Microneurosurgical treatment of a small perimesencephalic pure pial arterial malformation: an under-recognized etiology of angiographically occult subarachnoid hemorrhage. Illustrative case

Robert C. Sterner Department of Neurological Surgery, University of Wisconsin-Madison, Madison, Wisconsin; and

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Garret P. Greeneway Department of Neurological Surgery, University of Wisconsin-Madison, Madison, Wisconsin; and

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Ufuk Erginoglu Department of Neurological Surgery, University of Wisconsin-Madison, Madison, Wisconsin; and

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Jaime L. Martínez Santos Department of Neurological Surgery, University of Wisconsin-Madison, Madison, Wisconsin; and
Department of Neurological Surgery, Medical University of South Carolina, Charleston, South Carolina

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Mustafa K. Baskaya Department of Neurological Surgery, University of Wisconsin-Madison, Madison, Wisconsin; and

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BACKGROUND

Pial arterial malformations (PAMs) are rare vascular lesions consisting of dilated tortuous arteries without venous drainage. Current PAM understanding is limited by the lesion’s rarity, limited anatomopathological studies, and frequent misclassifications.

OBSERVATIONS

A 23-year-old male experienced two spontaneous subarachnoid hemorrhages (SAHs) over 6 months with initially unremarkable diagnostic cerebral angiograms. Magnetic resonance imaging (MRI) and angiography after the second SAH revealed a small perimesencephalic ovoid lesion within the left crural cistern, between the left superior and posterior cerebral arteries, appearing to be an exophytic cavernoma, a thrombosed aneurysm, or a hemorrhagic tumor. Microsurgical resection was achieved with a pterional craniotomy and anterior clinoidectomy. The resected lesion was characteristic of a pure PAM arising from superior cerebellar arterial branches.

LESSONS

Small pure PAMs can be deceitfully dynamic lesions causing episodes of hemorrhage, complete thrombosis (angiographically occult), recanalization, and rehemorrhage. Small thrombosed vascular malformations or aneurysms should be included in differential diagnoses of angiographically occult SAH. MRI can be diagnostic, but the true angioarchitecture can only be elucidated with microneurosurgery. The only definitive cure is removal. The microneurosurgical strategy should account for worst-case scenarios, provide adequate skull base exposures, and include bypass revascularization options when thrombosed aneurysms are encountered.

ABBREVIATIONS

ACA = anterior cerebral artery; AVM = arteriovenous malformation; CN = cranial nerve; CT = computed tomography; ICA = internal carotid artery; ICG = indocyanine green; MRA = magnetic resonance angiography; MRI = magnetic resonance imaging; PAM = pial arterial malformation; PCA = posterior cerebellar artery; PCoA = posterior communicating artery; SAH = subarachnoid hemorrhage; SCA = superior cerebellar artery

BACKGROUND

Pial arterial malformations (PAMs) are rare vascular lesions consisting of dilated tortuous arteries without venous drainage. Current PAM understanding is limited by the lesion’s rarity, limited anatomopathological studies, and frequent misclassifications.

OBSERVATIONS

A 23-year-old male experienced two spontaneous subarachnoid hemorrhages (SAHs) over 6 months with initially unremarkable diagnostic cerebral angiograms. Magnetic resonance imaging (MRI) and angiography after the second SAH revealed a small perimesencephalic ovoid lesion within the left crural cistern, between the left superior and posterior cerebral arteries, appearing to be an exophytic cavernoma, a thrombosed aneurysm, or a hemorrhagic tumor. Microsurgical resection was achieved with a pterional craniotomy and anterior clinoidectomy. The resected lesion was characteristic of a pure PAM arising from superior cerebellar arterial branches.

LESSONS

Small pure PAMs can be deceitfully dynamic lesions causing episodes of hemorrhage, complete thrombosis (angiographically occult), recanalization, and rehemorrhage. Small thrombosed vascular malformations or aneurysms should be included in differential diagnoses of angiographically occult SAH. MRI can be diagnostic, but the true angioarchitecture can only be elucidated with microneurosurgery. The only definitive cure is removal. The microneurosurgical strategy should account for worst-case scenarios, provide adequate skull base exposures, and include bypass revascularization options when thrombosed aneurysms are encountered.

ABBREVIATIONS

ACA = anterior cerebral artery; AVM = arteriovenous malformation; CN = cranial nerve; CT = computed tomography; ICA = internal carotid artery; ICG = indocyanine green; MRA = magnetic resonance angiography; MRI = magnetic resonance imaging; PAM = pial arterial malformation; PCA = posterior cerebellar artery; PCoA = posterior communicating artery; SAH = subarachnoid hemorrhage; SCA = superior cerebellar artery

McLaughlin et al.1,2 first defined pure pial arterial malformations (PAMs) as abnormally dilated, tortuous, and overlapping arteries that appear coil-like or form a mass of arterial loops with no venous component. PAMs are rare vascular malformations that are often misdiagnosed as entities that include arteriovenous malformations, aneurysms, or developmental anomalies.1–4 The absence of an associated venous component is critical to distinguish PAMs from arteriovenous malformations (AVMs).1,2,5 Given the low incidence and small number of reported cases of PAMs, their natural history is poorly understood. Prior reports have suggested that PAMs may have a benign natural history and be amenable to conservative therapy. Rarely have these lesions been reported to be associated with a subarachnoid hemorrhage (SAH) that requires surgical intervention.1,2,4–6 Here we present, to the best our knowledge, the first case of a perimesencephalic pure PAM of the superior cerebellar artery (SCA) that was associated with two SAHs that were initially occult on diagnostic cerebral angiography secondary to thrombosis and were ultimately identified via brain magnetic resonance imaging (MRI) and magnetic resonance angiography (MRA). Microsurgical exploration with indocyanine green (ICG) video angiography revealed a slow, delayed partial filling that suggested that recanalization ensued at some point between the last angiogram and surgery. This finding explains why the malformation was angiographically occult when thrombosed and why it rehemorrhaged when recanalized.

Illustrative Case

History and Examination

A 22-year-old male with an unremarkable medical history presented to an outside institution twice within a 6-month period for a severe sudden-onset headache associated with photophobia, meningeal irritation, nausea, vomiting, and right-sided paresthesias. The patient’s neurological examination was normal. Computed tomography (CT) of the head performed at each presentation was notable for diffuse SAH (Fisher grade III, Hunt and Hess grade I) involving the basal cisterns. Both computed tomography angiography of the head and neck and diagnostic cerebral angiography (Fig. 1) were performed at each presentation and were unremarkable for aneurysm or vascular malformations to explain the patient’s SAH.

FIG. 1.
FIG. 1.

Preoperative diagnostic cerebral angiograms, arterial phase anterior-posterior projection (A) and venous phase anterior-posterior projection (B), demonstrating no vascular etiology of the patient’s SAH.

Importantly, head MRI and MRA were not performed during the first SAH presentation (at an outside institution) but were performed during the subsequent presentation to our hospital. MRI and MRA demonstrated a small ovoid-appearing mass within the left crural cistern interposed between the P1 segment of the left posterior cerebral artery and the left superior cerebellar artery (Fig. 2). Given the lesion’s appearance on magnetic resonance sequencing and intimate association with the adjacent arteries, the differential diagnosis included an exophytic cavernoma, a thrombosed aneurysm, a hemorrhagic tumor, or an alternate vascular malformation. Given that this was deemed the likely culprit of the patient’s SAH, the patient was offered surgical exploration and treatment.

FIG. 2.
FIG. 2.

Preoperative axial contrasted T1-weighted MRI (A), axial T2-weighted MRI (B), and coronal contrasted T1-weighted MRI (C) demonstrating an avidly contrast-enhancing small ovoid lesion in the left ambient cistern at the level of the superior cerebellar artery.

Microsurgical Approach

A left pterional craniotomy was performed with an extradural anterior clinoidectomy to develop an inferior corridor toward the interpeduncular and crural cisterns, should we need a much wider exposure and a possible transcavernous approach (Fig. 3 and Video 1). In addition, we planned for dividing the internal carotid artery (ICA) dural rings and for a transcavernous approach with mobilization of cranial nerve (CN) III and CN IV in the event that vessel reconstruction and bypass would be necessary in the case of a thrombosed aneurysm. Always planning for the worst-case scenario and having complex skull base approaches in a neurosurgeon’s armamentarium are vital to achieving the best possible outcomes in cases such as this, where the pathology itself and its true angioarchitecture can only be fully elucidated intraoperatively. The oculomotor nerve was then completely skeletonized and the distal basilar tip, superior cerebellar artery, and posterior cerebral artery (Figs. 3A and 3H) including the P1 and P2 segments were identified.

VIDEO 1. Clip showing an operative video demonstrating a pterional craniotomy with extradural clinoidectomy for the microneurosurgical resection of a small pure PAM. Click here to view.

FIG. 3.
FIG. 3.

Intraoperative photograph after a left pterional craniotomy with extradural anterior clinoidectomy and development of a microsurgical corridor through the left carotid-oculomotor triangle toward the interpeduncular and left crural subarachnoid cisterns (A). A vascular malformation is exposed lateral to the left oculomotor nerve or CN III and cranial to the superior cerebellar artery. This malformation was inspected circumferentially and dissected off the pia. Microdissection revealed that its angioarchitecture consisted of three arterial feeders (arrows) reaching the malformation’s posterolateral pole with no venous drainage, therefore classifying it as a pure pial AVM. The inset (B) is an ICG video angiogram showing the fluorescence of these arterial feeders, but only partial fluorescence of the pial AVM, which suggests it was partially thrombosed. Intraoperative photographs showing the sequential disconnection of the pial arteriovenous malformation. First, the smallest arterial feeder located more anteriorly was bipolar coagulated (C) and divided. Next, the most posterior small arterial feeder was bipolar coagulated (D) and cut (E). The largest arterial feeder was skeletonized (F) and occluded with a 4-mm AVM clip (G). Finally, the larger arterial feeder was cut distal to the clip, and the pial AVM was removed. A final view of the surgical corridor shows the distal basilar artery, the ipsilateral superior cerebellar artery, the precommunicating posterior cerebral artery, and the left oculomotor nerve (CN III) (H).

A pure PAM was identified lateral to the oculomotor nerve along the ventral surface of the midbrain between the SCA and posterior cerebral artery (PCA) (Fig. 3). After a thorough circumferential microsurgical dissection, we could not identify a nidus or a draining vein. Three total feeding arteries reached the PAM on its posterolateral surface, and the main arterial trunk was in the middle (Fig. 3B). ICG video angiography revealed that the lesion was very slowly filling in a delayed fashion, and there was no obvious venous drainage (Fig. 3B). The smaller lateral arterial feeder and medial arterial feeder were bipolar coagulated and divided (Fig. 3C–H). A 4-mm AVM clip was used to occlude the larger main arterial trunk. Somatosensory evoked potentials and motor evoked potentials were monitored for 15 minutes after clipping, with no changes observed. We therefore proceeded to bipolar coagulate and divide this main trunk and remove the entire lesion in one piece. The lesion was sent as a permanent specimen for review by our pathology colleagues. The final histopathology demonstrated a thrombosed vessel fed by multiple smaller feeding vessels. The thrombosed vessel contained a discontinuity of its internal elastic lamina layer, and the smaller feeding vessels had an intact internal elastic lamina layer, thereby consistent with the final interpretation of this lesion as a pure PAM.

Postoperative Course

Postoperatively, the patient’s neurological examination was intact, and MRI revealed no residual PAM (Fig. 4). The patient was discharged on postoperative day 2. He continued to do well 3 months postoperatively.

FIG. 4.
FIG. 4.

Postoperative contrasted T1 axial MRI (A), T2 axial MRI (B), and contrasted T1 coronal MRI (C) demonstrating gross total resection of the preoperative avidly contrast enhancing small ovoid lesion in the left ambient cistern at the level of the superior cerebellar artery.

Patient Informed Consent

The necessary patient informed consent was obtained in this study.

Discussion

Observations

There is a paucity of PAM reports in the literature. The limited number of reported cases is at least partially attributable to the fact that PAMs are likely frequently misdiagnosed as an aneurysm or some other vascular malformation.1–3 In addition, PAMs may also be angiographically occult, and the true anatomy and angioarchitecture can only be defined through microsurgical exploration, which leads to a further decrease in the reported incidence of PAMs. Proper workup and diagnosis of PAMs is important, as these lesions can be a culprit of potentially life-threatening SAHs that likely may only be amenable to microsurgical interventions and not endovascular intervention.

Historically, digital subtraction angiography has been essential in the diagnostic evaluation of these vascular anomalies. Angiography provides high-resolution visualization and assessment of whether or not there is a venous component associated with the lesion, which is key for distinguishing between PAMs and AVMs.1–3 However, an angiography would not show any abnormality in the setting of a transiently thrombosed arterial malformation. The case we present here emphasizes the importance of understanding this phenomenon and for considering this less common entity of PAMs in the differential diagnosis of patients with angiographically occult SAHs.

To the best of our knowledge, there is only one prior reported case of a PAM diagnosed via MRA, in which Sako et al.7 reported a posterior inferior cerebellar artery with a pure arterial malformation. The present case, as reported here, is unique because it was a pure PAM arising from the left superior cerebellar artery, was a thrombosed malformation that was initially angiographically occult, and was only later identified on MRI and MRA upon rehemorrhage. The PAM proved to be dynamic because it thrombosed after the first hemorrhage, turning angiographically occult. Then it recanalized, rehemorrhaged, and rethrombosed, whereupon it turned angiographically occult again. Finally, when we explored microsurgically, it had partially recanalized.

Although we agree that cerebral angiography has the theoretical potential to provide a detailed evaluation, cerebral angiography is not always sufficient to distinguish between PAMs and other malformations or aneurysms. In contrast, MRI and MRA of the brain and upper cervical spine are less invasive diagnostic modalities that may be useful in working up angiographically occult SAHs, since they would detect small abnormal dilated and thrombosed vessels or vascular malformations. Furthermore, it may be beneficial to include a thin-cut constructive interference in steady-state MRI sequence of the cisternal compartment in question.

A literature review was conducted in the PubMed, Embase, and Google Scholar databases from their dates of inception to February 2023 using combinations of the following keywords: “vascular malformations” OR “central nervous system vascular malformations” OR “intracranial arterial diseases” AND “pure arterial malformation” OR “pure pial arterial malformation.” In a review of the English-language literature, a total of 50 cases (Table 1), including the present case, appear to meet the criteria for PAM as previously described by McLaughlin et al.1–33 These cases illustrate that PAMs can occur in all segments of the intracranial arterial tree, although a majority of reported cases seem to arise from the distal anterior cerebral arteries (ACAs) and the supraclinoid segment of the ICA, posterior communicating artery (PCoA), or PCA.1–3 To the best of our knowledge, the present case is the third reported case of an SCA PAM and the first SCA PAM to be associated with an SAH. Interestingly, there have been only five reports of PAMs identified in association with an SAH.4,5,17,31,33 The present case report is the first, to our knowledge, to report a PAM as the culprit of multiple SAHs. Of the 50 patients with anomalies that appear to fit the definition1,2 of PAM, there is a clear female predominance (32/50; 64%), which is consistent with other reports.3,6 PAMs also appear to occur primarily in young patients, with a mean and median age of 29.8 and 27, respectively, from the 50 reported cases.3,6 Other studies have suggested that a large majority of cases, up to 85%, are discovered incidentally.1–3

TABLE 1.

Summary of reported PAM cases

SexAge (yrs)Presenting Signs/SymptomsCT FindingsLesion LocationAssociated AneurysmTreatmentAuthors & Year
M49 Intermittent frontal HANoneBilat pericallosalNoneConservative therapyBeringer & Alenghat, 20048
M21 Seizures, agenesis of corpus callosumNoneBilat pericallosalNoneConservative therapyWolpert et al., 19729
M2Viral encephalitisNoneBilat A2sNoneConservative therapySacks & Lindenburg, 196910
M39 SeizuresNoneDistal lt ACANoneConservative therapyThompson et al., 197611
M1Infarct from moyamoyaNoneLt PCoA & PCANoneConservative therapyLanterna et al., 201412
M5Minimal rt hemiparesisBrainstem compressionLt ICA, PCoA, PCA, MCA, & lt SCANoneConservative therapyVanslambrouk et al., 200013
M42 HA w/ basal ganglia hemorrhageHemorrhage due to PAM (rt basal ganglia)Rt MCAYesConservative therapyFeliciano et al., 201414
M35 VertigoNoneLt PICANoneConservative therapySako et al.., 20167
M32 Cortical dysplasia, seizuresNoneSylvian branches, lt MCANoneConservative therapyAbe et al.., 199715
M11 IncidentalNoneLt PCoANoneConservative therapyBrinjikji et al.., 20183
M17 HANoneRt SCANoneConservative therapyBrinjikji et al.., 20183
M45 HA dizziness, gait instability, bilat papilledemaNoneP1 PCAYesSurgeryYue et al., 201916
M77 Sudden-onset HA, nausea, confusionSAHLt VAYesSurgery-trappingLi et al., 20205
M38 Progressive HA, nauseaSAHRt PICANoOnyx emboChua et al.., 202117
M51 Severe HASAHLt PICAYesSurgeryYao et al.., 20214
M49 Severe HASAHLt VAYesSurgeryYao et al., 20214
M15 Narrowing of visual fieldNoneRt PCoA, PCANoneSurgery-clipping PAMIwaki et al.., 202118
M23 2 episodes severe-onset HA, photophobia, neck pain, nausea, vomiting, rt-sided numbnessSAHSCAYesMicrosurgical clipping & removalSterner et al., (present case)
F37 ManiaNoneBilat pericallosalNoneConservative therapyTsukamoto et al.,198519
F14 Partial complex seizuresNoneBilat pre- & supracallosal segments of ACAsNoneConservative therapyDoran et al., 199520
F72 Aphasia, rt hemiplegiaNoneBilat distal ACAsNoneConservative therapyKryst-Widźgowska et al., 198021
F24 HA, dizzinessNoneLt PCoA & P2YesConservative therapyMcLaughlin et al., 20131
F4PHACE syndrome, rt hemiparesisInfarct due to PAMLt supraclinoid ICA & PCoANoneConservative therapyBaccin et al., 200722
F1PHACE syndrome, fever, & hypotensionNoneLt supraclinoid ICA, PCoA, P1; rt supraclinoid ICANoneConservative therapyBaccin et al., 200722
F8Sinus infectionNoneLt supraclinoid ICA & proximal M1NoneConservative therapyMcLaughlin et al., 20142
F1PHACE syndromeNoneLt MCA & supraclinoid ICANoneConservative therapyMetry et al., 200123
F17 Nausea & vomitingNoneLt supraclinoid ICA, M1, & ACANoneConservative therapyYamada et al., 198524
F40 Rt hemiparesisNoneRight supraclinoid ICA, M1, & ACANoneConservative therapyYamada et al., 198524
F41 Seizures, ipsilat cavernomaNoneLt MCANoneConservative therapyKanemototo et al., 199825
F25 Rt hemimegalencephalyNoneRt MCA, ACA, & PCANoneConservative therapyAraki et al., 198726
F43 DysarthriaNoneRt distal ICA & proximal M1 lt PCANoneEC-IC bypass, wrapped ectatic MCA w/ muscleHanakita et al., 198627
F35 Severe HANoneRt SCANoneConservative therapyUchino et al., 200328
F26 IncidentalNoneDistal rt PCANoneConservative therapyShankar et al., 200929
F25 HANoneLt supraclinoid ICA & M1YesConservative therapyBrinjikji et al., 20183
F25 HA after minor traumaNoneLt ACANoneConservative therapyBrinjikji et al., 20183
F34 HA, light traumaNoneLt ACANoneConservative therapyBrinjikji et al., 20183
F38 Transient hand numbnessNoneLt PICANoneConservative therapyBrinjikji et al., 20183
F47 Prior thunderclap HANoneRt ACANoneConservative therapyBrinjikji et al., 20183
F35 HANoneLt PCoA/PCAYesConservative therapyBrinjikji et al., 20183
F20 HA, traumaNoneRt ICA, P2, & lt P2NoneConservative therapyBrinjikji et al., 20183
F10 Severe lt-sided HANoneLt supraclinoid ICA, PCoA, & PCAYesCoil emboBrinjikji et al., 20183
F19 IncidentalNoneLt MCAYesConservative therapyBrinjikji et al., 20183
F27 HA, lt hemibody numbness & facial droopNoneBANoneConservative therapyBrinjikji et al., 20183
F17 Migraine w/ auraNoneRt PICANoneConservative therapySorenson et al., 201830
F37 HA blurry vision, partial lt CN III palsyIntracranial hemorrhage (SAH)P1 PCAYesSurgery-clippingMunich et al., 201931
F24 Occasional dizzinessNoneSupraclinoid rt ICAYesStent + coilLiu et al.., 202032
F43 Intermittent syncopeNoneLt ICANoneBypassLu et al., 202133
F53 HASAHRt P1 PCANoneBypassLu et al., 202133
F65 Sudden & severe HANoneRt PICAYesSurgery-clippingWójtowicz et al., 20226

BA = basilar artery; embo = embolization; HA = headache; ICA = internal carotid artery; MCA = middle cerebral artery; PHACE = posterior fossa malformations, hemangiomas, arterial abnormalities, cardiac abnormalities, eye abnormalities, sternal cleft; PICA = posterior inferior cerebellar artery; SAH = subarachnoid hemorrhage; VA = vertebral artery.

To date, the etiology and pathophysiology of PAMs remain unclear. Several potential etiologies have been proposed in the literature: congenital defects, secondary to an insult causing arterial dysplasia, infectious etiologies, chronic healed dissection, and somatic mutations affecting vulnerable arterial segments.9,10,15,22,23,26,34–36 The PAM presented herein was a dilated arterial wall with three posterolateral feeding arteries and no draining vein. Histopathologic examination confirmed an arterial vascular malformation and revealed a thrombosed vessel with areas of recanalization and multiple small arterial feeders. This abnormal saccular structure with no outflow conduit promoted turbulent flow and blood stasis that resulted in partial thrombosis. This pathophysiological mechanism explains why PAMs can be angiographically occult. One report has suggested that PAMs are associated with aneurysms in nearly half of these patients.6 Our literature review revealed that 14 of 50 reported PAM cases had an associated aneurysm, and of these patients with an aneurysm-associated PAM, 5 of 14 developed SAH/intracranial hemorrhage. Including the present case, 5 of 7 PAMs resulting in SAH had associated aneurysms, whereas 2 of 7 PAMs spontaneously caused SAH. The fact that there is a growing number of cases of SAHs secondary to PAMs challenges the idea that PAMs are a benign entity, as has previously been suggested. The fact that PAMs have been reported to cause SAH and intracranial hemorrhages with potentially devasting effects contradicts the idea that PAMs are indeed benign. As a result, it is highly likely that the phenotypic manifestations and differences in natural history are the result of a collection of the previously proposed etiologies.

Historically, the management of PAM has focused on conservative therapy with follow-up imaging and risk factor reduction by treating hypertension and smoking.1–3 In a majority of patients, conservative management with routine imaging follow-up is likely appropriate.1–3 PAMs with associated SAH, however, have been managed successfully with microsurgical clipping (3 cases), microsurgical clipping and removal (1 case), surgical clip trapping (1 case), proximal occlusion and superior temporal artery to P2 bypass to the second segment of the posterior cerebral artery (1 case), and Onyx embolization (1 case). The case we present herein suggests that follow-up brain MRI and head MRA can be useful diagnostic modalities as part of the long-term follow-up of patients with SAH. For patients with PAM with local aneurysm(s) or an intracranial hemorrhage, we recommend microsurgical intervention depending on the lesion characteristics and location.

Lessons

Small pure PAMs, as in this case, can be deceitfully dynamic lesions with episodes of hemorrhage, complete thrombosis (angiographically occult), recanalization, and rehemorrhage. Small thrombosed vascular malformations should be included in the differential diagnosis of an angiographically occult SAH. In such cases, high-resolution MRI can be diagnostic. However, the true angioarchitecture of any vascular lesion can only be elucidated fully with an open microneurosurgical exploration, and the only definitive cure is microneurosurgery. The microneurosurgical approach and strategy should account for all possible worst-case scenarios, provide adequate skull base exposures, and should include a plan for bypass revascularization options should this become necessary.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: all authors. Acquisition of data: Sterner, Greeneway, Erginoglu, Martínez Santos. Analysis and interpretation of data: Sterner, Greeneway, Erginoglu, Martínez Santos. Drafting the article: Sterner, Greeneway, Erginoglu, Martínez Santos. Critically revising the article: all authors. Reviewed submitted version of manuscript: Baskaya, Sterner, Erginoglu, Martínez Santos. Approved the final version of the manuscript on behalf of all authors: Baskaya. Statistical analysis: Sterner. Administrative/technical/material support: Sterner, Erginoglu, Martínez Santos. Study supervision: Baskaya, Martínez Santos.

Supplemental Information

Videos

Video 1. https://vimeo.com/830224888.

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    • Search Google Scholar
    • Export Citation
  • 23

    Metry DW, Dowd CF, Barkovich AJ, Frieden IJ. The many faces of PHACE syndrome. J Pediatr. 2001;139(1):117123.

  • 24

    Yamada K, Hayakawa T, Ushio Y, Mitomo M. Cerebral arterial dolichoectasia associated with moyamoya vessels. Surg Neurol. 1985;23(1):1924.

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    Kanemoto Y, Hisanaga M, Bessho H. Association of a dolichoectatic middle cerebral artery and an intracranial cavernous hemangioma--case report. Neurol Med Chir (Tokyo). 1998;38(1):4042.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Araki Y, Mori S, Kanoh M, Maeda Y, Kawai R, Mitomo M. Congenital hemicerebral arterial ectasia complicating unilateral megalencephaly. Br J Radiol. 1987;60(712):395400.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Hanakita J, Miyake H, Nagayasu S, Nishi S, Suzuki T. Surgically treated cerebral arterial ectasia with so-called moyamoya vessels. Neurosurgery. 1986;19(2):271273.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Uchino A, Abe M, Sawada A, Takase Y, Kudo S. Extremely tortuous superior cerebellar artery. Eur Radiol. 2003;13(suppl 6):L237L238.

  • 29

    Shankar JJS, Banerjee ST, Hogan M, terBrugge K, Lasjaunias P, dos Santos MP. A rare case of cerebral cortical dysplasia with arterial vascular dysplasia. Can J Neurol Sci. 2009;36(6):757760.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Sorenson TJ, Brinjikji W, Flemming KD, Lanzino G. Pure arterial malformation of the posterior inferior cerebellar artery with interspersed adipose tissue: case report. J Neurosurg Pediatr. 2018;22(3):261264.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Munich SA, Brunet MC, Starke RM, Morcos JJ. Clipping of basilar perforator pure arterial malformation aneurysm: 2-dimensional operative video. Oper Neurosurg (Hagerstown). 2019;17(2):E67.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Liu TY, Xu N, Wan Z, et al. Diagnosis and treatment of pure arterial malformation: three case reports and literature review. Medicine (Baltimore). 2020;99(21):e20229.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Lu X, Fang X, Huang Y, et al. Cerebral revascularization for the management of symptomatic pure arterial malformations. Front Neurol. 2021;12:755312.

  • 34

    Kim ST, Brinjikji W, Kallmes DF. Prevalence of intracranial aneurysms in patients with connective tissue diseases: a retrospective study. AJNR Am J Neuroradiol. 2016;37(8):14221426.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Kim ST, Brinjikji W, Lanzino G, Kallmes DF. Neurovascular manifestations of connective-tissue diseases: A review. Interv Neuroradiol. 2016;22(6):624637.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Lasjaunias PL. Segmental identity and vulnerability in cerebral arteries. Interv Neuroradiol. 2000;6(2):113124.

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  • FIG. 1.

    Preoperative diagnostic cerebral angiograms, arterial phase anterior-posterior projection (A) and venous phase anterior-posterior projection (B), demonstrating no vascular etiology of the patient’s SAH.

  • FIG. 2.

    Preoperative axial contrasted T1-weighted MRI (A), axial T2-weighted MRI (B), and coronal contrasted T1-weighted MRI (C) demonstrating an avidly contrast-enhancing small ovoid lesion in the left ambient cistern at the level of the superior cerebellar artery.

  • FIG. 3.

    Intraoperative photograph after a left pterional craniotomy with extradural anterior clinoidectomy and development of a microsurgical corridor through the left carotid-oculomotor triangle toward the interpeduncular and left crural subarachnoid cisterns (A). A vascular malformation is exposed lateral to the left oculomotor nerve or CN III and cranial to the superior cerebellar artery. This malformation was inspected circumferentially and dissected off the pia. Microdissection revealed that its angioarchitecture consisted of three arterial feeders (arrows) reaching the malformation’s posterolateral pole with no venous drainage, therefore classifying it as a pure pial AVM. The inset (B) is an ICG video angiogram showing the fluorescence of these arterial feeders, but only partial fluorescence of the pial AVM, which suggests it was partially thrombosed. Intraoperative photographs showing the sequential disconnection of the pial arteriovenous malformation. First, the smallest arterial feeder located more anteriorly was bipolar coagulated (C) and divided. Next, the most posterior small arterial feeder was bipolar coagulated (D) and cut (E). The largest arterial feeder was skeletonized (F) and occluded with a 4-mm AVM clip (G). Finally, the larger arterial feeder was cut distal to the clip, and the pial AVM was removed. A final view of the surgical corridor shows the distal basilar artery, the ipsilateral superior cerebellar artery, the precommunicating posterior cerebral artery, and the left oculomotor nerve (CN III) (H).

  • FIG. 4.

    Postoperative contrasted T1 axial MRI (A), T2 axial MRI (B), and contrasted T1 coronal MRI (C) demonstrating gross total resection of the preoperative avidly contrast enhancing small ovoid lesion in the left ambient cistern at the level of the superior cerebellar artery.

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    Baccin CE, Krings T, Alvarez H, Ozanne A, Lasjaunias PL. A report of two cases with dolichosegmental intracranial arteries as a new feature of PHACES syndrome. Childs Nerv Syst. 2007;23(5):559567.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Metry DW, Dowd CF, Barkovich AJ, Frieden IJ. The many faces of PHACE syndrome. J Pediatr. 2001;139(1):117123.

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    Yamada K, Hayakawa T, Ushio Y, Mitomo M. Cerebral arterial dolichoectasia associated with moyamoya vessels. Surg Neurol. 1985;23(1):1924.

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    Kanemoto Y, Hisanaga M, Bessho H. Association of a dolichoectatic middle cerebral artery and an intracranial cavernous hemangioma--case report. Neurol Med Chir (Tokyo). 1998;38(1):4042.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Araki Y, Mori S, Kanoh M, Maeda Y, Kawai R, Mitomo M. Congenital hemicerebral arterial ectasia complicating unilateral megalencephaly. Br J Radiol. 1987;60(712):395400.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Hanakita J, Miyake H, Nagayasu S, Nishi S, Suzuki T. Surgically treated cerebral arterial ectasia with so-called moyamoya vessels. Neurosurgery. 1986;19(2):271273.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Uchino A, Abe M, Sawada A, Takase Y, Kudo S. Extremely tortuous superior cerebellar artery. Eur Radiol. 2003;13(suppl 6):L237L238.

  • 29

    Shankar JJS, Banerjee ST, Hogan M, terBrugge K, Lasjaunias P, dos Santos MP. A rare case of cerebral cortical dysplasia with arterial vascular dysplasia. Can J Neurol Sci. 2009;36(6):757760.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Sorenson TJ, Brinjikji W, Flemming KD, Lanzino G. Pure arterial malformation of the posterior inferior cerebellar artery with interspersed adipose tissue: case report. J Neurosurg Pediatr. 2018;22(3):261264.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Munich SA, Brunet MC, Starke RM, Morcos JJ. Clipping of basilar perforator pure arterial malformation aneurysm: 2-dimensional operative video. Oper Neurosurg (Hagerstown). 2019;17(2):E67.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Liu TY, Xu N, Wan Z, et al. Diagnosis and treatment of pure arterial malformation: three case reports and literature review. Medicine (Baltimore). 2020;99(21):e20229.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Lu X, Fang X, Huang Y, et al. Cerebral revascularization for the management of symptomatic pure arterial malformations. Front Neurol. 2021;12:755312.

  • 34

    Kim ST, Brinjikji W, Kallmes DF. Prevalence of intracranial aneurysms in patients with connective tissue diseases: a retrospective study. AJNR Am J Neuroradiol. 2016;37(8):14221426.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Kim ST, Brinjikji W, Lanzino G, Kallmes DF. Neurovascular manifestations of connective-tissue diseases: A review. Interv Neuroradiol. 2016;22(6):624637.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Lasjaunias PL. Segmental identity and vulnerability in cerebral arteries. Interv Neuroradiol. 2000;6(2):113124.

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