Springer Nature is making SARS-CoV-2 and COVID-19 research free View research | View latest news | Sign up for updates

Permeability Imaging as a Biomarker of Leptomeningeal Collateral Flow in Patients with Intracranial Arterial Stenosis

Abstract

Different methods of angiography are of great clinical utility; however, it still remains unstandardized as which method would be suitable to determine cerebral collateral circulation. Here we compared digital subtraction angiography (DSA), computer tomography angiography (CTA) and dynamic contrast-enhanced T1-weighted imaging magnetic resonance imaging (MRI) findings in seven patients with severe intracranial arterial stenosis, and determine whether volume transfer constant (K trans) maps of permeability imaging could be used as the biomarkers of cerebral collateral circulation. We retrospectively reviewed seven adult patients with severe intracranial arterial stenosis or occlusion with a complete parenchymal and vascular imaging work-up. DSA, CTA source imaging (CTA-SI), arterial spin labeling (ASL), and K trans maps were used to assess their collateral flow. Cohen’s Kappa coefficient was calculated to test the consistency of their collateral scores. A reasonable agreement was found between DSA and K trans maps (Kappa = 0.502, P < 0.001) when all 15 regional vascular sites were included, and a better agreement found after exclusion of perforating artery territories (N = 10 sites, Kappa = 0.766, P < 0.001). The agreement between CTA-SI and DSA was moderate on all 15 sites (Kappa = 0.413, P < 0.001) and 10 sites (Kappa = 0.329, P < 0.001). The agreement between ASL and DSA was least favorable, no matter for all 15 sites (Kappa = 0.270, P < 0.001) or 10 sites (Kappa = 0.205, P = 0.002). K trans maps are useful and promising for leptomeningeal collateral assessment, when compared to CTA-SI or ASL. Further studies are requited for verify its validity in a large registry of patients.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2

Abbreviations

DSA:

Digital subtraction angiography

MRI:

Magnetic resonance imaging

CT:

Computer tomography

CTA:

Computer tomography angiography

CTA-SI:

CTA source imaging

BBB:

Blood brain barrier

ASL:

Arterial spin labeling

DCE T1:

Dynamic contrast-enhanced T1-weighted imaging

ASPECTS:

Alberta stroke program early CT score

References

  1. 1.

    Shuaib, A., Butcher, K., Mohammad, A. A., Saqqur, M., & Liebeskind, D. S. (2011). Collateral blood vessels in acute ischaemic stroke: a potential therapeutic target. The Lancet Neurology, 10, 909–921.

  2. 2.

    McVerry, F., Liebeskind, D., & Muir, K. (2012). Systematic review of methods for assessing leptomeningeal collateral flow. American Journal of Neuroradiology, 33, 576–582.

  3. 3.

    Scalzo, F., Alger, J. R., Hu, X., Saver, J. L., Dani, K. A., Muir, K. W., et al. (2013). Multi-center prediction of hemorrhagic transformation in acute ischemic stroke using permeability imaging features. Magnetic Resonance Imaging, 31, 961–969.

  4. 4.

    Lim, M., Cheshier, S., & Steinberg, G. K. (2006). New vessel formation in the central nervous system during tumor growth, vascular malformations, and Moyamoya. Current Neurovascular Research, 3, 237–245.

  5. 5.

    Wu, B., Lou, X., Wu, X., & Ma, L. (2013). Intra- and interscanner reliability and reproducibility of 3D whole-brain pseudo-continuous arterial spin-labeling MR perfusion at 3T. Journal of Magnetic Resonance Imaging.

  6. 6.

    Tofts, P. S. (1997). Modeling tracer kinetics in dynamic Gd-DTPA MR imaging. Journal of Magnetic Resonance Imaging, 7, 91–101.

  7. 7.

    Johnson, G., Wetzel, S. G., Cha, S., Babb, J., & Tofts, P. S. (2004). Measuring blood volume and vascular transfer constant from dynamic, T 2*-weighted contrast-enhanced MRI. Magnetic Resonance in Medicine, 51, 961–968.

  8. 8.

    Kim, J. J., Fischbein, N. J., Lu, Y., Pham, D., & Dillon, W. P. (2004). Regional angiographic grading system for collateral flow correlation with cerebral infarction in patients with middle cerebral artery occlusion. Stroke, 35, 1340–1344.

  9. 9.

    Liebeskind, D. S. (2003). A novel CT angiography scale for assessment of collaterals in acute stroke. Stroke, 34, 265.

  10. 10.

    Zaharchuk, G., Do, H. M., Marks, M. P., Rosenberg, J., Moseley, M. E., & Steinberg, G. K. (2011). Arterial spin-labeling MRI can identify the presence and intensity of collateral perfusion in patients with Moyamoya disease. Stroke, 42, 2485–2491.

  11. 11.

    Barber, P. A., Demchuk, A. M., Zhang, J., & Buchan, A. M. (2000). Validity and reliability of a quantitative computed tomography score in predicting outcome of hyperacute stroke before thrombolytic therapy. The Lancet, 355, 1670–1674.

  12. 12.

    Zhu, G., Jovin, T., Aghaebrahim, A., Michel, P., Zhang, W., & Wintermark, M. (2012). Does perfusion imaging add value compared with plain parenchymal and vascular imaging? Journal of Neurointerventional Surgery, 4, 246–250.

  13. 13.

    Liebeskind, D. S. (2009). Imaging the future of stroke: I. Ischemia. Ann Neurol, 66, 574–590.

  14. 14.

    Arenillas, J. F., Álvarez-Sabín, J., Montaner, J., Rosell, A., Molina, C. A., Rovira, A., et al. (2005). Angiogenesis in symptomatic intracranial atherosclerosis predominance of the inhibitor endostatin is related to a greater extent and risk of recurrence. Stroke, 36, 92–97.

  15. 15.

    Rigau, V., Morin, M., Rousset, M., de Bock, F., Lebrun, A., Coubes, P., et al. (2007). Angiogenesis is associated with blood–brain barrier permeability in temporal lobe epilepsy. Brain, 130, 1942–1956.

  16. 16.

    Liu, H., Chung, H., Chou, M., Liou, M., Wang, C., Kao, H., et al. (2013). Effects of microvascular permeability changes on contrast-enhanced T1 and pharmacokinetic MR imagings after ischemia. Stroke, 44, 1872–1877.

  17. 17.

    Hom, J., Dankbaar, J., Soares, B., Schneider, T., Cheng, S., Bredno, J., et al. (2011). Blood-brain barrier permeability assessed by perfusion CT predicts symptomatic hemorrhagic transformation and malignant edema in acute ischemic stroke. American Journal of Neuroradiology, 32, 41–48.

  18. 18.

    Wardlaw, J. (2010). Blood-brain barrier and cerebral small vessel disease. Journal of the Neurological Sciences, 299, 66–71.

  19. 19.

    Topakian, R., Barrick, T., Howe, F., & Markus, H. (2010). Blood–brain barrier permeability is increased in normal-appearing white matter in patients with lacunar stroke and leucoaraiosis. Journal of Neurology, Neurosurgery and Psychiatry, 81, 192–197.

  20. 20.

    Starr, J. M., Farrall, A. J., Armitage, P., McGurn, B., & Wardlaw, J. (2009). Blood–brain barrier permeability in Alzheimer’s disease: a case–control MRI study. Psychiatry Research: Neuroimaging, 171, 232–241.

  21. 21.

    Demir, C. F., İnci, M. F., Özkan, F., & Özdemir, H. H. (2013). Is it possible to detect active multiple sclerosis plaques using MR thermometry techniques? Medical Hypotheses, 80, 321–324.

  22. 22.

    Lee, K., Latour, L., Luby, M., Hsia, A., Merino, J., & Warach, S. (2009). Distal hyperintense vessels on FLAIR An MRI marker for collateral circulation in acute stroke? Neurology, 72, 1134–1139.

  23. 23.

    Wu, B., Wang, X., Guo, J., Xie, S., Wong, E., Zhang, J., et al. (2008). Collateral circulation imaging: MR perfusion territory arterial spin-labeling at 3T. American Journal of Neuroradiology, 29, 1855–1860.

  24. 24.

    Chng, S. M., Petersen, E. T., Zimine, I., Sitoh, Y., Lim, C. T., & Golay, X. (2008). Territorial arterial spin labeling in the assessment of collateral circulation comparison with digital subtraction angiography. Stroke, 39, 3248–3254.

  25. 25.

    Okell, T. W., Chappell, M. A., Woolrich, M. W., Günther, M., Feinberg, D. A., & Jezzard, P. (2010). Vessel-encoded dynamic magnetic resonance angiography using arterial spin labeling. Magnetic Resonance in Medicine, 64, 430–438.

Download references

Acknowledgments

This study was supported by National Natural Science Foundation of China (Grant Nos. 81371286 and 81101034).

Author information

Correspondence to Weiwei Zhang or Xin Lou.

Additional information

Hui Chen and Bing Wu have contributed equally to this study.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Chen, H., Wu, B., Zhu, G. et al. Permeability Imaging as a Biomarker of Leptomeningeal Collateral Flow in Patients with Intracranial Arterial Stenosis. Cell Biochem Biophys 71, 1273–1279 (2015). https://doi.org/10.1007/s12013-014-0343-4

Download citation

Keywords

  • Magnetic resonance imaging
  • Collateral circulation
  • Intracranial stenosis
  • Permeability
  • K trans