Top

Published in:

01-03-2018 | Functional Neuroradiology

Increased variability of watershed areas in patients with high-grade carotid stenosis

Authors: Stephan Kaczmarz, Vanessa Griese, Christine Preibisch, Michael Kallmayer, Michael Helle, Isabel Wustrow, Esben Thade Petersen, Hans-Henning Eckstein, Claus Zimmer, Christian Sorg, Jens Göttler

Published in: Neuroradiology | Issue 3/2018

Abstract

Purpose

Watershed areas (WSAs) of the brain are most susceptible to acute hypoperfusion due to their peripheral location between vascular territories. Additionally, chronic WSA-related vascular processes underlie cognitive decline especially in patients with cerebral hemodynamic compromise. Despite of high relevance for both clinical diagnostics and research, individual in vivo WSA definition is fairly limited to date. Thus, this study proposes a standardized segmentation approach to delineate individual WSAs by use of time-to-peak (TTP) maps and investigates spatial variability of individual WSAs.

Methods

We defined individual watershed masks based on relative TTP increases in 30 healthy elderly persons and 28 patients with unilateral, high-grade carotid stenosis, being at risk for watershed-related hemodynamic impairment. Determined WSA location was confirmed by an arterial transit time atlas and individual super-selective arterial spin labeling. We compared spatial variability of WSA probability maps between groups and assessed TTP differences between hemispheres in individual and group-average watershed locations.

Results

Patients showed significantly higher spatial variability of WSAs than healthy controls. Perfusion on the side of the stenosis was delayed within individual watershed masks as compared to a watershed template derived from controls, being independent from the grade of the stenosis and collateralization status of the circle of Willis.

Conclusion

Results demonstrate feasibility of individual WSA delineation by TTP maps in healthy elderly and carotid stenosis patients. Data indicate necessity of individual segmentation approaches especially in patients with hemodynamic compromise to detect critical regions of impaired hemodynamics.

Available only for authorised users

Momjian-Mayor I, Baron JC (2005) The pathophysiology of watershed infarction in internal carotid artery disease: review of cerebral perfusion studies. Stroke 36(3):567–577. https://doi.org/10.1161/01.STR.0000155727.82242.e1 CrossRefPubMed

D'Amore C, Paciaroni M (2012) Border-zone and watershed infarctions. Front Neurol Neurosci 30:181–184. https://doi.org/10.1159/000333638 CrossRefPubMed

Enzinger C, Smith S, Fazekas F, Drevin G, Ropele S, Nichols T, Behrens T, Schmidt R, Matthews PM (2006) Lesion probability maps of white matter hyperintensities in elderly individuals: results of the Austrian stroke prevention study. J Neurol 253(8):1064–1070. https://doi.org/10.1007/s00415-006-0164-5 CrossRefPubMed

Brundel M, de Bresser J, van Dillen JJ, Kappelle LJ, Biessels GJ (2012) Cerebral microinfarcts: a systematic review of neuropathological studies. J Cereb Blood Flow Metab 32(3):425–436. https://doi.org/10.1038/jcbfm.2011.200 CrossRefPubMedPubMedCentral

Suter OC, Sunthorn T, Kraftsik R, Straubel J, Darekar P, Khalili K, Miklossy J (2002) Cerebral hypoperfusion generates cortical watershed microinfarcts in Alzheimer disease. Stroke 33(8):1986–1992. https://doi.org/10.1161/01.STR.0000024523.82311.77 CrossRefPubMed

van der Zwan A, Hillen B, Tulleken CA et al (1992) Variability of the territories of the major cerebral arteries. J Neurosurg 77(6):927–940. https://doi.org/10.3171/jns.1992.77.6.0927 CrossRefPubMed

Van Laar PJ, Hendrikse J, Mali WP et al (2007) Altered flow territories after carotid stenting and carotid endarterectomy. J Vasc Surg 45(6):1155–1161. https://doi.org/10.1016/j.jvs.2006.11.067 CrossRefPubMed

Hendrikse J, van der Zwan A, Ramos LM et al (2005) Altered flow territories after extracranial-intracranial bypass surgery. Neurosurgery 57(3):486–494. https://doi.org/10.1227/01.NEU.0000170563.70822.10 CrossRefPubMed

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 3T. AJNR Am J Neuroradiol 29(10):1855–1860. https://doi.org/10.3174/ajnr.A1259 CrossRefPubMed

10.

Helle M, Rufer S, van Osch MJ et al (2013) Superselective arterial spin labeling applied for flow territory mapping in various cerebrovascular diseases. J Magn Reson Imaging 38(2):496–503. https://doi.org/10.1002/jmri.24041 CrossRefPubMed

11.

Arteaga DF, Strother MK, Davis LT, Fusco MR, Faraco CC, Roach BA, Scott AO, Donahue MJ (2017) Planning-free cerebral blood flow territory mapping in patients with intracranial arterial stenosis. J Cereb Blood Flow Metab 37(6):1944–1958. https://doi.org/10.1177/0271678X16657573 CrossRefPubMed

12.

Hendrikse J, Petersen ET, van Laar PJ, Golay X (2008) Cerebral border zones between distal end branches of intracranial arteries: MR imaging. Radiology 246(2):572–580. https://doi.org/10.1148/radiol.2461062100 CrossRefPubMed

13.

Mildner T, Muller K, Hetzer S et al (2014) Mapping of arterial transit time by intravascular signal selection. NMR Biomed 27(5):594–609. https://doi.org/10.1002/nbm.3098 CrossRefPubMed

14.

Petersen ET, Mouridsen K, Golay X, all named co-authors of the QUASAR test-retest study (2010) The QUASAR reproducibility study, part II: results from a multi-center arterial spin labeling test-retest study. NeuroImage 49(1):104–113. https://doi.org/10.1016/j.neuroimage.2009.07.068 CrossRefPubMed

15.

van Osch MJ, Teeuwisse WM, van Walderveen MA et al (2009) Can arterial spin labeling detect white matter perfusion signal? Magn Reson Med 62(1):165–173. https://doi.org/10.1002/mrm.22002 CrossRefPubMed

16.

Chen DY, Kuo YS, Hsu HL et al (2016) Loss of labelling efficiency caused by carotid stent in pseudocontinuous arterial spin labelling perfusion study. Clin Radiol 71(1):e21–e27. https://doi.org/10.1016/j.crad.2015.10.004 CrossRefPubMed

17.

Nasel C, Azizi A, Wilfort A, Mallek R, Schindler E (2001) Measurement of time-to-peak parameter by use of a new standardization method in patients with stenotic or occlusive disease of the carotid artery. AJNR Am J Neuroradiol 22(6):1056–1061PubMed

18.

Neumann-Haefelin T, Wittsack HJ, Wenserski F, Siebler M, Seitz RJ, Modder U, Freund HJ (1999) Diffusion- and perfusion-weighted MRI. The DWI/PWI mismatch region in acute stroke. Stroke 30(8):1591–1597. https://doi.org/10.1161/01.STR.30.8.1591 CrossRefPubMed

19.

Helle M, Norris DG, Rufer S et al (2010) Superselective pseudocontinuous arterial spin labeling. Magn Reson Med 64(3):777–786. https://doi.org/10.1002/mrm.22451 CrossRefPubMed

20.

North American Symptomatic Carotid Endarterectomy Trial (1991) Methods, patient characteristics, and progress. Stroke 22:711–720CrossRef

21.

Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA (1987) MR signal abnormalities at 1.5 T in Alzheimer's dementia and normal aging. AJR Am J Roentgenol 149(2):351–356. https://doi.org/10.2214/ajr.149.2.351 CrossRefPubMed

22.

Alsop DC, Detre JA, Golay X, Günther M, Hendrikse J, Hernandez-Garcia L, Lu H, MacIntosh BJ, Parkes LM, Smits M, van Osch MJP, Wang DJJ, Wong EC, Zaharchuk G (2015) Recommended implementation of arterial spin-labeled perfusion MRI for clinical applications: a consensus of the ISMRM perfusion study group and the European consortium for ASL in dementia. Magn Reson Med 73(1):102–116. https://doi.org/10.1002/mrm.25197 CrossRefPubMed

23.

Kluge A, Lukas M, Toth V et al (2015) Analysis of three leakage-correction methods for DSC-based measurement of relative cerebral blood volume with respect to heterogeneity in human gliomas. Magn Reson Imaging 34:410–421CrossRefPubMed

24.

John JP, Wang L, Moffitt AJ, Singh HK, Gado MH, Csernansky JG (2006) Inter-rater reliability of manual segmentation of the superior, inferior and middle frontal gyri. Psychiatry Res 148(2-3):151–163. https://doi.org/10.1016/j.pscychresns.2006.05.006 CrossRefPubMed

25.

Richter V, Helle M, van Osch MJ et al (2017) MR imaging of individual perfusion reorganization using superselective pseudocontinuous arterial spin-labeling in patients with complex extracranial steno-occlusive disease. AJNR Am J Neuroradiol 38(4):703–711. https://doi.org/10.3174/ajnr.A5090 CrossRefPubMed

26.

Kanda T, Ishii K, Kawaguchi H, Kitajima K, Takenaka D (2014) High signal intensity in the dentate nucleus and globus pallidus on unenhanced T1-weighted MR images: relationship with increasing cumulative dose of a gadolinium-based contrast material. Radiology 270(3):834–841. https://doi.org/10.1148/radiol.13131669 CrossRefPubMed

27.

Kanda T, Oba H, Toyoda K, Furui S (2016) Macrocyclic gadolinium-based contrast agents do not cause hyperintensity in the dentate nucleus. AJNR Am J Neuroradiol 37(5):E41. https://doi.org/10.3174/ajnr.A4710 CrossRefPubMed

28.

Radbruch A, Haase R, Kieslich PJ, Weberling LD, Kickingereder P, Wick W, Schlemmer HP, Bendszus M (2017) No signal intensity increase in the dentate nucleus on unenhanced T1-weighted MR images after more than 20 serial injections of macrocyclic gadolinium-based contrast agents. Radiology 282(3):699–707. https://doi.org/10.1148/radiol.2016162241 CrossRefPubMed

29.

van Laar PJ, Hendrikse J, Klijn CJ et al (2007) Symptomatic carotid artery occlusion: flow territories of major brain-feeding arteries. Radiology 242(2):526–534. https://doi.org/10.1148/radiol.2422060179 CrossRefPubMed

30.

Fisher JA, Sobczyk O, Crawley A, Poublanc J, Dufort P, Venkatraghavan L, Sam K, Mikulis D, Duffin J (2017) Assessing cerebrovascular reactivity by the pattern of response to progressive hypercapnia. Hum Brain Mapp in press. https://doi.org/10.1002/hbm.23598

31.

Xie S, Hui LH, Xiao JX, Zhang XD, Peng Q (2011) Detecting misery perfusion in unilateral steno-occlusive disease of the internal carotid artery or middle cerebral artery by MR imaging. AJNR Am J Neuroradiol 32(8):1504–1509. https://doi.org/10.3174/ajnr.A2523 CrossRefPubMed

32.

Derdeyn CP, Videen TO, Grubb RL Jr et al (2001) Comparison of PET oxygen extraction fraction methods for the prediction of stroke risk. J Nucl Med 42(8):1195–1197PubMed

33.

Silvestrini M, Vernieri F, Pasqualetti P, Matteis M, Passarelli F, Troisi E, Caltagirone C (2000) Impaired cerebral vasoreactivity and risk of stroke in patients with asymptomatic carotid artery stenosis. JAMA 283(16):2122–2127. https://doi.org/10.1001/jama.283.16.2122 CrossRefPubMed

34.

Moustafa RR, Momjian-Mayor I, Jones PS, Morbelli S, Day DJ, Aigbirhio FI, Fryer TD, Warburton EA, Baron JC (2011) Microembolism versus hemodynamic impairment in rosary-like deep watershed infarcts: a combined positron emission tomography and transcranial Doppler study. Stroke 42(11):3138–3143. https://doi.org/10.1161/STROKEAHA.111.616334 CrossRefPubMed

35.

ten Dam VH, van den Heuvel DM, de Craen AJ, Bollen EL, Murray HM, Westendorp RG, Blauw GJ, van Buchem MA (2007) Decline in total cerebral blood flow is linked with increase in periventricular but not deep white matter hyperintensities. Radiology 243(1):198–203. https://doi.org/10.1148/radiol.2431052111 CrossRefPubMed

36.

Schmidt R, Petrovic K, Ropele S, Enzinger C, Fazekas F (2007) Progression of leukoaraiosis and cognition. Stroke 38(9):2619–2625. https://doi.org/10.1161/STROKEAHA.107.489112 CrossRefPubMed

37.

van den Heuvel DM, ten Dam VH, de Craen AJ, Admiraal-Behloul F, Olofsen H, Bollen EL, Jolles J, Murray HM, Blauw GJ, Westendorp RG, van Buchem MA (2006) Increase in periventricular white matter hyperintensities parallels decline in mental processing speed in a non-demented elderly population. J Neurol Neurosurg Psychiatry 77(2):149–153. https://doi.org/10.1136/jnnp.2005.070193 CrossRefPubMedPubMedCentral

38.

Mortby ME, Janke AL, Anstey KJ, Sachdev PS, Cherbuin N (2013) High "normal" blood glucose is associated with decreased brain volume and cognitive performance in the 60s: the PATH through life study. PLoS One 8(9):e73697. https://doi.org/10.1371/journal.pone.0073697 CrossRefPubMedPubMedCentral

39.

Aanerud J, Borghammer P, Chakravarty MM, Vang K, Rodell AB, Jónsdottir KY, Møller A, Ashkanian M, Vafaee MS, Iversen P, Johannsen P, Gjedde A (2012) Brain energy metabolism and blood flow differences in healthy aging. J Cereb Blood Flow Metab 32(7):1177–1187. https://doi.org/10.1038/jcbfm.2012.18 CrossRefPubMedPubMedCentral

40.

Alosco ML, Gunstad J, Xu X, Clark US, Labbe DR, Riskin-Jones HH, Terrero G, Schwarz NF, Walsh EG, Poppas A, Cohen RA, Sweet LH (2014) The impact of hypertension on cerebral perfusion and cortical thickness in older adults. J Am Soc Hypertens 8(8):561–570. https://doi.org/10.1016/j.jash.2014.04.002 CrossRefPubMedPubMedCentral

Title: Increased variability of watershed areas in patients with high-grade carotid stenosis
Authors: Stephan Kaczmarz
Vanessa Griese
Christine Preibisch
Michael Kallmayer
Michael Helle
Isabel Wustrow
Esben Thade Petersen
Hans-Henning Eckstein
Claus Zimmer
Christian Sorg
Jens Göttler
Publication date: 01-03-2018
Publisher: Springer Berlin Heidelberg
Published in: Neuroradiology / Issue 3/2018
Print ISSN: 0028-3940
Electronic ISSN: 1432-1920
DOI: https://doi.org/10.1007/s00234-017-1970-4

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Increased variability of watershed areas in patients with high-grade carotid stenosis

Abstract

Purpose

Methods

Results

Conclusion

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 3/2018

MRI findings in glutamic acid decarboxylase associated autoimmune epilepsy

Transit time corrected arterial spin labeling technique aids to overcome delayed transit time effect

Alteration of putaminal fractional anisotropy in Parkinson’s disease: a longitudinal diffusion kurtosis imaging study

Combining monoenergetic extrapolations from dual-energy CT with iterative reconstructions: reduction of coil and clip artifacts from intracranial aneurysm therapy

The T1 shine through effect on susceptibility weighted imaging: an under recognized phenomenon

Generalized q-sampling imaging fiber tractography reveals displacement and infiltration of fiber tracts in low-grade gliomas