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Arterial Spin Labeling Measurements of Cerebral Perfusion Territories in Experimental Ischemic Stroke

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Abstract

Collateral circulation, defined as the supplementary vascular network that maintains cerebral blood flow (CBF) when the main vessels fail, constitutes one important defense mechanism of the brain against ischemic stroke. In the present study, continuous arterial spin labeling (CASL) was used to quantify CBF and obtain perfusion territory maps of the major cerebral arteries in spontaneously hypertensive rats (SHRs) and their normotensive Wistar-Kyoto (WKY) controls. Results show that both WKY and SHR have complementary, yet significantly asymmetric perfusion territories. Right or left dominances were observed in territories of the anterior (ACA), middle and posterior cerebral arteries, and the thalamic artery. Magnetic resonance angiography showed that some of the asymmetries were correlated with variations of the ACA. The leptomeningeal circulation perfusing the outer layers of the cortex was observed as well. Significant and permanent changes in perfusion territories were obtained after temporary occlusion of the right middle cerebral artery in both SHR and WKY, regardless of their particular dominance. However, animals with right dominance presented a larger volume change of the left perfusion territory (23 ± 9%) than animals with left dominance (7 ± 5%, P < 0.002). The data suggest that animals with contralesional dominance primarily safeguard local CBF values with small changes in contralesional perfusion territory, while animals with ipsilesional dominance show a reversal of dominance and a substantial increase in contralesional perfusion territory. These findings show the usefulness of CASL to probe the collateral circulation.

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References

  1. Liebeskind DS. Collateral circulation. Stroke. 2003;34(9):2279–84.

    Article  PubMed  Google Scholar 

  2. Bang OY, Saver JL, Kim SJ, Kim GM, Chung CS, Ovbiagele B, et al. Collateral flow predicts response to endovascular therapy for acute ischemic stroke. Stroke. 2011;42(3):693–9.

    Article  PubMed  Google Scholar 

  3. Maas MB, Lev MH, Ay H, Singhal AB, Greer DM, Smith WS, et al. Collateral vessels on CT angiography predict outcome in acute ischemic stroke. Stroke. 2009;40(9):3001–5.

    Article  PubMed  Google Scholar 

  4. Bang OY, Saver JL, Buck BH, Alger JR, Starkman S, Ovbiagele B, et al. Impact of collateral flow on tissue fate in acute ischaemic stroke. J Neurol Neurosurg Psychiatry. 2008;79(6):625–9.

    Article  PubMed  CAS  Google Scholar 

  5. Liebeskind DS. Collaterals in acute stroke: beyond the clot. Neuroimaging Clin N Am. 2005;15(3):553–73. x.

    Article  PubMed  Google Scholar 

  6. Detre JA, Leigh JS, Williams DS, Koretsky AP. Perfusion imaging. Magn Reson Med. 1992;23(1):37–45.

    Article  PubMed  CAS  Google Scholar 

  7. Golay X, Hendrikse J, Lim TC. Perfusion imaging using arterial spin labeling. Top Magn Reson Imaging. 2004;15(1):10–27.

    Article  PubMed  Google Scholar 

  8. Williams DS, Detre JA, Leigh JS, Koretsky AP. Magnetic resonance imaging of perfusion using spin inversion of arterial water. Proc Natl Acad Sci U S A. 1992;89(1):212–6.

    Article  PubMed  CAS  Google Scholar 

  9. Hoffman JM, Coleman RE. Perfusion quantitation using positron emission tomography. Invest Radiol. 1992;27 Suppl 2:S22–6.

    PubMed  Google Scholar 

  10. Villringer A, Rosen BR, Belliveau JW, Ackerman JL, Lauffer RB, Buxton RB, et al. Dynamic imaging with lanthanide chelates in normal brain: contrast due to magnetic susceptibility effects. Magn Reson Med. 1988;6(2):164–74.

    Article  PubMed  CAS  Google Scholar 

  11. Detre JA, Zhang W, Roberts DA, Silva AC, Williams DS, Grandis DJ, et al. Tissue specific perfusion imaging using arterial spin labeling. NMR Biomed. 1994;7(1–2):75–82.

    Article  PubMed  CAS  Google Scholar 

  12. Paiva FF, Tannus A, Silva AC. Measurement of cerebral perfusion territories using arterial spin labelling. NMR Biomed. 2007;20(7):633–42.

    Article  PubMed  Google Scholar 

  13. van Laar PJ, van der Grond J, Hendrikse J. Brain perfusion territory imaging: methods and clinical applications of selective arterial spin-labeling MR imaging. Radiology. 2008;246(2):354–64.

    Article  PubMed  Google Scholar 

  14. Chng SM, Petersen ET, Zimine I, Sitoh YY, Lim CC, Golay X. Territorial arterial spin labeling in the assessment of collateral circulation: comparison with digital subtraction angiography. Stroke. 2008;39(12):3248–54.

    Article  PubMed  Google Scholar 

  15. Jones CE, Wolf RL, Detre JA, Das B, Saha PK, Wang J, et al. Structural MRI of carotid artery atherosclerotic lesion burden and characterization of hemispheric cerebral blood flow before and after carotid endarterectomy. NMR Biomed. 2006;19(2):198–208.

    Article  PubMed  CAS  Google Scholar 

  16. Hendrikse J, Petersen ET, Cheze A, Chng SM, Venketasubramanian N, Golay X. Relation between cerebral perfusion territories and location of cerebral infarcts. Stroke. 2009;40(5):1617–22.

    Article  PubMed  Google Scholar 

  17. van Laar PJ, Hendrikse J, Klijn CJ, Kappelle LJ, van Osch MJ, van der Grond J. Symptomatic carotid artery occlusion: flow territories of major brain-feeding arteries. Radiology. 2007;242(2):526–34.

    Article  PubMed  Google Scholar 

  18. Zaharchuk G, Do HM, Marks MP, Rosenberg J, Moseley ME, Steinberg GK. Arterial spin-labeling MRI can identify the presence and intensity of collateral perfusion in patients with Moyamoya disease. Stroke. 2011;42(9):2485–91.

    Article  PubMed  Google Scholar 

  19. Amenta F, Di Tullio MA, Tomassoni D. Arterial hypertension and brain damage–evidence from animal models (review). Clin Exp Hypertens. 2003;25(6):359–80.

    Article  PubMed  Google Scholar 

  20. Longa EZ, Weinstein PR, Carlson S, Cummins R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke. 1989;20(1):84–91.

    Article  PubMed  CAS  Google Scholar 

  21. Maccotta L, Detre JA, Alsop DC. The efficiency of adiabatic inversion for perfusion imaging by arterial spin labeling. NMR Biomed. 1997;10(4–5):216–21.

    Article  PubMed  CAS  Google Scholar 

  22. Silva AC, Zhang W, Williams DS, Koretsky AP. Multi-slice MRI of rat brain perfusion during amphetamine stimulation using arterial spin labeling. Magn Reson Med. 1995;33(2):209–14.

    Article  PubMed  CAS  Google Scholar 

  23. Zhang W, Silva AC, Williams DS, Koretsky AP. NMR measurement of perfusion using arterial spin labeling without saturation of macromolecular spins. Magn Reson Med. 1995;33(3):370–6.

    Article  PubMed  CAS  Google Scholar 

  24. Alsop DC, Detre JA. Reduced transit-time sensitivity in noninvasive magnetic resonance imaging of human cerebral blood flow. J Cereb Blood Flow Metab. 1996;16(6):1236–49.

    Article  PubMed  CAS  Google Scholar 

  25. McCabe C, Gallagher L, Gsell W, Graham D, Dominiczak AF, Macrae IM. Differences in the evolution of the ischemic penumbra in stroke-prone spontaneously hypertensive and Wistar-Kyoto rats. Stroke. 2009;40(12):3864–8.

    Article  PubMed  Google Scholar 

  26. Gerriets T, Stolz E, Walberer M, Muller C, Kluge A, Bachmann A, et al. Noninvasive quantification of brain edema and the space-occupying effect in rat stroke models using magnetic resonance imaging. Stroke. 2004;35(2):566–71.

    Article  PubMed  CAS  Google Scholar 

  27. Herscovitch P, Raichle ME. What is the correct value for the brain–blood partition coefficient for water? J Cereb Blood Flow Metab. 1985;5(1):65–9.

    Article  PubMed  CAS  Google Scholar 

  28. Zhang W, Williams DS, Koretsky AP. Measurement of rat brain perfusion by NMR using spin labeling of arterial water: in vivo determination of the degree of spin labeling. Magn Reson Med. 1993;29(3):416–21.

    Article  PubMed  CAS  Google Scholar 

  29. Sokoloff L, Reivich M, Kennedy C, Des Rosiers MH, Patlak CS, Pettigrew KD, et al. The [14 C]deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure, and normal values in the conscious and anesthetized albino rat. J Neurochem. 1977;28(5):897–916.

    Article  PubMed  CAS  Google Scholar 

  30. Brown JO. The morphology of circulus arteriosus cerebri in rats. Anat Rec. 1966;156(1):99–106.

    Article  PubMed  CAS  Google Scholar 

  31. Paiva FF, Tannus A, Talagala SL, Silva AC. Arterial spin labeling of cerebral perfusion territories using a separate labeling coil. J Magn Reson Imaging. 2008;27(5):970–7.

    Article  PubMed  Google Scholar 

  32. Hendrikse J, van der Grond J, Lu H, van Zijl PC, Golay X. Flow territory mapping of the cerebral arteries with regional perfusion MRI. Stroke. 2004;35(4):882–7.

    Article  PubMed  Google Scholar 

  33. van Laar PJ, Hendrikse J, Golay X, Lu H, van Osch MJ, van der Grond J. In vivo flow territory mapping of major brain feeding arteries. NeuroImage. 2006;29(1):136–44.

    Article  PubMed  Google Scholar 

  34. Brint S, Jacewicz M, Kiessling M, Tanabe J, Pulsinelli W. Focal brain ischemia in the rat: methods for reproducible neocortical infarction using tandem occlusion of the distal middle cerebral and ipsilateral common carotid arteries. J Cereb Blood Flow Metab. 1988;8(4):474–85.

    Article  PubMed  CAS  Google Scholar 

  35. Iadecola C, Davisson RL. Hypertension and cerebrovascular dysfunction. Cell Metab. 2008;7(6):476–84.

    Article  PubMed  CAS  Google Scholar 

  36. Brozici M, van der Zwan A, Hillen B. Anatomy and functionality of leptomeningeal anastomoses: a review. Stroke. 2003;34(11):2750–62.

    Article  PubMed  Google Scholar 

  37. Omura-Matsuoka E, Yagita Y, Sasaki T, Terasaki Y, Oyama N, Sugiyama Y, et al. Hypertension impairs leptomeningeal collateral growth after common carotid artery occlusion: restoration by antihypertensive treatment. J Neurosci Res. 2011;89(1):108–16.

    Article  PubMed  CAS  Google Scholar 

  38. Tuttle JL, Sanders BM, Burkhart HM, Fath SW, Kerr KA, Watson WC, et al. Impaired collateral artery development in spontaneously hypertensive rats. Microcirculation. 2002;9(5):343–51.

    PubMed  CAS  Google Scholar 

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Acknowledgments

The authors acknowledge the excellent technical assistance of Mrs. Xianfeng (Lisa) Zhang. This research was supported by the Intramural Research Program of the NIH, NINDS (Alan P. Koretsky, Scientific Director), and FAPESP (2006/05706-5, 2003/13399-7, 2005/56663-1).

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Authors and Affiliations

  1. Cerebral Microcirculation Unit, Laboratory of Functional and Molecular Imaging, National Institute of Neurological Disorders and Stroke, National Institutes of Health, 10 Center Drive MSC 1065, Building 10 Room B1D106, Bethesda, MD, 20892-1065, USA

    Renata F. Leoni, Fernando F. Paiva, Byeong-Teck Kang, George C. Nascimento & Afonso C. Silva

  2. Departamento de Física, FFCLRP, Universidade de São Paulo, Ribeirao Preto, Sao Paulo, 14040-901, Brazil

    Renata F. Leoni

  3. Departamento de Física e Informática, IFSC, Universidade de São Paulo, São Carlos, São Paulo, 13560-970, Brazil

    Fernando F. Paiva & Alberto Tannús

  4. Section on Stroke Diagnostics and Therapeutics, National Institute of Neurological Disorders and Stroke, NIH, Bethesda, MD, 20892-1063, USA

    Erica C. Henning

  5. Instituto do Cérebro, Hospital Universitário Onorio Lopes, Universidade Federal do Rio Grande do Norte Natal, Rio Grande do Norte, 590560-450, Brazil

    Dráulio B. De Araújo

Authors
  1. Renata F. Leoni
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  2. Fernando F. Paiva
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  3. Byeong-Teck Kang
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  4. Erica C. Henning
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  5. George C. Nascimento
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  6. Alberto Tannús
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  7. Dráulio B. De Araújo
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  8. Afonso C. Silva
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Corresponding author

Correspondence to Afonso C. Silva.

Additional information

Renata F. Leoni and Fernando F. Paiva contributed equally to this work

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Leoni, R.F., Paiva, F.F., Kang, BT. et al. Arterial Spin Labeling Measurements of Cerebral Perfusion Territories in Experimental Ischemic Stroke. Transl. Stroke Res. 3, 44–55 (2012). https://doi.org/10.1007/s12975-011-0115-z

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  • DOI: https://doi.org/10.1007/s12975-011-0115-z

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