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 Table of Contents  
Year : 2021  |  Volume : 9  |  Issue : 2  |  Page : 84-89

Do intra operative brain conditions during clipping for ruptured intra cranial aneurysms affect the outcome? Being devil's advocate

1 Department of Neurosurgery, PGIMER, Chandigarh, India
2 Department of Neurosurgery, Nizam's Institute of Medical Sciences, Hyderabad, Telangana, India
3 Department of Anaesthesia, PGIMER, Chandigarh, India

Date of Submission23-Jan-2022
Date of Decision29-Jan-2022
Date of Acceptance02-Feb-2022
Date of Web Publication5-Apr-2022

Correspondence Address:
Dr. Ashish Aggarwal
Department of Neurosurgery, PGIMER, Chandigarh
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jcvs.jcvs_11_22

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Introduction: For a disease like aneurysmal subarachnoid haemorrhage (aSAH) which continues to have high morbidity and mortality, prognostication is imperative. This gives realistic goals to both the health-care worker and the patient. Unfavourable brain conditions during surgery like dural bulge, brain swelling, petechial haemorrhages, need for ventricular tap are conventionally thought to be harbingers of poor outcomes. But is it really so?
Methods: Fifty-four consecutively operated patients of aSAH were studied. Clinical grade at admission (H and H, World Federation of Neurosurgical Societies (WFNS)), Dural bulge, brain swelling, petechial haemorrhages, need for ventricular tap, and brain pulsatility were studied for outcome parameters like Glasgow outcome scale (GOS) at 1 and 3 months and development of focal deficits.
Results: H and H and WFNS grades had a significant correlation with GOS. We found that the need for augmentation duraplasty had a significant association with the outcome and appearance of focal deficits. However, unfavourable brain conditions like--dural bulge, brain swelling, petechial haemorrhages, need for ventricular tap, absence of brain pulsatility during surgery did not have a significant impact on the outcome.
Conclusions: Clinical grading by far remains the best predictor of outcome. Intra-operative brain conditions did not have a bearing on the outcome. The mechanism by which poor grade patients exhibit poor outcomes remains elusive. At least in the present study, it was not by way of manifesting as unfavourable brain conditions. A word of caution--further large studies are required before definite conclusions can be drawn.

Keywords: Aneurysmal subarachnoid haemorrhage, brain bulge, brain pulsatility, H and H, WFNS

How to cite this article:
Singla N, Reddy K R, Aggarwal A, Chhabra R, Bhagat H. Do intra operative brain conditions during clipping for ruptured intra cranial aneurysms affect the outcome? Being devil's advocate. J Cerebrovasc Sci 2021;9:84-9

How to cite this URL:
Singla N, Reddy K R, Aggarwal A, Chhabra R, Bhagat H. Do intra operative brain conditions during clipping for ruptured intra cranial aneurysms affect the outcome? Being devil's advocate. J Cerebrovasc Sci [serial online] 2021 [cited 2022 May 22];9:84-9. Available from: http://www.jcvs.com/text.asp?2021/9/2/84/342555

  Introduction Top

Aneurysmal subarachnoid haemorrhage (aSAH) despite advances in diagnostic and therapeutic measures continues to be a disease with high morbidity and mortality.[1],[2],[3]

Few well-documented factors which affect prognosis are– age, presence or absence of comorbidities, clinical-grade at admission (WFNS, H and H), fisher grade, vasospasm, hydrocephalus, intra-operative aneurysm rupture, duration of temporary clipping.[4],[5],[6],[7],[8],[9],[10]

It is a commonly accepted that poor brain conditions, encountered intraoperatively, do not auger well with the outcome.[8] Unfavourable intra-operative conditions such as dural bulge, brain swelling, petechial haemorrhages actually are a manifestation of severe brain damage and hence should have a worse outcome. Brain bulge, for example, may portend a poor outcome because of the need to use retractors, increased incidence of pial breach during dissection and lack of proper working space with inadequate visualisation of vascular anatomy. All these appear logical and have been accepted as generally true. However, the effects of intra-operative brain conditions on outcome have been scarcely studied objectively in the past. The present study is an attempt in this direction.

  Methods Top

A prospective study was done on 54 consecutive cases of ruptured intracranial aneurysm. Patients underwent clipping by a single surgeon at a tertiary care medical centre. Approval was taken from the institute ethics committee (reference no. NK/1417/M.Ch./2833) Informed consent was obtained from the patients.

As per department protocol, after clinical examination and relevant investigations, patients were categorized into good and poor grades based on H and H and WFNS. Good grade Subarachnoid haemorrhage (SAH) patients underwent surgery. Poor grade patients were managed conservatively till they improved. Excluded from the study were patients with unruptured aneurysm, pregnant patients or if there was.

During surgery the following intraoperative brain parameters were observed and recorded namely dural bulge, brain bulge, any petechial haemorrhages over the brain surface, brain laxity after cisternal drainage, need for ventricular tap, pial breach during dissection, difficult aneurysmal dissection, brain laxity after clipping and at the time of dural closure, requirement of augmentation duroplasty. Cases in whom there was intra-operative rupture were excluded from the study.

Anaesthetic techniques were fairly standardised. Patients were induced with thiopentone/propofol and maintained with IV anaesthetics. Target PaCO2 was between 30 and 35 mm Hg. Normotension and Normothermia were maintained. Twenty percent mannitol (w/v) was given at the dose 0.5–1.0 g/kg at the time of skin incision. Patients were excluded if there was any deviation from the protocol.

Brain bulge was measured using four-point scale: 1 = no swelling, 2 = minimal swelling but acceptable, 3 = serious swelling but no specific change in management required, 4 = severe brain swelling requiring some intervention such as a change in position, further reduction in PaCO2 and additional mannitol or furosemide.

The primary outcome was GOS at 3 months. The secondary outcome was measured in the form of– a. Focal deficit b. GOS at 1st month.

  Observation and Results Top

Demographic data

The median age of the study group was 48 years with a range from 17 to 65 years. There were 30 males and 24 females in the study population.

Grading of subarachnoid haemorrhage patients

The clinical grading of SAH patients was done at the time of hospital admission by H and H and WFNS grading system [Table 1]. H and H Grade 3, 4, 5 and WFNS Grade 3, 4 were categorized as poor grade for the analysis.
Table 1: Distribution of patients amongst various grading scales

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Intra operative brain parameters

During surgery, various intraoperative parameters were noted [Table 2]. We noticed that the degree of the dural bulge and brain swelling usually go hand in hand. After opening the dura, the pulsatility of the brain was noted before starting microscopic dissection.
Table 2: Intra operative brain conditions

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Furthermore, petechial hemorrhages were seen in 10 patients (18.5%), ventricular tap was done in two patients (3.7%), pial breach was present in 11 patients (20.4%), aneurysm dissection was difficult in 25 patients (46.3%).


All the above-mentioned factors were studied both as univariate and multivariate variables. For multivariate analysis, the following methodology was used. We combined five unfavourable factors:

  • brain swelling--Grade 3 and 4,
  • brain pulsatility--none to moderate
  • difficult aneurysmal dissection,
  • presence of pial breach
  • presence of petechial haemorrhages.

A score of one point was given for each of these unfavourable factors. These patients were then classified into two groups. Group A had <3 unfavourable factors and Group B had ≥3 unfavorable factors. These groups were then analyzed for outcome parameters.

Analysis of various pre and intra-operative parameters against GOS at 1 month and development of focal deficits revealed that significant parameters were H and H, WFNS grading and need for augmentation duraplasty. Intra-operative brain conditions largely do not have an effect on GOS [Table 3]. Group B patients did not have any correlation with GOS but had higher chances of developing focal deficits. Surprisingly, even patients with difficult aneurysm dissection did not have an increased incidence of focal deficits.
Table 3: Various intra-operative brain parameters versus GOS at first month and focal deficits

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Similar results were obtained when these parameters were analysed at 3 months [Table 4]. H and H and WFNS grading at admission and need for augmentation duraplasty had statistically significant correlation with GOS at 3 months. The rest of the brain conditions did not affect the outcome significantly.
Table 4: Various intra-operative brain parameters and GOS score at three months

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An analysis of clinical-grade with intra-operative findings was done [Table 5] and the results were a little surprising. Distribution of intra-operative poor brain conditions among good and poor H and H and WFNS grades was comparable with no statistical difference among the two. A poor clinical grade did not manifest itself as unfavourable intra-operative brain conditions.
Table 5: Comparison of H and H grade and WFNS grade and intra op findings

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  Discussion Top

Aneurysmal SAH is a multifactorial disease in terms of aetiology and prognosis. For a disease which continues to have a high morbidity and mortality, it is imperative to categorise the factors which affect the outcome. This helps in prognostication and sets realistic goals of outcome based on scientific evidence.

We studied the effect of various pre-operative and intra-operative variables against outcome at 1 and 3 months. Our search of the English literature failed to reveal any such previous study.

Poor grade H and H and WFNS patients had more incidence of focal deficits and worse GOS at 3 months. This has been brought out earlier in large no of studies.[4],[10],[11] However, a rather eye-opening finding was the failure of correlation of unfavourable brain conditions with the development of focal deficits or GOS at 1 and 3 months. Even a difficult aneurysm dissection did not produce added deficits which was surprising.

Amazingly, even multivariate analysis; i.e., Group B patients failed to show any significant effect on GOS, though they had significant correlation with focal deficits. This is in contrast to findings by Mahaney et al. in a study of 1000 patients.[11]

The findings of the study show a very unique and unexpected trend. Conventional wisdom tells us that intra-operative findings like– dural bulge, swollen brain, petechial haemorrhages portray a picture of underlying severe brain insult and hence, should have a poor outcome.[12],[13],[14],[15] Furthermore, difficult aneurysm dissection has more potential for damage to small perforators in the vicinity of aneurysm in addition to prolonging the surgical time. All these should translate into a poor outcome with increased chances of focal deficits. However, results to the contrary were obtained in the present study.

An analysis of pre-operative clinical grading and intra-operative findings was done with the following query in mind--Do the patients of poor grade SAH manifest unfavourable brain conditions during surgery? The results answered this query in negative. There was comparable distribution of unfavourable brain conditions among good and poor grade patients.

However then, the question arises–What is the mechanism by which a poor clinical grade patient has a poor outcome if it is not via bad brain conditions?

Before the study, our accepted wisdom was that poor grade patients have suffered a severe form of brain damage at the time of ictus itself. This severe brain insult should have manifested as dural bulge, brain swelling or petechial haemorrhages (so-called angry-looking brain). By this simple corollary poor outcome can be explained (poor grade SAH– poor brain conditions---poor outcome). However, the present study busted this myth. During analysis, the findings as depicted in [Table 5] were eye-openers.

A plausible explanation for this somewhat bizarre finding is that patients in the poor clinical grade were not operated on at the outset. Good grade patients were operated on immediately. A subset of patients who were initially poor grade but improved, later on, were taken up for surgery. We assume that in these patients the adverse brain conditions might have improved over a period of time. And by the time we took them up for surgery, the brain swelling, etc., would have settled. However, this still fails to explain poor GOS in these very patients. Patients who were poor grades on H and H and WFNS had bad outcomes, but this unfavorable outcome could not be explained by unfavourable brain conditions.

Conversely, looking at the data of patients who were in good clinical grade but had bad intra-operative conditions, we again realised that clinical-grade itself was predictor of outcome irrespective of brain conditions. This came out whatsoever way the data were analysed.

Does this imply that in poor-grade patients there are some other mechanisms (yet unidentified) which accounts for and explain major brain insult and hence their poor clinical grade?

A plausible explanation can be extrapolated from the traumatic brain injury (TBI) model. Recent literature review suggests that cisternostomy while operating on TBI gives better results.[15]

We have no hesitation in accepting that even we were surprised by the results of this study. It is a totally contrarian view to the accepted wisdom. Even we are taking the results with a pinch of salt. However, we feel that this is how sometimes some longstanding myths are broken. Definitely, several long-term studies with more number of patients are required.

  Conclusions Top

Clinical grading of aSAH patients still remains by far the best predictor of outcome. Various unfavourable brain conditions failed to reach statistical significance to have a bearing on the outcome. The mechanism by which poor grade patients behave badly remains unexplained. At least it is not bad intra-operative brain conditions. The surgeon should not get bogged down by bad brain conditions thinking that patient is going to have a poor outcome but rather should let anaesthetic agents have their effect and then proceed confidently.

Limitations of the study

The study population had too few patients and future studies with a larger number of patients are needed to reach a meaningful conclusion.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants/their attendants included in the study.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

  References Top

Bederson JB, Connolly ES Jr., Batjer HH, Dacey RG, Dion JE, Diringer MN, et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: A statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke 2009;40:994-1025.  Back to cited text no. 1
Graf CJ, Nibbelink DW. Cooperative study of intracranial aneurysms and subarachnoid hemorrhage. Report on a randomized treatment study. 3. Intracranial surgery. Stroke 1974;5:557-601.  Back to cited text no. 2
King JT Jr. Epidemiology of aneurysmal subarachnoid hemorrhage. Neuroimaging Clin N Am 1997;7:659-68.  Back to cited text no. 3
Aggarwal A, Dhandapani S, Praneeth K, Sodhi HB, Pal SS, Gaudihalli S, et al. Comparative evaluation of H&H and WFNS grading scales with modified H&H (sans systemic disease): A study on 1000 patients with subarachnoid hemorrhage. Neurosurg Rev 2018;41:241-7.  Back to cited text no. 4
Auer LM. Unfavorable outcome following early surgical repair of ruptured cerebral aneurysms – A critical review of 238 patients. Surg Neurol 1991;35:152-8.  Back to cited text no. 5
Chandler JP, Getch CC, Batjer HH. Intraoperative aneurysm rupture and complication avoidance. Neurosurg Clin N Am 1998;9:861-8.  Back to cited text no. 6
Chong JY, Kim DW, Jwa CS, Yi HJ, Ko Y, Kim KM. Impact of cardio-pulmonary and intraoperative factors on occurrence of cerebral infarction after early surgical repair of the ruptured cerebral aneurysms. J Korean Neurosurg Soc 2008;43:90-6.  Back to cited text no. 7
Guy J, McGrath BJ, Borel CO, Friedman AH, Warner DS. Perioperative management of aneurysmal subarachnoid hemorrhage: Part 1. Operative management. Anesth Analg 1995;81:1060-72.  Back to cited text no. 8
Niskanen MM, Hernesniemi JA, Vapalahti MP, Kari A. One-year outcome in early aneurysm surgery: Prediction of outcome. Acta Neurochir (Wien) 1993;123:25-32.  Back to cited text no. 9
Sodhi HB, Savardekar AR, Mohindra S, Chhabra R, Gupta V, Gupta SK. The clinical profile, management, and overall outcome of aneurysmal subarachnoid hemorrhage at the neurosurgical unit of a tertiary care center in India. J Neurosci Rural Pract 2014;5:118-26.  Back to cited text no. 10
[PUBMED]  [Full text]  
Mahaney KB, Todd MM, Bayman EO, Torner JC, IHAST Investigators. Acute postoperative neurological deterioration associated with surgery for ruptured intracranial aneurysm: Incidence, predictors, and outcomes. J Neurosurg 2012;116:1267-78.  Back to cited text no. 11
Säveland H, Hillman J, Brandt L, Edner G, Jakobsson KE, Algers G. Overall outcome in aneurysmal subarachnoid hemorrhage. A prospective study from neurosurgical units in Sweden during a 1-year period. J Neurosurg 1992;76:729-34.  Back to cited text no. 12
Seiler RW, Reulen HJ, Huber P, Grolimund P, Ebeling U, Steiger HJ. Outcome of aneurysmal subarachnoid hemorrhage in a hospital population: A prospective study including early operation, intravenous nimodipine, and transcranial Doppler ultrasound. Neurosurgery 1988;23:598-604.  Back to cited text no. 13
Whittle IR, Viswanathan R. Acute intraoperative brain herniation during elective neurosurgery: Pathophysiology and management considerations. J Neurol Neurosurg Psychiatry 1996;61:584-90.  Back to cited text no. 14
Cherian I, Bernardo A, Grasso G. Cisternostomy for traumatic brain injury: Pathophysiologic mechanisms and surgical technical notes. World Neurosurg 2016;89:51-7.  Back to cited text no. 15


  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]


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