In this study, we found that the presence of an associated intracranial hematoma significantly influenced the severity of the clinical picture after a SAH in our series (Table 1). Although its influence as independent predictor of the final outcome did not appear confirmed in the multivariate analysis (Table 2), in the specific case of MCA aneurysms, this aspect has an important epidemiological value as an ICH or an ISH occur in association with SAH from MCA aneurysms rupture up to almost 44% out of cases in literature [4, 10, 23], and even 48% in our series.
In general, a linear relationship can be observed between the severity of the clinic onset and the size of the hematoma as patients showing larger ICH/ISH have also a worse clinical status at admission [1, 5, 20].
Locksley found that 90% of the patients who died within 3 days from the onset of an aneurysmal SAH harbored an ICH [9]. In our series, instead, the occurrence of a hematoma did not reach a statistically significant increasing of mortality rate, even though the percentage of deaths among patients with a hematoma was almost double if compared to those with pure SAH (Table 1).
Although exploring the different prognostic factors in these patients is important to choose the optimal management strategy, in general an early surgical management is advocated in case of larger ICHs or ISHs [2, 11, 13]. Nevertheless, in agreement to previous experiences in literature [3], we also found a significantly higher rate of treatment related complications in presence of SAH with associated intracranial hematomas.
Currently, consistent evidences indicating the different clinical impact between ISH and ICH on clinical status at admission and outcome are still lacking in literature.
It is therefore of a certain importance the radiological discrimination between ICH and ISH at first round of CT/angio-CT scan. Van de Zande et al. proposed the presence of intra-hematoma contrast-enhancing vessels as the diagnosis criteria for ISH [22]. However, in their series they did not find a direct relationship between the presence of intra-hematoma vessels enhancement and clinical condition or functional outcome [22]. Similarly, no significant differences in clinical conditions at admission and outcome were reported in the series of SAH by Yashimoto et al. [21] and Saito et al. [12] discriminating between ICH and ISH. In disagreement with the above findings, in our series, as shown in Tables 3–4, patients harboring an ICH had a significantly worse Hunt-Hess at admission compared to ISH cases. Moreover, only 5% of ICH patients had a good Hunt-Hess at arrival (1 or 2) compared with 43% of patients of ISH subgroup. Good Hunt-Hess status at onset was associated with good outcome in both groups and Hunt-Hess score was the only independent outcome predictor in patients with SAH associated with hematoma at multivariate analysis (Table 5). The low frequency of good Hunt-Hess cases in ICH subgroup probably explains the lack of significance of mean H-H in this subgroup at univariate analysis.
Other authors have instead focused their attention on the angioarchitecture of the aneurysm and the association with one or the other type of hematoma. Zhang et al. for example assumed that the angle between the pointing direction of aneurysm and the M1 trunk could indicate the hematoma type. In particular, an angle between 109° and 216° would have indicated an ISH, while aneurysms with an angle beyond this range would have ultimately led to an ICH [23]. In our series, we found that the larger size of the aneurysm, rather than then its pointing direction, was associated with the risk of an intracerebral hematoma (Table 3). In fact, while an ISH is a voluminous accumulation of subarachnoid blood in a cisternal space, the formation of an ICH requires a greater breaking force to overcome the resistance of the pia mater and dissect the fibers of the white matter.
A different pathogenetic theory between the two hemorrhagic patterns was proposed by Suzuki et al. They observed that the characteristics of extravasation in sylvian hematomas indicated cotton-like multiple bleeding points, and these findings differed markedly from those of previously reported extravasation from aneurysms. According to their experience, in fact, these authors described multiple extravasations from small vessels different from the ruptured aneurysms, thus hypothesizing that these are the specific bleeding sources of ISH [18].
In agreement with some authors [6, 23], in our multicenter series, we found that the occurrence of an ICH was associated with a worse Hunt-Hess score at admission compared with the presence of an ISH. On the contrary, other authors found that an ISH had a worse prognostic value than an ICH [7]. Several reasons can be advocated for a worse outcome in ISH group: first of all, an early surgical evacuation is generally easier in ICH and a significant post-operative clinical improvement can be expected due to the immediate internal decompression [8, 23]; secondly, a thorough evacuation of an ISH is instead a demanding and risky task due to the subarachnoid location of fibro-adhesive clots to the branches of the MCA and its small perforating vessels [12, 21]; thirdly, an aggressive attempt of intrasylvian clots evacuation may expose to the risk of vascular lesions as well as the excessive vessels manipulation may increase the risk of vasospasm. On the other hand, however, the presence of a large residual amount of ISH represents one of the most important risk factors for the development of a postoperative brain swelling with the risk of a secondary decompressive craniotomy.
Although an early open surgery still represents the treatment of choice in many neurosurgical units in almost all cases of MCA aneurysms especially when associated with larger ICH or ISH [17], different treatment paradigms are prevalent in other centers where the vascular neurosurgery expertise has progressively declining and the endovascular obliteration emerges as the first approach in all ruptured aneurysms [14–16], including those associated with hematomas whose evacuation is therefore delayed after having secured the aneurysm. Nevertheless, a combined endovascular obliteration first and hematoma evacuation after has been advocated also by teams having strong expertise in vascular neurosurgery as reasonable option in selected patients with SAH and associated ICH as this treatment paradigm can transform a complex surgery in an easier and quicker decompression [19]. Probably, in the future, a new generation of cerebrovascular surgeons with double vascular/endovascular expertise and dedicated hybrid operating rooms may contribute to shorten the time between the two procedures and make this mixed option preferable in some patients. However, preserving an expertise in open neurovascular surgery is still mandatory, as a high percentage of MCA aneurysms are irregular in morphology and a full embolization often requires a stent assistance and double anti-platelet therapy even in acute conditions after bleeding [17]. Thus, an attitude towards a hybrid procedure not only may delay the evacuation of the blood clot, but also increases the risk of a new hemorrhagic infarction after the second surgery due to antiplatelets therapy during the endovascular procedure.
Study limitations
Current study has some limitations. First, due to the retrospective design of the study, choice of treatment was given by treating Centers according to local experience and expertise. Second, due to the low number of cases we did not evaluate the influence of hematoma volume in clinical presentation and outcome. However, this could be more relevant in ICH cases than in pure ISH cases, as in larger hematoma volumes it is common to have a mixed pattern with ICH prevalence. Third, we did not evaluate the role of timing of hematoma evacuation from A&E arrival, which is intuitively longer in cases where coiling was performed before hematoma evacuation. However, an indirect answer to this question is given by the similar outcome of endovascular cases compared with clipping ones.