The impact of residual hematoma after evacuation on the outcomes of patients with ruptured intracranial aneurysms with intracerebral hematoma: A longitudinal single-center observational study

Abstract

Intracerebral hematoma (ICH) as a result of ruptured of intracranial aneurysms often arises in patients with subarachnoid hemorrhage. Few studies focused on risk factors for ICH and not the impact of residual hematoma after evacuation on the outcomes of the patients. Therefore, 2 questions need to be answered: does residual hematoma after evacuation have impact on the outcome of patients who present with ICH as a result of ruptured intracranial aneurysms? Is radical pursuit of the hematoma necessary?

The study was a single-center longitudinal observational type. Data of 2044 consecutive patients with subarachnoid hemorrhage from January 2009 to December 2019 were reviewed. ICHs were established and the locations of aneurysms as well as hematoma volumes were measured by computed tomographic scan before aneurysm occlusion. Only patients who received aneurysm clipping were included. Patients were stratified into hematoma evacuation without residuals versus residual hematoma after evaluation groups, and outcome was assessed according to the modified Rankin Scale (mRS) at 6 months.

Out of the 1365 patients who received clipping, 476 patients presented in poor grade, whereas 889 patients’ good grade. Our mRS scores revealed that patients who attained hematoma evacuation without residuals in the good-grade category attained better functional outcome than those with residual hematoma after evacuation. Contrarily, our mRS scores did not establish any significant difference in outcome between the poor-grade patients with hematoma evacuation without residuals and patients with residual hematoma after evacuation. Furthermore, our logistic regression model showed that advance age, poor Hunt-Hess grade, and vascular injury due to surgery were contributing factors for poor outcome of patients with ICH.

Our data suggested that aggressive hematoma evacuation may not benefit the poor-grade patients. Majority of poor outcomes were due to surgical complications which were vascular related as a result of excessive pursuit of ICH.

1. Introduction

Intracerebral hematoma (ICH) as a result of ruptured of intracranial aneurysms (IAs) arises in about 42.6% of patients with subarachnoid hemorrhage (SAH).^[1,2] Usually, intracranial pressure rises transiently higher than mean arterial pressure, resulting in low or absent intracranial blood flow leading to hypoperfusion ischemia at the time of aneurysm rupture.^[3–5] Also, the hematoma causes mass effect resulting in a persistent increase in intracranial pressure leading to early brain injury.^[3,6] Studies have shown that the presence of aneurysmal ICH may negatively influence the patient’s clinical outcome because of the increased possibilities of rehemorrhage, vasospasm, cerebral edema, seizures, and hydrocephalus.^[3–5]

Devastating outcomes with 12-month mortality rates ranging from 43 to 100% have been observed in patients with poor Hunt-Hess (HH) grade (grade 4 and 5).^[3,7] Furthermore, magnetic resonance imaging (MRI) of patients with SAH with HH grades 4 and 5 has established ischemia in 71% to 86% of patients within the first 24 to 96 hours of aneurysm rupture.^[3,8–10] The diagnosis of SAH with ICH is often established clinically with computerized tomography (CT) scan evidence of subarachnoid clots as well as intraparenchymal hemorrhage with a volume >10 mL.^[11] Studies have implicated hematoma size or interval from the onset of SAH and surgery as prognostic factors in patients with SAH with ICH.^[3,11,12]

However, there are less evidence on predictors as well as clinical impact of ICH size. In particular, there are no unique recommendations for SAH patients on treatment decisions derived from the volume of ICH. Also, few studies focused on risk factors for ICH volume and not the impact of residual hematoma after evacuation on the outcomes of the patients with ICH. Therefore, does residual hematoma after evacuation have impact on the outcome of patients who present with SAH with ICH as a result of ruptured IAs? Is radical pursuit of the hematoma necessary? Our study therefore focuses on the impact of residual hematoma after evacuation on the outcomes of the patients with ruptured IAs with ICH.

2. Materials and Methods

This study was based on a single-center observational database comprising 2044 consecutive patients with SAH admitted to our hospital from January 1, 2009 to December 31, 2019. This study was approved by West China Hospital Research Committee. Patients and relatives were dually informed about our intention to involve them in a study and they fully consented to the use of their documents. Written informed consents were obtained from all the patients. Also, written consents for publication were signed by all the patients. The hospital also concerted to the use of their information for publication. The study parameters included 5 broad categories: demographic, clinical, radiological, surgical treatments, and outcomes. Patients who received endovascular coiling were excluded in the final analysis.

2.1. Demography and clinical evaluation

Demographic data such age and sex as well as history of preexisting comorbidities at admission were recorded from in-house electronic medical records. Also, only patients with hospital admission within 72 hours after clinical onset were included in this analysis. The time of bleeding was recorded from emergency physicians’ reports. Clinical presentations on admission were assessed according to HH: Good HH grade = 1 to 3 and Poor HH grade = 4 or 5. HH grading of a patient could alter on admission subsequent to surgery since the grading is not fix for patients all the time. Functional outcomes were judged as favorable or unfavorable using modified Rankin Scale score (mRS). Favorable (mRS = 0–2) while unfavorable (mRS = 3–6). Mortality rate was also stratified according to the HH grading.

2.2. Radiological evaluation

Radiological characteristics of ICH were assessed from the initial CT scan. Angiographic proofs of IAs as causes of bleeding were reviewed. Computed tomography angiography and/or digital subtraction angiography were the main angiographic methods used in evaluating the patients. The radiological features of the ruptured aneurysms were documented upon 3-dimensional reconstructions of computed tomography angiography and/or digital subtraction angiography images. In all patients included in the final analysis, the locations of hematomas were attributed to the corresponding ruptured aneurysms and the volumes were recorded according to the formula A × B × C/2.^[13] All follow-up CT scans up to 6 weeks after bleeding were assessed with regard to hypodensities representing cerebral infarctions as a result of possible vascular injuries. In addition, the SAH patients with and without ICH were correlated with regard to the features of clinical course. Residual hematomas were identified incidentally on first postoperative CT scans done 2 to 4 hours after clipping of the aneurysms and evacuation of the ICHs.

2.3. Intensive care unit managements

All patients were managed in the intensive care unit. As a standard protocol, all patients received oral nimodipine for 3 weeks for the prevention of vasospasm before, during and after the surgery. Also, patients’ comorbidities such as cerebral edema, seizures, and hydrocephalus were adequately managed at the intensive care unit.

2.4. Surgical treatments, outcomes, and follow-ups

The mode of treatment for the patients included in the final analysis involved clipping of the aneurysm and/or hematoma evacuation based on an interdisciplinary approach. Patients who received endovascular coiling were excluded in the analysis. Patients were stratified into poor grade (G1) versus good grade (G2) based on a patient’s HH grade on admission. Moreover, G1 were further categorized into Group 1a (poor grade with evacuation of hematoma without residuals) and Group 1b (poor grade with residual hematoma after evaluation) while G2 were further categorized into Group 2a (good grade with evacuation of hematoma without residuals) and Group 2b (poor grade with residual hematoma after evaluation). The hematoma volume and time of surgery were documented in all patients included in this study. Surgical complications such as vascular injury, direct brain injury, direct nerve damage, recurrence of hematoma and bone flap infection were documented. Hematoma was said to be recurrent if the residual hematoma increased in size ≥2 cm on repeated postoperative CT scan after the first postoperative CT scan in patient with residual hematoma. The mRS and clinical parameters were used to assess patients’ outcomes during hospital stay and at discharge. Also, the mRS score at 6 months intervals was assessed based on follow-up visits in the outpatient clinic.

2.5. Statistical analysis

The data were entered and maintained for analyzed using SPSS (version 21; SPSS Inc, IBM, Chicago, IL) statistical software. Further data analysis was performed using PRISM (version 5.0). For all correlations, differences with P ≤ .05 were considered statistically significant. The predictive value of ICH for functional outcome, as well as the independent predictors of ICH occurrence and volume, was assessed by using multivariate logistic and linear regression analyses, respectively. The differences between continuous variables were analyzed using the student t test (for normally distributed data), the Mann–Whitney U test (for nonnormally distributed data) or analysis of variance test; associations between categorical variables were analyzed using χ² test or Fisher exact test, as appropriate.

3. Results

3.1. Patients’ stratifications and comorbidities

In all, a total of 2044 patients with aneurysms were documented. Out of the total number above, 679 patients received endovascular coiling and thus were excluded from the final analysis (Fig. 1). Anatomically (Fig. 2), out of the 1365 patients who received clipping of the aneurysms, 36% of the aneurysms were found in the posterior communication artery while 32 % of the aneurysms were found in the anterior communicating artery (AcomA). Also, 17% were found in the middle cerebral artery (MCA) while 11% were found in the internal carotid artery (ICA). Furthermore, 3% were found in the posterior circulation (PC) while 1% were found in the ophthalmic artery (OpthA).

Figure 1.

Patient selection and exclusion. Group 1a = poor grade with evacuation of hematoma without residuals, group 1b = poor grade with residual hematoma after evaluation, group 2a = good grade with evacuation of hematoma without residuals, group 2b = poor grade with residual hematoma after evaluation.

Figure 2.

Anatomic location of aneurysms in 1365 patients. ICH = intracerebral hematoma.

Out of 1365 patients with clipped aneurysms included in the analysis, 476 patients were poor grade while 889 of them were good grade. Also, out of the 476 poor-grade patients, 330 were without ICH while 146 had ICH. Furthermore, out of the 146 patients with ICH, hematoma evacuation without residuals was observed in 45 (1a) patients while in 101 (1b) patients, residual hematomas were observed after evacuation of the ICH (Fig. 1).

Out of the 889 good-grade patients, 657 of the were without ICH while 232 patients had ICH. Also, out of the 232 with ICH, hematoma evacuation without residuals was observed in 68 (2a) patients while in 164 (2b) patients, residual hematomas were observed after evacuation of the ICH (Fig. 1). Thus, a total of 378 patients were with ICHs. Also, ICH was observed on initial CT scan in 146 poor-grade cases (146/476, 30.67%), while 232 good-grade patients were also harboring ICHs (232/1568, 14.8%; Fig. 1 and Table 1).

Table 1.

Age and sex distribution of patients with ICH.

Age (yr)	Group 1		Group 2
	Male	Female	Male	Female
0–39	7	10	16	16
40–49	15	14	21	38
50–59	10	34	20	40
60–69	11	32	19	41
70–79	5	7	8	13
80–89	0	1	0	0
Total	48	98	84	148

Group 1 = poor grade with ICH, group 2 = good grade with ICH.

The 2-way ANOVA was used.

ANOVA = analysis of variance, ICH = intracerebral hematoma.

Females were predominant in both poor and good grades and ages of all patients ranged from 0 to 89 (Table 1). The histories of the patients preexisting comorbidities profile at admission as recorded from in-house electronic medical records predominantly included hypertension, diabetics, ischemic heart diseases, hyperlipidemia, osteoarthritis, sleep apnea, gout, and others (Table 2). These factors did not have any significant effects on the outcome of treatment because they were well managed.

Table 2.

Shows patients history of preexisting comorbidities profile at admission were recorded from in-house electronic medical records.

Comorbidity profile	Group 1a	Group 1b	Group 2a	Group 2b
Hypertension	40 (88.9%)	86 (85.1%)	42 (61.8%)	95 (57.9%)
Diabetes	25 (55.6%)	52 (51.4%)	24 (35.3%)	54 (32.9%)
Ischemic heart disease	15 (33.3%)	32 (31.6%)	12 (17.6%)	35 (20.7%)
Hyperlipidemia	20 (44.4%)	40 (39.6%)	18 (26.4%)	37 (22.5%)
Osteoarthritis	14 (31.1%)	35 (34.6%)	12 (17.6%)	15 (9.1%)
Sleep apnea	12 (26.7%)	30 (29.7%)	8 (11.7%)	12 (7.3%)
Gout	8 (17.8%)	20 (19.8%)	5 (7.4%)	10 (6.1%)
Others	6 (13.3%)	16 (15.8%)	8 (11.7%)	11 (6.7%)

3.2. Hunt & Hess gradings on arrival in the hospital

In all the 1365 patients with clipped aneurysms included in the analysis, patients were grouped into patients with hematoma and patients without hematoma during CT scan evaluation prior to admission. Also, HH grading of the patients were assessed according to the grouping above (Fig. 3). In all 489 patients present with HH1, 132 presented with hematoma while 357 did not have hematoma. Also, a total of 400 patients presented with HH2; out of which 100 presented with hematoma while 300 did not have hematoma. Furthermore, in all the 304 patients present with HH3, 85 presented with hematoma while 220 did not have hematoma. Additionally, in all the 97 patients presented with HH4, 32 presented with hematoma while 65 did not have hematoma. Finally, 75 patients presented with HH5; out of which 30 presented with hematoma while 45 did not have hematoma. In all the patients P = .072.

Figure 3.

Stratification of 1365 patients according to the HH grade on arrival in the hospital: good HH grade =1 to 3 and poor HH grade = 4 or 5. In all the patients P = .072. Chi-square test was used. HH = Hunt and Hess.

3.3. Surgical outcomes

In all, a total of 113 patients in both poor and good grade had hematoma evacuations without residuals based on a patient’s HH grade prior to surgery. Contrarily, a total 265 patients had residual hematomas after evacuation of the ICH in both poor and good-grade patients. Also, out of the 146 patients with poor grade, 45(1a) patients had evacuation of the hematoma without residuals. Furthermore, out of 232 patients with good grade, 68(2a) had evacuation of the hematoma without residuals.

Our study revealed that the good-grade patients with their space-occupying hematoma removed without residuals actually achieved better functional outcome than patients with residual hematomas after evacuation of the ICH. Furthermore, we did not find any significant difference in outcome between the poor-grade patients with and without residuals hematomas. In both poor and good-grade patients, females were predominant and their ages were between 50 and 59 (Table 3). They were no significantly different between hematoma volume and timing of surgery in all 4 groups.

Table 3.

Hematoma volume and time of surgery in ICH patients with hematoma evacuation and without hematoma evacuation.

	Group 1a	Group 1b	Group 2a	Group 2b
No. of patients	45	101	68	164
Male/female	16/29	49/52	24/44	54/102
Age (yr)	55.6 ± 5	54.5 ± 7	54.6 ± 5	55.5 ± 7
Hematoma volume (mL)	25 ± 8	27 ± 6	28 ± 7	26 ± 9
Time from onset to surgery (h)	8.5 ± 4.2	7.4 ± 5.7	7.4 ± 3.2	8.4 ± 4.5

Group 1a = poor grade with evacuation of hematoma without residuals, group 1b = poor grade with residual hematoma after evaluation, group 2a = good grade with evacuation of hematoma without residuals, group 2b = poor grade with residual hematoma after evaluation.

The 2-way ANOVA was used.

ANOVA = analysis of variance, ICH = intracerebral hematoma.

3.4. Surgical complications, hospital stay and follow-ups

In the patients with poor-grade group (G1), analysis revealed that vascular injury and nerve damage were significantly different between Group 1a and Group 1b (P < .05; Table 4). Nevertheless, complications were not observed in patients in the good-grade group (G2). Length of hospital stay showed significant differences between Group 1a and Group 1b but a slight difference in Group 2a and Group 2b (Table 5).

Table 4.

Long-term outcome measured by mRS scale.

Favorable outcome	Group 1a	Group 1b	Group 2a	Group2b
Length of hospital stay (d)	61 ± 31*	47 ± 32*	14 ± 9	18 ± 12
Favorable outcome at 6 mo	19 (42.2%)	42 (41.6%)	59 (86.7%)*	42 (41.6%) *

χ² test was used.

Favorable outcome = mRS score 0–2, unfavorable outcome = mRS score 3–6.

mRS = modified Rankin Scale.

^*P < .05.

Table 5.

Surgical complications of 146 patients and their distribution in group 1a and group 1b.

Complication	Postoperative morbidity	Group 1a	Group 1b
Vascular injury	21 (14.4%)	13 (28.9%)*	8 (8%)*
Direct brain injury	4 (3%)	2 (4.4%)	2 (2%)
Direct nerve damage	9 (6.2%)	7 (15.6%)*	2 (2%)*
Hematoma	2 (1.4%)	2 (4.4%)	0
Bone flap infection	1 (0.7%)	1 (0.2%)	0

t test was used.

^*P < .05.

On follow-ups, there were no significant difference in favorable outcome between Group 1a and Group 1b, whereas Group 2a and Group 2b differed significantly in terms of favorable outcomes (Table 5). Overall, logistic regression model showed advance age, poor HH grade, and surgical vascular injury were contributing factors for poor outcome (P = .005, .03, and <.01 respectively; Table 6).

Table 6.

Results of the final logistic regression model.

Variable	P value	Adjusted odds ratio	95% confidence interval
Age	.005	1.11	1.02–1.18
Poor Hunt-Hess grade	.03	5.42	1.01–20.13
Surgical vascular complication	<.01	61.2	13.23–298.07

Liner regression was used.

3.5. Functional outcomes and mortality rate

In group 1, a favorable outcome (mRS = 0–2) was achieved in 19 patients (42.2%) in the ICH evacuation without residuals hematoma group, whereas 42 patients achieved favorable outcome in the ICH evacuation with residual hematoma group (P = .053; Table 4). Also, in group 2, a favorable outcome (mRS = 0–2) was achieved in 59 patients (86.7%) in the ICH evacuation without residuals hematoma group, whereas 42 patients achieved favorable outcome in the ICH evacuation with residual hematoma group (P < .05; Table 4). We observed a mortality rate of 25.4% (347/1365). The mortality stratification according the HH grading is as shown in Figure 4. P = .837 as per all the deceased patients. In all the deceased patients, mortality occurred after the first 6 mouths follow-up. No patient was lost on follow-ups.

Figure 4.

Mortality rates stratified by higher grades SAH (P = .837). The Mann–Whitney U test was used. SAH = subarachnoid hemorrhage.

3.6. Illustrative cases

3.6.1. Case 1.

This case was selected from group 1a: The patient was 61 years old female with an aneurysm in the left AcomA (Fig. 5A–C). She presented with HH-4. Clipping of the aneurysm was done with radical hematoma removal 6 hours after ictus (Fig. 5C, D). Postoperative CT scan did not show any residual hematoma after ICH evacuation. She was discharged 56 days after the surgery. She had mRS score = 1 at 6-month follow-up.

Figure 5.

(A–D) Are images for illustrative case 1 who was selected from group 1a. (A) Is a preoperative CT scan showing hematoma. (B) Is a preoperative DSA image showing the aneurysm. Red arrow = aneurysm. (C) Is a preoperative CTA image showing the aneurysm. Red arrow = aneurysm. (D) Is a postoperative CTA image showing the clip in situ. Red arrow = clip. CT = computerized tomography.

3.6.2. Case 2.

This case was selected from group 1b: The patient was a 54-year-old man with an aneurysm in the left AcomA (Fig. 6A, B). She presented with HH-4. Clipping of the aneurysm was done 7 hours after the ictus. Postoperative CT scan showed residual hematoma after ICH evacuation (Fig. 6C). He was subsequently managed conservatively (Fig. 6D). Patient waked up from coma 20 days after surgery, and transferred to rehabilitation center for another 36 days before discharge. She had mRS score = 1 at 6-month follow-up.

Figure 6.

(A–D) Are images for illustrative case 2 who was selected from group 1b. (A) Is a preoperative CT scan showing hematoma and SAH. (B) Is a preoperative DSA image showing the aneurysm. Red arrow = aneurysm. (C) Is a preoperative CTA image showing the clip in situ. Red arrow = clip. (D) Is a postoperative CT image showing disappearance of the hematoma. CT = computerized tomography, SAH = subarachnoid hemorrhage.

3.6.3. Case 3.

This case was selected from group 2b: The patient was a 52 years old female with an aneurysm in the right AcomA (Fig. 7A–C). She presented with HH-2. Clipping of the aneurysm was done 12 hours after ictus. Postoperative CT scan showed residual hematoma after ICH evacuation (Fig. 7D, E). She also developed right frontal-temporal infarction as a result of vascular injury and underwent a second decompressive craniectomy (Fig. 7F). She stayed in the hospital for 30 days before being transferred to a local hospital after both surgeries. She had mRS score = 2 at 6-month follow-up.

Figure 7.

(A–F) Are images for illustrative case 3 who was selected from group 2b. (A) Is a preoperative CT scan showing hematoma. (B) Is a preoperative DSA image showing the aneurysm. Red arrow = aneurysm. (C) Is a preoperative CTA image showing the aneurysm. Red arrow = aneurysm. (D&E) Are postoperative CT scan images. (D) Show residual hematoma after evacuation. (E) Shows the clip in situ. Red arrow = clip. (F) Is a postoperative decompressive craniectomy showing swelling of the brain. CT = computerized tomography.

4. Discussion

Patients who have an SAH with an additional ICH because of a ruptured IA are traditionally described as being associated with poor HH grade and having an unfavorable outcome.^[14–19] Especially in the case of a space-occupying hematoma, the initial clinical presentation may be dramatic.^[14,19] Our study revealed that the good-grade patients with ICH evacuated without residual hematoma actually achieved better functional outcome than those whose ICH were evacuated with residual hematoma. Furthermore, we did not find any significant difference in outcome among the poor-grade patients with and without residual hematoma after evacuation. Thus, hematoma evacuation without residual hematoma did not benefit the poor-grade patients. Our logistic regression model further showed that advance age, poor HH grade, and surgical vascular injury were contributing factors for poor outcome of patients with ICH. In both poor and good-grade patients, females were predominant and their mid ages were between 50 and 59.

Initial studies have demonstrated that ICH often occurs from aneurysms of the MCA and distal anterior cerebral arteries (ACA), less characteristically from aneurysms of the ICA, and only seldom from aneurysms of the PC.^[2,20,21] Contrarily, our data revealed that aneurysm was more frequent from the posterior communication artery and AcomA, followed by the MCA and the ICA, and less frequently from the PC and the ophthalmic artery. It was postulated that aneurysms found amid cerebral cortices tend to hemorrhage into the parenchyma.^[2,22] Also, it further postulated that the anatomic direction of the aneurysm dome toward the cortex may contribute to the formation of ICH.^[2,11,22]

Interestingly, Bruder et al^[23] did not find any association between ICH location and outcome of patients. Lok et al^[24] observed that many factors namely age, individual brain compliance, location of the aneurysm, high blood pressure, and arteriosclerosis were also the contributing factors of poor-grade SAH. Jabbarli et al^[2] also identified aneurysm location as well as size, history of arterial hypertension, as well as diabetes mellitus as risk factors for ICH in association with IA rupture. They thus initiated a risk score that might permit the assessment of the risk of aneurysmal ICH before the bleeding event.^[2]

Clinical grading scale for IAs as proposed by Hunt and Hess Grade is as follows: 0—unruptured aneurysm, 1—asymptomatic or minimal headache, nuchal rigidity, 2—moderate to severe headache, nuchal rigidity, no neurological deficit other than cranial nerve palsy, 3—drowsiness, confusion, mild focal deficit, 4—stupor, moderate to severe hemiparesis, possible early decerebrate rigidity and vegetative disturbances, 5—deep coma, decerebrate rigidity, moribund appearance, and +1 grade—for vasospasm or systemic disease.^[7,25]

Schramm observed that IA rupture did not essentially correlate with poor surgical outcome. He indicating that in his study, 94.1% of the patients were HH grades 1 to 3.^[19] Sandalcioglu et al observed that IA rupture has no influence on outcome, neither in patients with good initial condition (HH grades 1–3) nor in poor-grade patients (HH grades 4 and 5).^[14] A sizable number of our patients presented with HH grade 1 to 3 while very few patients presented with HH grades 4 and 5. Also, in the patients who presented with HH grade 1 to 3, most of them were without hematoma while a smaller number of them presented with hematoma. Similar pattern was observed in patients who presented with HH grades 4 and 5. Contrary to early studies above, our logistic regression model showed that poor HH grade was a contributing factor for poor outcome of patients with ICH.

Marvin et al observed that patients with larger hematomas presented in poorer initial clinical state and were more likely to require further neurosurgical interventions such as decompressive craniectomy or hematoma evacuation.^[6] Studies have shown that larger sized IA are often associated with increased risk of IA rupture resulting in ICH in patients with SAH.^{[1,2,12,26,27]} Although arbitrary cutoff values are often applied, life-threatening hematoma volume of aneurysmal ICH associated with poor outcome has been estimated to be about 25 mL.^[6,11,28] Nevertheless, cutoffs for decompressive craniectomy and hematoma evacuation were estimated to be about 17 mL.^[6] Our data revealed that they were no significant differences between hematoma volume and outcome of patients with aneurysmal ICH.

Current treatment options for patients with aneurysmal ICH include coiling with conservative hematoma treatment and surgical aneurysm obliteration with or without hematoma evacuation.^[15–18] Nevertheless, for clinical decision-making, there are two emerging questions: what kind of treatment is beneficial for the patient? and are there prognostic factors that can help guide treatment? Current studies stipulate that the objectives of early or ultra-early surgery as compared to late surgery are as follows: firstly, early or ultra-early surgery averts an abrupt second rupture, thus decreasing the daily risk of rebleeding of the aneurysm which is a recognized risk factor for worse clinical outcome. Secondly, early removal of vasospasmogenic agents such as blood clots, which are in contact with cerebral arteries, decreases the risk of vasospasm. Thirdly, critical medical treatment of vasospasm is often achieved via the induction of arterial hypertension as well as hypervolemia with no risk of aneurysm bleeding.^[15–18,29]

Thus, early surgery policies have been adapted in various centers, predominantly in good-grade patients, while delayed surgery is still reserved to poor-grade patients.^[15–18] In our series of consecutive patients with prospective data sampling SAH and additional ICH, the good-grade patients with ICH evacuated without residual hematoma actually achieved better functional outcome than those whose ICH were evacuated with residual hematoma, although their average hospital stays did not differ that much. This is probably because residual hematoma and associated mass effect are important in the etiology of vasospasm and focal neurologic deficits following SAH. Thus, we also stress that successful evacuation without residual hematoma is therefore likely to significantly reduce the incidence of symptomatic vasospasm and associated infarction.

Surprisingly, we did not find any significant difference in outcome between the poor-grade patients with and without residual hematoma after evacuation. This suggests that the poor grade may not be the result of the presence of residual hematoma. Thus, hematoma evacuation without residual hematoma may not benefit the poor-grade patients. Surgeons who did not attain total evaluation of ICH ought not worry because, our study demonstrated that patients with hematoma evacuation without residual hematoma had complications and longer hospital stay. A further look into the reasons behind the longer hospital stays of the Group 2a patients revealed that vascular injury and direct nerve damage were the most likely reasons of longer hospital stay. Vascular injury can occur during dissection and/ or during clip placement. Although direct brain damage may be low, added direct vascular and nerve injury may be increased during the pursuit of hematoma. In poor-grade patients, the brain itself may be swollen and the subarachnoid space may be tightly packed with blood, making it very difficult to access the hematoma, while forceful dissection and radical pursuit of those hematomas may do more harm than good.

An initial study by Ryu and Shim^[30] demonstrated that ischemic damage and brain swelling are serious threats to outcome because of the potential injury as a result of brain retraction. Another study revealed that the use of brain retractors mostly triggers mechanical cortical as well as subcortical compression and thus decreases regional perfusion resulting in local ischemia.^[31] The authors indicated that dynamic retractors or retractorless techniques for open microsurgical clipping of IAs may avert these kind of brain injuries as well as attain a better patients’ outcome.^[31] Noteworthily, rebleeding as well as vasospasm may lead to a vicious circle of ischemia and deteriorating brain swelling that could precisely obscure a delayed surgery.^[15]

Most authors are of the opinion that patients presenting with up to HH grade 3 should receive ultra-early surgery to avert rebleeding as well as eventual vasospasm.^[15,32,33] The mRS is a 6-point disability scale with attainable scores varying from 0 to 5.^[34] An extra distinct score of 6 is often added for patients who expire. It is a trustworthy as well as easy neurology assessment record for evaluating life-threatening neurological patients.^[34] Our mRS scores revealed that the good-grade patients with ICH evacuated without residual hematoma actually achieved better functional outcome than those whose ICH were evacuated with residual hematoma.

Contrarily, our mRS scores did not establish any significant difference in outcome between the poor-grade patients with and without residual hematoma after evacuation. A similar study like ours established that 90% of patients with SAH who died within 72 hours also had ICH.^[35] Another study established that overall mortality rate of SAH patients with ICH ranges from 38 to 58%.^[36] We observed a mortality rate of 25.4%. Also, patients with preexisting comorbidities such as hypertension, diabetics, ischemic heart diseases, hyperlipidemia, osteoarthritis, sleep apnea, gout, and others did not have any significant effects on the outcome of treatment because they were well managed.

5. Conclusions

Our data suggested that residual hematoma after evacuation of ICH may not be a threat to recovery of patients. Good-grade patients with space-occupying ICH were the most likely ones to benefit from total hematoma evacuation or without residuals. Aggressive hematoma evacuation may not benefit the poor-grade patients. Patients’ poor outcomes in this group were due to surgical complications which were vascular related due to excessive pursuit of ICH. It may be beneficial not to overstress the importance of total hematoma evacuation with patients’ relatives before surgery for poor-grade aneurysms.

Author contributions

All authors contributed toward data collection, drafting and critically revision of the paper and agree to be accountable for all aspects of the work. Seidu A. Richard did the final analysis and wrote the paper. All the authors read and approved the final paper.

Conceptualization: Yifan Yang, Seidu A. Richard, Zhigang Lan.

Data curation: Yifan Yang, Seidu A. Richard, Zhigang Lan.

Formal analysis: Yifan Yang, Seidu A. Richard, Zhigang Lan.

Funding acquisition: Zhigang Lan.

Investigation: Seidu A. Richard, Zhigang Lan.

Methodology: Yifan Yang, Seidu A. Richard, Zhigang Lan.

Resources: Zhigang Lan.

Software: Yifan Yang, Seidu A. Richard, Zhigang Lan.

Writing – original draft: Seidu A. Richard.

Writing – review & editing: Yifan Yang, Seidu A. Richard, Zhigang Lan.