Reversible cerebral vasoconstriction syndrome

Reversible cerebral vasoconstriction syndrome

Reversible cerebral vasoconstriction syndrome (RCVS), AKA Call-Fleming syndrome, 1) a group of disorders sharing the cardinal clinical and angiographic features of reversible segmental multifocal cerebral vasoconstriction with severe headaches, focal ischemia, and/or seizures. May present as a hemorrhage restricted to a cortical sulcus

Epidemiology

RCVS has been reported to occur more frequently in women aged 20 to 50 years.

Etiology

Several mechanisms have been postulated involving transient deregulation of cerebral arterial tone, small vessel endothelial dysfunction, biochemical factors, hormonal deregulation, oxidative stress, and genetic predisposition. All these mechanisms and triggers are related with sympathetic over-activation which eventually produce vasoconstriction. RCVS is distinguished by acute severe recurrent thunderclap headaches with or without other neurological symptoms. However, the diagnosis can be challenging and most likely underdiagnosed requiring a high level of suspicion from the clinician 2).

Clinical features

Reversible cerebral vasoconstriction syndrome (RCVS) has emerged as the most frequent cause of thunderclap headache (TCH) in patients without aneurysmal subarachnoid hemorrhage, and as the most frequent cause of recurrent TCHs.

The typical TCHs of RCVS are multiple, recurring over a few days to weeks, excruciating, short-lived, and brought up by exertion, sexual activities, emotion, Valsalva maneuvers, or bathing, among other triggers. All these triggers induce sympathetic activation. In a minority of cases with RCVS, TCH heralds stroke and rarely death. Early diagnosis of RCVS in patients who present with isolated headache enables proper management and might reduce the risk of eventual stroke 3).

Outcome

Reversible cerebral vasoconstriction syndrome (RCVS) is characterized by severe headache and diffuse segmental constriction of cerebral arteries that resolves spontaneously within a few months. Although manifestations of stroke are not included in diagnostic criteria of RCVS, it is known that some cases may be associated with stroke, including intracerebral hemorrhage, subarachnoid hemorrhage, or cerebral infarction.


Intracerebral hemorrhage is the most common vascular complication in hospitalized RCVS patients, resulting in longer hospitalizations with more invasive procedures and higher healthcare expenditure. However, overall outcomes are excellent regardless of types of ICH, with no inpatient mortality observed in patients with hemorrhagic RCVS. Female sex and middle to older age-group are associated with higher odds of ICH. 4).

Case series

162 patients with RCVS. Clinical, brain imaging, and angiography data were analyzed.

The mean age was 44±13 years, 78% women. Hemorrhages occurred in 43% including 21 patients with intracerebral hemorrhage (ICH) and 62 with convexal subarachnoid hemorrhage (cSAH). The frequency of triggers (eg, vasoconstrictive drugs) and risk factors (eg, migraine) were not significantly different between hemorrhagic and nonhemorrhagic RCVS or between subgroups (ICH versus non-ICH, isolated cSAH versus normal scan). Hemorrhagic lesions occurred within the first week, whereas infarcts and vasogenic edema accumulated during 2 to 3 weeks (P<0.001). Although all ICHs occurred before cSAH, their time course was not significantly different (P=0.11). ICH and cSAH occurred earlier than infarcts (P≤0.001), and ICH earlier than vasogenic edema (P=0.009). Angiogram analysis showed more severe vasoconstriction in distal versus proximal segments in all lesion types (ICH, cSAH, infarction, vasogenic edema, and normal scan). The isolated infarction group had more severe proximal vasoconstriction, and those with normal imaging had significantly less vasoconstriction. Multivariable analysis failed to uncover independent predictors of hemorrhagic RCVS; however, female sex predicted ICH (P=0.048), and angiographic severity predicted infarction (P=0.043).

ICH and cSAH are common complications of RCVS. Triggers and risk factors do not predict lesion subtype but may alter central vasomotor control mechanisms resulting in centripetal angiographic evolution. Early distal vasoconstriction is associated with lobar ICH and cSAH, and delayed proximal vasoconstriction with infarction 5).

Case reports

2018

Reversible Cerebral Vasoconstriction Syndrome Without Typical Thunderclap Headache Complicated by Intracranial Hemorrhage and Posterior Reversible Encephalopathy Syndrome:A Case Report 6).


Al-Mufti et al. from the Rutgers New Jersey Medical School, describe a case of medically refractory Reversible cerebral vasoconstriction syndrome (RCVS) that required treatment with intra-arterial (IA) verapamil and subsequent nimodipine, resulting in both angiographic and clinical improvement after failing to respond to hemodynamic augmentation.

They also supplement a description of the case with a review of other case studies and case series in which IA calcium channel blockers were used to treat RCVS. They propose that the case they outline demonstrates that neurointerventional management with IA verapamil is appropriate and effective as an early intervention of medically refractory RCVS.

Using PubMed and Google Scholar, they performed a search of the English language literature with several combinations of the keywords “intra-arterial”, “calcium channel blockers”, “reversible cerebral vasoconstriction syndrome”, “RCVS”, “nimodipine”, “verapamil”, “milrinone”, and “nicardipine” to identify studies in which RCVS was treated with IA calcium channel blockers.

They identified eight case studies and case series that met our inclusion criteria. Eighteen patients are encompassed in these eight studies.

IA administration of calcium channel blockers has been shown to return cerebral vessels to their normal caliber in patients with medically refractory RCVS. However, there are no randomized controlled trials of the treatment of RCVS, and further studies are needed to elucidate the optimal treatment protocol for medically refractory RCVS 7).


Gonsales et al., present an unusual case of an 18-year-old female who developed RCVS after embolization of a dural arteriovenous fistula with onyx embolic material. A cerebral angiogram was performed and verapamil was administered intra-arterially demonstrating slight improvement of the constricted vessels with clinical improvement. The patient was maintained on oral verapamil during hospitalization. At 7-month follow-up, the patient was neurologically stable and a cerebral angiogram demonstrated no signs of vasoconstriction.

Endovascular procedures are a rare trigger for the development of RCVS and may be misdiagnosed. Prompt recognition of symptoms and diagnosis with treatment are necessary to reduce the risk of stroke. The management should follow the premise of discontinuing precipitating drugs and administering CCBs 8).

2016

A 19-year-old woman had a thunderclap headache, followed by left hemiparesis and left homonymous hemianopsia. Laboratory tests showed no signs of infection and immunological test results were unremarkable. MRI revealed a cerebral infarction in the right posterior cerebral artery territory, and digital subtraction angiography(DSA)showed right posterior cerebral artery stenosis on day 2. The first follow-up DSA demonstrated an irregular, bead-like appearance on day 9, but the stenotic lesion returned to normal on day 21. Reversible cerebral vasoconstriction syndrome should be suspected in cases of rapid resolution of symptoms 9).

2014

Ishi et al. present three cases of RCVS associated with various types of stroke, and then review the literature. Case 1:A 49-year-old woman presented with a headache followed by left hemiparesis and dysarthria. One month before the onset, she was transfused for severe anemia caused by uterus myoma. CT images revealed intracerebral hemorrhages in the right putamen and right occipital lobe. Angiography revealed multiple segmental constrictions of the cerebral arteries. One month after the onset, these vasoconstrictions improved spontaneously. Case 2:A postpartum 38-year-old woman who had a history of migraine presented with thunderclap headache. Imaging revealed a focal subarachnoid hemorrhage in the right postcentral sulcus and segmental vasoconstriction of the right middle cerebral artery. One week after the onset, this vasoconstriction improved spontaneously. Case 3:A 32-year-old woman who had a history of migraine presented with headache followed by left homonymous hemianopsia. Imaging revealed a cerebral infarction of the right occipital lobe and multiple constrictions of the right posterior cerebral artery. These vasoconstrictions gradually improved spontaneously 10).

References

1)

Call GK, Fleming MC, Sealfon S, et al. Reversible cerebral segmental vasoconstriction. Stroke. 1988; 19:1159–1170
2) , 8)

Gonsales D, das Gracas F, Santos R, Aguilar-Salinas P, Hanel RA. Reversible Cerebral Vasoconstriction Syndrome as an Unusual Complication of a Dural Arteriovenous Fistula treated with Onyx Embolization. World Neurosurg. 2018 May 8. pii: S1878-8750(18)30931-8. doi: 10.1016/j.wneu.2018.04.211. [Epub ahead of print] PubMed PMID: 29751188.
3)

Ducros A, Wolff V. The Typical Thunderclap Headache of Reversible Cerebral Vasoconstriction Syndrome and its Various Triggers. Headache. 2016 Apr;56(4):657-73. doi: 10.1111/head.12797. Epub 2016 Mar 26. Review. PubMed PMID: 27015869.
4)

Patel SD, Topiwala K, Saini V, et al. Hemorrhagic reversible cerebral vasoconstriction syndrome: A retrospective observational study [published online ahead of print, 2020 Sep 7]. J Neurol. 2020;10.1007/s00415-020-10193-y. doi:10.1007/s00415-020-10193-y
5)

Topcuoglu MA, Singhal AB. Hemorrhagic Reversible Cerebral Vasoconstriction Syndrome: Features and Mechanisms. Stroke. 2016 Jun 7. pii: STROKEAHA.116.013136. [Epub ahead of print] PubMed PMID: 27272485.
6)

Miki K, Takemoto K, Morishita T, Kouzaki Y, Irie Y, Iwaasa M, Abe H, Inoue T. [Reversible Cerebral Vasoconstriction Syndrome Without Typical Thunderclap Headache Complicated by Intracranial Hemorrhage and Posterior Reversible Encephalopathy Syndrome:A Case Report]. No Shinkei Geka. 2018 Dec;46(12):1111-1115. doi: 10.11477/mf.1436203877. Japanese. PubMed PMID: 30572309.
7)

Al-Mufti F, Dodson V, Wajswol E, El-Ghanem M, Alchaki A, Nuoman R, Thabet A, Sutherland A, Roychowdhury S, Hidalgo A, Gupta G. Chemical angioplasty for medically refractory reversible cerebral vasoconstriction syndrome(). Br J Neurosurg. 2018 Sep 12:1-5. doi: 10.1080/02688697.2018.1479512. [Epub ahead of print] PubMed PMID: 30207193.
9)

Koh M, Tsuboi Y, Fukuda O. [A Case of Juvenile Cerebral Infarction due to Reversible Cerebral Vasoconstriction Syndrome]. No Shinkei Geka. 2016 Nov;44(11):965-969. Japanese. PubMed PMID: 27832620.
10)

Ishi Y, Sugiyama T, Echizenya S, Yokoyama Y, Asaoka K, Itamoto K. [Reversible cerebral vasoconstriction syndrome associated with stroke: three case reports]. No Shinkei Geka. 2014 Feb;42(2):129-36. Japanese. PubMed PMID: 24501186.

Middle cerebral artery aneurysm case series

Middle cerebral artery aneurysm case series

A study of Gou et al. from the Beijing Neurosurgical Institute, included 285 cases of middle cerebral artery aneurysm surgery with MEP monitoring. The effects of MEP changes on postoperative motor function were assessed, and the key time point for minimizing the incidence of postoperative motor dysfunction was found through receiver operating characteristic (ROC) curve analysis. Motor dysfunction was significantly associated with the occurrence of MEP changes, and patients with irreversible changes were more likely to suffer motor dysfunction than were those with reversible changes. The critical duration of MEP changes that minimized the risk of postoperative motor dysfunction was 8.5 min. This study revealed that MEP monitoring is an effective method for preventing ischemic brain injury during surgical treatment of MCA aneurysm and proposes a critical cutoff for the duration of MEP deterioration of 8.5 min for predicting postoperative motor dysfunction 1).

2018

Esposito et al. from the Department of Neurosurgery, Clinical Neuroscience Center Zurich, report on a consecutive case-series of 50 patients who received clipping of 54 ruptured/unruptured middle cerebral artery aneurysm (MCA-aneurysms) by means of lateral supraorbital approach (LS) or minipterional craniotomy. The distance between MCA (M1)-origin and the aneurysmal neck is key to select the approach: LS was used for MCA-aneurysm located <15mm of the M1-origin and MP for MCA-aneurysms located ≥15mm of the M1-origin.

11 out of 50 patients presented with subarachnoid hemorrhage (10 ruptured MCA aneurysms). Overall, 59 aneurysms were successfully clipped (54 of the MCA). The mean distance between the M1-origin and the aneurysmal neck was 10.1-mm (range: 4-17mm) for patients treated by LS and 20-mm (range: 15-30mm) for MP. All but one MCA aneurysms were successfully treated. At last follow-up (mean 14 months), no reperfusion of the clipped aneurysms was observed.

The strategy for selecting the keyhole approach based on the depth of the aneurysm within the Sylvian fissure is efficient and safe. They suggest the use of LS approach when the aneurysm is located <15mm from the M1-origin and MP approach when the aneurysm is located ≥15mm from the M1-origin 2).

2015

Eighteen intracranial aneurysms, including 13 unruptured and 5 ruptured aneurysms, were treated with LVIS Jr stent-assisted coil embolization.

A total of 18 stents were successfully delivered to the target aneurysms, and the technical success rate was 100%. There was complete occlusion in 8 (44.4%) of 18 cases, neck remnants in 7 (38.9%) cases, and partial occlusion in 3 (16.7%) cases. In-stent thrombosis occurred in 1 case, and the symptoms disappeared after transvenous tirofiban injection. The modified Rankin Scale score at discharge was 0 in 14 patients, 1 in 3 patients, and 2 in 1 patient.

The LVIS Jr stent provided excellent trackability and deliverability and is safe and effective for the treatment of wide-necked MCA aneurysms with tortuous and smaller parent vessels 3).

2014

Clinical and radiological data of 103 patients interdisciplinary treated for unruptured MCA aneurysms over a 5-year period were analyzed in endovascular (n = 16) and microsurgical (n = 87) cohorts. Overall morbidity (Glasgow Outcome Score <5) after 12-month follow-up was 9 %. There was no significant difference between the two cohorts. Complete or “near complete” aneurysm occlusion was achieved in 97 and 75 % in the microsurgical, respective endovascular cohort. A “complex” aneurysm configuration had a significant impact on complete aneurysm occlusion in both cohorts, however, not on clinical outcome. Treatment of unruptured MCA aneurysms can be performed with a low risk of repair using both approaches. However, the risk for incomplete occlusion was higher for the endovascular approach in this series 4).

2013

Five hundred forty-three patients with 631 MCA aneurysms were managed with a “clip first” policy, with 115 patients (21.2%) referred from the Neurointerventional Radiology service and none referred from the Neurosurgical service for endovascular management.

Two hundred eighty-two patients (51.9%) had ruptured aneurysms and 261 (48.1%) had unruptured aneurysms. MCA aneurysms were treated with clipping (88.6%), thrombectomy/clip reconstruction (6.2%), and bypass/aneurysm occlusion (3.3%). Complete aneurysm obliteration was achieved with 620 MCA aneurysms (98.3%); 89.7% of patients were improved or unchanged after therapy, with a mortality rate of 5.3% and a permanent morbidity rate of 4.6%. Good outcomes were observed in 92.0% of patients with unruptured and 70.2% with ruptured aneurysms. Worse outcomes were associated with rupture (P = .04), poor grade (P = .001), giant size (P = .03), and hemicraniectomy (P < .001).

At present, surgery should remain the treatment of choice for MCA aneurysms. Surgical morbidity was low, and poor outcomes were due to an inclusive policy that aggressively managed poor-grade patients and complex aneurysms. This experience sets a benchmark that endovascular results should match before considering endovascular therapy an alternative for MCA aneurysms 5).

1995

Ogilvy et al., reviewed 65 middle cerebral aneurysms in 62 patients operated on over a 5-year interval where a choice of operative approach was made based on preoperative evaluation of available radiological studies.

The superior temporal gyrus was used when intraparenchymal hematoma was present in the temporal lobe or when the length of the middle cerebral artery trunk was long (average length 2.44 +/- 0.41 SE cm). This approach was used in 20 operations on 22 aneurysms. The sylvian fissure approach was used in cases where the middle cerebral artery main trunk was short (1.32 +/- 0.41 SE cm) or the direction of the aneurysm was favorable. This approach was used in 38 operations. In 4 operations (5 aneurysms) we combined the two approaches to remove clot, obtain adequate exposure, and secure control of the proximal MCA.

In most cases of MCA aneurysms the decision as to which surgical approach to use is made preoperatively depending on the presence of intraparenchymal clot, size of aneurysm, direction of aneurysm, and length of the proximal middle cerebral artery 6).

References

1)

Guo D, Fan X, You H, Tao X, Qi L, Ling M, Li Z, Liu J, Qiao H. Prediction of postoperative motor deficits using intraoperative motor-evoked potentials in middle cerebral artery aneurysm. Neurosurg Rev. 2020 Jan 22. doi: 10.1007/s10143-020-01235-0. [Epub ahead of print] PubMed PMID: 31965363.
2)

Esposito G, Dias SF, Burkhardt JK, Fierstra J, Serra C, Bozinov O, Regli L. Selection strategy for optimal keyhole approaches for MCA aneurysms: lateral supraorbital versus minipterional craniotomy. World Neurosurg. 2018 Oct 13. pii: S1878-8750(18)32344-1. doi: 10.1016/j.wneu.2018.09.238. [Epub ahead of print] PubMed PMID: 30326308.
3)

Feng Z, Li Q, Zhao R, Zhang P, Chen L, Xu Y, Hong B, Zhao W, Liu J, Huang Q. Endovascular Treatment of Middle Cerebral Artery Aneurysm with the LVIS Junior Stent. J Stroke Cerebrovasc Dis. 2015 Jun;24(6):1357-62. doi: 10.1016/j.jstrokecerebrovasdis.2015.02.016. Epub 2015 Apr 4. PubMed PMID: 25851343.
4)

Dammann P, Schoemberg T, Müller O, Özkan N, Schlamann M, Wanke I, Sandalcioglu IE, Forsting M, Sure U. Outcome for unruptured middle cerebral artery aneurysm treatment: surgical and endovascular approach in a single center. Neurosurg Rev. 2014 Oct;37(4):643-51. doi: 10.1007/s10143-014-0563-5. Epub 2014 Jul 9. PubMed PMID: 25005630.
5)

Rodríguez-Hernández A, Sughrue ME, Akhavan S, Habdank-Kolaczkowski J, Lawton MT. Current management of middle cerebral artery aneurysms: surgical results with a “clip first” policy. Neurosurgery. 2013 Mar;72(3):415-27. doi: 10.1227/NEU.0b013e3182804aa2. PubMed PMID: 23208060.
6)

Ogilvy CS, Crowell RM, Heros RC. Surgical management of middle cerebral artery aneurysms: experience with transsylvian and superior temporal gyrus approaches. Surg Neurol. 1995 Jan;43(1):15-22; discussion 22-4. PubMed PMID: 7701417.

Middle cerebral artery

Middle cerebral artery

The middle cerebral artery (MCA) is the largest and most complex of the three major cerebral arteries 1).

Most of the authors who have carried out anatomical studies of the middle cerebral artery agree on this being one of the least variable arteries. Nevertheless, they describe early bifurcationtrifurcationquadrifurcationduplication, single non-bifurcating trunk, hypoplasiafenestrations, etc. Considered to be having one of the most extensive irrigation territories in the brain. The artery arises below the anterior perforated substance, lateral to the optic chiasm. It runs along the sylvian fissure up to the limen insulae, where it bends at an angle which can be upto 90° and it is at that point where the bifurcation usually occurs.

The MCA arises from the internal carotid artery and continues into the lateral sulcus where it then branches and projects to many parts of the lateral cerebral cortex. It also supplies blood to the anterior temporal lobes and the insula. The artery supplies a portion of the frontal lobe and the lateral surface of the temporal and parietal lobes, including the primary motor and sensory areas of the face, throat, hand and arm, and in the dominant hemisphere, the areas for speech.

The left and right MCAs rise from trifurcations of the internal carotid arteries and thus are connected to the anterior cerebral artery and the posterior communicating artery, which connect to the posterior cerebral artery. The MCAs are not considered a part of the Circle of Willis.

The angular artery is a significant terminal branch of the anterior or middle trunk of the middle cerebral artery (MCA).

Variations

Duplicated middle cerebral artery.

Accessory Middle cerebral artery 2).

Teal et al. 3) further classified two types of accessory MCAs based on the origin of variant vessels, which can be proximal (type 1) or distal (type 2) segments of the ACA 4).

Classification

MCA was studied by Gunnal et al., in detail and classified it in four different types as bifurcated, trifurcated, quadrifurcated MCA and MCA with no trunks or single main trunk as per the termination 5).

Kahilogullari et al. proposed a way of classification made in relation to the terminology of the intermediate trunk, which is still a subject of debate. The intermediate trunk was present in 61% of cadavers and originated from a superior trunk in 55% and from an inferior trunk in 45%. Cortical branches supplying the motor cortex (precentral, central, and postcentral arteries) significantly originated from the intermediate trunk, and the diameter of the intermediate trunk significantly increased when it originated from the superior trunk. In measurements of the angles between the superior and intermediate trunks, it was found that the intermediate trunk had significant dominance in supplying the motor cortex as the angle increased. The intermediate trunk was classified into 3 types based on the angle values and the distance to the bifurcation point as Group A (pseudotrifurcation type), Group B (proximal type), and Group C (distal type). Group A trunks were seemingly closer to the trifurcation structure that has been reported on in the literature and was seen in 15%. Group B trunks were the most common type (55%), and Group C trunks were characterized as the farthest from the bifurcation point. Group C trunks also had the smallest diameter and fewest cortical branches. Similarities were found between the angles in cadaver specimens and on 3D CT cerebral angiography images. Beyond the separation point of the MCA, trunk structures always included the superior trunk and inferior trunk, and sometimes the intermediate trunk.

Interrelations of these vascular structures and their influences on the cortical branches originating from them are clinically important. The information presented in this study will ensure reliable diagnostic approaches and safer surgical interventions, particularly with MCA selective angiography 6).

Areas

The MCA territory was divided into 12 areas: orbitofrontal, prefrontal, precentral, central, anterior parietal, posterior parietal, angular, temporo-occipital, posterior temporal, middle temporal, anterior temporal, and temporopolar. The smallest cortical arteries arose at the anterior end and the largest one at the posterior end of the Sylvian fissure. The largest cortical arteries supplied the temporo-occipital and angular areas 7).

Perforators

Three distinct patterns of perforators arising from the proximal middle cerebral artery were found 8).


Marinković et al., divided it into medial, middle, and lateral groups. Those in the medial group usually arose directly from the MCA main trunk close to the carotid bifurcation. There were usually three vessels in the middle group, which originated not only from the MCA trunk, but also from the MCA collateral (cortical) branches. Common stems, when present, gave rise to individual perforating vessels and occasionally to thin olfactory and insular rami. Perforating arteries in the lateral group varied from one to nine in number. In addition to an origin from the MCA trunk, they also arose from cortical branches supplying the frontal and temporal lobes. The fact that lateral perforating vessels often originated from division sites and from terminal branches of the MCA is of clinical significance, because aneurysms are more commonly located at the MCA bifurcation. Anastomoses were not found among the perforating arteries. In two specimens, a fusion between a perforating artery and the MCA trunk was noted. Since the perforating vessels are obviously end arteries, injury to them must be avoided during operations for MCA aneurysms 9).

Segments

Branches

Pathology

References

1)

Rhoton AL., Jr The supratentorial arteries. Neurosurgery. 2002;51(Suppl 4):53–120.
2)

Uchino A, Kato A, Takase Y, Kudo S. Middle cerebral artery variations detected by magnetic resonance angiography. Eur Radiol. 2000;10(4):560-3. PubMed PMID: 10795531.
3)

Teal JS, Rumbaugh CL, Bergeron RT, Segall HD. Anomalies of the middle cerebral artery: accessory artery, duplication, and early bifurcation. Am J Roentgenol Radium Ther Nucl Med. 1973 Jul;118(3):567-75. PubMed PMID: 4723180.
4) , 7)

Gibo H, Carver CC, Rhoton AL Jr, Lenkey C, Mitchell RJ. Microsurgical anatomy of the middle cerebral artery. J Neurosurg. 1981 Feb;54(2):151-69. PubMed PMID: 7452329.
5)

Gunnal SA, Farooqui MS, Wabale RN. Study of Middle Cerebral Artery in Human Cadaveric Brain. Ann Indian Acad Neurol. 2019 Apr-Jun;22(2):187-194. doi: 10.4103/0972-2327.144289. PubMed PMID: 31007431; PubMed Central PMCID: PMC6472224.
6)

Kahilogullari G, Ugur HC, Comert A, Tekdemir I, Kanpolat Y. The branching pattern of the middle cerebral artery: is the intermediate trunk real or not? An anatomical study correlating with simple angiography. J Neurosurg. 2012 May;116(5):1024-34. doi: 10.3171/2012.1.JNS111013. Epub 2012 Feb 24. PubMed PMID: 22360571.
8)

Grand W. Microsurgical anatomy of the proximal middle cerebral artery and the internal carotid artery bifurcation. Neurosurgery. 1980 Sep;7(3):215-8. PubMed PMID: 7207737.
9)

Marinković SV, Kovacević MS, Marinković JM. Perforating branches of the middle cerebral artery. Microsurgical anatomy of their extracerebral segments. J Neurosurg. 1985 Aug;63(2):266-71. PubMed PMID: 4020447.
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