Pseudoaneurysm formation due to rupture of intracranial aneurysms: Case series and literature review

Abstract

Background

Intracranial pseudoaneurysm formation due to a ruptured non-traumatic aneurysm is extremely rare. We describe the radiological findings and management of pseudoaneurysms due to ruptured cerebral aneurysms in our case series and previously reported cases.

Patients and methods

Four additional and 20 reported patients presenting with subarachnoid hemorrhage (SAH) are included. Radiological findings and clinical features of these patients were reviewed.

Results

In our series, three-dimensional computed tomographic angiography (3D-CTA) and/or angiography showed an irregular- or snowman-shaped cavity extending from the parent artery. The radiological examination additionally revealed delayed filling and retention of contrast medium. These findings were the same as previously reported cases. One patient underwent direct clipping of the true aneurysm. For the other three patients with aneurysms at the basilar and anterior communicating arteries, the true portion of the aneurysm was embolized with platinum coils. During the procedures, care was taken not to insert the coils into the distal pseudoaneurysm portion to prevent rupture. The review of 24 cases revealed that the location of the aneurysms was most frequent in the anterior communicating artery (41.7%), and 86.7% of patients were in a severe stage of SAH (>Grade 3 in WFNS or Hunt & Kosnik grading) implying abundant SAH.

Conclusions

Pseudoaneurysm formation in SAH after non-traumatic aneurysm rupture is rare. However, in cases with an irregular-shaped aneurysm cavity, pseudoaneurysm formation should be taken into consideration.

Introduction

Pseudoaneurysms usually result from trauma, mycotic infection, vessel dissection, or congenital collagen deficiency.^1–3 We previously reported a case of pseudoaneurysm in a thrombus located at the rupture site of a cerebral aneurysm for the first time.² Since then, several reports describing pseudoaneurysm formation after aneurysmal rupture have been published.^4–12 However, intracranial pseudoaneurysm formation due to a ruptured non-traumatic aneurysm is still rare, and remains to be clarified.^3–12 Furthermore, pseudoaneurysms are difficult to manage and associated with a high risk of rupture during treatment. Recently, we encountered four additional cases of pseudoaneurysm formation at the rupture site of cerebral aneurysms. In this report, we present a case series and a review of the literature for reported cases of pseudoaneurysms formed after cerebral aneurysm rupture. We describe and review the clinical course, radiological findings, and management of this rare condition.

Case presentation

Four cases and 20 reported cases with ruptured aneurysms accompanied by pseudoaneurysms are summarized in Table 1. The mean patient age was 58.4 (range 28–87) years.

Table 1.

Summary of the cases with pseudoaneurysms.

Case	Age (y.o.)	Sex	Location of aneurysm	Initial symptom	Grade (H&K)	Treatment	Treatment day	Size of an. (mm)	Modality	Radiological findings	Pathological findings	Outcome	Others	Reference
1	44	F	Left ICA-AChA		IV	Coiling	0	4	Angiography	Rough wall		Good recovery	Coil migration Extravasation	3
2	67	F	Left ICA-PCoA		III	Coiling	4	3	Angiography	Rough wall CM retention		Death	Coil perforation Extravasation	3
3	45	M	AComA		II	Coiling (trial)→ clipping	0	3	3D-CTA angiography	Lobular CM retention Incomplete filling of CM		Good recovery	Aneurysm thrombosis	3
4	76	F	Left ICA-PCoA		IV	Coiling	1	4	3D-CTA angiography	Elongation Tapering Delayed filling of CM Irregular accessory cavity		Death	Perforation extravasation	3
5	63	M	AComA		IV	Coiling (partial)	45	10	3D-CTA angiography	Lobular Delayed filling of CM		Vegetative state		3
6	28	M	Right MCA		I	Clipping	0	3	3D-CTA angiography	Elongation CM retention Delayed filling of CM		Good recovery		3
7	38	F	Right ICA-PCoA		III	Clipping	1	5	Angiography	Dumbbell shape Incomplete filling of CM CM retention		Moderate disability	Right third nerve palsy	3
8	50	F	AComA		III	Clipping	0	6	3D-CTA angiography	Elongation Tapering Delayed filling of CM Irregular accessory cavity		Good recovery		3
9	42	M	Left MCA	Headache		Clipping	36		3D-CTA angiography	Irregular-shaped an. Snowman-like appearance Delayed opacification Delayed clearance of CM	Fibrin layer Hemosiderin deposition	Good recovery	Premature bleeding	4
10	77	F	Right MCA	Headache Vomiting	WFNS V	Clipping	0	4	3D-CTA angiography	Irregular-shaped an. Heterogeneously opacified Delayed filling Partially remained CM		Vegetative state		5
11	73	F	Right A1/2	Cons. loss	WFNS V	Clipping	0	6	3D-CTA angiography	Irregular-shaped an. Late opacification Changing shape Retention of CM		Died on day 16	Hypertension	5
12	63	F	Left ICA (C2, blister an.)	Headache	IV	Coiling	40		Angiography	Stasis of CM		Moderate disability	Rerupture on Day 40	6
13	37	M	AComA	Headache		Clipping			Angiography	Irregular	Blood clot enclosed with connective tissue	Good recovery	Rerupture during dissection	7
14	55	M	AComA	None → seizure Headache		Clipping	1	3 × 2	3D-CTA angiography	Irregular-shaped an. Delayed filling Outpouching of CM		Good recovery	Family history of aneurysmal SAH	8
15	52	F	BA apex	Headache Cons. loss		Coiling	0	True: 4–5	Angiography	Delayed and unequal filling Irregular stasis and delayed washout of CM		Good recovery		9
16	61	M	Left MCA	Speech dist. Cons. loss	IV	Clipping	5		3D-CTA	Like a large an.	Thrombus destroyed an. wall	Died on day 10	On warfarin	10
17	79	F	AComA	Headache Cons. loss	IV	Coiling	0		Angiography	Irregular shape Delayed appearance Changing shape Unclear neck Retention of CM		Moderate disability	Embolization of the proximal true part	11
18	87	M	AComA	Headache Cons. loss	WFNS IV	Coiling	2	True: 3 Pseudo: 5	Angiography	Delayed filling Changing shape Unclear neck Retention of CM		Died on day 9	Embolization of the proximal true part	12
19	60	M	AComA	Headache Cons. loss	WFNS V	Coiling	9	True: 2 Pseudo: 3 → 7	Angiography	Irregular shape		mRS: 3	Embolization of both true and false lumen	12
20	79	F	AComA	Headache Cons. loss	WFNS IV	Coiling	1	True: 3 Pseudo: 7	Angiography	Delayed appearance Changing shape Unclear neck Retention of CM		mRS: 3	Embolization of the proximal true part	12
Present case 1	56	F	Left A2/3	Cons. loss	3	Clipping	0	9 × 6 × 5	3D-CTA	Distal: oval Proximal: thin cavity	Fresh thrombus without aneurysm wall	3	On warfarin
Present case 2	53	M	BA-SCA	Cons. loss	5	Coiling	0	True: 10 × 6 × 5 Pseudo: 20 × 5 × 5	3D-CT Aangiography	Irregular-shaped an. Delayed filling Retention of CM	NA	6	Hypertension
Present case 3	43	M	AComA	Cons. loss	4	Coiling	0	2.7 × 2.2 × 2	3D-CTA	Irregular-shaped an. not detected on angiography	NA	3	Coil compaction → second coiling
Present case 4	73	F	BA tip	Cons. loss	4	Coiling	0	True: 6 × 4 × 3 Pseudo: 4.5 × 3.5 × 3	Angiography	Delayed opacification Faint	NA	5	Four years ago: coil embolization

an.: aneurysm; 3D-CTA: three dimensional-computed tomography angiography; AComA: anterior communicating artery; AChoA: anterior choroidal artery; BA: basilar artery; CM: contrast medium; cons: consciousness; F: female; H&K: Hunt and Kosnik; ICA: internal carotid artery; M: male; MCA: middle cerebral artery; mRS: modified Rankin Scale; NA: not applicable; PCoA: posterior communicating artery; SAH: subarachnoid hemorrhage; SCA: superior cerebellar artery; y.o.: years old; WFNS: World Federation of Neurological Surgeons.

Case 1

A 56-year-old woman with a past history of multiple aneurysms in systemic arteries was found unconscious. She had been taking warfarin. Computed tomography (CT) demonstrated subarachnoid hemorrhage (SAH), an intracerebral hematoma around the A2/3 portion of the anterior cerebral artery (ACA), and ventricular enlargement (Figure 1(a)). Three-dimensional CT angiography (3D-CTA) demonstrated an irregular-shaped aneurysm at the left A2/3 junction of the ACA (Figure 1(b)). The aneurysm configuration was composed of a distal oval portion and thin proximal cavity, and the inner surface was smooth on 3D-CTA. After the intravenous administration of menatetrenone and factor IX, an emergency craniotomy was performed. The aneurysm was exposed via the interhemispheric fissure. The round aneurysm was found. However, the wall of the aneurysm seemed to be very thin (Figure 1(c)), and different from that of a common aneurysm. During manipulation of the aneurysm, several points of the lesion ruptured and bled. The aneurysm wall was extremely prone to rupture. The lesion with thin wall was considered to be a pseudoaneurysm covered with connective tissue formed at the rupture point of a true aneurysm. Clipping of the pseudoaneurysm with multiple clips achieved transient hemostasis. Then, the pseudoaneurysm was carefully dissected from the surrounding tissue, and the neck of the true aneurysm was found at the junction of A2/3 behind the pseudoaneurysm. The aneurysm neck was clipped and complete hemostasis was achieved (Figure 1(d)). The portion thought to be the pseudoaneurysm dome was incised and subjected to pathological examination. The examination revealed that the specimen was consistent with a fresh thrombus without an aneurysm wall (Figure 1(e)). These findings indicated that the lesion observed on 3D-CTA was composed of a proximal true aneurysm and distal pseudoaneurysm formed at the rupture point of the aneurysm. The pseudoaneurysm portion was much larger than the true aneurysm. After clipping, an intra-arterial injection of fasudil hydrochloride for vasospasm and ventricle-peritoneal shunt for hydrocephalus were necessary. She was transferred to another hospital for rehabilitation on the 66th day.

Figure 1.

(a) CT demonstrating SAH and intracerebral hematoma around A2/3 of the ACA. An aneurysm is demonstrated as a low-density lesion (arrow). (b) 3D-CTA showing an irregular-shaped lesion at A2/3 (arrow). (c) Intra-operative photograph showing a round and thin-walled portion of the aneurysm. (d) The true aneurysm portion is clipped. (e) Microphotograph showing that the specimen is composed of a thrombus without a vascular wall. Hematoxylin and eosin, ×40.

CT: computed tomography; SAH: subarachnoid hemorrhage; ACA: anterior cerebral artery; 3D-CTA: three-dimensional computed tomography angiography.

Case 2

A 53-year-old man with hypertension developed consciousness disturbance. CT on admission demonstrated SAH and ventricular enlargement (Figure 2(a)). 3D-CTA demonstrated an irregular-shaped aneurysm of the basilar artery (BA) at the bifurcation of the superior cerebellar artery (SCA) (Figure 2(b)). Endovascular treatment was performed immediately after the insertion of a ventriculo-external drainage tube. Angiography demonstrated a snowman-shaped aneurysm of the BA. Opacification of the distal side of the aneurysm was delayed and retention of the contrast medium (CM) was seen (Figure 2(c)). Therefore, the distal part of the aneurysm was considered as a pseudoaneurysm formed at the rupture point of the BA-SCA true aneurysm. The proximal portion of the aneurysm was embolized with a total of 12 platinum coils (Figure 2(d)). Postoperatively, he was treated with propofol to control the intracranial pressure; however, he died five days after embolization.

Figure 2.

CT demonstrating SAH (a), and 3D-CTA (b) showing a BA-SCA aneurysm (arrow) and a cavity (arrowhead) extending from the aneurysm. (c) The distal portion of the aneurysm showing delayed CM filling and washout on angiography. (d) Only the proximal portion of the aneurysm is embolized.

CT: computed tomography; SAH: subarachnoid hemorrhage; 3D-CTA: three-dimensional computed tomography angiography; BA-SCA: basilar artery-superior cerebellar artery.

Case 3

A 43-year-old man without a significant past history was found unconscious. CT demonstrated diffuse SAH (Figure 3(a)). 3D-CTA demonstrated an irregular-shaped aneurysm at the portion of the anterior communicating artery (AComA) (Figure 3(b)). Angiography demonstrated an aneurysm at AComA (2.7 × 2.2 × 2 mm) (Figure 3(c)). The irregular-shaped aneurysm observed on 3D-CTA was diagnosed as a pseudoaneurysm formed at the rupture point of a true aneurysm, or the extravasation of CM. The aneurysm was embolized with four platinum coils. Several loops of the second coil protruded into the pseudoaneurysm cavity (Figure 3(d)). Twenty-seven days after onset, a right ventriculo-peritoneal shunt operation was performed. Sixty-three days after the first endovascular treatment, additional endovascular treatment was performed because of coil compaction. This may have been because the aneurysm with pseudoaneurysm had shrunk during the acute stage of aneurysm rupture. He was transferred to another hospital for rehabilitation with mild right hemiparesis 72 days after onset.

Figure 3.

(a) CT demonstrating SAH. (b) 3D-CTA demonstrating an irregular-shaped aneurysm cavity at AComA. (c) Angiography demonstrating an aneurysm at the AComA (arrow). However, an irregular-shaped additional cavity observed on 3D-CTA is not demonstrated. (d) The true aneurysm portion is embolized with platinum coils. A few loops of coils protrude outside the aneurysm.

CT: computed tomography; SAH: subarachnoid hemorrhage; 3D-CTA: three-dimensional computed tomography angiography; AComA: anterior communicating artery.

Case 4

A 73-year-old woman was found unconscious. She had suffered from SAH four years ago, and a ruptured BA tip aneurysm had been embolized in another hospital. CT on admission revealed SAH with ventricular rupture and hydrocephalus (Figure 4(a)). Emergency angiography demonstrated a partially embolized aneurysm at the BA tip. After embolization of the anterior part of the aneurysm, the posterior protrusion (4.5 × 3.5 × 3 mm) was still opacified with CM. Continuing from the posterior portion of the aneurysm, a cavity with delayed opacification and retention of CM was observed protruding to the right (Figure 4(b)). This portion was considered as a pseudoaneurysm formed in the thick SAH. The portion of the true aneurysm was embolized with seven platinum coils. After embolization, the pseudoaneurysm portion was not opacified (Figure 4(c)). During the procedures, only the true portion was embolized, and care was taken not to insert the coils into the pseudoaneurysm portion.

Figure 4.

(a) CT showing SAH. (b) Angiography demonstrating a cavity protruding to the right from the recurrent BA tip aneurysm. Angiography showing delayed filling and washout of CM in the additional cavity. (c) Post-embolization angiography demonstrating complete obliteration of the aneurysm and disappearance of the pseudoaneurysm.

CT: computed tomography; SAH: subarachnoid hemorrhage; CM: contrast medium.

Discussion

Pseudoaneurysm formation at the rupture site of a non-traumatic cerebral aneurysm is extremely rare.^3,4 A pseudoaneurysm is formed in a blood clot adhering to the rupture point. There are several reports describing cerebral pseudoaneurysms.^3–12

Recently, we encountered four additional patients with pseudoaneurysms. One patient with an A2/3 aneurysm (Case 1) was treated by direct clipping, and three other cases (Cases 2–3) with BA and AComA aneurysms were treated with an endovascular technique. For Case 1, preoperative 3D-CTA clearly showed a round lesion with a proximal stem-like portion. The small proximal portion continued from the parent artery, and the initial diagnosis was a large aneurysm. In this case, preoperative 3D-CTA showed features of a pseudoaneurysm. For the other three cases with pseudoaneurysms, endovascular treatment was performed. In Case 2, the pseudoaneurysm was observed on both 3D-CTA and angiography. In Case 3, the pseudoaneurysm was observed on preoperative 3D-CTA, but not on angiography. The pseudoaneurysm cavity continued from the AComA true aneurysm. This pseudoaneurysm cavity might be a space formed in a thick SAH. In the fourth case with a previously embolized aneurysm, a pseudoaneurysm was detected on angiography. In Cases 2 and 4, opacification of pseudoaneurysms were faint on angiography. As mentioned above, a pseudoaneurysm can be detected with both 3D-CTA and angiography. However, it cannot always be detected with both modalities at the same time. These variations might be due to differences in the timing of examinations, intracranial pressure, and injection power of the CM.

We initially reported that the radiological findings of the pseudoaneurysms were irregular aneurysm wall, delayed opacification of the lesion, and delayed washout and retention of the CM.³ Ide et al.⁴ reported a pseudoaneurysm case with a snowman-like appearance. Mori et al.⁵ additionally reported radiological characteristics such as delayed appearance, late opacification, changing shape, and retention of the CM after venous phase. They proposed calling the aneurysm with pseudoaneurysm a “ghost aneurysm.” Other reports described similar radiological findings, unequal filling or outpouching of the CM, and unclear neck^6–12 as shown in Table 1. These radiological features are identical to those of traumatic pseudoaneusyms.^1,2 Even though the etiology is different, a pseudoaneurysm is composed without a vascular wall. A pseudoaneurysm due to a ruptured cerebral aneurysm is located in the thrombus. Therefore, the pseudoaneurysm wall is very weak and prone to rupture during manipulation. Special care of the pseudoaneurysm portion is necessary during operation procedures.

The pseudoaneurysm at the tip of the true aneurysm was formed in the thick SAH or intracerebral hematoma. Mori et al.⁵ described that an extraluminal hematoma may recanalize or remain in communication with the true aneurysm arising from the parent artery. Therefore, for pseudoaneurysm formation, thick hematoma around the aneurysm is necessary. D’Urso et al.⁸ reported a case of AComA aneurysm, in which a pseudoaneurysm newly developed after the second bleeding. Initial SAH around the AComA aneurysm was thin. The second rupture resulted in a sufficient amount of SAH for a pseudoaneurysm to be formed. In fact, in cases of aneurysms accompanied by pseudoaneurysms, SAH was thick, including a pseudoaneurysm cavity in the hematoma. Therefore, most of the cases with pseudoaneurysms were in a severe state with abundant SAH. Our four cases were graded 3–5 on the Hunt and Kosnik (H&K) scale of SAH grading. And in a previous 11 cases with detailed description, nine were graded more than 3 of H&K or World Federation of Neurological Surgeons (WFNS) grading. In cases with thick hematoma, if the aneurysm possesses an unusual radiological countenance, pseudoaneurysm formation should be taken into consideration. For cases with pseudoaneurysms, accurate diagnosis and appropriate treatment are mandatory.

As for location of the aneurysm with pseudoaneurysm, 41.7% of the lesions were located at the AComA, followed by 16.6% each of the middle cerebral artery (MCA) and the internal carotid artery (ICA). Incidence of pseudoaneurysm occurring in the AComA is almost twice the distribution of common AComA aneurysms. In cases with AComA aneurysms, thick hematoma may be formed around the aneurysm in the interhemispheric fissure. Interhemispheric fissure is usually tight compared to Sylvian fissure and carotid cistern. Atrophic change around the AComA is usually less than that of the superficial brain. And further, the parent arteries are complex. Around an AComA aneurysm, there are at least four normal arteries. These anatomical features may contribute to form localized thick hematoma around the AComA and further pseudoaneurysm.

Concerning treatment for an aneurysm with a pseudoaneurysm, among 24 cases including ours, 11 cases were treated by direct clipping and the 13 other cases underwent endovascular treatment. Advancement of endovascular technique enabled us to treat cerebral aneurysms with pseudoaneurysms safely. Reports describing the usefulness of endovascular embolization have been published.^9,11,12 In these reports, only the true portion of the aneurysm was embolized with platinum coils in most cases. In one case reported by Ito et al.,¹² both true and pseudoaneurysm were embolized on day 9. The authors described that fibrosis might occur around the pseudoaneurysm in the nine days after onset, and possibility of rupture during procedure might decrease. Our three patients underwent endovascular embolization on day 0, and the true aneurysm was embolized, which resulted in the successful disappearance of the lesions. For direct surgery, if the aneurysm neck is easily recognized before manipulating the pseudoaneurysm portion, direct clipping might be performed safely as in Case 16.¹⁰ However, if the pseudoaneurysm portion is shallow in the operative field, observation of the true portion behind the large pseudoaneurysm is difficult. As in Case 1 of our series, the pseudoaneurysm portion is very fragile and easy to bleed. Manipulation of the pseudoaneurysm before exposure of the true aneurysm neck resulted in intraoperative hemorrhage. For such a case, direct clipping might not be easy, and endovascular embolization may be a suitable treatment. Or an operative approach to be able to expose the true aneurysm prior to the pseudoaneurysm portion should be selected.

Conclusion

Pseudoaneurysm formation after rupture of an intracranial aneurysm is rare. However, in a case with an irregular-shaped aneurysm cavity, pseudoaneurysm formation should be taken into consideration.

Conflict of interest

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.