Abstract

Background: Pseudoaneurysm arising from the distal segment of an intracranial artery is a rare cause of subdural hematoma (SDH). We report a patient diagnosed with a pseudoaneurysm of a cortical branch of the distal anterior cerebral artery (ACA) during planned middle meningeal artery embolization for SDH and present a systematic review to summarize the present literature.

Methods: A systematic literature search was conducted across EMBASE, MEDLINE, CINAHL, the Cochrane Library, and Scopus to identify studies reporting SDH due to pseudoaneurysms in the terminal intracranial artery segments. Details regarding clinical presentation, management, and outcomes were extracted.

Results: Twenty patients from the 18 retrospective studies and the patient from the present report were included in the review. The mean age of the patients was 49.4 years; 80.9% of the patients were males. A history of nonpenetrating head trauma was present in 11 (52.4%) patients. The most common presenting symptoms were hemiparesis and altered mental status. Catheter angiography established the diagnosis in the majority of the patients (85.7%). Angiography was performed due to a clinical/radiological suspicion for a pseudoaneurysm in 6 (28.5%) patients. In the majority of the patients (66.7%), angiography was performed for a different indication. Middle cerebral artery (15 patients, 71.4%) was the most common location of the pseudoaneurysm, followed by ACA, posterior cerebral artery, and posterior inferior cerebellar artery. Pseudoaneurysm was treated surgically in 14 patients (66.7%) and by endovascular modalities in 5 patients (23.8%). One patient undergoing endovascular treatment required surgical evacuation of SDH. The majority of the patients in both treatment groups (surgical – 72.7%, endovascular – 80%) recovered without severe disability (modified Rankin Scale ≤ 4).

Conclusion: Pseudoaneurysms of distal segments of intracranial arteries are a very rare cause of SDH. A high index of suspicion is required for their identification. While a definitive diagnosis requires catheter angiography, indications to perform angiography in SDH are unclear. Pseudoaneurysms with SDH can be treated safely with both microsurgical and endovascular modalities. Microsurgery has the advantage of draining SDH at the same time. The relative efficacy of different treatment approaches and the indications for each are not yet defined.

Keywords: Endovascular, Microsurgery, Pseudoaneurysm, Subdural hematoma, Trauma

INTRODUCTION

Subdural hematomas (SDHs) are one of the most common intracranial pathologies encountered worldwide. They are usually treated by surgical evacuation through burr holes or craniotomy, when symptomatic. Recently, middle meningeal artery (MMA) embolization by endovascular means is gaining traction as a treatment modality in both the upfront and recurrent setting. Although multiple predisposing factors such as head trauma, alcohol abuse, antiplatelet, or anticoagulant medications have been recognized, structural vascular etiologies (aneurysms, pial arteriovenous malformation, or dural arteriovenous fistula) causing predominantly SDH are rare. Of these, pseudoaneurysm arising from the terminal segment of an intracranial artery bleeding into the adjacent subdural space is a very rare cause of SDH.

SDH due to pseudoaneurysm may progress rapidly, leading to an acute neurological deterioration. Moreover, it may tend to recur if treated by surgical drainage alone, without securing the pseudoaneurysm. Pseudoaneurysms are rarely recognized in conventional structural imaging (computed tomography [CT]/magnetic resonance imaging [MRI] brain) and are usually diagnosed in an angiographic study. However, an angiographic study is not performed routinely for a patient presenting with SDH, and the indications for performing an angiogram in SDH patients are not very clear. Hence, a high index of suspicion and awareness regarding the possibility of a pseudoaneurysm are essential for diagnosis and appropriate treatment in this rare clinical scenario.

We report a patient whose pseudoaneurysm was identified at angiography during planned MMA embolization for SDH. We also conducted a systematic review to summarize the present literature on pseudoaneurysms of terminal intracranial artery segments causing SDH, emphasizing their clinical presentation, mode of diagnosis, and treatment approach. We aim to highlight different clinical scenarios leading to the diagnosis of pseudoaneurysm in patients with SDH and describe management strategies for pseudoaneurysm-related SDH.

CASE DESCRIPTION

A 91-year-old male with a history of coronary artery disease, hypertension (HTN), atrial fibrillation, cirrhosis, colon cancer, thrombocytopenia (platelet count <150,000/mm³), and on low-dose aspirin therapy (81 mg daily) presented to our hospital after a ground-level fall. He was diagnosed with a thin left frontotemporoparietal acute SDH, which was managed conservatively. Two weeks later, he presented with dysphasia and subtle right hemiparesis. Repeat head CT showed progression with conversion to chronic SDH [ Figure 1 ]. Due to the thrombocytopenia and subtle symptoms, MMA embolization was planned to prevent further progression. During angiography of the ipsilateral internal carotid artery (ICA), a pseudoaneurysm measuring 5.04 × 4.77 mm was noted, arising from a frontal cortical branch of A4 – anterior cerebral artery (ACA) [ Figures 2a - f ].

Figure 1:

Computed tomography head and magnetic resonance imaging brain-T1 sequence showing left frontotemporoparietal subdural hematoma (blue arrows). (a) CT head, (b) MRI brain T1 sequence

Figure 2:

Cerebral angiogram showing pseudoaneurysm (arrows) arising from a frontal cortical branch of the A4 segment of the anterior cerebral artery. Pseudoaneurysm shows delayed filling (beginning in the late arterial phase) and delayed washout during different phases of the angiogram, which are seen classically in a pseudoaneurysm. (a) Early arterial phase, (b) late arterial phase, (c) capillary phase, (d) early venous phase, (e) late venous phase, (f) selective arterial injection of the parent artery.

Microcatheter angiography revealed en passage flow to the normal brain distally [ Figure 2f ], and embolization with liquid embolic agents was deferred. Afferent flow into the pseudoaneurysm was not favorable for coil embolization. Therefore, surgical treatment was pursued. The patient underwent craniotomy for excision of the pseudoaneurysm and surgical evacuation of SDH. The pseudoaneurysm was embedded in the SDH and was attached to the membranes of the hematoma. It was in close relation to a frontal cortical branch of distal ACA that could be safely sacrificed with the excision of the pseudoaneurysm. Histopathological examination confirmed the diagnosis of pseudoaneurysm [ Figure 3 ]. Postoperative imaging showed no complications, and the patient improved neurologically over the next 10 days. Unfortunately, he subsequently declined due to hepatic encephalopathy and pneumonia and died due to medical complications on postoperative day 25.

Figure 3:

Pseudoaneurysm formation with layered fibrin clotting products, recanalized lumen, and an absence of a true vessel wall (Movat trichrome, ×200).

SYSTEMATIC REVIEW

Methods

EMBASE (through embase.com, 1974-present version), MEDLINE (through EBSCOhost), CINAHL (through EBSCOhost), the Cochrane Library (through Wiley), and Scopus were searched on October 15, 2024, by a medical librarian with expertise in systematic reviews. Keywords and subject headings (when available) were used for the “pseudoaneurysm” and the “SDH or hemorrhage” concepts. When subject headings were available, articles indexed as concerning animals only were removed. English language filters were used. All types of publications were included. No publication date limits were used.

All the search results were imported into the project’s database. EndNote and Zotero duplicate detection tools and manual scans were used to identify duplicates, which were removed. The titles and abstracts of the remaining records were reviewed by two authors independently. Pseudoaneurysms arising only from the terminal segments of different intracranial arteries were included in the review, as shown in Table 1 . Standard segmental nomenclature for cerebral arteries was used. The nomenclature for cerebellar arteries was adopted from the system proposed by Rodríguez-Hernández et al.[ 16 ] Only patients with pseudoaneurysms that showed a classical radiological appearance or patients with aneurysms confirmed to be pseudoaneurysms based on intraoperative appearance or histopathological evaluation were included in the study. Reports describing cases without SDH, SDH due to causes other than pseudoaneurysm, pseudoaneurysms of MMA, other extracranial vessels or veins, pseudoaneurysms arising from proximal segments, other types of aneurysms, and an associated history of penetrating trauma were excluded from the study.

Table 1:

Segments of intracranial arteries included in the review.

Details regarding the following variables were collected from the selected reports using Microsoft Excel version 2402: details of the report (first author, year of publication, number of patients, and location of the reporting center), patient demographics, history of trauma and comorbidities, presenting symptoms, investigations, underlying indication for angiography, characteristics of pseudoaneurysm (number and location), treatment modalities, postoperative course and complications, and clinical outcomes at discharge and follow-up. Clinical outcomes were studied in terms of the modified Rankin scale. A narrative synthesis of the collected data was performed.

RESULTS

The Preferred Reporting Items for Systematic Reviews and Meta-Analyses flowchart detailing the screening strategy and reasons for exclusion is shown in Figure 4 . Out of the 1223 records produced by the search, 18 studies with 20 patients were identified for inclusion in the review.[ 1 - 15 , 17 - 19 ] All the included studies had retrospective designs (case reports – 16 and case series – 2). A summary of the included studies is provided in Table 2 .

Figure 4:

The preferred reporting items for systematic reviews and meta-analyses flowchart for selection of studies.

Table 2:

Summary of the studies included in the review.

Patient characteristics

A total of 21 patients, including the case reported in this study, were included in the final analysis. The mean age of the patients was 49.4 ± 23.8 years (range: 1 month–91 years). The majority (80.9%) of the patients were males. A history of nonpenetrating head trauma was present in 11 patients (52.4%). Comorbidities noted in the patients were the following: diabetes mellitus (2 patients), HTN (4 patients), atrial fibrillation (3 patients), history of ischemic heart disease or stroke (1 patient), liver cirrhosis (1 patient), and hepatocellular carcinoma (1 patient). Details regarding the use of antiplatelets or anticoagulants were not reported in the majority of the studies. One patient had ongoing apixaban therapy, and two patients had ongoing antiplatelet therapy.

Clinical presentation and diagnosis

The most common presenting symptoms were hemiparesis (52.3%, 11 patients), altered mental status (42.8%, 9 patients), seizures (14.3%, 3 patients), speech disturbances (23.8%, 5 patients), and headache (14.3%, 3 patients). Diagnosis of pseudoaneurysm was established on a catheter angiogram in the majority of the patients (18 patients, 85.7%). It was diagnosed based on a CT angiogram and a magnetic resonance angiogram in one patient each; one patient was diagnosed during the surgery for SDH. Indications for performing an angiographic study in these patients are described in Table 3 .

Table 3:

Indications for performing angiography in patients with SDH. One patient did not undergo any angiographic study and was diagnosed during the surgery for SDH.

Aneurysm characteristics

Only one patient had two pseudoaneurysms (ACA and MMA); all other patients had a single pseudoaneurysm. Pseudoaneurysm was most commonly found in the MCA (15, 71.4%), followed by ACA (3, 14.3%), posterior cerebral artery (PCA) (2, 9.5%), and posterior inferior cerebellar artery (1, 4.7%).

Treatment

Pseudoaneurysm was treated surgically in 14 patients (66.7%) and by endovascular modalities in 5 patients (23.8%) [ Figure 5 ]. Conservative management was adopted in one patient, with spontaneous resolution on follow-up imaging.[ 6 ] One patient deteriorated rapidly following surgery for evacuation of SDH and died before undergoing any treatment for the pseudoaneurysm.[ 9 ] Patients undergoing surgical treatment of the pseudoaneurysm underwent simultaneous evacuation of SDH. Histopathological confirmation of pseudoaneurysm was reported in 9 patients. Wherever available, it has been described as a full-thickness vessel wall disruption with the presence of a thrombus of varying size. No other associated pathologies were reported on histopathological examination. Among the patients undergoing endovascular management, one patient (20%) required surgical evacuation of SDH, which was performed before the diagnosis of the aneurysm.

Figure 5:

Modalities of treatment used for pseudoaneurysms. Excision repair involved excision of the pseudoaneurysm and repair of the parent artery, whereas trapping/parent vessel sacrifice involved parent artery sacrifice with or without excision of pseudoaneurysm. Bypass was not performed for any of the patients undergoing trapping/parent vessel sacrifice.

Outcomes and complications

In the surgical group (n = 14 patients), data regarding the postoperative course were not available for 3 patients. Eight out of the remaining 11 patients (72.7%) had an unremarkable postoperative course and recovered without severe disability (modified Rankin Scale ≤ 4) at discharge. One patient had recollection of SDH in the postoperative period, which required re-exploration and evacuation.[ 8 ] One patient remained in an altered mental state and died due to irreversible brain damage secondary to raised intracranial pressure; the patient in our report died due to medical complications.[ 9 ] In the endovascular group (n = 5 patients), one patient developed a left PCA territory infarct and remained in an altered mental state (Glasgow Coma Scale = 11) at the time of discharge and was transferred to neurorehabilitation.[ 5 ] He improved over time and had a mRS = 4 at the 6-month follow-up. The remaining four patients (80%) experienced good clinical status at discharge.

Follow-up details were available for 7 (33.3%) patients with a mean follow-up duration of 14.9 months. Six patients (85.7%) recovered without severe disability (mRS ≤4) at the past follow-up. No patients had a recurrence of pseudoaneurysm or SDH at the time of follow-up.

DISCUSSION

This study summarizes different clinical scenarios in patients with SDH leading to the diagnosis of a pseudoaneurysm in the terminal segment of an intracranial artery. Angiography was performed due to a clinical/radiological suspicion for a pseudoaneurysm in a few patients (28.5%) only. In the majority of the patients (66.7%), angiography was performed for a different indication. Both surgical and endovascular modalities were found to be safe and efficacious for the treatment of pseudoaneurysms causing SDH.

Pseudoaneurysms are typically diagnosed on an angiographic study with their classical radiological appearance of delayed filling and delayed washout, as shown in Figure 2 . They can be suspected occasionally on structural imaging (CT/MRI) if they have grown large enough or in the presence of supportive radiological findings, such as adjacent subarachnoid hemorrhage or intraparenchymal hematoma. A vascular pathology was suspected in a very small number of patients in the present series. The majority of the patients were diagnosed with a pseudoaneurysm on an angiographic study performed for some other purpose. This reflects the need to be aware of the rare possibility of pseudoaneurysms in patients with SDH. Given their rarity, definitive indications for angiographic study are difficult to provide and essentially remain case-based.

Several patients in our study were diagnosed on an angiogram, which was performed as a modality for structural imaging before the advent of CT and MRI scans. After CT and MRI imaging became widely available, angiographic studies are performed rarely in patients with SDH. Moreover, the indications for performing angiographic studies in SDH are not well-defined. This may explain the rarity of published reports describing cases of pseudoaneurysm-related SDH. With the increasing use of MMA embolization in patients with SDHs (in our case as an example), more frequent diagnosis of this rare entity may be possible.

Only one study (out of 18) in our review reported conservative management; the indication for adopting the same was not specified. Moreover, there is no other reliable data available on the natural course (resolution/progression/recurrence) of untreated pseudoaneurysms causing SDH. Given the fact that the pseudoaneurysm is almost certain to be ruptured when associated with SDH, it would typically require active management as described in the majority of the reports. However, conservative management could be considered in patients with thin asymptomatic SDH with small pseudo-aneurysm size (? Cutoff ~ 5 mm) and who are at high periprocedural risk for either surgical or endovascular treatment. In such cases, patients would require close imaging follow-up to confirm resolution or at least stability of the pseudoaneurysm.

Both microsurgical and endovascular modalities have shown efficacy and safety in the literature. Endovascular modalities have been described only recently, in studies published after the year 2000. All studies reported before 2000 exclusively employed microsurgery for the treatment of pseudoaneurysms. Microsurgery has the benefits of (1) being technically more feasible for distal segments of the vessels and (2) evacuating SDH simultaneously. Endovascular modalities are less invasive but are often challenging for distal segments of the vessel and frequently require the use of periprocedural anticoagulation (which might pose a risk of hematoma progression).

Limitations

All the studies included in the review were retrospective; hence, the strength of this review is limited by the accuracy of retrospective data. Re-rupture rates of the pseudoaneurysms and comparative efficacy of surgical and endovascular modalities could not be studied due to nonuniform and inadequate data across the studies.

CONCLUSION

Pseudoaneurysms of distal segments of intracranial arteries are a very rare cause of SDH. A high index of suspicion is required for their identification. While a definitive diagnosis requires catheter angiography, indications to perform angiography in SDH are unclear. Pseudoaneurysms with SDH can be treated safely with both microsurgical and endovascular modalities. However, microsurgery has the advantage of draining the SDH simultaneously. The relative efficacy of different treatment approaches and the indications for each are not yet defined.

Ethical approval:

Institutional Review Board approval is not required.

Declaration of patient consent:

The authors certify that they have obtained all appropriate patient consent.

Financial support and sponsorship:

Nil.

Conflicts of interest:

There are no conflicts of interest.

Use of artificial intelligence (AI)-assisted technology for manuscript preparation:

The authors confirm that there was no use of artificial intelligence (AI)-assisted technology for assisting in the writing or editing of the manuscript and no images were manipulated using AI.

Disclaimer

The views and opinions expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Journal or its management. The information contained in this article should not be considered to be medical advice; patients should consult their own physicians for advice as to their specific medical needs.

References

1. Acosta C, Williams PE, Clark K. Traumatic aneurysms of the cerebral vessels. J Neurosurg. 1972. 36: 531-6

2. Bassett RC, Lemmen LJ. Subdural hematoma associated with bleeding intracranial aneurysm. J Neurosurg. 1952. 9: 443-50

3. Bergstrom K, Hemmingsson A. False cortical aneurysm in subdural hematoma following head injury without fracture. Acta Radiol Diagn. 1973. 14: 657-61

4. Cho WS, Batchuluun B, Lee SJ, Kang HS, Kim JE. Recurrent subdural hematoma from a pseudoaneurysm at the cortical branch of the middle cerebral artery after mild head injury: Case report. Neurol Med Chir (Tokyo). 2011. 51: 217-21

5. Ciochon UM, Brandt EG, Stavngaard T. Acute tentorial subdural hematoma caused by rupture of the posterior cerebral artery after minor trauma-A case report. Diagnostics (Basel). 2020. 10: 175

6. Dharsono F, Phatouros CC. Arterial origin subdural hematoma and associated pial pseudoaneurysm following minor head trauma. Clin Imaging. 2013. 37: 750-2

7. Dujardin CE, Cloft H, Wijdicks EF. Brushing against the tentorium: Traumatic pseudoaneurysm of the posterior cerebral artery. Neurocrit Care. 2020. 33: 607-9

8. Eichler A, Story JL, Bennett DE, Galo MV. Traumatic aneurysm of a cerebral artery. Case report. J Neurosurg. 1969. 31: 72-6

9. Go KG, Penning L, Oen TS. Acute subdural haematoma in connection with angiographically demonstrated traumatic rupture of a cortical cerebral artery (presenting as false aneurysm. A report of 2 cases. Neuroradiology. 1971. 2: 107-10

10. Iza-Vallejo B, Mateo-Sierra O, Fortea-Gil F, Ruiz-Juretschke F, Martín YR. Acute subdural hematoma secondary to distal middle cerebral artery aneurysm rupture in a newborn infant. J Neurosurg Pediatr. 2009. 3: 435-8

11. Jeon YS, Lee JG, Chun YI, Cho J, Choe WJ. Traumatic pseudoaneurysm related to calcified nodules of cerebral convexity Dura mater in an American college football player. J Cerebrovasc Endovasc Neurosurg. 2016. 18: 322-6

12. Lee SH, Moon JU, Choi SK, Choi MK, Lee J, Sung JY. Pseudoaneurysm at the distal posterior inferior cerebellar artery after blunt head trauma: A case report and review of the literature. World Neurosurg. 2016. 92: 580.e11-5

13. Miyazaki S, Fukushima H, Kamata K, Ishii S. False aneurysm with subdural hematoma and symptomatic vasospasm following head injury. Surg Neurol. 1981. 16: 443-7

14. Murakami M, Kakita K, Hosokawa Y. Ruptured traumatic aneurysm after trivial injury mimicking acute spontaneous subdural hematoma--case report. Neurol Med Chir (Tokyo). 2003. 43: 130-3

15. Park I, Park H. Uncommon stroke disorders endovascular management of traumatic pseudoaneurysm of the pericallosal artery-case report. Int J Stroke. 2014. 9: 316

16. Rodríguez-Hernández A, Rhoton AL, Lawton MT. Segmental anatomy of cerebellar arteries: A proposed nomenclature. Laboratory investigation. J Neurosurg. 2011. 115: 387-97

17. Terceño M, Remollo S, Silva Y, Bashir S, Castaño C, Serena J. Intracranial hemorrhage secondary to a delayed cerebral pseudoaneurysm rupture 18 years after cranial trauma. Case Rep Neurol. 2019. 11: 325-9

18. Tirado SR, Bass DI, Feroze A, Johnston B, Bi WL, Du R. Ruptured traumatic pseudoaneurysm of the middle cerebral artery following minor trauma treated with an MCA-MCA bypass: A case report. Surg Neurol Int. 2024. 15: 247

19. Yanagawa T, Yamashita K, Harada Y, Hatayama T, Kono T. Location of hemorrhage with nontraumatic acute subdural hematoma due to ruptured microaneurysm. Surg Neurol Int. 2021. 12: 401