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Published in: European Radiology 6/2011

01-06-2011 | Vascular-Interventional

Nonenhanced ECG-gated time-resolved 4D Steady-state free precession (SSFP) MR angiography (MRA) for assessment of cerebral collateral flow: comparison with digital subtraction angiography (DSA)

Authors: Rotem Shlomo Lanzman, Patric Kröpil, Peter Schmitt, Xiaoming Bi, Michael Gliem, Falk R. Miese, Daniel Hänggi, Marcel Kamp, Axel Scherer, Bernd Turowski, Dirk Blondin

Published in: European Radiology | Issue 6/2011

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Abstract

Objectives

To evaluate a nonenhanced time-resolved 4D SSFP MRA for dynamic visualization of intracranial collateral blood flow.

Methods

22 patients (59.0 ± 11.8 years) with steno-occlusive disease of brain-supplying arteries were included in this study. 4D SSFP MRA of the intracranial arteries was acquired with 15 temporal phases and a temporal resolution of 115 ms using 1.5 T MR. Cerebral DSA served as the reference standard and was available in all patients.

Results

Nonenhanced 4D SSFP MRA allowed for detailed dynamic visualization of blood flow in the circle of Willis and its branches in 21 of 22 (95.5%) patients. Collateral flow was excluded with both 4D SSFP MRA and DSA in 4 patients. In 17 patients, DSA detected anterior collateral flow (n = 8), posterior collateral flow via the right (n = 8) and left (n = 7) posterior communicating artery as well as patent EC-IC bypasses (n = 8). 29 of 31 collateral flow pathways were visualized by 4D SSFP MRA. As compared to DSA, 4D SSFP MRA showed a high sensitivity (92.3%), specificity (100%), positive predictive value (100%) and negative predictive value (95.2%) for visualization of intracranial collateral flow.

Conclusions

4D SSFP MRA is a promising non-invasive imaging technique for dynamic visualization of intracranial collateral flow.
Literature
1.
go back to reference Rosamond W, Flegal K, Furie K et al (2007) Heart disease and stroke statistics: 2007 update—a report from the American Heart Association statistics committee and stroke statistics subcommittee. Circulation 115:e172CrossRef Rosamond W, Flegal K, Furie K et al (2007) Heart disease and stroke statistics: 2007 update—a report from the American Heart Association statistics committee and stroke statistics subcommittee. Circulation 115:e172CrossRef
2.
go back to reference Halliday A, Mansfield A, Marro J, Peto C, Peto R, Potter J, Thomas D, MRC Asymptomatic Carotid Surgery Trial (ASCT) Collaborative Group (2004) Prevention of disabling and fatal strokes by successful carotid endarterectomy in patients without recent neurological symptoms: randomised controlled trial. Lancet 363:1491–502PubMedCrossRef Halliday A, Mansfield A, Marro J, Peto C, Peto R, Potter J, Thomas D, MRC Asymptomatic Carotid Surgery Trial (ASCT) Collaborative Group (2004) Prevention of disabling and fatal strokes by successful carotid endarterectomy in patients without recent neurological symptoms: randomised controlled trial. Lancet 363:1491–502PubMedCrossRef
3.
go back to reference Liebeskind DS (2003) Collateral circulation 34:2279–84 Liebeskind DS (2003) Collateral circulation 34:2279–84
4.
go back to reference Kaufmann TJ, Huston J III, Mandrekar JN, Schleck CD, Thielen KR, Kallmes DF (2007) Complications of diagnostic cerebral angiography: evaluation of 19, 826 consecutive patients. Radiology 243:812–819PubMedCrossRef Kaufmann TJ, Huston J III, Mandrekar JN, Schleck CD, Thielen KR, Kallmes DF (2007) Complications of diagnostic cerebral angiography: evaluation of 19, 826 consecutive patients. Radiology 243:812–819PubMedCrossRef
5.
go back to reference Hadizadeh DR, von Falkenhausen M, Gieseke J, Meyer B, Urbach H, Hoogeveen R, Schild HH, Willinek WA (2008) Cerebral arteriovenous malformation: Spetzler-Martin classification at subsecond-temporal-resolution four-dimensional MR angiography compared with that at DSA. Radiology 246:205–13PubMedCrossRef Hadizadeh DR, von Falkenhausen M, Gieseke J, Meyer B, Urbach H, Hoogeveen R, Schild HH, Willinek WA (2008) Cerebral arteriovenous malformation: Spetzler-Martin classification at subsecond-temporal-resolution four-dimensional MR angiography compared with that at DSA. Radiology 246:205–13PubMedCrossRef
6.
go back to reference Willinek WA, Hadizadeh DR, von Falkenhausen M, Urbach H, Hoogeveen R, Schild HH, Gieseke J (2008) 4D time-resolved MR angiography with keyhole (4D-TRAK): more than 60 times accelerated MRA using a combination of CENTRA, keyhole, and SENSE at 3.0 T. J Magn Reson Imaging 27:1455–60PubMedCrossRef Willinek WA, Hadizadeh DR, von Falkenhausen M, Urbach H, Hoogeveen R, Schild HH, Gieseke J (2008) 4D time-resolved MR angiography with keyhole (4D-TRAK): more than 60 times accelerated MRA using a combination of CENTRA, keyhole, and SENSE at 3.0 T. J Magn Reson Imaging 27:1455–60PubMedCrossRef
7.
go back to reference Lim RP, Shapiro M, Wang EY, Law M, Babb JS, Rueff LE, Jacob JS, Kim S, Carson RH, Mulholland TP, Laub G, Hecht EM (2008) 3D time-resolved MR angiography (MRA) of the carotid artery with time-resolved imaging with stochastic trajectories: comparison with 3D contrast-enhanced bolus-chase MRA and 3D time-of-flight MRA. Am J Neuroradiol 29:1847–54PubMedCrossRef Lim RP, Shapiro M, Wang EY, Law M, Babb JS, Rueff LE, Jacob JS, Kim S, Carson RH, Mulholland TP, Laub G, Hecht EM (2008) 3D time-resolved MR angiography (MRA) of the carotid artery with time-resolved imaging with stochastic trajectories: comparison with 3D contrast-enhanced bolus-chase MRA and 3D time-of-flight MRA. Am J Neuroradiol 29:1847–54PubMedCrossRef
8.
go back to reference Grobner T (2006) Gadolinium—a specific trigger for the development of nephrogenic systemic fibrosing dermopathy and nephrogenic systemic fibrosis? Nephrol Dial Transplant 21:1104–8PubMedCrossRef Grobner T (2006) Gadolinium—a specific trigger for the development of nephrogenic systemic fibrosing dermopathy and nephrogenic systemic fibrosis? Nephrol Dial Transplant 21:1104–8PubMedCrossRef
9.
go back to reference Marckmann P, Skov L, Rossen K, Dupont A, Damholt MB, Heaf JG, Thomsen HS (2006) Nephrogenic systemic fibrosis: suspected causative role of gadodiamide used for contrast-enhanced magnetic resonance imaging. J Am Soc Nephrol 17:2359–62PubMedCrossRef Marckmann P, Skov L, Rossen K, Dupont A, Damholt MB, Heaf JG, Thomsen HS (2006) Nephrogenic systemic fibrosis: suspected causative role of gadodiamide used for contrast-enhanced magnetic resonance imaging. J Am Soc Nephrol 17:2359–62PubMedCrossRef
10.
go back to reference Koktzoglou I, Edelman RR (2008) Fast projective carotid MR angiography using arterial spin-labeled balanced SSFP. J Magn Reson Imaging 28:778–829PubMedCrossRef Koktzoglou I, Edelman RR (2008) Fast projective carotid MR angiography using arterial spin-labeled balanced SSFP. J Magn Reson Imaging 28:778–829PubMedCrossRef
11.
go back to reference Lanzman RS, Voiculescu A, Walther C, Ringelstein A, Bi X, Schmitt P, Freitag SM, Won S, Scherer A, Blondin D (2009) ECG-gated nonenhanced 3D steady-state free precession (SSFP) MR angiography (MRA) in assessment of transplant renal arteries: comparison with digital substraction angiography (DSA). Radiology 252:914–21PubMedCrossRef Lanzman RS, Voiculescu A, Walther C, Ringelstein A, Bi X, Schmitt P, Freitag SM, Won S, Scherer A, Blondin D (2009) ECG-gated nonenhanced 3D steady-state free precession (SSFP) MR angiography (MRA) in assessment of transplant renal arteries: comparison with digital substraction angiography (DSA). Radiology 252:914–21PubMedCrossRef
12.
go back to reference Katoh M, Spüntrup E, Kuehl H, Stuber M, Günther RW, Botnar RM (2009) Flow-targeted inversion-prepared b-TFE coronary MR angiography: initial results in patients. Fortschr Roentgenstr 181:1050–5CrossRef Katoh M, Spüntrup E, Kuehl H, Stuber M, Günther RW, Botnar RM (2009) Flow-targeted inversion-prepared b-TFE coronary MR angiography: initial results in patients. Fortschr Roentgenstr 181:1050–5CrossRef
13.
go back to reference Glockner JF, Takahashi N, Kawashima A, Woodrum DA, Stanley DW, Takei N, Miyoshi M, Sun W (2010) Non-contrast renal artery MRA using an inflow inversion recovery steady-state free precession technique (Inhance): Comparison with 3D contrast-enhanced MRA. J Magn Reson Imaging 31:1411–1418PubMedCrossRef Glockner JF, Takahashi N, Kawashima A, Woodrum DA, Stanley DW, Takei N, Miyoshi M, Sun W (2010) Non-contrast renal artery MRA using an inflow inversion recovery steady-state free precession technique (Inhance): Comparison with 3D contrast-enhanced MRA. J Magn Reson Imaging 31:1411–1418PubMedCrossRef
14.
go back to reference Maki JH, Wilson GJ, Eubank WB, Glickerman DJ, Pipavath S, Hoogeveen RM (2007) Steady-state free precession MRA of the renal arteries: breath-hold and navigator-gated techniques vs. CE-MRA. J Magn Reson Imaging 26:966–973PubMedCrossRef Maki JH, Wilson GJ, Eubank WB, Glickerman DJ, Pipavath S, Hoogeveen RM (2007) Steady-state free precession MRA of the renal arteries: breath-hold and navigator-gated techniques vs. CE-MRA. J Magn Reson Imaging 26:966–973PubMedCrossRef
15.
go back to reference Edelman RR, Siewert B, Darby DG, Thangaraj V, Nobre AC, Mesulam MM, Warach S (1994) Qualitative mapping of cerebral blood flow and functional localization with echo-planar MR imaging and signal targeting with alternating radio frequency. Radiology 192:513–20PubMed Edelman RR, Siewert B, Darby DG, Thangaraj V, Nobre AC, Mesulam MM, Warach S (1994) Qualitative mapping of cerebral blood flow and functional localization with echo-planar MR imaging and signal targeting with alternating radio frequency. Radiology 192:513–20PubMed
16.
go back to reference Bi X, Weale P, Schmitt P, Zuehlsdorff S, Jerecic R (2010) Non-contrast-enhanced four-dimensional (4D) intracranial MR angiography: A feasibility study. Magn Reson Med 63:835–41PubMedCrossRef Bi X, Weale P, Schmitt P, Zuehlsdorff S, Jerecic R (2010) Non-contrast-enhanced four-dimensional (4D) intracranial MR angiography: A feasibility study. Magn Reson Med 63:835–41PubMedCrossRef
17.
go back to reference Yan L, Wang S, Zhuo Y, Wolf RL, Stiefel MF, An J, Ye Y, Zhang Q, Melhem ER, Wang DJ (2010) Unenhanced Dynamic MR Angiography: High Spatial and Temporal Resolution by Using True FISP-based Spin Tagging with Alternating Radiofrequency. Radiology 256:270–9PubMedCrossRef Yan L, Wang S, Zhuo Y, Wolf RL, Stiefel MF, An J, Ye Y, Zhang Q, Melhem ER, Wang DJ (2010) Unenhanced Dynamic MR Angiography: High Spatial and Temporal Resolution by Using True FISP-based Spin Tagging with Alternating Radiofrequency. Radiology 256:270–9PubMedCrossRef
18.
go back to reference Kim SG (1995) Quantification of relative cerebral blood flow change by flow-sensitive alternating inversion recovery (FAIR) technique: application to functional mapping. Magn Reson Med 34:293–301PubMedCrossRef Kim SG (1995) Quantification of relative cerebral blood flow change by flow-sensitive alternating inversion recovery (FAIR) technique: application to functional mapping. Magn Reson Med 34:293–301PubMedCrossRef
19.
go back to reference Henderson RD, Eliasziw M, Fox AJ, Rothwell PM, Barnett HJ, for the North American Symptomatic Carotid Endarterectomy Trial (NASCET) Group (2002) Angiographically defined collateral circulation and risk of stroke in patients with severe carotid artery stenosis. Stroke 31:128–132 Henderson RD, Eliasziw M, Fox AJ, Rothwell PM, Barnett HJ, for the North American Symptomatic Carotid Endarterectomy Trial (NASCET) Group (2002) Angiographically defined collateral circulation and risk of stroke in patients with severe carotid artery stenosis. Stroke 31:128–132
20.
go back to reference Lopez-Bresnahan MV, Kearse LA, Yanez P, Young TI (1993) Anterior communicating artery collateral flow protection against ischemic change during carotid endarterectomy. J Neurosurg 79:379–382PubMedCrossRef Lopez-Bresnahan MV, Kearse LA, Yanez P, Young TI (1993) Anterior communicating artery collateral flow protection against ischemic change during carotid endarterectomy. J Neurosurg 79:379–382PubMedCrossRef
21.
go back to reference Schneider PA, Ringelstein EB, Rossman ME, Dilley RB, Sobel DF, Otis SM, Bernstein EF (1988) Importance of cerebral collateral pathways during carotid endarterectomy. Stroke 19:1328–1334PubMed Schneider PA, Ringelstein EB, Rossman ME, Dilley RB, Sobel DF, Otis SM, Bernstein EF (1988) Importance of cerebral collateral pathways during carotid endarterectomy. Stroke 19:1328–1334PubMed
22.
go back to reference Harrison MJ, Koch C, Eckert B, Becker V, Kromer H, Heesen C, Gryska U, Freitag HJ, Rother J, Zeumer H (2003) Collateral circulation is an independent radiological predictor of outcome after thrombolysis in acute ischemic stroke. Neuroradiology 45:11–18 Harrison MJ, Koch C, Eckert B, Becker V, Kromer H, Heesen C, Gryska U, Freitag HJ, Rother J, Zeumer H (2003) Collateral circulation is an independent radiological predictor of outcome after thrombolysis in acute ischemic stroke. Neuroradiology 45:11–18
23.
go back to reference Hendrikse J, Hartkamp MJ, Hillen B, Mali WPTM, van der Grond J (2001) Collateral ability of the circle of Willis in patients with unilateral internal carotid artery occlusion—Border zone infarcts and clinical symptoms. Stroke 32:2768–2773PubMedCrossRef Hendrikse J, Hartkamp MJ, Hillen B, Mali WPTM, van der Grond J (2001) Collateral ability of the circle of Willis in patients with unilateral internal carotid artery occlusion—Border zone infarcts and clinical symptoms. Stroke 32:2768–2773PubMedCrossRef
24.
go back to reference Bisschops RHC, Klijn CJM, Kapelle LJ, van Huffelen AC, van der Grond J (2003) Collateral flow and ischemic brain lesions in patients with unilateral carotid artery occlusion. Neurology 60:1435–1441PubMed Bisschops RHC, Klijn CJM, Kapelle LJ, van Huffelen AC, van der Grond J (2003) Collateral flow and ischemic brain lesions in patients with unilateral carotid artery occlusion. Neurology 60:1435–1441PubMed
25.
go back to reference Fried LF, Shlipak MG, Crump C, Bleyer AJ, Gottdiener SJ, Kronmal RA, Kuller LH, Newman AB (2003) Renal insufficiency as a predictor of cardiovascular outcomes and mortality in elderly individuals. J Am Coll Cardiol 41:1364–72PubMedCrossRef Fried LF, Shlipak MG, Crump C, Bleyer AJ, Gottdiener SJ, Kronmal RA, Kuller LH, Newman AB (2003) Renal insufficiency as a predictor of cardiovascular outcomes and mortality in elderly individuals. J Am Coll Cardiol 41:1364–72PubMedCrossRef
26.
go back to reference Hope MD, Purcell DD, Hope TA, von Morze C, Vigneron DB, Alley MT, Dillon WP (2009) Complete intracranial arterial and venous blood flow evaluation with 4D flow MR imaging. Am J Neuroradiol 30:362–366PubMedCrossRef Hope MD, Purcell DD, Hope TA, von Morze C, Vigneron DB, Alley MT, Dillon WP (2009) Complete intracranial arterial and venous blood flow evaluation with 4D flow MR imaging. Am J Neuroradiol 30:362–366PubMedCrossRef
27.
go back to reference Wetzel S, Meckel S, Frydrychowicz A, Bonati L, Radue EW, Scheffler K, Henning J, Markl M (2007) In vivo assessment and visualization of intracranial arterial hemodynamics with flow-sensitized 4D MR imaging at 3 T. Am J Neuroradiol 28:433–438PubMed Wetzel S, Meckel S, Frydrychowicz A, Bonati L, Radue EW, Scheffler K, Henning J, Markl M (2007) In vivo assessment and visualization of intracranial arterial hemodynamics with flow-sensitized 4D MR imaging at 3 T. Am J Neuroradiol 28:433–438PubMed
28.
go back to reference Bokkers RPH, van Laar PJ, van de Ven KCC, Kapelle LJ, Klijn CJM, Hendrikse J (2008) Arterial spin-labeling MR imaging measurements of timing parameters in patients with a carotid artery occlusion. Am J Neuroradiol 29:1698–1703PubMedCrossRef Bokkers RPH, van Laar PJ, van de Ven KCC, Kapelle LJ, Klijn CJM, Hendrikse J (2008) Arterial spin-labeling MR imaging measurements of timing parameters in patients with a carotid artery occlusion. Am J Neuroradiol 29:1698–1703PubMedCrossRef
29.
go back to reference Chng SM, Petersen ET, Zimine I, Sitoh YY, Lim CCT, Golay X (2008) Territorial arterial spin labeling in the assessment of collateral circulation: comparison with digital subtraction angiography. Stroke 39:3248–3254PubMedCrossRef Chng SM, Petersen ET, Zimine I, Sitoh YY, Lim CCT, Golay X (2008) Territorial arterial spin labeling in the assessment of collateral circulation: comparison with digital subtraction angiography. Stroke 39:3248–3254PubMedCrossRef
30.
go back to reference Wu B, Wang X, Guo J, Xie S, Wong EC, Zhang J, Jiang X, Fang J (2008) Collateral circulation imaging: MR perfusion territory arterial spin labeling at 3 T. Am J Neuroradiol 29:1855–1860PubMedCrossRef Wu B, Wang X, Guo J, Xie S, Wong EC, Zhang J, Jiang X, Fang J (2008) Collateral circulation imaging: MR perfusion territory arterial spin labeling at 3 T. Am J Neuroradiol 29:1855–1860PubMedCrossRef
31.
go back to reference van Osch MJ, Hendrikse J, Golay X, Bakker CJ, van der Grond J (2006) Non-invasive visualization of collateral blood flow patterns of the circle of Willis by dynamic MR angiography. Med Image Anal 10:59–70PubMedCrossRef van Osch MJ, Hendrikse J, Golay X, Bakker CJ, van der Grond J (2006) Non-invasive visualization of collateral blood flow patterns of the circle of Willis by dynamic MR angiography. Med Image Anal 10:59–70PubMedCrossRef
32.
go back to reference Salustio F, Kern R, Günther M, Szabo K, Griebe M, Meairs S, Hennerici M, Gass A (2008) Assessment of intracranial collateral flow by using dynamic arterial spin labeling MRA and transcranial color-coded duplex ultrasound. Stroke 39:1894–1897CrossRef Salustio F, Kern R, Günther M, Szabo K, Griebe M, Meairs S, Hennerici M, Gass A (2008) Assessment of intracranial collateral flow by using dynamic arterial spin labeling MRA and transcranial color-coded duplex ultrasound. Stroke 39:1894–1897CrossRef
33.
go back to reference Warmuth C, Rüping M, Förschler A, Koennecke H, Valdueza JM, Kauert A, Schreiber SJ, Siekmann R, Zimmer C (2005) Dynamic spin labeling angiography in extracranial carotid artery stenosis. Am J Neuroradiol 26:1035–1043PubMed Warmuth C, Rüping M, Förschler A, Koennecke H, Valdueza JM, Kauert A, Schreiber SJ, Siekmann R, Zimmer C (2005) Dynamic spin labeling angiography in extracranial carotid artery stenosis. Am J Neuroradiol 26:1035–1043PubMed
34.
go back to reference Edelman RR, Siewert B, Adamis M, Gaa J, Laub G, Wielopolski P (1994) Signal targeting with alternating radiofrequency (STAR) sequences: application to MR angiography. Magn Res Med 31:233–8CrossRef Edelman RR, Siewert B, Adamis M, Gaa J, Laub G, Wielopolski P (1994) Signal targeting with alternating radiofrequency (STAR) sequences: application to MR angiography. Magn Res Med 31:233–8CrossRef
35.
go back to reference Schmitt P, Speier P, Bi X, Weale P, Müller E (2010) Non-contrast-enhanced 4D intracranial MR angiography: Optimizations using a variable flip angle approach. Proceedings of the 18th ISMRM Scientific Meeting; Stockholm, Sweden: 402 Schmitt P, Speier P, Bi X, Weale P, Müller E (2010) Non-contrast-enhanced 4D intracranial MR angiography: Optimizations using a variable flip angle approach. Proceedings of the 18th ISMRM Scientific Meeting; Stockholm, Sweden: 402
Metadata
Title
Nonenhanced ECG-gated time-resolved 4D Steady-state free precession (SSFP) MR angiography (MRA) for assessment of cerebral collateral flow: comparison with digital subtraction angiography (DSA)
Authors
Rotem Shlomo Lanzman
Patric Kröpil
Peter Schmitt
Xiaoming Bi
Michael Gliem
Falk R. Miese
Daniel Hänggi
Marcel Kamp
Axel Scherer
Bernd Turowski
Dirk Blondin
Publication date
01-06-2011
Publisher
Springer-Verlag
Published in
European Radiology / Issue 6/2011
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-010-2051-9

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