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 »  Abstract
 »  Introduction
 »  Material and Methods
 »  Results
 »  Discussion
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Table of Contents    
ORIGINAL ARTICLE
Year : 2011  |  Volume : 59  |  Issue : 2  |  Page : 212-217

Poor-grade subarachnoid hemorrhage: Is surgical clipping worthwhile?


Department of Neurosurgery, Postgraduate Institute of Medical Education and Research, Chandigarh, India

Date of Submission02-Oct-2010
Date of Decision25-Oct-2010
Date of Acceptance29-Dec-2010
Date of Web Publication7-Apr-2011

Correspondence Address:
Sunil K Gupta
Department of Neurosurgery, Postgraduate Institute of Medical Education & Research, Chandigarh
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0028-3886.79144

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 » Abstract 

Background : Management of patients with poor-grade aneurysmal subarachnoid hemorrhage (SAH) is difficult and the protocols followed differ from center to center. Material and Methods : In this report, we present our experience with aneurysmal clipping in patients with poor-grade SAH. Patients with poor Hunt and Hess (H and H) grade (Grade IV and Grade V) were offered surgery after stabilization of their hemodynamic and metabolic parameters. The status was recorded as favorable (good recovery, mild to moderate disability but independent), unfavorable (severe disability, vegetative) and dead. Results : Out of a total of 1196 patients who underwent aneurysmal clipping, 165(13.8%) were in poor grade. Of the 165 patients, 99 (60%) were in H and H Grade IV and 66 (40%) were in Grade V. More than half of the patients (58%) were operated within 24 h of admission. There was an overall mortality of 50.9%. In the long term, of the survivors who were followed up, about 72% achieved a favorable outcome. Conclusions : With an aggressive approach aimed at early clipping, the chances of rebleed are reduced and vasospasm can be managed more aggressively. This protocol resulted in survival in a significant proportion of patients who would have otherwise died. In the long-term follow-up, the surviving patients showed significant improvement from the status at discharge.


Keywords: Aneurysm clipping, long-term outcome, poor-grade subarachnoid hemorrhage


How to cite this article:
Gupta SK, Ghanta RK, Chhabra R, Mohindra S, Mathuriya SN, Mukherjee KK, Umredkar AU, Singla N. Poor-grade subarachnoid hemorrhage: Is surgical clipping worthwhile?. Neurol India 2011;59:212-7

How to cite this URL:
Gupta SK, Ghanta RK, Chhabra R, Mohindra S, Mathuriya SN, Mukherjee KK, Umredkar AU, Singla N. Poor-grade subarachnoid hemorrhage: Is surgical clipping worthwhile?. Neurol India [serial online] 2011 [cited 2018 Dec 14];59:212-7. Available from: http://www.neurologyindia.com/text.asp?2011/59/2/212/79144



 » Introduction Top


The management of patients with poor-grade aneurysmal subarachnoid hemorrhage (SAH) remains controversial. These patients are usually managed conservatively, and those who survive and show clinical improvement are selected for aneurysmal clipping. Surgery in these patients is associated with high morbidity and mortality. [1],[2],[3],[4],[5],[6],[7] However, with non-operative treatment almost all patients finally die [1],[2],[3],[7],[8],[9],[10] from the effects of the primary bleed, from rebleed or from the effects of delayed ischemic events. In recent years, there have been several reports demonstrating improved outcome with early surgery and aggressive medical management, also in select patients with poor-grade aneurysmal SAH. [1],[2],[3],[4],[6],[7],[8],[9],[10],[11],[12],[13] Most authors are reluctant to report results of surgical treatment in poor-grade patients because of the high mortality and morbidity. We present here, our results following aneurysmal clipping in 165 patients with poor-grade aneurysmal SAH, which is probably one of the largest series reported till date.


 » Material and Methods Top


From January 1999 to June 2005 a total of 1196 patients with aneurysmal SAH were operated. Out of these, 165 were in poor grade. The grading was as per Hunt and Hess (H and H) grade. The following patients were considered as poor grade: H and H Grade IV and H and H Grade V. Patients who were either dull or drowsy were not considered as poor grade even if they had associated co-morbid factors like chronic obstructive airway disease (COAD), hypertension or diabetes. The H and H grade at surgery was taken for analysis in this study.

Routine biochemical and hematological parameters were assessed in all the patients. Initial medical treatment included nimodipine, dexamethasone, and anticonvulsants. All the patients underwent a computed tomography (CT) scan, and a digital subtraction angiography (DSA). In addition, CT angiography was performed, if considered necessary to better delineate the anatomy of the aneurysm and its relation to perforators. External ventricular drain was inserted in patients who had significant hydrocephalus and intraventricular hemorrhage. The patients were stabilized hemodynamically and metabolically. The protocol followed at our hospital is that patients who have a ruptured anterior circulation aneurysm are offered surgery. However, patients with anterior circulation aneurysms in intracavernous carotid and carotid cave location are managed by guglielmi detachable (GD)-coiling. Patients with ruptured posterior circulation aneurysms are also managed by the neuroradiologists by GD-coiling. Patients who cannot afford GD-coiling or in whom GD-coiling is technically not possible are clipped. Patients with no motor response and/or those with bilateral dilated fixed pupils were managed conservatively. Aneurysm clipping was performed as per standard protocol. All these patients with poor-grade SAH were also given the option of GD-coiling. Most could not afford the cost and in a few, the neuroradiologist thought that it was technically not possible. The clinical status was noted at the time of discharge and recorded as follows: (1) Excellent: good recovery, independent, with mild disability; (2) Good: moderate disability, but independent; (3) Fair: severe disability, dependent; (4) Poor: vegetative state; and (5) Dead. The outcomes were classified as follows: (1) Favorable: Excellent and good; (2) Unfavorable: fair and poor; and (3) Dead. The clinical details of all patients, the CT scan findings, Fisher grade, site and size of aneurysm, the presence or absence of vasospasm, the timing of surgery and the outcome at discharge and in follow-up were recorded.


 » Results Top


One hundred and sixty-five patients in poor-grade SAH (H and H Grade IV and V) underwent aneurysmal clipping upon over a 6-1/2 years period. These comprised 13.8% of all patients of aneurysmal SAH operated during this period. Of these, 98 were males and 67 were females. The average age of the patients was 46.2 years (age range 14-75 years), 99 (60%) of patients were in H and H Grade IV and 66 (40%) were in Grade V. Associated co-morbidity was present in a significant number of patients; with 86 (52.1%) having hypertension/cardiac disease and 61(37%) having chronic obstructive airway disease. Diabetes was present in 10(6.1%) patients. Most of the patients (88.5%) were in Fisher Grade III and IV. Preoperative CT scan demonstrated hydrocephalus in 23.4% patients and an infarct in 4.1%. A ventriculo-peritoneal shunt was done in 15.8% of patients. Vasospasm was detected in a total of 41% patients. The most common location of the aneurysm was anterior communicating artery (37%) followed by middle cerebral artery (23%). Twenty (12.1%) patients had multiple aneurysms [Table 1]. One hundred and twenty-seven (77%) patients had small (< 11 mm) aneurysms and 38 (23%) had large-sized (11-24 mm) aneurysms. More than half (96, 58.2%) were operated within 24 h of admission, and a further 43 (26.1%) were operated within three days while 20 (12.1%) were operated between 3-10 days and six (3.6%) were operated after 10 days. The delay in surgery after admission was usually due to the time taken to stabilize the general condition and metabolic parameters and in some cases, awaiting consent for surgery. The time interval between last ictus and surgery was less than 72 h in 58 (35.2%); 65 (39.4%) were operated between 3-10 days and 42 (25.5%) were operated 10 days after the ictus. In most patients, delay was due to delay in arrival at our institute. The average hospital stay of the patients was 27.4 days (range: 21-45 days). Once the patients stabilized neurologically, they were discharged from the hospital.
Table 1: Location of aneurysms in patients with poor-grade SAH


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Intra-operatively, after aneurysm clipping, the fundus was punctured to check the completeness of aneurysm occlusion. In a few patients, intra-operative transcranial Doppler was used to assess the flow in the distal vessels after clip placement. Postoperative DSA was not routinely done. There was an overall mortality of 50.9% (84 patients). The mortality was more (62.1%) in patients who were preoperatively in Grade V as compared to patients in Grade IV (43.4%). There was no correlation between Fisher grade and clinical status at discharge. Similarly, the site and size of aneurysm also had no significant effect on outcome. However, the mortality was least (22.2%) in patients with internal carotid artery (ICA) bifurcation aneurysms. In patients above 60 years the mortality was highest (71.4%) as compared to 54.3% mortality in the age range 40-60 years and 35.7% mortality in patients less than 40 years of age. Fifty-nine (35.8%) patients were either severely disabled or in a vegetative state at the time of discharge while 22 (13.3%) had a good neurological state (mild to moderate disability, but independent in daily activities) [Table 2]. However, at the time of discharge, overall only 2.4% had an excellent outcome i.e., with only mild disability. As expected, there was a statistically significant correlation between outcome at discharge and the H and H grade at the time of surgery [P<.05, [Table 2]]. As these patients were in the hospital for a period of about one month, on an average, these figures were taken as indicative of early results.
Table 2: Status at discharge according to H and H grade at surgery


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There was a high incidence of morbidity in the postoperative period. Postoperative CT scans demonstrated an infarct in 58% of patients. The infarcts were either bilateral, deep-seated involving basal ganglia or unilateral, involving one major vascular territory. Septicemia with a positive blood culture was seen in 21(12.7%) patients. There was also a high incidence of chest infections in the postoperative period, with almost a third, 55(33.3%) patients developing various degrees of chest complications leading to a prolonged intensive care unit (ICU) as well as hospital stay. Similarly, electrolyte abnormalities, mostly in relation to serum sodium levels were seen in as many as 50(30.3%) patients. Five (3%) developed deep vein thrombosis in the lower limbs. In the immediate postoperative period, 97(58.8%) patients needed ventilator support for varying interval of time and practically most of them, 95(57.5%), underwent a tracheostomy. The hospital stay ranged from 13 days to 34 days.

A few patients with posterior circulation and intracavernous carotid aneurysms were managed by GD coiling. Patients of posterior circulation aneurysms who could not afford coiling (four patients) were operated and the aneurysms clipped surgically. Poor-grade SAH patients with intracavernous carotid aneurysms were managed conservatively. We do not have clinical details and follow-up of the few patients managed with GD coiling.

Out of the 81 patients who were discharged, long-term follow-up was available for a total of 39 patients [Table 3]. The mean duration of follow-up was 31.8 months (range: 8-92 months). We do not have details of the rest of the patients, so the discussion of long-term results is limited to these 39 patients. While at the time of discharge only four (10.3%) patients had a glasgow outcome scale (GOS) of 5, in long-term follow-up the number of patients in this group increased to 17 (43.6%). The long-term outcome as assessed by GOS was significantly better in patients with H and H Grade IV as compared to Grade V [P<.05, [Table 3]]. The number of patients in the poor outcome group (18, 46.2%) also decreased to 10 (25.6%). Two patients died from cardiac events. When these patients were assessed by the modified Rankin scale, 27 (72.9%) had a good outcome. There was no statistically significant difference between Grade IV and V in terms of functional status as assessed by modified Rankin scale [P>.05, [Table 3]]. Thus, except for the two patients who died from unrelated causes, rest of the patients continued to show progressive neurological improvement.
Table 3: Long-term follow-up results


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 » Discussion Top


Most of the good results reported in the literature following clipping of aneurysmal SAH are in patients with a good preoperative H and H grade (Grades I-III). However, a significant percentage of SAH patients present in poor grade (Grades IV-V). The incidence of patients with poor-grade SAH varies from 24-45% in various series. [3],[4],[9],[11],[12] In the present study, almost 13.8% of patients were in poor clinical grade. There is no consensus on the optimal treatment of patients with poor-grade aneurysmal SAH. Traditionally, the outcome in these patients is expected to be poor and the majority are treated conservatively. [13] These patients are commonly treated expectantly, often with ventricular drainage. [1] Thus, Grade IV and V patients are excluded from early surgery in the hope of spontaneous improvement to a better grade. [14],[15],[16],[17],[18] Aneurysm surgery is usually performed in these patients, on a semi-selective basis, in those who demonstrate clinical improvement. [2],[6],[18] However, with this protocol, most patients die from brain damage due to the primary bleed, from recurrent hemorrhage or from the effects of delayed ischemic damage. [1],[2],[3],[4],[6],[7],[8],[9],[10] While one cannot do much about the primary brain damage, rebleed and vasospasm are potentially treatable conditions. It is well documented that the highest rebleeding after SAH occurs within the first 24 h. [19],[20],[21],[22],[23] There is also evidence that the rebleeding rate is actually higher in poor-grade patients than in good-grade patients. [5],[7],[24],[25],[26],[27],[28]

In recent years, there have been reports of aggressive surgical management of poor-grade SAH patients with significant proportions of patients achieving good results. [1],[2],[3],[4],[5],[6],[7],[8],[9],[10],[11],[29],[30] In most of these series, patients who have shown some improvement, have been selected for aneurysmal clipping [Table 4]. The most striking finding in all the series has been that in patients in whom no clipping of the aneurysms was performed, the mortality was almost 100%, the most common causes being either rebleed, or ischemic phenomenon (vasospasm). It is difficult to predict which patient will improve with conservative treatment and who will die while being observed for improvement. [3] Sasaki et al., [8] advocated close monitoring in the first 24 h for grade change to identify a select group that can benefit from surgery in early stage. In their series about half of the patients manifested improvement after hospitalization, indicating they did not have irreversible brain damage. Hutchinson et al., [2] followed a protocol of a 24-h period of sedation, paralysis and ventilation; blood gas, fluid and electrolyte resuscitation and assessment after stoppage of sedation. Patients less than 65 years of age and showing flexor response were selected for surgery. In the present study, poor-grade patients having ruptured posterior circulation aneurysms, or aneurysm in the carotid cave region or intracavernous carotid were managed by GD coiling. Surgery was offered to all other poor-grade patients except those with dilated fixed pupils and/or no motor response. It is our contention that since conservative treatment leads to almost 100% mortality and the most common cause is rebleed, early obliteration of the aneurysm is the only way to prevent this complication. Moreover, once the aneurysm is secured, vasospasm can be managed aggressively with triple H (hypervolemic hypertensive hemodilutional) therapy, which may be hazardous with an unclipped aneurysm. The timing of surgery in our patients depended upon stabilization of the hemodynamic and metabolic parameters.
Table 4: Recent series of poor grade aneurysmal SAH


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Most of the patients were operated within 72 h of admission, with more than half being operated within 24 h. The overall mortality though high is comparable to that reported in the literature. Most authors have followed a selection criterion in deciding surgical versus conservative treatment, with patients showing improvement undergoing surgery. No such selection was done in the present series. We did not include patients who were dull or drowsy even if they had significant co-morbid illness. A similar mortality of 45% following aneurysm clipping was observed by Laidlaw et al., [3] -the only other series where the authors advocated early surgery in all patients unselected by age or grade. Mortality was obviously less in patients with Grade IV SAH than in those with Grade V, a finding observed by other authors as well. [1],[6],[30] Similarly, a favorable outcome was much higher in patients with Grade IV than in Grade V. This reemphasizes the point that neurological status prior to surgery is a critical determinant of outcome.

Ultra early surgery (surgery performed within 24 h) has gained wider acceptance among neurosurgeons for treatment of good-grade SAH, though most surgeons are reluctant to do the same in poor-grade patients for fear of increased surgical difficulty. [3] However, there have been studies demonstrating that the incidence of complications such as failure to occlude the aneurysm, major vessel occlusion, intraoperative rupture or surgical contusions, were similar in poor-grade and good-grade patients. [3],[12] Le Roux et al., [12] concluded that except for severe cerebral swelling, the risk of surgical complications is similar in both groups. Patients with poor-grade SAH are more likely to have raised intracranial pressure as compared to good-grade patients. This may be because of associated infarcts or brain edema. In these patients a large craniotomy may be of advantage over GD-coiling to relieve the intracranial pressure (ICP). In the present series a large craniotomy was performed in all patients and in a few a decompressive hemicraniotomy was done at the time of primary surgery itself.

The protocol of early surgery to clip the aneurysm has resulted in saving a significant number of patients who would have otherwise died. Although about half the patients survived, overall favorable results in the present series were seen in only 13.3% of patients at the time of discharge. Of the patients who survived and were discharged from the hospital, almost 50% were lost to follow-up. It is quite possible that a significant proportion of these patients did not improve. Long-term follow-up was available in about half of these patients. Most of the patients who come to our Institute are from remote places with difficulties in transport, which is a major reason for incomplete follow-up in many patients. Of the patients who could be followed up, almost all continued to show progressive improvement in general condition and neurological status from the time of discharge. The improvement was seen in patients in with H and H Grade IV as well as V. This is an important observation demonstrating that a significant proportion of patients of poor-grade SAH can also have a near normal recovery in long-term follow-up. Therefore it may not be fair to deny patients with poor-grade SAH patients surgical treatment. Several authors have reported favorable outcome following endovascular treatment of patients with poor-grade SAH, ranging from 30-50% with a follow-up ranging from 6 months to 23 months. [31],[32],[33] Weir et al., [31] reported a mortality of 59%. High mean S100B values and persistent intracranial hypertension predicted a poor outcome. [33] These findings compare favorably with those published in surgical series for aggressively treated patients with H and H Grade IV or V.

Coiling therefore remains a good option for these patients. However, a majority of our patient population could not afford the cost. That prompted us to offer surgical clipping to these patients instead of the option of waiting for them to improve and allowing natural selection. In most of the recent series [Table 4], the results of conservative treatment have been dismal with almost 100% mortality. Favorable results after aneurysm clipping in poor-grade patients range from 27--76% [Table 4]. This variability is possibly due to the selection criteria for surgery. Possibly, an increasing number of poor-grade patients with ruptured anterior circulation aneurysms will be managed by interventional neuroradiologists. Sarrafzadeh et al.,[13] stated that aggressive treatment of patients with poor grade apparently reduced the mortality in some groups of patients. However, the reduction was at the expense of increasing the number of severely disabled survivors. [34] On the other hand, Laidlaw et al.,[3] found that only 15% of poor-grade surgical patients were alive but most were independent at three months. In our series also, more than two-thirds of the survivors who were available for long-term follow-up were independent. Therefore the perception that aggressive surgical management of patients with poor-grade SAH will yield a large number of severely disabled/vegetative persons may not be valid. The patients who survived demonstrated significant neurological improvement over a period of time. As it may not be possible to predict accurately preoperatively which patients will rebleed while waiting, it sounds reasonable to offer surgical clipping to patients with poor-grade SAH. In places where endovascular coiling is easily affordable, it remains a viable option.

 
 » References Top

1.Bailes JE, Spetzler RF, Hadley MN, Baldwin HZ. Management morbidity and mortality of poor -grade aneurysm patients. J Neurosurg 1990;72:559-66.  Back to cited text no. 1
[PUBMED]  [FULLTEXT]  
2.Hutchinson PJ, Power DM, Tripathi P, Kirkpatrick PJ. Outcome from poor grade aneurysmal subarachnoid haemorrhage-which poor grade subarachnoid haemorrhage patients benefit from aneurysm clipping? Br J Neurosurg 2000;14:105-9.  Back to cited text no. 2
[PUBMED]    
3.Laidlaw JD, Siu KH. Poor-grade aneurysmal subarachnoid hemorrhage: Outcome after treatment with urgent surgery. Neurosurgery 2003;53:1275-80.  Back to cited text no. 3
[PUBMED]  [FULLTEXT]  
4.Lee KC, Huh SK, Park HS, Shin YS, Lee KS. Management of poor-grade patients with ruptured intracranial aneurysm. Keio J Med 1997;46:69-73.  Back to cited text no. 4
[PUBMED]  [FULLTEXT]  
5.Le Roux PD, Elliott JP, Newell DW, Grady MS, Winn HR. Predicting outcome in poor-grade patients with subarachnoid hemorrhage: A retrospective review of 159 aggressively managed cases. J Neurosurg 1996;85:39-49.  Back to cited text no. 5
[PUBMED]  [FULLTEXT]  
6.Nowak G, Schwachenwald R, Arnold H. Early management in poor grade aneurysm patients. Acta Neurochir (Wien) 1994;126:33-7.  Back to cited text no. 6
[PUBMED]    
7.Sevrain L, Rabehenoina C, Hattab N, Freger P, Creissard P. Aneurysm with severe clinical manifestations (Hunt and Hess grade IV and V). A series of 66 cases. Neurochirurgie 1990;36:287-96.  Back to cited text no. 7
[PUBMED]    
8.Sasaki T, Sato M, Oinuma M, Sakuma J, Suzuki K, Matsumoto M, et al. Management of poor-grade patients with aneurysmal subarachnoid hemorrhage in the acute stage: Importance of close monitoring for neurological grade changes. Surg Neurol 2004;62:531-7.  Back to cited text no. 8
[PUBMED]  [FULLTEXT]  
9.Ungersbock K, Bocher-Schwarz H, Ulrich P, Wild A, Perneczky A. Aneurysm surgery of patients in poor grade condition. Indications and experience. Neurol Res 1994;16:31-4.  Back to cited text no. 9
    
10.Wilby MJ, Sharp M, Whitefield PC, Hutchinson PJ, Menon DK, Kirkpatrick PJ. Cost effective outcome for treating poor-grade subarachnoid hemorrhage. Stroke 2003;34:2508-11.  Back to cited text no. 10
    
11.Ogungbo B, Gregson BA, Blackburn A, Mendelow AD; Newcastle Subarachnoid Study Group. Trends over time in the management of subarachnoid haemorrhage in newcastle: Review of 1609 patients. Br J Neurosurg 2001;15:388-95.  Back to cited text no. 11
    
12.Le Roux PD, Elliott JP, Newell DW, Grady MS, Winn HR. The incidence of surgical complications is similar in good and poor grade patients undergoing repair of ruptured anterior circulation aneurysms: A retrospective review of 355 patients. Neurosurgery 1996;38:887-93.  Back to cited text no. 12
[PUBMED]  [FULLTEXT]  
13.Sarrafzadeh A, Haux D, Küchler I, Lanksch WR, Unterberg AW. Poor grade aneurysmal subarachnoid hemorrhage: Relationship of cerebral metabolism to outcome. J Neurosurg 2004;100:400-6.  Back to cited text no. 13
    
14.Auer LM. Acute operation and preventive nimodipine improve outcome in patients with ruptured cerebral aneurysms. Neurosurgery 1984;15:57-66.  Back to cited text no. 14
[PUBMED]    
15.Auer LM, Brandt L, Ebeling U, Gilsbach J, Groeger U, Harders A, et al. Nimodipine and early aneurysm operationfor good condition SAH patients. Acta Neurochir (Wien) 1986;82:7-13.  Back to cited text no. 15
[PUBMED]    
16.Gilsbach JM, Harders AG, Eggert HR, Harnyak ME. Early aneurysm surgery: A 7 year clinical practice report. Acta Neurochir (Wien) 1988;90:91-102.  Back to cited text no. 16
    
17.Ljunggren B, Saveland H, Brandt L, Zygmunt S. Early operation and overall outcome in aneurysmal subarachnoid haemorrhage. J Neurosurg 1985;62:547-51.  Back to cited text no. 17
    
18.Zentner J, Hoffmann C, Schramm J. Results of early surgery in poor-grade aneurysm patients. J Neurosurg Sci 1996;40:183-8.  Back to cited text no. 18
[PUBMED]    
19.Ando T, Sakai N, Yamada H, Iwai T, Nishimura Y, Hirata T, et al. Analysis of reruptured cerebral aneurysms and the prophylactic effects of barbiturate therapy on the early stage. Neurol Res 1989;11:245-8.  Back to cited text no. 19
[PUBMED]    
20.Aoyagi N, Hayakawa I. Study on early re-rupture of intracranial aneurysms. Acta Neurochir (Wien) 1996;138:12-8.  Back to cited text no. 20
[PUBMED]    
21.Fujii Y, Takeuchi S, Sasaki O, Minakawa T, Koike T, Tanaka R. Ultra-early rebleeding in spontaneous subarachnoid hemorrhage. J Neurosurg 1996;84:35-42.  Back to cited text no. 21
[PUBMED]  [FULLTEXT]  
22.Hillman J, von Essen C, Leszniewski W, Johansson I. Significance of "ultraearly" rebleeding in subarachnoid hemorrhage. J Neurosurg 1988;68:901-7.  Back to cited text no. 22
[PUBMED]  [FULLTEXT]  
23.Kassell NF, Torner JC. Aneurysmal rebleeding. A preliminary report from the Cooperative Aneurysm Study. Neurosurgery 1983;13:479-81.  Back to cited text no. 23
[PUBMED]    
24.Gruber A, Dietrich W, Czech T, Richling B. Recurrent aneurismal subarachnoid haemorrhage: Bleeding pattern and incidence of posthaemorrhagic ischaemic infarction. Br J Neurosurg 1997;11:121-6.  Back to cited text no. 24
[PUBMED]    
25.Inagawa T, Kamiya K, Ogasawara H, Yano T. Rebleeding of ruptured intracranial aneurysms in the acute stage. Surg Neurol 1987;28:93-9.  Back to cited text no. 25
[PUBMED]    
26.Pare L, Delfino R, Leblanc R. The relationship of ventricular drainage to aneurysmal rebleeding. J Neurosurg 1992;76:422-7.  Back to cited text no. 26
    
27.Rosenorn J, Eskesen V, Schmidt K, Ronde F. The risk of rebleeding from ruptured intracranial aneurysms. J Neurosurg 1987;67:329-32.  Back to cited text no. 27
    
28.Torner JC, Kassell NF, Wallace RB, Adams HP Jr. Preoperative prognostic factors for rebleeding and survival in aneurysm patients receiving antifibrinolytic therpy: Report of the Cooperative Aneurysm Study. Neurosurgery 1981;9:506-13.  Back to cited text no. 28
[PUBMED]    
29.Chiang VL, Claus EB, Awad IA. Toward more rational prediction of outcome in patients with high-grade subarachnoid hemorrhage. Neurosurgery 2000;46:28-35.  Back to cited text no. 29
[PUBMED]  [FULLTEXT]  
30.Gumprecht H, Winkler R, Gerstner W, Lumenta CB. Therapeutic management of grade IV aneurysm patients. Surg Neurol 1997;47:54-8.  Back to cited text no. 30
[PUBMED]  [FULLTEXT]  
31.Weir RU, Marcellus ML, Do HM, Steinberg GK, Marks MP. Aneurysmal subarachnoid hemorrhage in patients with Hunt and Hess grade 4 or 5: Treatment using the Guglielmi detachable coil system. AJNR Am J Neuroradiol 2003;24:585-90.  Back to cited text no. 31
[PUBMED]  [FULLTEXT]  
32.Bergui M, Bradac GB. Acute endovascular treatment of ruptured aneurysms in poor-grade patients. Neuroradiology 2004;46:161-4.  Back to cited text no. 32
[PUBMED]  [FULLTEXT]  
33.Pereira AR, Sanchez-Peña P, Biondi A, Sourour N, Boch AL, Colonne C, et al. Predictors of 1-year outcome after coiling for poor-grade subarachnoid aneurysmal hemorrhage. Neurocrit Care 2007;7:18-26.  Back to cited text no. 33
    
34.Cesarini KG, Hardemark HG, Persson L. Improved survival after aneurismal subarachnoid hemorrhage: Review of case management during a 12-year period. J Neurosurg 1999;90:664-72.  Back to cited text no. 34
    



 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]

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[Pubmed] | [DOI]
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