Postprocedure she was transferred to the neuro high dependency unit in stable condition for further monitoring and care. Her subsequent course in hospital was uneventful. MRI was performed at 24 hours postprocedure (Fig. 15.8c) and demonstrated a small region of restricted diffusion involving the posterior third of the right insular cortex, extending slightly into the lateral-most aspect of the right precentral gyrus, with no evidence of diffusion restriction elsewhere. The infarct was small compared with the ischemic penumbra on the CT perfusion study obtained prior to treatment. There was no evidence of hemorrhagic transformation. Aspirin 81 mg daily was commenced following the MRI. Echocardiography was performed to rule out a cardioembolic source, given her history of rheumatic heart disease and mitral stenosis. This demonstrated a dilated left atrium, moderate mitral stenosis, and mild to moderate mitral regurgitation. There was no evidence of patent foramen ovale or septal defect, and no thrombus. Given her history, she was started on warfarin prior to discharge. Blood pressure control was optimized. She was discharged home (modified Rankin scale [mRS] of 0), at 4 days following her presentation and intervention.
15.3 Discussion
15.3.1 Background
The MCA is one of the terminal branches of the ICA, together with the ACA. Embryologically, at approximately ninth week of fetal life, the MCA develops from the fusion of several ACA perforators of the lateral striate group in response to the significant growth of the cerebral hemispheres that constitute the telencephalon. The first segment, denominated M1, is usually constituted by a single trunk with a diameter of approximately 3 mm, which courses laterally parallel to the floor of the middle cranial fossa. Distal to the main trunk, the artery typically (78% of cases) divides into two divisions (termed superior and inferior); less commonly there are three (12%) or greater than three divisions (10%). There is some controversy regarding the location of the transition point of the M1 and M2 segments. The traditional transition point described by Fischer (1938) was considered to occur when the artery performs a 90-degree turn to enter the vertical portion of the Sylvian fissure; thus, the M1 segment would include a pre- and post-bifurcation segment. This does not, however, have practical relevance. A more practical concept is to consider that the M1 segment ends when the main trunk bifurcates, a definition which is now also used in the recent consensus statement regarding recommendations on angiographic revascularization grading standards for acute ischemic stroke.
Mechanical thrombectomy is now the standard of care for acute ischemic stroke with occlusion of the M1 segment of MCA. The M1 segment of MCA was the most common location of intracranial arterial occlusion in the recently published randomized controlled trials which showed benefit for endovascular treatment in large artery occlusive stroke. For example, in MR CLEAN, M1 occlusion accounted for 66.1% of cases in the interventional group and 62% of cases in the control group. Similarly in the ESCAPE trial, M1 or effective M1 occlusions accounted for 68.1% of cases in the interventional group and 71.4% of cases in the control group, while in EXTEND-IA M1 occlusions accounted for 57% of cases in the interventional and 51% of cases in the control groups.
There are a number of important anatomical considerations in M1 segment of MCA occlusion, which can have a significant impact on patient outcome, the most important being the lenticulostriate arteries. The lenticulostriate arteries are a group of small caliber perforators arising from the proximal segments of the ACA and MCA. The following groups can be identified: from the ACA the recurrent artery of Heubner and the medial lenticulostriate arteries, and from the MCA the lenticulostriate arteries can be divided into a smaller medial group and a larger lateral group. There is a broad range of variations related to these perforating arteries. Most commonly, the lenticulostriate arteries of the MCA arise from the posterosuperior aspect of the M1 segment, although in approximately 20% of cases they can originate from the superior or inferior divisions of MCA, or less commonly from an early cortical branch of MCA. The medial group of lenticulostriate arteries from MCA are in equilibrium with the medial lenticulostriate arteries from the ACA and the recurrent artery of Heubner. Territory includes the anteroinferior portion of the head of caudate nucleus, the anterior third of the putamen, the anterior limb of internal capsule, the anterolateral edge of the globus pallidus, the medial aspect of the anterior commissure, and the anterior part of the hypothalamus. Territory of the lateral group of lenticulostriate arteries includes the upper portion of the head and body of caudate nucleus, the putamen, the lateral segment of globus pallidus, the lateral half of the anterior commissure, and the superior segments of both limbs of the internal capsule. The blood supply to the structures lateral to the putamen, including the claustrum and external capsule, is derived from perforators arising from the insular branches of the MCA.
As the lenticulostriates are end arteries, thrombus in the M1 segment of MCA can occlude the ostium of these perforating arteries resulting in infarction in their territory of supply. Proximal occlusions of the M1 segment of the MCA incorporating the lenticulostriate perforator origins are associated with a poorer clinical outcome than distal M1 occlusions that spare these perforators.
Another important anatomical consideration is that, similar to carotid terminus occlusion, there is no possibility of antegrade collateral supply to the distal territory in M1 segment of MCA occlusion. Therefore, collateral supply to the distal territory, if it exists, must be retrograde due to filling of leptomeningeal collaterals from the ipsilateral ACA or posterior cerebral artery (PCA) territory. Various grading schemes have been applied to assess collateral supply to the occluded MCA territory in M1 occlusive stroke. Good collateral supply to the occluded territory has been shown to be an independent predictor of good functional outcome following interventional treatment in M1 occlusive stroke.
Finally, in terms of anatomical considerations, while true anomalies of the MCA are rare and less frequent than anomalies of other intracranial arteries given the relatively recent phylogenetic ancestry of this artery, anomalous anatomy and variations in branching patterns can be encountered, and must be recognized. These will be discussed later in more detail, but briefly encompass the duplicated/accessory MCA, fenestration of the M1 segment, early bifurcation of the M1 segment, variation in branching pattern/division of the M1 segment, and variation in dominance of the M2 trunks.