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Published in: Clinical Neuroradiology 2/2013

01-06-2013 | Original Article

Comparison of ESWAN, SWI-SPGR, and 2D T2*-Weighted GRE Sequence for Depicting Cerebral Microbleeds

Authors: L. F. Guo, MD, G. Wang, MD, X. Y. Zhu, MD, C. Liu, MD, L. Cui, MD

Published in: Clinical Neuroradiology | Issue 2/2013

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Abstract

Purpose

We aimed to compare images obtained with an Enhanced 3D multi-echo GRE T2*-weighted angiography (ESWAN) sequence with those obtained with a susceptibility-weighted imaging-spoiled gradient-recalled echo (SWI-SPGR) sequence and a two-dimensional (2D) T2*-weighted gradient-recalled echo (GRE) sequence for the description of cerebral microbleeds (CMBs) in hypertensive patients (elderly people).

Methods

A total of 273 elderly hypertensive patients were imaged in a 3.0-T MR scanner using ESWAN, SWI-SPGR, and 2D T2*-weighted GRE sequence, respectively. The presence, number, and location of CMBs and scanning and postprocessing time were recorded for both sequences, and the differences were tested using nonparametric McNemar and Friedman tests.

Results

CMBs were detected by 2D T2*-weighted GRE images in 54 participants, SWI-SPGR images in 83 participants, and ESWAN images in 88 participants. The participants with CMBs detected by 2D T2*-weighted GRE sequence were fewer than those with CMBs detected by SWI-SPGR or ESWAN sequences (P < 0.05). There was no significant difference between SWI-SPGR and ESWAN sequences to detect the CMBs in number (P > 0.05). Among the participants with CMBs visualized in both sequences, most patients had CMBs in the subcortical white matter and at deep locations. The participants who had CMBs in the infratentorial region were fewer. The acquisition time of ESWAN images was slightly longer than that of SWI-SPGR images.

Conclusions

ESWAN sequence was not superior to SWI-SPGR sequence in depicting CMBs at 3.0-T MR, but both of these sequences were superior to 2D T2*-weighted GRE sequence.
Literature
1.
go back to reference Cordonnier C, Al-Shahi Salman R, Wardlaw J. Spontaneous brain microbleeds: systematic review, subgroup analyses and standards for study design and reporting. Brain. 2007;130:1988–2003.PubMedCrossRef Cordonnier C, Al-Shahi Salman R, Wardlaw J. Spontaneous brain microbleeds: systematic review, subgroup analyses and standards for study design and reporting. Brain. 2007;130:1988–2003.PubMedCrossRef
2.
go back to reference Nakata-Kudo Y, Mizuno T, Yamada K, Shiga K, Yoshikawa K, Mori S, Nishimura T, Nakajima K, Nakagawa M. Microbleeds in Alzheimer disease are more related to cerebral amyloid angiopathy than cerebrovascular disease. Dement Geriatr Cogn Disord. 2006;22:8–14.PubMedCrossRef Nakata-Kudo Y, Mizuno T, Yamada K, Shiga K, Yoshikawa K, Mori S, Nishimura T, Nakajima K, Nakagawa M. Microbleeds in Alzheimer disease are more related to cerebral amyloid angiopathy than cerebrovascular disease. Dement Geriatr Cogn Disord. 2006;22:8–14.PubMedCrossRef
3.
go back to reference Nishikawa T, Ueba T, Kajiwara M, Fujisawa I, Miyamatsu N, Yamashita K. Cerebral microbleeds predict first-ever symptomatic cerebrovascular events. Clin Neurol Neurosurg. 2009;111:825–8.PubMedCrossRef Nishikawa T, Ueba T, Kajiwara M, Fujisawa I, Miyamatsu N, Yamashita K. Cerebral microbleeds predict first-ever symptomatic cerebrovascular events. Clin Neurol Neurosurg. 2009;111:825–8.PubMedCrossRef
4.
go back to reference Henskens LH, van Oostenbrugge RJ, Kroon AA, de Leeuw PW, Lodder J. Brain microbleeds are associated with ambulatory blood pressure levels in a hypertensive population. Hypertension. 2008;51:62–8.PubMedCrossRef Henskens LH, van Oostenbrugge RJ, Kroon AA, de Leeuw PW, Lodder J. Brain microbleeds are associated with ambulatory blood pressure levels in a hypertensive population. Hypertension. 2008;51:62–8.PubMedCrossRef
5.
go back to reference Staals J, van Oostenbrugge RJ, Knottnerus IL, Rouhl RP, Henskens LH, Lodder J. Brain microbleeds relate to higher ambulatory blood pressure levels in first-ever lacunar stroke patients. Stroke. 2009;40:3264–8.PubMedCrossRef Staals J, van Oostenbrugge RJ, Knottnerus IL, Rouhl RP, Henskens LH, Lodder J. Brain microbleeds relate to higher ambulatory blood pressure levels in first-ever lacunar stroke patients. Stroke. 2009;40:3264–8.PubMedCrossRef
6.
go back to reference Fan YH, Zhang L, Lam WW, Mok VC, Wong KS. Cerebral microbleeds as a risk factor for subsequent intracerebral hemorrhages among patients with acute ischemic stroke. Stroke. 2003;34:2459–62.PubMedCrossRef Fan YH, Zhang L, Lam WW, Mok VC, Wong KS. Cerebral microbleeds as a risk factor for subsequent intracerebral hemorrhages among patients with acute ischemic stroke. Stroke. 2003;34:2459–62.PubMedCrossRef
7.
go back to reference Imaizumi T, Horita Y, Hashimoto Y, Niwa J. Dotlike hemosiderin spots on T2*-weighted magnetic resonance imaging as a predictor of stroke recurrence: a prospective study. J Neurosurg. 2004;101:915–20.PubMedCrossRef Imaizumi T, Horita Y, Hashimoto Y, Niwa J. Dotlike hemosiderin spots on T2*-weighted magnetic resonance imaging as a predictor of stroke recurrence: a prospective study. J Neurosurg. 2004;101:915–20.PubMedCrossRef
8.
go back to reference Lim JB, Kim E. Silent microbleeds and old hematomas in spontaneous cerebral hemorrhages. J Korean Neurosurg Soc. 2009;46:38–44.PubMedCrossRef Lim JB, Kim E. Silent microbleeds and old hematomas in spontaneous cerebral hemorrhages. J Korean Neurosurg Soc. 2009;46:38–44.PubMedCrossRef
9.
go back to reference Naka H, Nomura E, Wakabayashi S, Kajikawa H, Kohriyama T, Mimori Y, Nakamura S, Matsumoto M. Frequency of asymptomatic microbleeds on T2*-weighted MR images of patients with recurrent stroke: association with combination of stroke subtypes and leukoaraiosis. AJNR Am J Neuroradiol. 2004;25:714–9.PubMed Naka H, Nomura E, Wakabayashi S, Kajikawa H, Kohriyama T, Mimori Y, Nakamura S, Matsumoto M. Frequency of asymptomatic microbleeds on T2*-weighted MR images of patients with recurrent stroke: association with combination of stroke subtypes and leukoaraiosis. AJNR Am J Neuroradiol. 2004;25:714–9.PubMed
10.
go back to reference Nighoghossian N, Hermier M, Adeleine P, Blanc-Lasserre K, Derex L, Honnorat J, Philippeau F, Dugor JF, Froment JC, Trouillas P. Old microbleeds are a potential risk factor for cerebral bleeding after ischemic stroke: a gradient-echo T2*-weighted brain MRI study. Stroke. 2002;33:735–42.PubMedCrossRef Nighoghossian N, Hermier M, Adeleine P, Blanc-Lasserre K, Derex L, Honnorat J, Philippeau F, Dugor JF, Froment JC, Trouillas P. Old microbleeds are a potential risk factor for cerebral bleeding after ischemic stroke: a gradient-echo T2*-weighted brain MRI study. Stroke. 2002;33:735–42.PubMedCrossRef
11.
go back to reference Fiehler J, Albers GW, Boulanger JM, Derex L, Gass A, Hjort N, Kim JS, Liebeskind DS, Neumann-Haefelin T, Pedraza S, Rother J, Rothwell P, Rovira A, Schellinger PD, Trenkler J. Bleeding risk analysis in stroke imaging before thromboLysis (BRASIL): pooled analysis of T2*-weighted magnetic resonance imaging data from 570 patients. Stroke. 2007;38:2738–44.PubMedCrossRef Fiehler J, Albers GW, Boulanger JM, Derex L, Gass A, Hjort N, Kim JS, Liebeskind DS, Neumann-Haefelin T, Pedraza S, Rother J, Rothwell P, Rovira A, Schellinger PD, Trenkler J. Bleeding risk analysis in stroke imaging before thromboLysis (BRASIL): pooled analysis of T2*-weighted magnetic resonance imaging data from 570 patients. Stroke. 2007;38:2738–44.PubMedCrossRef
12.
go back to reference Orken DN, Kenangil G, Uysal E, Forta H. Cerebral microbleeds in ischemic stroke patients on warfarin treatment. Stroke. 2009;40:3638–40.PubMedCrossRef Orken DN, Kenangil G, Uysal E, Forta H. Cerebral microbleeds in ischemic stroke patients on warfarin treatment. Stroke. 2009;40:3638–40.PubMedCrossRef
13.
go back to reference Jeerakathil T, Wolf PA, Beiser A, Hald JK, Au R, Kase CS, Massaro JM, DeCarli C. Cerebral microbleeds: prevalence and associations with cardiovascular risk factors in the Framingham study. Stroke. 2004;35:1831–5.PubMedCrossRef Jeerakathil T, Wolf PA, Beiser A, Hald JK, Au R, Kase CS, Massaro JM, DeCarli C. Cerebral microbleeds: prevalence and associations with cardiovascular risk factors in the Framingham study. Stroke. 2004;35:1831–5.PubMedCrossRef
14.
go back to reference Haacke EM, Xu Y, Cheng YC, Reichenbach JR. Susceptibility weighted imaging (SWI). Magnet Reson Med. 2004;52:612–8.CrossRef Haacke EM, Xu Y, Cheng YC, Reichenbach JR. Susceptibility weighted imaging (SWI). Magnet Reson Med. 2004;52:612–8.CrossRef
15.
go back to reference Sehgal V, Delproposto Z, Haacke EM, Tong KA, Wycliffe N, Kido DK, Xu Y, Neelavalli J, Haddar D, Reichenbach JR. Clinical applications of neuroimaging with susceptibility-weighted imaging. J Magn Reson Imaging. 2005;22:439–50.PubMedCrossRef Sehgal V, Delproposto Z, Haacke EM, Tong KA, Wycliffe N, Kido DK, Xu Y, Neelavalli J, Haddar D, Reichenbach JR. Clinical applications of neuroimaging with susceptibility-weighted imaging. J Magn Reson Imaging. 2005;22:439–50.PubMedCrossRef
16.
go back to reference Zeng QS, Kang XS, Li CF, Zhou GY. Detection of hemorrhagic hypointense foci in radiation injury region using susceptibility-weighted imaging. Acta Radiol. 2011;52(1):115–9.PubMedCrossRef Zeng QS, Kang XS, Li CF, Zhou GY. Detection of hemorrhagic hypointense foci in radiation injury region using susceptibility-weighted imaging. Acta Radiol. 2011;52(1):115–9.PubMedCrossRef
17.
go back to reference Nandigam RN, Viswanathan A, Delgado P, Skehan ME, Smith EE, Rosand J, Greenberg SM, Dickerson BC. MR imaging detection of cerebral microbleeds: effect of susceptibility-weighted imaging, section thickness, and field strength. AJNR Am J Neuroradiol. 2009;30:338–43.PubMedCrossRef Nandigam RN, Viswanathan A, Delgado P, Skehan ME, Smith EE, Rosand J, Greenberg SM, Dickerson BC. MR imaging detection of cerebral microbleeds: effect of susceptibility-weighted imaging, section thickness, and field strength. AJNR Am J Neuroradiol. 2009;30:338–43.PubMedCrossRef
18.
go back to reference Haacke EM, Cheng NY, House MJ, Liu Q, Neelavalli J, Ogg RJ, Khan A, Ayaz M, Kirsch W, Obenaus A. Imaging iron stores in the brain using magnetic resonance imaging. Magn Reson Imaging. 2005;23:1–25.PubMedCrossRef Haacke EM, Cheng NY, House MJ, Liu Q, Neelavalli J, Ogg RJ, Khan A, Ayaz M, Kirsch W, Obenaus A. Imaging iron stores in the brain using magnetic resonance imaging. Magn Reson Imaging. 2005;23:1–25.PubMedCrossRef
19.
go back to reference Haacke EM, Mittal S, Wu Z, Neelavalli J, Cheng YC. Susceptibility-weighted imaging: technical aspects and clinical applications. Part 1. AJNR Am J Neuroradiol. 2009;30:19–30.PubMedCrossRef Haacke EM, Mittal S, Wu Z, Neelavalli J, Cheng YC. Susceptibility-weighted imaging: technical aspects and clinical applications. Part 1. AJNR Am J Neuroradiol. 2009;30:19–30.PubMedCrossRef
20.
go back to reference McAuley G, Schrag M, Sipos P, Sun SW, Obenaus A, Neelavalli J, Haacke EM, Holshouser B, Madacsi R, Kirsch W. Quantification of punctate iron sources using magnetic resonance phase. Magn Reson Med. 2010;63:106–15.PubMed McAuley G, Schrag M, Sipos P, Sun SW, Obenaus A, Neelavalli J, Haacke EM, Holshouser B, Madacsi R, Kirsch W. Quantification of punctate iron sources using magnetic resonance phase. Magn Reson Med. 2010;63:106–15.PubMed
21.
go back to reference Cordonnier C, Potter GM, Jackson CA, Doubal F, Keir S, Sudlow CL, Wardlaw JM, Al-Shahi Salman R. Improving interrater agreement about brain microbleeds: development of the Brain Observer MicroBleed Scale (BOMBS). Stroke. 2009;40:94–9.PubMedCrossRef Cordonnier C, Potter GM, Jackson CA, Doubal F, Keir S, Sudlow CL, Wardlaw JM, Al-Shahi Salman R. Improving interrater agreement about brain microbleeds: development of the Brain Observer MicroBleed Scale (BOMBS). Stroke. 2009;40:94–9.PubMedCrossRef
22.
go back to reference Lee SH, Bae HJ, Yoon BW, Kim H, Kim DE, Roh JK. Low concentration of serum total cholesterol is associated with multifocal signal loss lesions on gradient-echo magnetic resonance imaging: analysis of risk factors for multifocal signal loss lesions. Stroke. 2002;33:2845–9.PubMedCrossRef Lee SH, Bae HJ, Yoon BW, Kim H, Kim DE, Roh JK. Low concentration of serum total cholesterol is associated with multifocal signal loss lesions on gradient-echo magnetic resonance imaging: analysis of risk factors for multifocal signal loss lesions. Stroke. 2002;33:2845–9.PubMedCrossRef
23.
go back to reference Altman DG. Practical statistics for medical research. Boca Raton: Chapman & Hall; 1999. Altman DG. Practical statistics for medical research. Boca Raton: Chapman & Hall; 1999.
24.
go back to reference Sun S, Gao P, Sui B, Xue J, Wang H, Wang Q, Jing L, Zhai R. Association between cerebral microbleeds and the first onset of intracerebral hemorrhage—a 3.0-T MR study. Acta Radiol. 2012;53:203–7.PubMedCrossRef Sun S, Gao P, Sui B, Xue J, Wang H, Wang Q, Jing L, Zhai R. Association between cerebral microbleeds and the first onset of intracerebral hemorrhage—a 3.0-T MR study. Acta Radiol. 2012;53:203–7.PubMedCrossRef
25.
go back to reference Boulanger JM, Coutts SB, Eliasziw M, Gagnon AJ, Simon JE, Subramaniam S, Sohn CH, Scott J, Demchuk AM. Cerebral microhemorrhages predict new disabling or fatal strokes in patients with acute ischemic stroke or transient ischemic attack. Stroke. 2006;37:911–4.PubMedCrossRef Boulanger JM, Coutts SB, Eliasziw M, Gagnon AJ, Simon JE, Subramaniam S, Sohn CH, Scott J, Demchuk AM. Cerebral microhemorrhages predict new disabling or fatal strokes in patients with acute ischemic stroke or transient ischemic attack. Stroke. 2006;37:911–4.PubMedCrossRef
26.
go back to reference Poels MM, Ikram MA, Van Der Lugt A, Hofman A, Krestin GP, Breteler MM, Vernooij MW. Incidence of cerebral microbleeds in the general population: the Rotterdam Scan Study. Stroke. 2011;42:656–61.PubMedCrossRef Poels MM, Ikram MA, Van Der Lugt A, Hofman A, Krestin GP, Breteler MM, Vernooij MW. Incidence of cerebral microbleeds in the general population: the Rotterdam Scan Study. Stroke. 2011;42:656–61.PubMedCrossRef
27.
go back to reference Van Es AC, Van Der Grond J, de Craen AJ, Admiraal-Behloul F, Blauw GJ, van Buchem MA. Risk factors for cerebral microbleeds in the elderly. Cerebrovasc Dis. 2008;26:397–403.PubMedCrossRef Van Es AC, Van Der Grond J, de Craen AJ, Admiraal-Behloul F, Blauw GJ, van Buchem MA. Risk factors for cerebral microbleeds in the elderly. Cerebrovasc Dis. 2008;26:397–403.PubMedCrossRef
28.
go back to reference Bokura H, Saika R, Yamaguchi T, Nagai A, Oguro H, Kobayashi S, Yamaguchi S. Microbleeds are associated with subsequent hemorrhagic and ischemic stroke in healthy elderly individuals. Stroke. 2011;42:1867–71.PubMedCrossRef Bokura H, Saika R, Yamaguchi T, Nagai A, Oguro H, Kobayashi S, Yamaguchi S. Microbleeds are associated with subsequent hemorrhagic and ischemic stroke in healthy elderly individuals. Stroke. 2011;42:1867–71.PubMedCrossRef
29.
go back to reference Gregoire SM, Brown MM, Kallis C, Jager HR, Yousry TA, Werring DJ. MRI detection of new microbleeds in patients with ischemic stroke: five-year cohort follow-up study. Stroke. 2010;41:184–6.PubMedCrossRef Gregoire SM, Brown MM, Kallis C, Jager HR, Yousry TA, Werring DJ. MRI detection of new microbleeds in patients with ischemic stroke: five-year cohort follow-up study. Stroke. 2010;41:184–6.PubMedCrossRef
30.
go back to reference Coutts S, Frayne R, Sevick R, Demchuk A. Microbleeding on MRI as a marker for hemorrhage after stroke thrombolysis. Stroke. 2002;33:1457–8.PubMedCrossRef Coutts S, Frayne R, Sevick R, Demchuk A. Microbleeding on MRI as a marker for hemorrhage after stroke thrombolysis. Stroke. 2002;33:1457–8.PubMedCrossRef
31.
go back to reference Vernooij MW, Ikram MA, Wielopolski PA, Krestin GP, Breteler MM, Van Der Lugt A. Cerebral microbleeds: accelerated 3D T2*-weighted GRE MR imaging versus conventional 2D T2*-weighted GRE MR imaging for detection. Radiology. 2008;248:272–7.PubMedCrossRef Vernooij MW, Ikram MA, Wielopolski PA, Krestin GP, Breteler MM, Van Der Lugt A. Cerebral microbleeds: accelerated 3D T2*-weighted GRE MR imaging versus conventional 2D T2*-weighted GRE MR imaging for detection. Radiology. 2008;248:272–7.PubMedCrossRef
32.
go back to reference Mittal S, Wu Z, Neelavalli J, Haacke EM. Susceptibility-weighted imaging: technical aspects and clinical applications. Part 2. AJNR Am J Neuroradiol. 2009;30:232–52.PubMedCrossRef Mittal S, Wu Z, Neelavalli J, Haacke EM. Susceptibility-weighted imaging: technical aspects and clinical applications. Part 2. AJNR Am J Neuroradiol. 2009;30:232–52.PubMedCrossRef
33.
go back to reference Roob G, Schmidt R, Kapeller P, Lechner A, Hartung HP, Fazekas F. MRI evidence of past cerebral microbleeds in a healthy elderly population. Neurology. 1999;52:991–4.PubMedCrossRef Roob G, Schmidt R, Kapeller P, Lechner A, Hartung HP, Fazekas F. MRI evidence of past cerebral microbleeds in a healthy elderly population. Neurology. 1999;52:991–4.PubMedCrossRef
Metadata
Title
Comparison of ESWAN, SWI-SPGR, and 2D T2*-Weighted GRE Sequence for Depicting Cerebral Microbleeds
Authors
L. F. Guo, MD
G. Wang, MD
X. Y. Zhu, MD
C. Liu, MD
L. Cui, MD
Publication date
01-06-2013
Publisher
Springer-Verlag
Published in
Clinical Neuroradiology / Issue 2/2013
Print ISSN: 1869-1439
Electronic ISSN: 1869-1447
DOI
https://doi.org/10.1007/s00062-012-0185-7

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