the SAH. Aneurysms located adjacent to the ventricular systems, including ACoA and those of the posterior circulation, tend to cause IVH, and PCoA aneurysm sometimes presents as subdural hematoma (SDH) albeit rarely.9)19) In addition to the specific locations, time interval between rupture and subsequent radiographic acquisition might be responsible for non-visualization of SAH. In spite of the above factors, rapid detection and management of the ruptured aneurysm should be attempted to achieve definite
occlusion and to prevent further bleeding and progressive brain damage.
We describe 9 cases of such non-SAH intracranial bleeding due to the aneurysmal rupture with special
emphasis on their clinical and radiographic characteristics, operative methods (clipping or endovascular occlusion), and ultimate outcome. In doing so, some crucial, but easily overlooked clues or pitfalls can be reminded.
Material and Methods
From our aneurysm registry, a total of 341 patients who had been admitted as a diagnosis of ruptured aneurysms were identified during the period between July 2003 and June 2007. Among them, 273 patients underwent surgical treatment (242 microsurgical clipping and 31 endovascular embolization) while remaining 68 patients did not receive further treatment due to either poor clinical condition (deep coma, severe co-morbidity hampering operative intervention; n=49) or immediate family member's refusal (n=19). Of these 341 patients with ruptured aneurysms, 332 patients showed SAH, and 9 patients (2.6%) showed non- SAH intracranial bleeding.
For the purpose of this study, SAH is defined as hemorrhage within the cisterns, sulci, or convexities instead of parenchymal or ventricular hemorrhage. Emergency
physicians and attending neurosurgeons all agreed with CT findings of these 9 patients that they showed non-SAH intracranial bleeding. Then after CT angiography (CTA) or
transfemoral catheter angiography (TFCA), ruptured aneurysm should have been identified to fulfill the criteria. For these 9 patients, a retrospective study was conducted by using medical charts, emergency room notes and radiographic images. Based on the factors regarding age, sex, mode of presentation, initial neurologic grade, comorbidity, characteristic features of the aneurysms, CT and angiographic findings, treatment methods, concomitant medical or pathophysiological conditions, final outcomes
were retrieved. The outcome was assessed on the basis of Glasgow outcome scale (GOS) at postoperative 6 months.
Results
According to Table 1, mean age of the patients was much younger than that of SAH patients; 42.56 years (range, 28 - 63) and female-to-male ratio was 4:5. Except for one case of moyamoya syndrome, all patients exhibited ICH on initial CT scans, and among these 8 patients, IVH was accompanied in two patients and SDH in three patients. Hemorrhage was identified on the right hemisphere in 5 patients, and on the left side in 4 patients. Except for one case, initial clinical grade was grave in 8 patients (Hunt-Hess grade Ⅳ and Ⅴ). Pertaining to aneurysm locations, all of them arose at the anterior circulation. Two cases were located around the circle of Willis including PCoA and proximal ACA, and remaining 7 cases were located in more distally beyond the circle of Willis, such as 1 MCA
bifurcation, 4 distal MCA, 1 distal ACA, and 1 distal anterior choroidal artery (AchA). The causes of the
aneurysms were spontaneous in 4, trauma in 2, infective endocarditis in 2, and moyamoya syndrome in 1 patient, respectively. In 8 cases, head CT scans were obtained on the day of rupture, and on the next day to the ictus for the remaining case. In one case of delayed rupture, aneurysm was identified on 50th day from the initial head injury. In another case of distal ACA aneurysm, hematocrit was low (22%) due to the underlying renal failure, but intraoperative finding confirmed the lack of SAH.
As for the radiographic examination, CTA did not always identify ruptured aneurysms. In 3 cases, TFCA was mandated to confirm the presence of the aneurysms in addition to the CTA. Among them, 2 cases had infective endocarditis as a causative lesion, and in only 4 patients, aneurysms could be found at the initial clinical attention. The causes of delayed diagnosis were infective endocarditis in 2 patients, delayed traumatic rupture in 1, spontaneous in 1 and moyamoya syndrome in 1 patient. All patients had
treatment including 6 cases of craniotomy and clipping or trapping and 3 cases with endovascular occlusion. During microsurgical operation, intraoperative rupture was noted in 3 patients (50%), and all these aneurysms had laterally projecting fundus. Outcome was favorable in 4 patients at postoperative 6 months. Two patients died, and their causes of death were the impact of initial large hematoma and
multiple organ failure, respectively. Remaining three patients did not recover and still remained as a persistent vegetative state.
Illustrative Cases
Case 1
A 48-year-old man without significant prior medical history was brought in to the emergency room for sudden unconsciousness. On admission, he was semicomatose and showed non-reactive pupils and left hemiparesis (Grade 2/3) with extensor rigidity. An initial head CT scan showed a huge ICH and acute SDH on the right temporal region with significant midline shift (Fig. 1A and B). Subsequent CT
angiography showed an aneurysmal sac at the right PCoA with laterally projecting fundus (Fig. 1C). Microsurgical clipping was intended. Following right pterional craniotomy and dural reflection, intraoperative rupture was encountered and rapid corticectomy with retraction of temporal lobe
made the aneurysm clipping ameanable. He regained consciousness in the following days and made a gradual neurologic recovery (Fig. 1D). After successful rehabilitation, he walked without aid and was discharged from hospital. At last follow-up visit, he was free of any neuro-cognitive deficits.
Case 2
A 31-year-old woman physician was found unconscious at restroom. She was semicomatose, spastic quadriparetic and showed fixed non-reactive pupils. There was no similar episode prior to this incident. A initial head CT scan revealed a pure IVH (Fig. 2A). Because of rapid deterioration, emergency ventriculostomy was performed, but catheters were plugged with blood soon afterward. A CT
angiography showed increased amount of IVH and an aneurysm at the right distal AchA adjacent to trigone with feature of contrast extravasation (Fig. 2B, C and D). An ample temporoparietal craniotomy was created, and then a bilobed 5 mm aneurysm was found at the ventricular entrance of the right distal AchA. It was resected after trapping of the terminal AchA, and hematoma was evacuated. On the next day, catheter angiography was conducted to reveal moyamoya vessels in both hemispheres, but the aneurysm was already resolved (Fig. 2E). After three weeks from the surgery, she became fully awakened and was able to walk without aid.
Discussion
Initial presentation of a ruptured aneurysm as intracranial hemorrhage without SAH is a quite unusual phenomenon.2)4)5)7)9)14)18)
Thus, the incidence of 2.6 % in this series is not comparable to the other reports because there is
no accepted reference value or no large-cohort study, thus, it could not have sufficient consensus for solid definition. Although such cases are very limited in numbers or even anecdotal, ruptured cerebral aneurysm undoubtedly had presented as ICH, IVH, or acute SDH without SAH.8~10)16)19)
These conditions are possible to exist and should not be neglected or underestimated. In such cases, straightforward surgical decompression such as simple hematoma evacuation or extraventricular drainage is not curable although it provides temporary neurologic improvement. The brain is under a continuous threat of possible repeated bleeding into the same site, therefore, accurate diagnosis is essential to
attain total occlusion of the lesion.
Causes of non-SAH bleeding : with regard to the geometry of the aneurysm
Several possible etiologies of non-SAH bleeding can be addressed such as location of the aneurysm, timing of CT acquisition or physiological parameters.19)20)
Irrespective of the underlying pathophysiologic process of formation and rupture of the aneurysm, non-SAH bleeding is closely related to specific location of the aneurysm as described previously.9)11)19) The location of aneurysms can sometimes predispose them to direct bleeding into the parenchyma or
ventricular system. When considering the proximity of the location of the MCA or PCoA aneurysms to the temporal lobe, which is the weakest portion of resistance, it would directly rupture into the temporal lobe.19) In this series, one PCoA and 4 MCA aneurysms showed hemorrhages directly into the temporal lobe. All the aneurysms had laterally projecting fundus, and this feature supports the theoretical
basis of temporal lobe ICHs. Besides temporal lobe ICH, our series showed that the aneurysms of the distal ACA, proximal ACA and peripheral MCA exhibiting frontal ICH due to embedding of the aneurysm within the surrounding parenchyma.
In addition to the location of the aneurysm, main direction of arterial flow, i.e. direction of fundus with rupture into the weakest point of resistance, also seems to be a major factor for determining ICH location. For this reason, intraoperative rupture is frequently encountered during the hematoma
evacuation, with an incidence (rate) of 50% (3 out of 6 microsurgery) in this series. Moreover, it makes
microsurgical clipping more perplexing and dangerous. If a patient tolerates TFCA and endovascular intervention, early dome protection with coils and subsequent deliberate hematoma evacuation might be a strong alternative to direct clipping. Niemann et al.13) recommended that coil insertion prior to clot evacuation protects against aneurysm rupture and obviates the need for extensive dissection and retraction, thus, making the surgical procedure simpler and safer. By this protocol, he attained overall mortality of 21%, with a favorable outcome of 48%.
Causes of non-SAH bleeding : with regard to the etiology and location of the aneurysm In previous studies, it has been reported that the incidence of distal MCA aneurysms ranged from 2 to 4% of total
aneurysms.17)
Distal MCA aneurysms frequently result from infection caused by mycotic emboli and severe traumatic
brain injury.6) Infectious aneurysms are usually associated with endocarditis and occur most frequently on the MCA or its distal branches and less commonly on the posterior and anterior cerebral arteries.12) In such cases, angiography helps both in diagnosis and follow-up after antibiotic therapy or intervention to demonstrate total occlusion or detect newly developed lesions.3) Because infectious aneurysms, in almost
all cases, are extremely friable pseudoaneurysms, careful handling is mandated during microsurgical or endovascular management. In this series, two patients suffered from extravasation: one during CT angiography and the other during endovascular treatment. All these patients had pseudoaneurysms, and this extravasation was attributed to the incomplete vascular integrity. Therefore, extremely cautious
approach is required, if intervention is ever attempted.
Seven out of nine patients (77.8%) had peripheral aneurysms distal to the circle of Willis. Among these seven patients, aneurysms were located at the MCA system in 5 (one bifurcation, and 4 cortical branches), at distal ACA in one, and at distal AchA in one patient. With regard to the underlying mechanism, infectious endocarditis was responsible for aneurysm in 2 patients, trauma in 1, and
moyamoya syndrome in one patient respectively, and the remaining 3 patients spontaneously developed aneurysms. In traumatic brain injury, patient with peripheral MCA aneurysm, pathogenic mechanism is known to be nonpenetrating and has conditions such as a blunt type linear skull fracture, cortical contusion and acute SDH. When disproportionately huge ICH and/or acute SDH are combined with skull fracture in immediate resuscitation CT scan, associated vascular injury should be sought. Sentinel
hemorrhage or warning leak was observed in two patients, who both complained a headache in 1 to 2 weeks prior to the rupture. With relevant to the specific etiology, peripheral location, or warning leak, there was no practical clue to suspect the presence of an aneurysm or to render them to visit neurologic clinic.
Other causes of non-SAH bleeding on CT scan A CT imaging acquisition in quite early period of time
(within 6 hours from the onset) or delayed period of time (> 3 days) may not sufficiently display SAH. Because red blood cells are diluted with the cerebrospinal fluid, hemorrhage appears to be isodense to the brain parenchyma.20)
In this series, except for one patient with distal ACA aneurysm (Case No. 5) who underwent CT scan on next day to the ictus, all patients underwent CT scan within 6 hours from the onset. Because there were huge hemorrhages in their initial CT scans, it is more likely to be determined as other intracranial hemorrhages than SAH. In a patient with a low hematocrit or hemoglobin concentration, a CT scan may not exhibit hemorrhage. In this series, one patient (Case No. 5) had anemia (hematocrit 22) due to chronic renal failure. Intraoperative findings confirmed pure ICH on the frontal lobes with anterior and
lateral direction of the aneurysmal fundus. A CT scan acquisition time and innate patient’ physiologic factor hampering proper visualization of SAH did not influence in this series.
The occurrence of SAH associated with the acute SDH due to cerebral aneurysms varies from 0.5 to 7.9%, but pure acute SDH from ruptured aneurysm is extremely rare.8)14)16)
Some mechanisms have been proposed to explain the occurrence of acute SDH after aneurysm rupture. First, the aneurysm adherent to the arachnoid may directly bleed into the subdural space when the arachnoid tearing occurs soon after the aneurysm ruptures. Second mechanism is due to a
hemorrhage under high pressure, leading to pia-arachnoid rupture and extravasation of blood into the subdural space.10)
The most frequent site of aneurysm rupture that causes acute SDH is the origin of PCoA followed by the distal ACA and MCA.9) There were three patients exhibiting acute SDH in this series, where the patients developed spontaneous PCoA aneurysm, MCA bifurcation aneurysm from severe head trauma and distal MCA aneurysm from infective endocarditis. Relationship of the location of ruptured aneurysm to the adjacent dura is, thus, the most important factor that causes acute SDH. Conclusively, if a patient,
whether he or she has history of head trauma or not, shows a disproportionately massive acute SDH, a ruptured aneurysm should be considered as a possible source of bleeding, regardless of presence of SAH.
Who needs angiography? Factors that can increase the likelihood of aneurysm detection on cerebral angiography are reported as the presence of pure SAH, a history of hypertension, and age less than 50 years.1)15)
Zhu et al.21) also reported that a significantly higher incidence of vascular lesions in patients
less than 45 years old age and in those without preexisting hypertension. Angiography should be considered even when young, normotensive subject exhibits putaminal ICH because of possible microaneurysm.7)
The causes of delayed diagnosis and treatment were mainly related to overlooking the underlying
pathophysiologic process; infective endocarditis, traumatic brain injury, and moyamoya vessels. Only high index of suspicion can render detection of the ruptured aneurysm possible. And, in doing so, additional intervention might be avoided and source of bleeding can be eliminated.
Conclusion
Aneurysm rupture should be suspected even when there is no SAH, and cause of bleeding is not explained where the patient is in young age, shows no sign of hypertension, have unusual bleeding site, and also have history of infection.
Especially when infective endocarditis is present, or hemorrhage is disproportionately massive following head injury, there is likely chance to have aneurysm rupture.
When these situations are encountered, catheter angiography should be performed for the definite diagnosis and management. As shown in the current series, most of
patients exhibit poor neurological grade. To circumvent tragic consequences due to delayed diagnosis, careful interpretation of radiographic images and strong suspicion of
clinical situation should be placed prior to prompt management. The diagnosis also should be kept in mind while interpreting angiography and making preoperative
planning for evacuation of ICHs, IVHs, or acute SDHs.
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