Surgical Intervention of Intracerebral Hematoma Caused by Ruptured Middle Cerebral Artery Aneurysm in Neurosurgery Teaching Hospital, Baghdad, Iraq
Keywords: Aneurysm, intracerebral hematoma, middle cerebral artery, neurosurgeryKey Messages: The milestone of treating intracerebral hemorrhage due to Middle cerebral artery ruptured aneurysm is the early surgical intervention.
Intracerebral hematoma (ICH) due to rupture of intracranial aneurysm (IA) occurs in 10%–38% of cases with subarachnoid hemorrhage (SAH). It is commonly accepted that aneurysmal ICH complicates the natural course of the disease and is connected to increased morbidity and mortality. The mass effect caused by the hematoma might lead to a prolonged intracranial pressure known as one of the possible contributors to early brain injury (EBI). Aneurysms of the anterior circulation especially located in the middle cerebral artery (MCA) but also in the anterior cerebral artery (ACA) have been identified as risk factors for ICH occurrence.
Middle cerebral artery (MCA) aneurysms are most likely to result in an intracerebral and intrasylvian hematoma after their rupture., Early surgical management has been advocated, although few studies have focused on the outcome of patients with ruptured MCA aneurysms and concomitant ICH. It is important to explore different prognostic factors in this patient population to elucidate the optimal management strategy.
Autopsy series tend to report a higher incidence of 33%–60%.,
Acute hematoma evacuation without managing the aneurysm has demonstrated slightly better results, with mortality rates up to 75%. Patients who survive may suffer late epilepsy, severe hemiparesis, and visual deficits.
Several factors may predispose an aneurysm to rupture into the brain parenchyma. The main factor maybe the location of the aneurysm. The aneurysms located between cerebral cortices tend to hemorrhage into the parenchyma. If the rupture site is adherent to the pia mater, ICH may occur without any evidence of SAH.
ICH associated with a ruptured aneurysm tends to lead to higher HH grades on admission and less favorable 6-month outcome.
Middle cerebral artery aneurysms (MCA aneurysms) belong to the most frequent category of intracranial aneurysms. If treated adequately, including operative tactics and microsurgical techniques, a significant proportion of patients can achieve a favourable outcome. An MCA aneurysm with an intracerebral hematoma is one of the neurosurgical emergencies with an uncertain outcome.
Nonoperative management is nearly universally fatal, whereas prompt hematoma evacuation and aneurysm clipping can improve short- and long-term outcomes. MCA aneurysms are, in general, considered surgical lesions, and historical and modern outcomes after microsurgical clip obliteration are excellent. Ruptured MCA aneurysms with a temporal lobe or sylvian fissure hematomas can cause early uncal herniation and, as such, are imminently life-threatening. See [Figure 1] for cases examples.
We analysed 21 patients with intracerebral hematoma caused by ruptured middle cerebral artery aneurysm presented to the Neurosurgery teaching hospital in Baghdad, Iraq from January 2017 to January 2019. Parameters included five broad categories: demographic, clinical, radiological, surgical, and outcome.
Demographic: age and sex.
Clinical: Initial GCS, sudden severe headache, contralateral weakness (MRC grade), cranial nerves, vomiting, meningism, seizure, speech (dysphasia), history of hypertension, history of DM and previous attacks (minor hemorrhage), H and H grade, WFNS grading, coagulopathy or antiplatelet or anticoagulant drugs.
Radiological: ICH size/cc, midline shift, SAH, IVH, dilated ventricles, modified Fisher grade, MCkA aneurysm location, aneurysm side (right vs. left), aneurysm dome size/mm, aneurysm neck size, aspect ratio, Murphy's teat, other aneurysm, dome projection, and CT angiography vasospasm.
Surgical: rupture to surgery time/hours, No. of clips, duration of surgery/hours, temporary clipping, and intraoperative rupture.
Outcome and follow-up: postop GCS, postop weakness, postop vasospasm, postop seizure, remnant of postop CT angiography, days of admission, GOS on discharge, and GOS at 2-month follow-up.
Descriptive statistics were done for all variables with mean and standard deviation for continuous variables. Graphs were done showing initial GCS, postop GCS, GOS at discharge, and GOS at follow-up. Normal distribution of the data was assessed with the Shapiro–Wilk test. Frequency tables were done showing clinical, radiological, surgical and outcome and follow-up parameters. Wilcoxon signed-rank test used to assess the difference between initial and postop GCS and the difference between GOS at discharge and GOS at 2-month follow-up. Spearman's Rho used to show the correlations of the parameters with GOS at discharge and at 2-month follow-up. A regression model was used to check which one is real. All graphs were designed using Microsoft word office 2010, and all statistical analyses were performed using SPSS statistics (version 25, IBM) at a level of significance (P ≤ 0.05) with confidence intervals 95%.
Descriptive statistics of the studied parameters
The results of this study showed that out of 21 patients, there were 15 (71.4%) males and 6 (28.6%) females. The age of the patients distributed from 30 to 60 years (mean age 43 ± 6.993 years). About clinical parameters, the initial GCS was distributed between 7 and 15 with a mean equals 13 [Figure 1], the frequency of initial GCS, sudden severe headache, contralateral weakness (MRC grade), cranial nerves, vomiting, meningism, seizure, speech (dysphasia), history of hypertension, history of DM, and the previous attacks (minor hemorrhage) were all demonstrated in [Table 1].
About the radiological parameters, the CT findings were all 21 patients had intracerebral hematoma and the size of hematoma with a mean volume of 20.67 ± 9.552 cc (range: 4–45 cc), mean aneurysm dome size was 8.33 ± 1.623 mm (range: 6–11 mm), and mean of its neck was 4.19 ± 0.68 mm (range: 3–5 mm). The frequencies of ICH, midline shift, SAH, IVH, dilated ventricles, H and H grade, modified Fisher grade, WFNS grading, coagulopathy or antiplatelet or anticoagulant drugs, MCA aneurysm location, aneurysm side, aneurysm dome size, aneurysm neck size, aspect ratio, Murphy's teat, another aneurysm, dome projection, and CT angiography vasospasm were all demonstrated in [Table 2].
About surgical parameter, the mean duration of surgery was 3.14 ± 1.236 h (range: 2–6 h) and mean of rupture to the surgery time was 23.33 ± 23.193 h (range: 3–72 h). The frequencies of rupture to surgery time, number of clips, duration of surgery, temporary clipping, and intraoperative rupture were demonstrated in [Table 3].
About the outcome and follow-up, the postop, the mean GCS was 14 (range: 6–15), the mean of day of admission was 7 days (range: 4–16), mean of GOS at discharge was 4.2 (range: 1–5), and mean GOS at 2-month follow-up was 4.6 (range: 1–5). The frequencies of the postop GCS, postop weakness, postop vasospasm, postop seizure, the remnant of postop CT angiography, days of admission, GOS on discharge [Figure 2] and GOS at 2-months follow-up [Figure 3] were demonstrated in [Table 4].
GCS and GOS
There were significant differences between initial GCS and postop GCS (P-value = 0.022); in addition, there were significant differences between GOS at discharge and GOS at 2-months follow-up (P-value = 0.008) [Figure 2].
Correlations of the parameters with the GOS at discharge and at follow-up
There was a significant correlation of contralateral weakness with GOS at discharge (P = 0.007) and with the GOS at follow-up (P = 0.0.12). All patients had a sudden severe headache, so it assumed as a constant variable. The correlation coefficient (r) and P values of the clinical parameters with the GOS at discharge and with the GOS at 2-months follow-up were demonstrated in [Table 5].
About the radiological parameters, there were strong correlations of ICH size, IVH, and dilated ventricles with the GOS at discharge (P = 0.009, P = 0.007, and P = 0.007, respectively), while there were significant correlations of modified Fisher and aneurysm side with the GOS at 2-months follow-up (P = 0.012 and 0.001, respectively). There was no one had coagulopathy or taking antiplatelet or anticoagulant drugs, and MCA aneurysm location was on M1 bifurcation in all patients, so they were assumed as constant variables. The correlation coefficient (r) and P values of radiological parameters with the GOS at discharge and with the GOS at 2-months follow-up were demonstrated in [Table 6].
About the surgical parameters, there were significant correlations of the duration of surgery, rupture to surgery time, and intraoperative rupture with the GOS at 2-months follow-up (P = 0.017, P = 0.013 and P = 0.036, respectively), while there was no correlation of any surgical parameters with the GOS at discharge. The temporary clipping had been done for all patients so it was assumed as a constant variable. The correlation coefficient (r) and P values of the surgical parameters with the GOS at discharge and with the GOS at 2-months follow-up were demonstrated in [Table 7].
About surgical parameters, there was a strong correlation of the GOS at discharge with the GOS at 2-months follow-up (r = 0.577: P = 0.006); there was remnant of postop CT angio in all patients, so, it was assumed as a constant variable. The correlation coefficient (r) and P values of outcome and follow-up parameters with the GOS at discharge and with the GOS at 2-months follow-up were demonstrated in [Table 8].
The regression model assessed the relations between the parameters and the GOS at discharge and the GOS at 2-months follow-up; there were significant relations of 10, 11, 12, and 13 scores of initial GCS with the GOS at 2-months follow-up. For the radiological parameters, there was a significant relation of 4 in modified Fisher (P = 0.014) with GOS at 2-month follow-up. For surgical parameters, there was a significant relation of 6 h as the duration of surgery with the GOS at 2-month follow-up (P = 0.001). For outcome and follow-up, there were significant relations of 6 and 8 scores of postop GCS with the GOS at 2-months follow-up (P = 0.001). Other P values of parameters' relations with the GOS at discharge and the GOS at 2-months follow-up were demonstrated in [Table 9].
The incidence of ICH among patients with aneurysmal SAH ranges from 12%–34%. Autopsy series tend to report a higher incidence of 33%–60%. The presence of an aneurysm with ICH negatively influences the patient's presentation, course, and outcome, and may be associated with an increased rehemorrhage rate, vasospasm, cerebral edema, and hydrocephalus. Yoshimoto et al. analyzed 41 patients with ruptured MCA aneurysms with intraparenchymal hematoma larger than 30 mL and reported favourable outcomes in 28 patients (68.2%) after hematoma evacuation and aneurysm clipping. Although these data are encouraging, the study did not report the mean hematoma volume, and only 5 (12.2%) patients were Hunt and Hess grade V on presentation.
Although previous reports have demonstrated that patients with aneurysmal SAH with associated intraparenchymal hematomas present with worse Hunt and Hess grades and have poorer functional neurological outcomes than patients with SAH alone. Focusing specifically on MCA aneurysmal rupture, Yoshimoto et al. believed that the clinical-grade on admission for patients with an ICH _30 mm significantly correlated with a poor outcome. Prat and Galeano reported that a worse outcome (World Federation of Neurological Surgeons Scale [WFNS] 4–5) for patients with anisocoria at presentation, While our study showed that the preoperative Hunt and Hess grades is NOT significantly correlated with the outcome in patient with intracerebral Hematoma caused by ruptured Middle Cerebral Artery Aneurysm. Instead, our study showed that several preoperative parameters have a significant impact on the final outcome and we found that the preoperative cranial nerves deficit, dysphasia, more severe contralateral weakness, presence of dilated ventricles, IVH and higher Modified-Fisher grade can be considered as a poor prognostic factor. In addition, we found that the high initial GCS significantly correlated with a good outcome.
Recent studies focused on the identification of additional patient- and aneurysms–related risk factors for aneurysmal ICH. Premorbid conditions like arterial hypertension, diabetes and smoking as well as administration of antiplatelet drugs prior to ictus have been correlated with ICH occurrence. It has been reported that SAH patients with an additional ICH are more likely to present with the poor initial clinical condition and develop rebleeding prior to treatment., In larger aneurysms, size, location in the MCA and administration of aspirin prior to the bleeding event have been mentioned as risk factors for larger ICH volume in one study,,
The incidence of intracranial aneurysm ranges from 0.4-6%. Rupture of an intracranial aneurysm commonly results in subarachnoid hemorrhage (SAH), but may also lead to hematoma formation. Locksley found that 90% of the patients who died within 3 days of the onset of an aneurysmal SAH harbored an intracerebral hematoma (ICH).
Brott and Mandybur determined that the extent of hemorrhage correlated better with clinical outcome than the patient's presenting neurologic status.
Focusing specifically on MCA aneurysmal rupture, Yoshimoto et al. believed that the clinical grade on admission for patients with an ICH 30 mm significantly correlated with a poor outcome. Prat and Galeano reported a worse outcome (World Federation of Neurological Surgeons Scale [WFNS] 4–5) for patients with anisocoria at presentation. For a similar population, Niemann et al. reported a mortality rate of 24% (6 of 25) and a favorable outcome of 44% (11 of 25). Hauerberg et al. observed a favourable outcome in 33% (30 of 90) of patients, whereas 43% (39 of 90) died.
When compared to ruptured MCA aneurysms without ICH, the final outcome is worse. However, the patients in such a condition are considered potentially salvageable unless they have long-lasting bilateral mydriasis. Natarajan et al. present a modified Rankin score 0–2 in 42% of patients in all aneurysm locations with ICH and a mortality rate of 31%. Prat documented that evacuation of an ICH larger than 20 mL in volume is associated with a good result in about 50% of cases. In fact, of the 704 MCA aneurysms evaluated in the ISUIA (International Study of Unruptured Intracranial Aneurysms), 650 (92.3%) were microsurgically clipped, whereas only 54 (7.7%) were endovascularly coiled. Similarly, in the BRAT (Barrow Ruptured Aneurysm Trial), treatment crossed over to microsurgical clip obliteration in 21 (67.7%) of the 31 MCA aneurysms initially assigned to endovascular coil embolization. These data reflect the widespread knowledge that clinical and radiographic outcomes after microsurgical clipping of MCA aneurysms are excellent, with modern surgical series demonstrating occlusion rates exceeding 99%. Four complete radiographic occlusion rates after endovascular coiling, in contrast, are approximately 82%, and assist devices may be required for complete occlusion.
Our study showed that aneurysm located on the left side considered as a poor prognostic factor with statistically significant correlation. Similarly, Navratil et al. found ICHs on the right in their series are significantly larger than if localized in the left hemisphere. However, there was no statistical difference in outcome between the sides. They did not find an explanation for this, and the literature dealing with this topic is scarce. Possibly, the right hemisphere could tolerate larger ICHs with the same outcome.
In addition, we found there were strong correlations of ICH size, IVH, and dilated ventricles with the GOS at discharge, indicating a poor prognosis. Baskaya et al. also reported similar findings.
For surgical parameters analysis, we found that there are significant relations between the duration of surgery, time between rupture of aneurysm to the time of surgery, and intraoperative rupture with the GOS at 2-months follow-up with P value = 0.017, P = 0.013, and P = 0.036, respectively, with the duration of surgery more than 6 h and the occurrence of intraoperative rupture related significantly with poor outcome. While there was no correlation of other surgical parameters as a number of clips used, use temporary clip duration of the surgery with GOS at discharge and after two months.
Regarding the postoperative complications, we found that the poor postoperative GCS, occurrence postoperative vasospasm, more severe postoperative contralateral weakness, and the presence of postoperative seizure significantly correlated with poor outcome. The literature is scarce concerning this topic.
Tokuda et al., Niemann et al., Hauerberg et al., and Pasqualin et al. reported mortality rate of 25%, 24%, 43%, and 38%, respectively. Our study showed only 9.5% mortality rate; this finding may be related to the small sample size and the criteria of selection the patient for surgical intervention. None of the previous studies evaluated the outcome in detail using the GOS.
Pasqualin et al. and Guresir et al. believed that the most important factor is the time to treatment with an early surgery within 12 h of hemorrhage related to a favourable outcome. Other investigators have emphasized a time limit of six hours for surgery and achieved good results., In our study, the rupture to the surgery time was between 3 h to 72 h (mean equals 23.33 h) with 61.9% of surgeries done within the first 24 h from rupture and based on the outcome of our study, we advocate the implication of early surgery within the first 72 h before the vasospasm period.
In this study, our strategy was to evacuate the hematoma partially to decompress the angry brain then to dissect and clip the aneurysm followed by total hematoma evacuation. Similarly, in the study by Navratil et al., the approach performed is the removal of ICHs when they are large, and they aim not to leave behind a clot with a volume of more than 10 mL. Only in intrasylvian hematomas, they do not strictly follow this policy as the clot is adherent to the structures of the sylvian fissure and their removal may cause additional injury to neurovascular structures.
Early surgical intervention of intracerebral hematoma caused by ruptured middle cerebral artery aneurysm has a favourable outcome in general. The following factors significantly related with unfavourable patient outcome: Preoperative cranial nerves deficit, dysphasia, severe contralateral weakness, presence of dilated ventricles in CT scan, presence of IVH in CT scan, aneurysm location in the dominant (left) hemisphere, high modified-Fisher grade, duration of surgery more than 6 h, occurrence of intraoperative aneurysm rupture, poor postoperative GCS, occurrence postoperative vasospasm, more severe postoperative contralateral weakness, and the presence of postoperative seizure. While the good initial GCS and early surgery significantly related to favourable patient outcome. Lower mortality rate can be achieved with better selection criteria for patients amenable for surgical intervention.
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Conflicts of interest
There are no conflicts of interest.
[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8], [Table 9]