Radiological Estimation of Intracranial Blood Volume and Occurrence of Hydrocephalus Determines Stress-Induced Hyperglycemia After Aneurysmal Subarachnoid Hemorrhage

  • Joshua A Santucci
  • Stephen R Ross
  • John C Greenert
  • Faranak Aghaei
  • Lance Ford
  • Kimberly M Hollabaugh
  • Benjamin O Cornwell
  • Dee H Wu
  • Bin Zheng
  • Bradley N Bohnstedt
  • Bappaditya RayEmail author
Original Article


Acute phase after aneurysmal subarachnoid hemorrhage (aSAH) is associated with several metabolic derangements including stress-induced hyperglycemia (SIH). The present study is designed to identify objective radiological determinants for SIH to better understand its contributory role in clinical outcomes after aSAH. A computer-aided detection tool was used to segment admission computed tomography (CT) images of aSAH patients to estimate intracranial blood and cerebrospinal fluid volumes. Modified Graeb score (mGS) was used as a semi-quantitative measure to estimate degree of hydrocephalus. The relationship between glycemic gap (GG) determined SIH, mGS, and estimated intracranial blood and cerebrospinal fluid volumes were evaluated using linear regression. Ninety-four [94/187 (50.3%)] among the study cohort had SIH (defined as GG > 26.7 mg/dl). Patients with SIH had 14.3 ml/1000 ml more intracranial blood volume as compared to those without SIH [39.6 ml (95% confidence interval, CI, 33.6 to 45.5) vs. 25.3 ml (95% CI 20.6 to 29.9), p = 0.0002]. Linear regression analysis of mGS with GG showed each unit increase in mGS resulted in 1.2 mg/dl increase in GG [p = 0.002]. Patients with SIH had higher mGS [median 4.0, interquartile range, IQR 2.0–7.0] as compared to those without SIH [median 2.0, IQR 0.0–6.0], p = 0.002. Patients with third ventricular blood on admission CT scan were more likely to develop SIH [67/118 (56.8%) vs. 27/69 (39.1%), p = 0.023]. Hence, the present study, using unbiased SIH definition and objective CT scan parameters, reports “dose-dependent” radiological features resulting in SIH. Such findings allude to a brain injury-stress response-neuroendocrine axis in etiopathogenesis of SIH.


Hemorrhagic stroke Hyperglycemia Hydrocephalus Delayed cerebral ischemia Shunt 



Analysis of variance


Admission glucose


Aneurysmal subarachnoid hemorrhage


Area under receiver operator characteristic


Bicaudate index


Computer-aided detection


Confidence interval


Cerebrospinal fluid


Computed tomography


Delayed cerebral ischemia


External ventricular drain


Glycemic gap


Graphic user interface


Glycated hemoglobin


Hunt and Hess


Hounsfield unit


Interquartile range


Modified Fisher score


Modified Graeb score


Neurosciences intensive care unit


Receiver operating characteristic


Subarachnoid hemorrhage


Stress-induced hyperglycemia


Threshold Hounsfield


Ventriculoperitoneal shunt


World Federation of Neurological Surgeons



The authors would like to thank Blair Apple, BS, and Brittany Karfonta, BS, with Clinical Studies Unit in Department of Neurology, Oklahoma University Health Sciences Center for their support in data management of the present study.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

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

Not applicable due to retrospective nature of the study design.

Supplementary material

12975_2018_646_Fig6_ESM.png (394 kb)
Supplementary Figure 1

Segmentation software shows image processing of blood products with intracerebral hemorrhage (a,b), intraventricular hemorrhage (c,d) and subarachnoid hemorrhage (e,f) (PNG 394 kb)

12975_2018_646_MOESM1_ESM.tif (511 kb)
High resolution image (TIF 510 kb)
12975_2018_646_MOESM2_ESM.avi (6 mb)
Supplementary Figure 2 Video shows image analyses software in use (AVI 6125 kb)
12975_2018_646_Fig7_ESM.png (83 kb)
Supplementary Figure 3

Linear correlation noted between modified Graeb score with intracranial blood volume (a) and with intracranial blood+CSF volumes (b). (PNG 83 kb)

12975_2018_646_MOESM3_ESM.tif (118 kb)
High resolution image (TIF 118 kb)
12975_2018_646_Fig8_ESM.png (74 kb)
Supplementary Figure 4

ROC curves shows AUROC for various parameters determining cohort’s mortality (a) and stress-induced hyperglycemia (b). (PNG 73 kb)

12975_2018_646_MOESM4_ESM.tif (109 kb)
High resolution image (TIF 108 kb)


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Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Joshua A Santucci
    • 1
  • Stephen R Ross
    • 1
  • John C Greenert
    • 1
  • Faranak Aghaei
    • 2
  • Lance Ford
    • 3
  • Kimberly M Hollabaugh
    • 3
  • Benjamin O Cornwell
    • 4
  • Dee H Wu
    • 4
  • Bin Zheng
    • 2
  • Bradley N Bohnstedt
    • 5
  • Bappaditya Ray
    • 1
    Email author
  1. 1.Division of Critical Care Neurology, Department of Neurology, College of MedicineThe University of Oklahoma Health Sciences CenterOklahoma CityUSA
  2. 2.Electrical EngineeringUniversity of OklahomaNormanUSA
  3. 3.Epidemiology and Biostatistics, College of Public HealthThe University of Oklahoma Health Sciences CenterOklahoma CityUSA
  4. 4.Radiology, College of MedicineThe University of Oklahoma Health Sciences CenterOklahoma CityUSA
  5. 5.Neurosurgery, College of MedicineThe University of Oklahoma Health Sciences CenterOklahoma CityUSA

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