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Table of Contents    
Year : 2012  |  Volume : 60  |  Issue : 3  |  Page : 283-287

Impact of Hunt-Hess grade on the glycemic status of aneurysmal subarachnoid hemorrhage patients

1 Department of Neurosurgery, Thomas Jefferson University, Philadelphia, PA, USA, USA
2 Department of Biostatistics, The Rothman Institute, Philadelphia, PA, USA, USA
3 Department of Neurosurgery and Neurology, Thomas Jefferson University, Philadelphia, PA, USA

Date of Submission28-Feb-2012
Date of Decision14-Apr-2012
Date of Acceptance18-May-2012
Date of Web Publication14-Jul-2012

Correspondence Address:
Sayantani Ghosh
136, Dr. Meghnad Saha Road, Pratyasha Apartments, Flat-4C, Kolkata 700074, India
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0028-3886.98510

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 » Abstract 

Objective: This study has explored the impact of Hunt-Hess (H-H) grade of aneurysmal subarachnoid hemorrhage (aSAH) on the glycemic status of such patients during their intensive care unit (ICU) stay and has also analyzed whether H-H grade predicts their outcome independent of their glycemic status. Materials and Methods: This was a retrospective case record review of prospectively maintained database of 1090 previously non-diabetic aSAH patients admitted to Thomas Jefferson University Hospital, Philadelphia. H-H grade of SAH, serum and CSF glucose on admission, serum glucose on the day of surgery and 14 days post-surgery, as well as the extended Glasgow Outcome Score (GOS-E score) at discharge were noted. After univariate analysis, significant variables (P < 0.05) were entered into a logistic regression model to identify significant associations with admission H-H grade. Results: Although admission serum glucose was significantly higher for H-H grades 4-5 than grades 1-3 (P < 0.001); after postoperative day 4, the difference between the H-H grades got blurred. Admission CSF glucose was also significantly higher for H-H grades 3-4 than for grades 1-3 and 5 (P < 0.001). H-H grades 4-5 were related with higher incidences of both hypoglycemia (serum glucose level < 80 mg/dl) and hyperglycemia (serum glucose level > 200 mg/dl) (P < 0.001) during the 14-day period of ICU stay. Also, the relationship between serum and CSF glucose levels at admission increased with HH grades 1 through 4, but became negative and more tightly bound at H-H grade 5. Admission H-H grades 4-5 contributed to poor outcome compared to lower H-H grades (P < 0.0001). Conclusion: Poor admission H-H grades lead to poor immediate glycemic status as well as poor short-term outcome, and it is dependent on serum glucose but independent of CSF glucose in predicting the outcome.

Keywords: Aneurysmal subarachnoid hemorrhage, CSF glucose, H-H grade, outcome, serum glucose

How to cite this article:
Ghosh S, Dey S, Maltenfort M, Vibbert M, Urtecho J, Rincon F, Jallo J. Impact of Hunt-Hess grade on the glycemic status of aneurysmal subarachnoid hemorrhage patients. Neurol India 2012;60:283-7

How to cite this URL:
Ghosh S, Dey S, Maltenfort M, Vibbert M, Urtecho J, Rincon F, Jallo J. Impact of Hunt-Hess grade on the glycemic status of aneurysmal subarachnoid hemorrhage patients. Neurol India [serial online] 2012 [cited 2022 Jan 28];60:283-7. Available from: https://www.neurologyindia.com/text.asp?2012/60/3/283/98510

 » Introduction Top

Aneurysmal subarachnoid hemorrhage (aSAH) accounts for about 1.9-3% of all cerebrovascular diseases, [1] and 51% of the patients die in the first 30 days of the event and one-third of the survivors require lifelong care. [2] The commonly used grading scale to assess the clinical severity of SAH is that described by Hunt and Hess, where increasing grade is associated with worse outcome. [3] Hyperglycemia is a common problem in aSAH [4] and occurs in 70%-90% of patients. [5] Persistent hyperglycemia is associated with poor outcomes in different acute medical and surgical conditions. [6],[7] In aSAH, hyperglycemia has been shown to be associated with development of clinical vasospasm, [5] new neurologic deficits, [8] poor functional outcome, and increased hospital stay. [8] Some studies have shown that intensive insulin therapy improves the outcome. [9],[10],[11] Thus, treatment of persistent hyperglycemia is an attractive management strategy to improve outcomes in patients with aSAH. In this study, we have assessed the impact of admission Hunt-Hess (H-H) grade of aSAH patients on their serum and CSF glucose levels during their stay in the intensive care unit (ICU) in order to explore whether the severity of SAH affect the glycemic status of the patients. We have also considered whether H-H grade can predict the outcome of such patients independent of their glycemic status.

 » Materials and Methods Top

A retrospective review of aSAH patients, admitted from January 2006 to April 2010, was performed from a prospectively maintained database at Thomas Jefferson University Hospital, Philadelphia. Approval for the collection and review of data was obtained from the Institutional Review Board at the Thomas Jefferson University, Philadelphia. Diagnosis of aSAH was established on the basis of conventional computed tomography (CT) or CT/magnetic resonance (MR) angiography. Patients who were admitted >48 h after the onset of SAH (139 patients) and patients who had a prior history of diabetes (69 patients) were excluded from the study. Total 1090 patients met the inclusion criteria. Admission H-H grade, CSF and serum glucose levels, serum glucose on the day of surgery and on day 14 following surgery, and extended Glasgow Outcome Score (GOS-E) at discharge were documented. Patients with H-H grade 1-3 were considered as mild to moderate SAH and those with grade 4-5 as severe SAH. GOS-E score ≥ 7 has been taken as a good outcome. GOS-E score was further dichotomized into 1 and 2 to 8 for death and survival, respectively.

Statistical analysis

All data were analyzed using JMP 7.0.2, SAS Institute, Cary, NC. Chi-square test was performed for rate versus rate, and logistic regression was used for rate versus continuous variable or between two continuous variables, and P values and 95% confidence interval (CI) were calculated. Multivariate analysis was done to compare the effect of serum glucose, CSF glucose, and SAH grade with the outcome. Relationship between serum and CSF glucose was established via Spearman's rank correlation coefficient.

 » Results Top

Of the 1090 patients included in the study, 429 (39.36%) were males. The mean age of the females was 4 years less than that of the males. [Table 1] shows the baseline characteristics of the study population.
Table 1: Baseline characteristics of the study population

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Hyperglycemia at admission was termed as a serum glucose reading of >140 mg/dl on admission and 869 (74.22%) patients were found to have hyperglycemia at admission. Patients with hyperglycemia had 20.48% chance of a good outcome compared to a 64.85% chance of good outcome in patients with no hyperglycemia (P < 0.0001). Patients with hyperglycemia at admission also had a higher risk of death (20.58%). Odds ratio (OR) for a poor outcome per 1 mg/dl rise in serum glucose on the day of the admission was 1.015 (95% CI, 1.013-1.017) and OR for death with per 1 mg/ dl rise in serum glucose on admission was 1.0175 (95% CI, 1.015-1.02).

Of the 1090 patients, 760 (69.72%) patients had severe grade SAH (H-H grades 4-5) on admission. Patients with severe grade SAH had poor outcome compared to those who did not have (P < 0.0001) [Figure 1]. The admission serum glucose also differed significantly for different grades of SAH (P < 0.0001); with a trend of rising serum glucose with increasing SAH grades from 1 to 4 and then a slight dip in patient with grade 5. When the effect of admission SAH grade on the level of serum glucose throughout their stay in the ICU was analyzed, after the fourth postoperative day, the difference between the grades got blurred [Figure 2].
Figure 1: The effect of the severity of SAH on the patient outcome

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Figure 2: The effect of admission SAH grade on the glycemic status of the patients throughout their stay

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Nine hundred and three (75.75%) individuals had serum glucose reading of >200 mg/dl at least once in the 2 weeks following surgery. Of these patients, 29.46% had a good outcome (GOS-E score ≥ 7) compared to 65.4% in individuals who did not have a hyperglycemic episode (P < 0.0001). The mean level of serum glucose in the period of 14 days post-surgery was 5.46 mg/dl higher in patients having a worse prognosis (GOS-E score ≤ 6) than in those having a good outcome.

Hypoglycemia was considered when serum glucose was <80 mg/dl and was documented in 13.25% of the patients; 5.7% of patients with hypoglycemia had a good outcome compared to 75.85% of patients without hypoglycemia (P < 0.0001) and 48.10% of patients with hypoglycemia died compared to only 10.54% of patients without hypoglycemia (P < 0.0001). Of the patients with hypoglycemia, 95.57% of patients had a previous episode of hyperglycemia (serum glucose > 200 mg/dl), whereas only 72.73% of patients with no hypoglycemia had a single reading of serum glucose (>200 mg/dl). Incidences of both hypoglycemic episode and extreme hyperglycemic episode were found to be related to the severity of SAH. While the risk of hyperglycemic episodes in patients with severe grade SAH was 3.5- fold, the risk of hypoglycemic episodes was 16.5- fold (P < 0.0001) [Figure 3]. SAH grade was found to be dependent of serum glucose in determining both good outcome and mortality.
Figure 3: The distribution of hyperglycemic and hypoglycemic episodes according to the severity of SAH

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The OR for poor outcome per 1 mg/dl increase in admission CSF glucose level was 1.087 (95% CI, 1.078-1.096) and OR for death was 1.048 (95% CI, 1.041-1.055). The admission CSF glucose levels in patients with H-H grades 3 and 4 were significantly higher than for patients with H-H grades 1, 2, or 5 (P < 0.0001) [Figure 4]. Correlation between CSF and serum glucose at admission was 0.52. While studying the serum and CSF glucose for the individual H-H grades, the relationship was linear from Grade 1 to 4 (Spearman's ρ increased form 0.41 to 0.87), then it was negative but more tightly bound at H-H grade 5 [Figure 5]. SAH grade was found to be independent of CSF glucose in determining both good outcome and mortality.
Figure 4: The mean admission serum and CSF glucose levels for each of the grades

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Figure 5: The relationship between serum and CSF glucose for various grades of SAH

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 » Discussion Top

Hyperglycemia is a frequent finding in various types of brain injury and may be associated with premorbid diabetic glucose metabolism [12] or a stress response. [13],[14] Many experimental studies have indicated that hyperglycemia may increase brain edema, [5] inflammatory reaction, [15] free radical injury [16] or apoptotic cell death. [17] Hyperglycemia has been shown to be associated with more severe stroke. [18],[19] Several studies have analyzed the effect of hyperglycemia on the clinical outcome in SAH patients. [4],[7],[8],[11],[20],[21],[22],[23],[24],[25],[26],[27],[28] In one study, hyperglycemia has been shown to be associated with high short-term mortality, [25] whereas the other study failed to show such a relation. [28] Some studies have shown hyperglycemia as an independent predictor of poor outcome regardless of the severity of the hemorrhage. [7],[8],[11],[20],[21],[23],[24]

However, there is hardly any data on the impact of the severity of SAH on the glycemic status and discharge outcome. Our study showed that hyperglycemia at admission was associated with both poor outcome and increased mortality. This study also demonstrated poor outcome and increased mortality in individuals with serum glucose >200 mg/dl for at least once in the 2 weeks following the surgery and also in individuals with even a single episode of hypoglycemia. Both these associations were seen with more severe disease pathology. There was linear relation between serum glucose levels and the severity of SAH. When the effect of admission SAH grade on the level of serum glucose throughout the ICU stay was studied, it was apparent that after the postoperative day 4, there existed little difference between the grades. Severe SAH on admission contributed to poor outcome at discharge in most patients and SAH grade was found to be dependent on serum glucose in determining both good outcome and mortality. However, poor outcome in severe SAH may be a multi-factorial process where the glycemic status is one of the factors. Higher CSF glucose at admission was also associated with poor functional outcome and higher mortality. Admission CSF glucose was significantly higher in patients with SAH grades 3-4 than in patients with SAH grades 1, 2 or 5. Correlation between CSF and serum glucose at admission was 0.52. The relationship between serum glucose and CSF glucose increased from grade 1 to 4. SAH grade was found to be independent of CSF glucose in determining both good outcome and mortality.

Our study has certain limitations. It was a retrospective analysis; however, it was obtained from a prospectively designed database. The data was also limited to a single institution experience. The other limitation was that we studied the outcome on post-surgery day 14 and have not considered the outcome at 3 months of follow-up, in order to assess the long-term mortality. However, unlike the previous studies, we included patients with SAH within 48 h of onset only. Most of the previous studies either did not state the time between onset of SAH and admission or were limited by an enrollment period that was too long. Long interval between the onset and admission might explain the independent association observed between glucose levels and poor outcome as the clinical status can improve dramatically within 48 h of onset of SAH, whereas high glucose level on day 3 can still be a reflection of the severity of the SAH. Also, we have excluded known patients of diabetes to correctly assess the burden of hyperglycemia in SAH. Besides, we have taken a large sample size to validate the results.

We conclude that with the severity of the SAH, the immediate glycemic status also worsens resulting in poor short-term outcome. Higher SAH grade is dependent on the serum glucose level but independent of the CSF glucose level in predicting the outcome.

 » References Top

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2.Hop JW, Rinkel GJ, Algra A, van Gijn J. Case-fatality rates and functional outcome after subarachnoid hemorrhage: A systematic review. Stroke 1997;28:660-4.  Back to cited text no. 2
3.Hunt W, Hess R. Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg 1968;28:14-20.  Back to cited text no. 3
4.Nicolaysen L. Glykosurie bei meningealer Blutung. Acta Med Scand 1925;62:392-4.  Back to cited text no. 4
5.Badjatia N, Topcuoglu MA, Buonanno FS, Smith EE, Nogueira RG, Rordorf GA, et al. Relationship between hyperglycemia and symptomatic vasospasm after subarachnoid hemorrhage. Crit Care Med 2005;33:1603-9; quiz 1623.  Back to cited text no. 5
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7.Baird TA, Parsons MW, Phanh T, Butcher KS, Desmond PM, Tress BM, et al. Persistent post stroke hyperglycemia is independently associated with infarct expansion and worse clinical outcome. Stroke 2003;34:2208-14.  Back to cited text no. 7
8.Pasternak JJ, McGregor DG, Schroeder DR, Lanier WL, Shi Q, Hindman BJ, et al. IHAST Investigators. Hyperglycemia in patients undergoing cerebral aneurysm surgery: Its association with long-term gross neurologic and neuropsychological function. Mayo Clin Proc 2008;83:406-17.  Back to cited text no. 8
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10.Van den Berghe G, Wilmer A, Hermans G, Meersseman W, Wouters PJ, Milants I, et al. Intensive insulin therapy in the medical ICU. N Engl J Med 2006;354:449-61.  Back to cited text no. 10
11.Van den Berghe G, Wouters P, Weekers F, Verwaest C, Bruyninckx F, Schetz M, et al. Intensive insulin therapy in the critically ill patients. N Engl J Med 2001;345:1359-67.  Back to cited text no. 11
12.Latorre JG, Chou SH, Nogueira RG, Singhal AB, Carter SB, Ogilvy CS, et al. Effective glycemic control with aggressive hyperglycemia management is associated with improved outcome in aneurysmal subarachnoid hemorrhage. Stroke 2009;40:1644-52.  Back to cited text no. 12
13.Van Kooten F, Hoogerbrugge N, Naarding P, Koudstaal PJ. Hyperglycemia in the acute phase of stroke is not caused by stress. Stroke 1993;24:1129-32.  Back to cited text no. 13
14.Slowik A, Turaj W, Pankiewicz J, Dziedzic T, Szermer P, Szczudlik A. Hypercortisolemia in acute stroke is related to the inflammatory response. J Neurol Sci 2002;196:27-32.  Back to cited text no. 14
15.Weir CJ, Murray GD, Dyker AG, Lees KR. Is hyperglycaemia an independent predictor of poor outcome after acute stroke? Results of a long-term follow up study. BMJ 1997;314:1303-6.  Back to cited text no. 15
16.Gong C, Hoff JT, Keep RF. Acute inflammatory reaction following experimental intracerebral hemorrhage in rat. Brain Res 2000;871:57- 65.  Back to cited text no. 16
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18.Araki N, Greenberg JH, Sladky JT, Uematsu D, Karp A, Reivich M. The effect of hyperglycemia on intracellular calcium in stroke. J Cereb Blood Flow Metab 1992;12:469-76.  Back to cited text no. 18
19.Parsons MW, Barber PA, Desmond PM, Baird TA, Darby DG, Byrnes G, et al. Acute hyperglycemia adversely affects stroke outcome: A magnetic resonance imaging spectroscopy study. Ann Neurol 2002;52:20-8.  Back to cited text no. 19
20.Rincon F, Gordon E, Starke RM, Buitrago MM, Fernandez A, Schmidt JM, et al. Predictors of long-term shunt-dependent hydrocephalus after aneurysmal subarachnoid hemorrhage. J Neurosurg 2010;113:774-80.  Back to cited text no. 20
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26.Lee SH, Lim JS, Kim N, Yoon BW. Effects of admission glucose level on mortality after subarachnoid hemorrhage: A comparison between short-term and long-term mortality. J Neurol Sci 2008;275:18-21.  Back to cited text no. 26
27.Schlenk F, Nagel A, Graetz D, Sarrafzadeh AS. Hyperglycemia and cerebral glucose in aneurysmal subarachnoid hemorrhage. Intensive Care Med 2008;34:1200-7.  Back to cited text no. 27
28.Schlenk F, Vajkoczy P, Sarrafzadeh A. Inpatient hyperglycemia following aneurysmal subarachnoid hemorrhage: Relation to cerebral metabolism and outcome. Neurocrit Care 2009;11:56-63.  Back to cited text no. 28


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

  [Table 1]

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