Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Clinical Neuroradiology
Published in: Clinical Neuroradiology 1/2017

01-03-2017 | Original Article

Timing of Mean Transit Time Maximization is Associated with Neurological Outcome After Subarachnoid Hemorrhage

Authors: J. Caspers, MD, C. Rubbert, MD, B. Turowski, MD, D. Martens, MD, D. C. Reichelt, MD, R. May, MD, J. Aissa, MD, D. Hänggi, MD, N. Etminan, MD, C. Mathys, MD

Published in: Clinical Neuroradiology | Issue 1/2017

Login to get access

Abstract

Purpose

Computed tomography perfusion (CTP) has gained significant relevance for the radiological screening of patients at risk of developing delayed cerebral ischemia (DCI) after aneurysmal subarachnoid hemorrhage (aSAH). Particularly, the impact of MTTPEAK, i.e., the maximal mean transit time value in a series of CTP measurements, for the prediction of long-term outcome has recently been demonstrated by our group. Complementing this recent work, the present study investigated how the timing of MTTPEAK affected the long-term outcome after aneurysmal subarachnoid hemorrhage.

Methods

CTP examinations from 103 patients with clinical deterioration attributed to DCI after aSAH were retrospectively analyzed for time interval between SAH ictus and onset of MTTPEAK in association with modified Rankin Scale (mRS) 23.1 months after SAH.

Results

Patients with unfavorable outcome (mRS > = 2) suffered significant earlier MTTPEAK onsets than patients with favorable outcome (mRS = 0 and 1). MTTPEAK within the first week was associated with significantly higher mRS scores compared to later MTTPEAK. Timing of MTTPEAK together with the value of MTTPEAK and initial World Federation of Neurosurgical Societies (WFNS) grade was a significant predictor for an unfavorable outcome (mRS > = 2).

Conclusions

The current findings suggest a presumably higher vulnerability of the brain to early microcirculatory impairments after aSAH and highlight that timing of MTT elevations could be considered for the identification of patients at increased risk for poor neurological outcome due to DCI.
Literature
1.
van Gijn J, Kerr RS, Rinkel GJ. Subarachnoid haemorrhage. Lancet. 2007;369(9558):306–18. doi:10.1016/S 0140-6736(07)60153-6.CrossRefPubMed
2.
Ingall T, Asplund K, Mahonen M, Bonita R. A multinational comparison of subarachnoid hemorrhage epidemiology in the WHO MONICA stroke study. Stroke. 2000;31(5):1054–61.CrossRefPubMed
3.
Macdonald RL. Delayed neurological deterioration after subarachnoid haemorrhage. Nat Rev Neurol. 2014;10(1):44–58. doi:10.1038/nrneurol.2013.246.CrossRefPubMed
4.
Etminan N, Beseoglu K, Heiroth HJ, Turowski B, Steiger HJ, Hanggi D. Early perfusion computerized tomography imaging as a radiographic surrogate for delayed cerebral ischemia and functional outcome after subarachnoid hemorrhage. Stroke. 2013;44(5):1260–6. doi:10.1161/STROKEAHA.111.675975.CrossRefPubMed
5.
Nolan CP, Macdonald RL. Can angiographic vasospasm be used as a surrogate marker in evaluating therapeutic interventions for cerebral vasospasm? Neurosurg Focus. 2006;21(3):E1.CrossRefPubMed
6.
Etminan N, Vergouwen MD, Ilodigwe D, Macdonald RL. Effect of pharmaceutical treatment on vasospasm, delayed cerebral ischemia, and clinical outcome in patients with aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. J Cereb Blood Flow Metab. 2011;31(6):1443–51. doi:10.1038/jcbfm.2011.7.CrossRefPubMedPubMedCentral
7.
Rowland MJ, Hadjipavlou G, Kelly M, Westbrook J, Pattinson KT. Delayed cerebral ischaemia after subarachnoid haemorrhage: looking beyond vasospasm. Br J Anaesth. 2012;109(3):315–29. doi:10.1093/bja/aes264.CrossRefPubMed
8.
Dreier JP, Woitzik J, Fabricius M, Bhatia R, Major S, Drenckhahn C, Lehmann TN, Sarrafzadeh A, Willumsen L, Hartings JA, Sakowitz OW, Seemann JH, Thieme A, Lauritzen M, Strong AJ. Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain. 2006;129(Pt 12):3224–37. doi:10.1093/brain/awl297.CrossRefPubMed
9.
Vergouwen MD, Vermeulen M, Coert BA, Stroes ES, Roos YB. Microthrombosis after aneurysmal subarachnoid hemorrhage: an additional explanation for delayed cerebral ischemia. J Cereb Blood Flow Metab. 2008;28(11):1761–70. doi:10.1038/jcbfm.2008.74.CrossRefPubMed
10.
Yundt KD, Grubb RL, Jr., Diringer MN, Powers WJ. Autoregulatory vasodilation of parenchymal vessels is impaired during cerebral vasospasm. J Cereb Blood Flow Metab. 1998;18(4):419–24. doi:10.1097/00004647-199804000-00010.CrossRefPubMed
11.
Cremers CH, van der Schaaf IC, Wensink E, Greving JP, Rinkel GJ, Velthuis BK, Vergouwen MD. CT perfusion and delayed cerebral ischemia in aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. J Cereb Blood Flow Metab. 2014;34(2):200–7. doi:10.1038/jcbfm.2013.208.CrossRefPubMed
12.
Washington CW, Zipfel GJ. Detection and monitoring of vasospasm and delayed cerebral ischemia: a review and assessment of the literature. Neurocrit Care. 2011;15(2):312–7. doi:10.1007/s12028-011-9594-8.CrossRefPubMed
13.
Turowski B, Haenggi D, Wittsack J, Beck A, Moedder U. Cerebral perfusion computerized tomography in vasospasm after subarachnoid hemorrhage: diagnostic value of MTT. Rofo. 2007;179(8):847–54. doi:10.1055/s-2007-963197.CrossRefPubMed
14.
Wintermark M, Ko NU, Smith WS, Liu S, Higashida RT, Dillon WP. Vasospasm after subarachnoid hemorrhage: utility of perfusion CT and CT angiography on diagnosis and management. AJNR Am J Neuroradiol. 2006;27(1):26–34.PubMed
15.
Mathys C, Martens D, Reichelt DC, Caspers J, Aissa J, May R, Hänggi D, Antoch G, Turowski B. Long-term impact of perfusion CT data after subarachnoid hemorrhage. Neuroradiology. 2013;55(11):1323–31. doi:10.1007/s00234-013-1278-y.CrossRefPubMed
16.
Wilson JT, Hareendran A, Grant M, Baird T, Schulz UG, Muir KW, Bone I. Improving the assessment of outcomes in stroke: use of a structured interview to assign grades on the modified Rankin Scale. Stroke. 2002;33(9):2243–6.CrossRefPubMed
17.
Vergouwen MD, Vermeulen M, van Gijn J, Rinkel GJ, Wijdicks EF, Muizelaar JP, Mendelow AD, Juvela S, Yonas H, Terbrugge KG, Macdonald RL, Diringer MN, Broderick JP, Dreier JP, Roos YB. Definition of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage as an outcome event in clinical trials and observational studies: proposal of a multidisciplinary research group. Stroke. 2010;41(10):2391–5. doi:10.1161/STROKEAHA.110.589275.CrossRefPubMed
18.
Nabavi DG, LeBlanc LM, Baxter B, Lee DH, Fox AJ, Lownie SP, Ferguson GG, Craen RA, Gelb AW, Lee TY. Monitoring cerebral perfusion after subarachnoid hemorrhage using CT. Neuroradiology. 2001;43(1):7–16.CrossRefPubMed
19.
Honda M, Sase S, Yokota K, Ichibayashi R, Yoshihara K, Sakata Y, Masuda H, Uekusa H, Seiki Y, Kishi T. Early cerebral circulatory disturbance in patients suffering subarachnoid hemorrhage prior to the delayed cerebral vasospasm stage: xenon computed tomography and perfusion computed tomography study. Neurol Med Chir (Tokyo). 2012;52(7):488–94.CrossRef
20.
Schubert GA, Seiz M, Hegewald AA, Manville J, Thome C. Acute hypoperfusion immediately after subarachnoid hemorrhage: a xenon contrast-enhanced CT study. J Neurotrauma. 2009;26(12):2225–31. doi:10.1089/neu.2009.0924.CrossRefPubMed
21.
Tsuang FY, Chen JY, Lee CW, Li CH, Lee JE, Lai DM, Hu FC, Tu YK, Hsieh ST, Wang KC. Risk profile of patients with poor-grade aneurysmal subarachnoid hemorrhage using early perfusion computed tomography. World Neurosurg. 2012;78(5):455–61. doi:10.1016/j.wneu.2011.12.004.CrossRefPubMed
22.
Carr KR, Zuckerman SL, Mocco J. Inflammation, cerebral vasospasm, and evolving theories of delayed cerebral ischemia. Neurol Res Int. 2013;2013:506584. doi:10.1155/2013/506584.CrossRefPubMedPubMedCentral
23.
Dumont AS, Dumont RJ, Chow MM, Lin CL, Calisaneller T, Ley KF, Kassell NF, Lee KS. Cerebral vasospasm after subarachnoid hemorrhage: putative role of inflammation. Neurosurgery. 2003;53(1):123–33. (discussion 33–5).CrossRefPubMed
24.
Romano JG, Forteza AM, Concha M, Koch S, Heros RC, Morcos JJ, Babikian VL. Detection of microemboli by transcranial Doppler ultrasonography in aneurysmal subarachnoid hemorrhage. Neurosurgery. 2002;50(5):1026–30. (discussion 30–1).PubMed
25.
Leng LZ, Fink ME, Iadecola C. Spreading depolarization: a possible new culprit in the delayed cerebral ischemia of subarachnoid hemorrhage. Arch Neurol. 2011;68(1):31–6. doi:10.1001/archneurol.2010.226.CrossRefPubMed
26.
Vergouwen MD, Ilodigwe D, Macdonald RL. Cerebral infarction after subarachnoid hemorrhage contributes to poor outcome by vasospasm-dependent and -independent effects. Stroke. 2011;42(4):924–9. doi:10.1161/STROKEAHA.110.597914.CrossRefPubMed
27.
Bederson JB, Levy AL, Ding WH, Kahn R, DiPerna CA, Jenkins AL 3rd, Vallabhajosyula P. Acute vasoconstriction after subarachnoid hemorrhage. Neurosurgery. 1998;42(2):352–60. (discussion 60–2).CrossRefPubMed
28.
Kolias AG, Sen J, Belli A. Pathogenesis of cerebral vasospasm following aneurysmal subarachnoid hemorrhage: putative mechanisms and novel approaches. J Neurosci Res. 2009;87(1):1–11. doi:10.1002/jnr.21823.CrossRefPubMed
29.
Grote E, Hassler W. The critical first minutes after subarachnoid hemorrhage. Neurosurgery. 1988;22(4):654–61.CrossRefPubMed
30.
Claassen J, Carhuapoma JR, Kreiter KT, Du EY, Connolly ES, Mayer SA. Global cerebral edema after subarachnoid hemorrhage: frequency, predictors, and impact on outcome. Stroke. 2002;33(5):1225–32.CrossRefPubMed
31.
Ratsep T, Asser T. Cerebral hemodynamic impairment after aneurysmal subarachnoid hemorrhage as evaluated using transcranial doppler ultrasonography: relationship to delayed cerebral ischemia and clinical outcome. J Neurosurg. 2001;95(3):393–401. doi:10.3171/jns.2001.95.3.0393.CrossRefPubMed
32.
Otite F, Mink S, Tan CO, Puri A, Zamani AA, Mehregan A, Chou S, Orzell S, Purkayastha S, Du R, Sorond FA. Impaired cerebral autoregulation is associated with vasospasm and delayed cerebral ischemia in subarachnoid hemorrhage. Stroke. 2014;45(3):677–82. doi:10.1161/STROKEAHA.113.002630.CrossRefPubMedPubMedCentral
33.
Shigeno T, Fritschka E, Brock M, Schramm J, Shigeno S, Cervos-Navarro J. Cerebral edema following experimental subarachnoid hemorrhage. Stroke. 1982;13(3):368–79.CrossRefPubMed
34.
Hatake K, Wakabayashi I, Kakishita E, Hishida S. Impairment of endothelium-dependent relaxation in human basilar artery after subarachnoid hemorrhage. Stroke. 1992;23(8):1111–6. (discussion 6–7).CrossRefPubMed
35.
Park KW, Metais C, Dai HB, Comunale ME, Sellke FW. Microvascular endothelial dysfunction and its mechanism in a rat model of subarachnoid hemorrhage. Anesth Analg. 2001;92(4):990–6.CrossRefPubMed
36.
Laslo AM, Eastwood JD, Pakkiri P, Chen F, Lee TY. CT perfusion-derived mean transit time predicts early mortality and delayed vasospasm after experimental subarachnoid hemorrhage. AJNR Am J Neuroradiol. 2008;29(1):79–85. doi:10.3174/ajnr.A0747.CrossRefPubMed
37.
Povlsen GK, Johansson SE, Larsen CC, Samraj AK, Edvinsson L. Early events triggering delayed vasoconstrictor receptor upregulation and cerebral ischemia after subarachnoid hemorrhage. BMC Neurosci. 2013;14:34. doi:10.1186/1471-2202-14-34.CrossRefPubMedPubMedCentral
38.
Ohkuma H, Manabe H, Tanaka M, Suzuki S. Impact of cerebral microcirculatory changes on cerebral blood flow during cerebral vasospasm after aneurysmal subarachnoid hemorrhage. Stroke. 2000;31(7):1621–7.CrossRefPubMed
39.
Connolly ES, Jr., Rabinstein AA, Carhuapoma JR, Derdeyn CP, Dion J, Higashida RT, Hoh BL, Kirkness CJ, Naidech AM, Ogilvy CS, Patel AB, Thompson BG, Vespa P; American Heart Association Stroke Council; Council on Cardiovascular Radiology and Intervention; Council on Cardiovascular Nursing; Council on Cardiovascular Surgery and Anesthesia; Council on Clinical Cardiology. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/american Stroke Association. Stroke. 2012;43(6):1711–37. doi:10.1161/STR.0b013e3182587839.CrossRefPubMed
Metadata
Title
Timing of Mean Transit Time Maximization is Associated with Neurological Outcome After Subarachnoid Hemorrhage
Authors
J. Caspers, MD
C. Rubbert, MD
B. Turowski, MD
D. Martens, MD
D. C. Reichelt, MD
R. May, MD
J. Aissa, MD
D. Hänggi, MD
N. Etminan, MD
C. Mathys, MD
Publication date
01-03-2017
Publisher
Springer Berlin Heidelberg
Published in
Clinical Neuroradiology / Issue 1/2017
Print ISSN: 1869-1439
Electronic ISSN: 1869-1447
DOI
https://doi.org/10.1007/s00062-015-0399-6

Other articles of this Issue 1/2017

Clinical Neuroradiology 1/2017 Go to the issue

Original Article

A Novel Configuration of Pipeline Embolization Device for Internal Carotid Bifurcation Region Aneurysms: Horizontal Deployment

Editorial

SIESTA: Thrombectomy as you like

Clinical Case

Freiburg Neuropathology Case Conference: A Cystic Lesion of the Cerebellum in an Adolescent

Original Article

Visualization of the Abducens Nerve in its Petroclival Segment Using Contrast-Enhanced FIESTA MRI: The Size of the Petroclival Venous Confluence Affects Detectability

Original Article

Process of the Functional Reorganization of the Cortical Centers for Movement in GBM Patients: fMRI Study

Original Article

Extensive pneumatized air cells causing susceptibility artifacts in the petrosus part of the ICA