Successful treatment with urgent revascularization and parent artery occlusion for a ruptured intratumoral aneurysm following prior meningioma surgery: illustrative case

Abstract

BACKGROUND

An intratumoral aneurysm encased within the associated intracranial tumor is rare, and hemorrhage caused by its rupture is even more rare. While urgent and adequate surgical treatment is important, the treatment can be difficult given the limited understanding of this rare condition.

OBSERVATIONS

A 69-year-old man who had undergone meningioma surgery 30 years prior presented with a disturbance in consciousness. Magnetic resonance imaging revealed massive intracerebral and subarachnoid hemorrhage. A round, partially calcified mass, which was diagnosed as recurrent meningioma, was also observed. Subsequent cerebral angiography revealed that the source of the hemorrhage was an intratumoral aneurysm in the dorsal internal carotid artery (ICA) encased within the recurrent meningioma. Urgent surgical ICA trapping and high-flow graft bypass were conducted. The postoperative course was uneventful, and he was referred to another hospital for rehabilitation.

LESSONS

This is the first case report of a ruptured intratumoral aneurysm being treated with urgent combined revascularization and parent artery trapping surgery. This surgical approach may be a feasible treatment option for such a challenging condition. Additionally, this case highlights the importance of diligent long-term follow-up after skull-base surgery, as minor intraoperative vascular wall injury may trigger the development and rupture of an intracerebral aneurysm.

Despite recent advances in diagnostic technology, the coexistence of an intracranial tumor and a cerebral aneurysm is still uncommon, with estimated incidence rates ranging from 0.2% to 7.7%.^1–3 Previous research¹ suggests that the majority of aneurysms are located outside the tumor, and the relationship and pathogenesis of coexisting aneurysms with intracranial tumors are unknown. Hormonal influences from the tumor,⁴ gene mutations or loss of gene expression,² and increased hemodynamic stresses on the feeding vessel to the tumor⁵ are all possible pathogeneses of aneurysm development. Completely embedded intratumoral aneurysms are much rarer,¹ and their underlying pathogenesis and association with the surrounding tumor are unknown. Therefore, determining an optimal treatment strategy for such cases is complex.

In this case report, we describe a rare case of an intratumoral aneurysm that developed 30 years after meningioma surgery, whose rupture resulted in a massive intracerebral hemorrhage (ICH) and subarachnoid hemorrhage (SAH). Rupture of this rare aneurysm is an additional rarity and requires urgent and adequate treatment. To the best of our knowledge, this is the first reported case of a ruptured intratumoral aneurysm successfully treated with urgent revascularization surgery followed by parent artery occlusion. Our case study may offer a different therapeutic choice in this difficult scenario. Additionally, it is important to recognize that cerebral aneurysms, including those that present as intratumoral aneurysms encased within recurrent intracranial tumors, can develop after a long-term follow-up period following initial skull-base surgery. Thus, careful follow-up is essential, even in cases in which vascular injuries are not evident during the initial operation.

Illustrative Case

History and Examination

A 69-year-old man experienced a sudden-onset headache, which was followed by progressive consciousness disturbance. He had a medical history of meningioma treatment more than 30 years earlier but had been lost to follow-up.

Neurological examination showed severe consciousness disturbance with a Glasgow Coma Scale score of 7, anisocoria, total aphasia, and severe right hemiparesis at the time of hospitalization. A computed tomography (CT) scan revealed diffuse SAH and massive ICH in the left temporal lobe, as well as a partially calcified, high-density round mass in the parasellar region (Fig. 1A). The round mass was directly connected to the hemorrhages. Magnetic resonance imaging (MRI) revealed an extra-axial mass with partial contrast enhancement in a parasellar lesion (Fig. 1B). Recurrent meningioma was the most likely diagnosis based on the patient’s medical history. Both T2-weighted imaging and gadolinium-enhanced T1-weighted imaging showed encased vasculature within the recurrent meningioma, which was later identified as an intratumoral aneurysm. CT angiography (Fig. 2A) and digital subtraction angiography (Fig. 2B) were used to further investigate the source of the hemorrhage. In both examinations, an intratumoral aneurysm in the dorsal ICA was found, which was completely embedded inside the recurrent meningioma. Moreover, diffuse narrowing of the left ICA was observed, indicating strong adhesion between the vascular wall and the surrounding tumor. We determined that the diffuse SAH and ICH were caused by the rupture of an intratumoral aneurysm in the dorsal ICA, necessitating immediate surgical intervention to prevent rebleeding. Given the difficulties associated with simple clipping or coiling and the unknown pathogenesis of the aneurysm, the surgical strategy of trapping the left ICA with revascularization was selected to ensure safety.

FIG. 1.

Preoperative CT imaging (A) and MRI (B). Diffuse SAH and massive ICH in the left temporal lobe, along with a partially calcified, high-density round mass in the parasellar region (A). MRI of the parasellar region revealed an extra-axial mass with moderate contrast enhancement. Encased vasculature inside the tumor (B) was seen, which was considered as the intratumoral aneurysm.

FIG. 2.

Preoperative CT angiograms (A) and digital subtraction angiograms (B) show an intratumoral aneurysm (white arrows) in the dorsal ICA, which was completely embedded inside the tumor. Diffuse narrowing of the ICA is visible (arrowheads).

Operation

The patient had a left anterior temporal craniotomy, and a high-flow graft bypass was performed using an anastomosis of the external carotid artery graft, radial artery (RA) graft, and middle cerebral artery (MCA) for ICA revascularization (Fig. 3A). During dissection of the left Sylvian fissure, a reddish-gray firm tumor was encountered in front of the ICA. The branching site of the anterior choroidal artery was confirmed after partial tumor resection and dissection around the top of the ICA. Then, a titanium aneurysm clip was applied to the ICA just proximal to the branching site (Fig. 3B) to interrupt its antegrade flow. The cervical ICA was also interrupted to completely trap the ICA flow after confirming good blood flow to the MCA territory supplied by the RA graft bypass (Fig. 3C). Finally, additional partial tumor resection was performed. The pathological diagnosis was transitional meningioma (World Health Organization grade I).

FIG. 3.

Intraoperative photographs. A: High-flow graft bypass using an anastomosis of the external carotid artery–RA–MCA was performed. B: A parasellar meningioma that was related to the ICA was surrounding it. The ICA was captured using a trap. C: Intraoperative indocyanine green showed good blood flow to the MCA territory.

Postoperative Course

The patient’s postoperative course was uneventful, with no hemorrhagic or ischemic complications. The patient’s neurological symptoms improved gradually, and MRI (Fig. 4) revealed good bypass patency as well as the complete disappearance of the intratumoral aneurysm and antegrade flow of the left ICA. The patient was transferred to another hospital for additional rehabilitation due to neurological sequelae, right hemiparesis, and motor-dominant aphasia (modified Rankin scale score 3 at 3 months after onset).

FIG. 4.

Postoperative magnetic resonance angiography (A) showed good bypass patency and complete disappearance of the intratumoral aneurysm. MRI (B) indicated the disappearance of a massive hemorrhage.

Discussion

We report a rare case of a ruptured intratumoral aneurysm located in the dorsal ICA, encased inside an associated recurrent parasellar meningioma. The development of the intratumoral aneurysm within the recurrent meningioma was observed 30 years after the initial surgery, despite the lack of evidence of intraoperative vascular injury. As the underlying pathogenesis of the aneurysm development and its nature remained unclear, we performed urgent surgical revascularization of the ICA and its trapping, which, to our knowledge, is the first reported case. The patient’s clinical result was good, with minimal neurological sequelae.

Observations

Only 19 cases of an intratumoral aneurysm have been reported in the past.^1,6–11 The pathology of associated tumors was varied, including meningioma, glioma, and pituitary adenoma in 8, 5, and 3 cases, respectively. This diversity of tumor pathology suggests that there are numerous potential mechanisms for the emergence of this rare entity, and these potential pathogeneses appear to be complexly contributing. In our case, we speculated that the minor vascular injury or physical stress that occurred during the initial surgery, although unrecognized at the time, may have served as a trigger for the subsequent development of an aneurysm. Along with this minor vascular injury, direct invasion of the regrowing and surrounding meningioma to this site over more than 30 years may have accelerated the development, enlargement, and potential collapse of the intratumoral aneurysm. Although no microscopic examination was performed, intraoperative observations of strong adhesion between the surrounding tumor and the encased ICA support our speculation. According to the degree of adhesion between the tumor and attached vessels, Al-Mefty¹² classified meningiomas into 3 types. In group 1, the tumor adheres directly to the adventitia without the presence of an arachnoid membrane. A preoperative angiogram was used to determine the degree of adhesion, which revealed narrowing of the encased arteries as a characteristic finding in group 1.¹² In our case, preoperative angiography and CT angiography (Fig. 2) revealed the concordant finding, supporting our hypothesis that direct damage or invasion to the vascular wall, which may have had preexisting minor injuries from the initial surgery, could be occurring in the encased vasculature. This complex process could contribute to the development and collapse of an intratumoral aneurysm. However, other possible factors, such as genetic background,² stimulated vascular proliferation,¹³ and increased hemodynamic stress,⁵ or even simple coincidence, cannot be ruled out. To truly verify the possible mechanisms of intratumoral aneurysm development, further detailed microscopic investigations are warranted.

The rupture of an intratumoral aneurysm is another rare condition, but it is significant because it can result in serious neurological sequalae. According to our literature review of ruptured cases, only 3 case reports demonstrated the coexistence of an intratumoral aneurysm and meningioma. Ogino et al.² described a 70-year-old woman with a ruptured intratumoral aneurysm in the anterior communicating artery, which was surrounded by a tuberculum sellae–derived meningioma. Because there were no radiological findings indicating adhesion between the encased aneurysm and the associated tumor, the authors had planned to conduct tumor resection and direct clipping at the same time. The patient’s postoperative course was uneventful, and the clinical outcome was excellent (modified Rankin scale score of 1). Alnaami et al.⁷ reported a 34-year-old man with a ruptured distal anterior cerebral artery aneurysm surrounded by a falx meningioma. The intratumoral aneurysm in this case became detectable 4 weeks after intratumoral hemorrhage, which was not identifiable at the time of onset. As we discussed in our case, this morphological time course change may indicate that a pseudoaneurysm or dissection due to tumor invasion to the vascular wall may be the pathogenesis of intratumoral aneurysm development. The authors conducted endovascular parent artery occlusion for the intratumoral aneurysm, and the patient’s clinical outcome was also excellent.

Lessons

In our case, we performed surgical revascularization and trapping of the left ICA to treat a ruptured intratumoral aneurysm in the dorsal ICA. We assumed that minor vascular wall injury during the initial skull-base surgery, even at an unrecognized level, triggered the development of a cerebral aneurysm. Recurrence and regrowth of the meningioma at this injured site over a long period of time might have accelerated the development, enlargement, and even collapse of the intratumoral aneurysm via tumor invasion toward the vascular wall. Characteristic radiographic findings indicating firm adhesion between the surrounding tumor and aneurysm and the potential vulnerability of the aneurysm wall led us to choose this treatment strategy instead of simple clipping or coiling. The surgery proceeded safely as planned, and the patient’s postoperative course was uneventful.

Although this is the first case report of an intratumoral aneurysm treated with combined revascularization and parent artery trapping, this established surgical technique is widely accepted for the treatment of difficult large intracranial aneurysms. As we have demonstrated, this surgical procedure is 1 feasible treatment option for intratumoral aneurysms. However, compared with simple clipping or coiling, the technique is more complicated, requiring more sophisticated techniques and a longer procedure time, which can be invasive. Instead of this surgical approach, an endovascular technique using flow-diversion treatment may be a good alternative and is less invasive than surgical treatment. In addition, this case report highlights the significance of diligent and long-term follow-up after skull-base surgery. Minor injuries or physical stress to the vascular wall may serve as a trigger for the development and subsequent rupture of a cerebral aneurysm, which is a rare but serious complication.

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: Kurisu, Okuyama, Hokari, Asaoka. Acquisition of data: Kurisu, Okuyama, Hokari, Uchida, Itamoto. Analysis and interpretation of data: Kurisu, Okuyama, Hokari, Uchida, Fujimura. Drafting of the article: Kurisu, Okuyama. Critically revising the article: Fujimura. Reviewed submitted version of the manuscript: Kurisu, Itamoto. Approved the final version of the manuscript on behalf of all authors: Kurisu. Administrative/technical/material support: Miyata. Study supervision: Asaoka.