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Disturbance of CT perfusion within 24 h after onset is associated with WFNS grade but not development of DCI in patients with aneurysmal SAH

Acta Neurochirurgica volume 159, pages 2319–2324 (2017)Cite this article

Abstract

Background

Delayed cerebral ischemia (DCI) is a serious complication following aneurysmal SAH (aSAH) and remains a leading cause of morbidity and mortality. We investigated whether data from CT perfusion (CTP) within 24 h after onset are associated with DCI and its outcome.

Methods

We retrospectively examined plain CT, CTP, and CT angiography (CTA) of aSAH patients on arrival. We measured the average mean transit time (aMTT) and compared it with several clinical factors, such as the age, WFNS grade, Fisher group, delayed cerebral infarction, cerebral vasospasm, and modified Rankin scale (mRS), at 1 month. Regions of interest (ROIs) were quantitatively determined in cortical and two basal ganglia areas.

Results

Delayed cerebral ischemia (DCI) developed in 11 patients and cerebral vasospasm in 28 patients out of a total of 86 aSAH patients scanned within 24 h after onset. The average MTT was correlated with the WFNS grade (p = 0.000), but not mRS (p = 0.128), age (p = 0.759), DCI (p = 0.669), or cerebral vasospasm (p = 0.306). On the other hand, DCI was associated with the Fisher group (p = 0.0056), mRS (p = 0.0052), and cerebral vasospasm (p = 0.000). Moreover, there were no significant differences in the average MTT within 24 h after onset between territories with and without DCI, or between patients with and without DCI.

Conclusions

The current findings suggest that disturbance of CT perfusion soon after the onset is associated with the WFNS grade but not with the development of DCI. Delayed cerebral ischemia may be solely caused by cerebral vasospasm due to a clot in the cistern, but not associated with early brain injury.

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Abbreviations

ACA:

anterior cerebral artery

aMTT:

average mean transit time

aSAH:

aneurysmal subarachnoid hemorrhage

CBF:

cerebral blood flow

CBV:

cerebral blood volume

CT:

computed tomography

CTA:

computed tomography angiography

CT perfusion:

computed tomography perfusion

DCI:

delayed cerebral ischemia

ICP:

intracranial pressure

MCA:

middle cerebral artery

MRI:

magnetic resonance imaging

mRS:

modified Rankin scale

PCA:

posterior cerebral artery

ROI:

region of interest

WFNS:

World Federation of Neurosurgical Societies

References

  1. Cremers CH, van der Schaaf IC, Wensink E, Greving JP, Rinkel GJ, Velthuis BK, Vergouwen MD (2014) CT perfusion and delayed cerebral ischemia in aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. J Cereb Blood Flow Metab 34:200–207

    Article  PubMed  Google Scholar 

  2. Dankbaar JW, de Rooij NK, Rijsdijk M, Velthuis BK, Frijns CJ, Rinkel GJ, van der Schaaf (2010) Diagnostic threshold values of cerebral perfusion measured with computed tomography for delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. Stroke 41:1927–1932

    Article  PubMed  Google Scholar 

  3. de Rooij NK, Rinkel GJ, Dankbaar JW, Frijns CJ (2013) Delayed cerebral ischemia after subarachnoid hemorrhage: a systematic review of clinical, laboratory, and radiological predictors. Stroke 44:43–54

    Article  PubMed  Google Scholar 

  4. Drake CG (1988) Report of world Federation of Neurological Surgeons Committee on a universal subarachnoid hemorrhage grading scale. J Neurosurg 68:985–986 (letter)

    Google Scholar 

  5. Etminan N, Beseoglu K, Heiroth HJ, Turowski B, Steiger HJ, Hänggi D (2013) Early perfusion computerized tomography imaging as a radiographic surrogate for delayed cerebral ischemia and functional outcome after subarachnoid hemorrhage. Stroke 44:1260–1266

    Article  PubMed  Google Scholar 

  6. Fisher CM, Kistler JP, Davis JM (1980) Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 6:1–9

    CAS  Article  PubMed  Google Scholar 

  7. Francoeur CL, Mayer SA (2016) Management of delayed cerebral ischemia after subarachnoid hemorrhage. Crit Care 20:277–288

    Article  PubMed  PubMed Central  Google Scholar 

  8. Inagawa T (2016) Risk factors for cerebral vasospasm following aneurysmal subarachnoid hemorrhage: a review of the literature. World Neurosurg 85:56–76

    Article  PubMed  Google Scholar 

  9. Kasuya H (2016) Trends in vasospasm research: impact of CONSCIOUS-2. J Neurol Sci 364:244

    Article  Google Scholar 

  10. Kimball MM, Velat GJ, Hoh BL (2011) The participants in the international multi-disciplinary consensus conference on the critical care management of subarachnoid hemorrhage critical care guidelines on the endovascular management of cerebral vasospasm. Neurocrit Care 15:336–341

    Article  PubMed  Google Scholar 

  11. Lagares A, Cicuendez M, Ramos A, Salvador E, Alén JF, Kaen A, Jiménez-Roldán L, Millián JM (2012) Acute perfusion changes after spontaneous SAH: a perfusion CT study. Acta Neurochir 154:405–412

    Article  PubMed  Google Scholar 

  12. Laslo AM, Eastwood JD, Pakkiri P, Chen F, Lee TY (2019) CT perfusion-derived mean transit time predicts mortality and delayed vasospasm after experimental subarachnoid hemorrhage. AJNR 29:79–85

    Article  Google Scholar 

  13. Lin CF, Hsu SP, Lin CJ, Guo WY, Liao CH, Chu WF, Hung SC, Shih YS, Lin YT (2016) Prolonged cerebral circulation time is the best parameter for predicting vasospasm during initial CT perfusion in subarachnoid hemorrhagic patients. PLoS One 11:e0151772

    Article  PubMed  PubMed Central  Google Scholar 

  14. Macdonald RL (2014) Delayed neurological deterioration after subarachnoid haemorrhage. Nat Rev Neurol 10:44–58

    CAS  Article  PubMed  Google Scholar 

  15. Malinova V, Dolatowski K, Schramm P, Moerer O, Rohde V, Mielke D (2016) Early whole-brain CT perfusion for detection of patients at a risk for delayed cerebral ischemia after subarachnoid hemorrhage. J Neurosurg 125:128–136

    Article  PubMed  Google Scholar 

  16. Marbacher S, Neuschmelting V, Andereggen L, Widmer HR, von Gunten M, Takala J, Jakob SM, Fandino J (2014) Early brain injury linearly correlates with reduction in cerebral perfusion pressure during the hyperacute phase of subarachnoid hemorrhage. Intensive Care Med Exp 2:30

    Article  PubMed  PubMed Central  Google Scholar 

  17. Mir DI, Gupta A, Dunning A, Puchi L, Robinson CL, Epstein HA, Sanelli PC (2014) CT perfusion for detection of delayed cerebral ischemia in aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. AJNR 35:866–871

    CAS  Article  PubMed  Google Scholar 

  18. Nosko M, Weir BK, Lunt A, Grace M, Allen P, Mielke B (1987) Effect of clot removal at 24 hours on chronic vasospasm after SAH in the primate model. J Neurosurg 66:416–422

    CAS  Article  PubMed  Google Scholar 

  19. Rowland MJ, Hadjipavlou G, Kelly M, Westbrook J, Pattinson KT (2012) Delayed cerebral ischaemia after subarachnoid haemorrhage: looking beyond vasospasm. Br J Anaesth 109:315–329

    CAS  Article  PubMed  Google Scholar 

  20. Sanelli PC, Anumula N, Johnson CE, Comunale JP, Tsiouris AJ, Segal AZ, Stieg PE, Zimmerman RD, Mushlin AI (2013) Evaluating CT perfusion using outcome measures of delayed cerebral ischemia in aneurysmal subarachnoid hemorrhage. AJNR 34:292–298

    CAS  Article  PubMed  Google Scholar 

  21. Sanelli PC, Ugorec I, Johnson CE, Tan J, Segal AZ, Fink M et al (2011) Using quantitative CT perfusion for evaluation of delayed cerebral ischemia following aneurysmal subarachnoid hemorrhage. AJNR 32:2047–2053

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. Sasahara A, Suzuki K, Takahashi Y, Koseki H, Hirota K, Ohbuchi H, Kasuya H (2016) Prognostic assessment of aneurysmal subarachnoid hemorrhage patients with WFNS grade V by CT perfusion on arrival. World Neurosurg 92:1–6

    Article  PubMed  Google Scholar 

  23. Sehba FA, Pluta RM, Zhang JH (2011) Metamorphosis of subarachnoid hemorrhage research: from delayed vasospasm to early brain injury. Mol Neurobiol 43:27–40

    CAS  Article  PubMed  Google Scholar 

  24. Shirao S, Yoneda H, Ishihara H, Kajiwara K, Suzuki M, and for the Survey Study Members of Japan Neurosurgical Society (2011) A proposed definition of symptomatic vasospasm based on treatment of cerebral vasospasm after subarachnoid hemorrhage in Japan: consensus 2009, a project of the 25th spasm symposium. Surg Neurol Int 2:74

    PubMed  PubMed Central  Google Scholar 

  25. Udoetuk JD, Stiefel MF, Hurst RW, Weigele JB, LeRoux PD (2007) Admission angiographic cerebral circulation time may predict subsequent angiographic vasospasm after aneurysmal subarachnoid hemorrhage. Neurosurgery 61:1152–1161

    Article  PubMed  Google Scholar 

  26. van der Schaaf I, Wermer MJ, van der Graaf Y, Hoff RG, Rinkel GJ, Velthuis BK (2006) CT after subarachnoid hemorrhage: relation of cerebral perfusion to delayed cerebral ischemia. Neurology 66:1533–1538

    Article  PubMed  Google Scholar 

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Funding

No funding was received for this research.

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Affiliations

  1. Department of Neurosurgery, Tokyo Women’s Medical University Medical Center East, 2-1-10 Nishiogu, Arakawa-ku, Tokyo, 116-8567, Japan

    Yuichi Takahashi, Atsushi Sasahara, Kei Yamazaki, Mayuko Inazuka & Hidetoshi Kasuya

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  1. Yuichi Takahashi
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  2. Atsushi Sasahara
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  3. Kei Yamazaki
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  4. Mayuko Inazuka
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  5. Hidetoshi Kasuya
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Corresponding author

Correspondence to Atsushi Sasahara.

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We declare that we have no conflict of interest.

Ethical approval

This study was approved by the institutional ethics committee of Tokyo Women’s Medical University (no. 2813). For this type of study formal consent is not required.

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Informed consent was obtained from all individual participants included this study.

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Takahashi, Y., Sasahara, A., Yamazaki, K. et al. Disturbance of CT perfusion within 24 h after onset is associated with WFNS grade but not development of DCI in patients with aneurysmal SAH. Acta Neurochir 159, 2319–2324 (2017). https://doi.org/10.1007/s00701-017-3362-2

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  • DOI: https://doi.org/10.1007/s00701-017-3362-2

Keywords

  • Cerebral vasospasm
  • Delayed cerebral ischemia
  • CT perfusion
  • Mean transit time (MTT)