Vascular steal and associated intratumoral aneurysms in highly vascular brain tumors: illustrative case

Abstract

BACKGROUND

Intratumoral aneurysms in highly vascular brain tumors can complicate resection depending on their location and feasibility of proximal control. Seemingly unrelated neurological symptoms may be from vascular steal that can help alert the need for additional vascular imaging and augmenting surgical strategies.

OBSERVATIONS

A 29-year-old female presented with headaches and unilateral blurred vision, secondary to a large right frontal dural-based lesion with hypointense signal thought to represent calcifications. Given these latter findings and clinical suspicion for a vascular steal phenomenon to explain the blurred vision, computed tomography angiography was obtained, revealing a 4 × 2–mm intratumoral aneurysm. Diagnostic cerebral angiography confirmed this along with vascular steal by the tumor from the right ophthalmic artery. The patient underwent endovascular embolization of the intratumoral aneurysm, followed by open tumor resection in the same setting without complication, minimal blood loss, and improvement in her vision.

LESSONS

Understanding the blood supply of any tumor, but highly vascular ones in particular, and the relationship with normal vasculature is undeniably important in avoiding potentially dangerous situations and optimizing maximal safe resection. Recognition of highly vascular tumors should prompt thorough understanding of the vascular supply and relationship of intracranial vasculature with consideration of endovascular adjuncts when appropriate.

A thorough understanding of peritumoral vasculature is key to a maximal safe resection of brain tumors, particularly for highly vascularized entities such as high-grade gliomas, hemangioblastomas, and meningiomas, among others.^1,2 In very rare instances, aneurysms have been described in tumor vasculature and can present a unique challenge depending on the location of the aneurysm relative to the tumor and the accessibility for proximal control. Hemangiopericytomas are rare meningeal solitary fibrous tumors that make up less than 1% of all intracranial tumors and can be highly vascular as they arise from the pericytes within the walls of dural capillaries leading to an atypical build-up of blood vessels.³ We describe a case of a hemangiopericytoma where a combination of radiographic and clinical suspicion for a vascular steal phenomenon led to detection of an intratumoral aneurysm preoperatively, which was successfully treated along with the tumor being removed.

Illustrative Case

A 29-year-old right-handed female presented with persistent headaches, along with blurred vision in her right eye. Past medical and family histories were noncontributory. Her neurological exam was unremarkable. Magnetic resonance imaging (MRI) revealed a large, homogeneously enhancing mass in the right frontal region with significant associated vasogenic edema and mass effect, causing effacement of the frontal horn of the right lateral ventricle (Fig. 1A and B). T2-weighted fluid-attenuated inversion recovery (FLAIR) sequences revealed hypodense areas, initially read by outside radiology as “tumor calcifications.” However, upon referral and review at our institution, and in the context of the aggressive appearance of the tumor, these hypointensities were instead felt to be concerning for intratumoral flow voids and possibly indicative of prominent vasculature and a potential large feeding artery. A computed tomography angiogram (CTA) was obtained and revealed a hypervascular extra-axial tumor with a 4 × 2–mm aneurysm within its inferior aspect arising from one of the feeding arteries supplied by the right A2 segment of the anterior cerebral artery (ACA) (Fig. 1C and D). It was postulated that the aneurysm likely arose as a weakening in the tumor feeding artery due to high flow to the tumor. Given that the feeding artery aneurysm arose deep to the tumor and was tucked within a highly vascular tumor and edematous brain, early proximal control of the aneurysm could prove challenging during open surgery. Rather, a combined endovascular and open surgical approach to first safely treat the aneurysm and then resect the tumor in the same setting was planned in our hybrid operating room with biplane angiography capabilities.

FIG. 1.

T1-weighted MRI after gadolinium contrast administration (A) and T2-weighted MRI with FLAIR (B) demonstrate a large, heterogeneously enhancing mass in the right frontal lobe with associated vasogenic edema and effacement of the right lateral ventricle. The signal void (arrow) was found to be the aneurysm. Conventional CTA (C) and three-dimensional reconstruction (D) show a 4 × 2–mm aneurysm along the inferior extent of the tumor arising from a branch off the right A2 segment.

The patient first underwent a diagnostic 6-vessel cerebral angiogram. Injection of the right internal carotid artery affirmed the findings from the preoperative CTA of multiple, prominent right ACA feeders to the tumor, including a major tumor blood vessel stemming off the A2 segment en route to a conspicuous intratumoral aneurysm (Fig. 2A). Additionally, there was notable vascular steal from the right ophthalmic artery into the tumor, likely explaining the patient’s preoperative complaints of ipsilateral blurred vision. The aneurysm was successfully obliterated with Onyx (Micro Therapeutics, Inc.) liquid embolic material. Final runs demonstrated excellent tumor penetration with casting of the intratumoral aneurysm and its arterial feeder (Fig. 2B). Although not a routine part of the operating neurosurgeon’s tumor surgery practice, the 2 hypertrophied branches of the right middle meningeal artery supplying the tumor were also embolized with 30% Trufill n-butyl cyanoacrylate glue mixture with 5% dextrose solution (Codman Neuro). Analysis of the glue cast and postinjection control runs confirmed excellent intratumoral penetration. Protamine was given to fully reverse the heparinization from the endovascular procedure, and a normal activated clotting time was verified prior to proceeding with open surgery.

FIG. 2.

A: Selective injection of the right internal carotid artery during digital subtraction angiography demonstrates multiple, prominent right ACA feeders to the tumor, including a major vessel off A2, as well as a prominent intratumoral aneurysm. B: The same injection performed after Onyx embolization shows excellent tumor penetration with casting of the intratumoral aneurysm and its arterial feeder.

The patient was then prepared for open resection of the tumor. A curvilinear incision behind the hairline and right frontal craniotomy was performed immediately after the endovascular intervention to prevent additional brain swelling. The tumor was near completely resected, except for a small area where it was invading the patent superior sagittal sinus. The large feeding artery with the intratumoral aneurysm was encountered along the medial and inferior aspects and was disconnected at a point just distal to where the artery had been thrombosed, without any associated bleeding.

Final pathology was consistent with an anaplastic hemangiopericytoma. Prominent intermixed, thin-walled branching vascular channels were found histologically (Fig. 3A) and the Ki-67 labeling index exceeded 8%–10%. Whole-exome sequencing of the tumor revealed a NAB2-exon 6 and STAT-exon 16 fusion, which has previously been reported in hemangiopericytomas.^4,5

FIG. 3.

A: Hematoxylin and eosin staining demonstrates a cellular spindle cell neoplasm with patternless architecture and a variably prominent hyaline collagenous stroma, composed of randomly oriented oval to spindled cells with scant cytoplasm and nuclear atypia with intermixed thin-walled branching vascular channels (original magnification ×200). B: There is diffuse nuclear positivity for STAT6 (original magnification ×400).

The patient was neurologically intact and discharged home on postoperative day 2 with notable resolution of her headaches and visual symptoms. Given the high-grade pathology, the patient opted to undergo proton beam therapy for a total of 66 Gy in 2-Gy fractions to her known area of residual disease and 59.4 Gy in 1.8-Gy fractions to the surgical cavity. As of her last follow-up 7.5 years after surgery, she continues to remain radiographically free from disease recurrence and neurologically intact.

Discussion

Observations

The incidence of aneurysms occurring within brain tumors is undeniably rare, reportedly less than 1%, and is most commonly associated with meningiomas, pituitary adenomas, and gliomas.^1,2 Despite these statistics, preoperative recognition of tumors that may harbor underlying complicating vascular features is essential to help the surgeon develop a successful and safe surgical strategy. The presence of intratumoral flow voids on T2-weighted MRI is a key indicator of significant vascularity that may prompt further dedicated vascular imaging, such as a CTA or formal angiogram.⁶ In addition, increased edema in relation to tumor volume may also predict greater tumor vascularity.^7,8

There is a paucity of data regarding the pathophysiology of aneurysm formation in tumors. Several theories exist, including weakening of fragile and potentially necrotic neoplastic vessels from local tumor invasion,⁹ hemodynamic stress secondary to increased directional blood flow in feeding vessels,^2,10 and arteriovenous shunting leading to aneurysm formation of intratumoral vessels.¹¹ Considering that our patient’s tumor exhibited vascular steal from a major vessel during diagnostic catheter angiography, we suspect that the aneurysm formation was due to high-flow hemodynamic stress on the vessel wall.

While there are several reports of aneurysms associated with brain tumors,^12–14 there are no definitive guidelines for the optimal treatment strategy. Zhong et al.¹⁴ described a case series of 12 patients who underwent combined management of concurrent brain tumors and aneurysms and proposed a therapeutic strategy based on location of the aneurysm in relationship to the tumor. For aneurysms encased by the tumor, as in our case, preoperative embolization can be quite reasonable to avoid the complication of intraoperative aneurysmal rupture without assurance of proximal control. Those feeding arteries that can be well controlled at the time of surgery, with early access and visualization, can safely be managed under clip ligature without the need for a separate procedure.

When considering preoperative embolization of large vascular tumors, access to a hybrid operating room, such as ours, is critical as it can obviate the potential life-threatening risk of tumor infarction and subsequent hemorrhage and edema that can lead to an acute increase in intracranial pressure and herniation syndromes.¹⁵ As exemplified in this case, embolization can be immediately followed by craniotomy for tumor resection after appropriate reversal. Other authors have also reported craniotomy and tumor exposure before embolization is performed but this can become more complicated when anticoagulants are needed for safe endovascular ligation.¹⁶

Lessons

Not surprisingly, most patients with intratumoral aneurysms present with symptoms attributable to the tumor rather than the aneurysm. In the patient presented here, her unilateral blurred vision did not necessarily coincide with her tumor location and presentation but was related to the vascular steal into the tumor from her ophthalmic artery as seen on angiogram. Such symptoms or signs that do not necessarily correlate with the patient’s tumor should prompt consideration of an underlying vascular steal phenomenon, especially in tumors with more malignant features and high vascularity. Along those lines, the initial MRI was misinterpreted by others as “calcifications,” a feature more commonly associated with more benign, slow-growing tumors. However, this tumor was quite large and associated with significant edema, central necrosis, mass effect, and shift. The patient had a short history of symptoms. As such, these features prompted suspicion for a more aggressive tumor pathology and not one we might expect to be associated with calcifications. Therefore, considering vascular flow voids in such a circumstance is important. During brain tumor surgery in general, it is our approach to understand the relevant vascular anatomy relative to the tumor and to address the main tumor feeders first to obtain proximal control and facilitate more efficient and safe resection. In rare cases where an embedded intratumoral aneurysm is present, preoperative endovascular intervention may be helpful to minimize the risk of rupture during microsurgical tumor resection if the presence of the tumor may preclude early clip ligation or coagulation and control.

In summary, this was a rare case of a tumor-related aneurysm embedded within a hemangiopericytoma that was managed through a combined endovascular and open surgical approach. Although intratumoral aneurysms are rare, the need for control of abnormal tumor vessels in highly vascular tumors is not and underscores the importance of a vascular approach to brain tumor resection. Tumors can be quite vascular and recruit their own blood supply. While not every tumor requires preoperative vascular imaging, radiographic and clinical cues such as the vascular steal phenomenon observed in our patient should be a telltale sign for further workup prior to resection. Dedicated vascular imaging should be considered in suspected cases of highly vascular tumors, as the possibility of aneurysm formation secondary to vascular steal remains and can influence management strategies. These highly vascular tumors should be approached from a “vascular neurosurgery” perspective in addition to that of neurosurgical oncology.

Disclosures

Dr. Moliterno reports personal fees from BK Medical outside the submitted work.

Author Contributions

Conception and design: Moliterno, Hong. Acquisition of data: Hong, Barak, Baehring. Analysis and interpretation of data: Moliterno, Hong, Marianayagam, Morales-Valero, Tabor, Baehring, Erson-Omay. Drafting of the article: Moliterno, Hong, Marianayagam, Morales-Valero, Tabor, O’Brien. Critically revising the article: Moliterno, Hong, Marianayagam, Morales-Valero, Tabor, O’Brien, Huttner, Baehring, Erson-Omay, Fulbright, Matouk. Reviewed submitted version of the manuscript: Hong, Marianayagam, Morales-Valero, Barak, Tabor, O’Brien, Huttner, Baehring, Gunel, Erson-Omay, Fulbright, Matouk. Approved the final version of the manuscript on behalf of all authors: Moliterno. Administrative/technical/material support: Moliterno, Hong. Study supervision: Moliterno, Hong.