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Non-invasive evaluation of cerebral perfusion in patients with transient ischemic attack: an fMRI study

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Abstract

Detection of hypoperfused tissue due to the ischemia is considered to be important in understanding the cerebral perfusion status and may be helpful in guiding therapeutic decisions for patients with transient ischemic attack (TIA). We hypothesized that the combination of two non-invasive fMRI techniques: resting-state BOLD-fMRI time-shift analysis (TSA) approach and 3D ASL, could detect the cerebral hemodynamic status in TIA patients noninvasively. From April 2015 to June 2016, 51 TIA patients were recruited in this study. We calculated the time delay between the resting-state BOLD signal at each voxel and the whole-brain signal using TSA approach and compared the results to CBF map derived from ASL. Out of the 51 patients, 24 patients with normal arrival time and CBF were in Stage 0; 14 patients who showed delayed arrival time and normal CBF which indicated elevated CBV were in Stage I; the other 13 patients who had both delayed arrival time and decreased CBF were in Stage II, the group average spatial overlap, i.e., Dice coefficient, of the two measurements was 0.55. Four patients in Stage 0 (17.4%), three patients in Stage I (23.1%) and five patients in Stage II (45.5%) suffered ischemic stroke or TIA symptoms in 1 year after MRI scan. The patients in Stage II was at highest risk of subsequent events when compared to other two stages. The combination of resting-state BOLD-fMRI and ASL hold the potential to noninvasively identify the hemodynamic status in TIA patients and help predict the risk of subsequent events.

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References

  1. Easton JD, Saver JL, Albers GW, Alberts MJ, Chaturvedi S, Feldmann E, Hatsukami TS, Higashida RT, Johnston SC, Kidwell CS, Lutsep HL, Miller E, Sacco RL (2009) Definition and evaluation of transient ischemic attack: a scientific statement for healthcare professionals from the American Heart Association/American Stroke Association Stroke Council; Council on Cardiovascular Surgery and Anesthesia; Council on Cardiovascular Radiology and Intervention; Council on Cardiovascular Nursing; and the Interdisciplinary Council on Peripheral Vascular Disease. The American Academy of Neurology affirms the value of this statement as an educational tool for neurologists. Stroke 40:2276–2293. https://doi.org/10.1161/STROKEAHA.108.192218

    Article  PubMed  Google Scholar 

  2. Giles MF, Rothwell PM (2007) Risk of stroke early after transient ischaemic attack: a systematic review and meta-analysis. Lancet Neurol 6(12):1063–1072. https://doi.org/10.1016/S1474-4422(07)70274-0

    Article  PubMed  Google Scholar 

  3. Johnston SC, Rothwell PM, Nguyen-Huynh MN, Giles MF, Elkins JS, Bernstein AL, Sidney S (2007) Validation and refinement of scores to predict very early stroke risk after transient ischaemic attack. Lancet 369:283–292. https://doi.org/10.1016/S0140-6736(07)60150-0

    Article  PubMed  Google Scholar 

  4. Ay H, Oliveira-Filho J, Buonanno FS, Schaefer PW, Furie KL, Chang YC, Rordorf G, Schwamm LH, Gonzalez RG, Koroshetz WJ (2002) ‘Footprints’ of transient ischemic attacks: a diffusion-weighted MRI study. Cerebrovasc Dis 14:177–186. https://doi.org/10.1159/000065682

    Article  PubMed  Google Scholar 

  5. Giles MF, Albers GW, Amarenco P, Arsava EM, Asimos AW, Ay H, Calvet D, Coutts SB, Cucchiara BL, Demchuk AM, Johnston SC, Kelly PJ, Kim AS, Labreuche J, Lavallee PC, Mas JL, Merwick A, Olivot JM, Purroy F, Rosamond WD, Sciolla R, Rothwell PM (2011) Early stroke risk and ABCD2 score performance in tissue- vs time-defined TIA: a multicenter study. Neurology 77:1222–1228. https://doi.org/10.1212/WNL.0b013e3182309f91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Ay H, Arsava EM, Johnston SC, Vangel M, Schwamm LH, Furie KL, Koroshetz WJ, Sorensen AG (2009) Clinical- and imaging-based prediction of stroke risk after transient ischemic attack: the CIP model. Stroke 40:181–186. https://doi.org/10.1161/STROKEAHA.108.521476

    Article  PubMed  Google Scholar 

  7. Calvet D, Touze E, Oppenheim C, Turc G, Meder JF, Mas JL (2009) DWI lesions and TIA etiology improve the prediction of stroke after TIA. Stroke 40:187–192. https://doi.org/10.1161/STROKEAHA.108.515817

    Article  PubMed  Google Scholar 

  8. Coutts SB, Eliasziw M, Hill MD, Scott JN, Subramaniam S, Buchan AM, Demchuk AM (2008) An improved scoring system for identifying patients at high early risk of stroke and functional impairment after an acute transient ischemic attack or minor stroke. Int J Stroke 3:3–10. https://doi.org/10.1111/j.1747-4949.2008.00182.x

    Article  PubMed  Google Scholar 

  9. Giles MF, Albers GW, Amarenco P, Arsava MM, Asimos A, Ay H, Calvet D, Coutts SB, Cucchiara BL, Demchuk AM, Johnston SC, Kelly PJ, Kim AS, Labreuche J, Lavallee PC, Mas JL, Merwick A, Olivot JM, Purroy F, Rosamond WD, Sciolla R, Rothwell PM (2010) Addition of brain infarction to the ABCD2 Score (ABCD2I): a collaborative analysis of unpublished data on 4574 patients. Stroke 41:1907–1913. https://doi.org/10.1161/STROKEAHA.110.578971

    Article  PubMed  Google Scholar 

  10. Krol AL, Coutts SB, Simon JE, Hill MD, Sohn CH, Demchuk AM, Group VS (2005) Perfusion MRI abnormalities in speech or motor transient ischemic attack patients. Stroke 36:2487–2489. https://doi.org/10.1161/01.STR.0000185936.05516.fc

    Article  PubMed  Google Scholar 

  11. Menon BK, Demchuk AM (2011) Computed Tomography angiography in the assessment of patients with stroke/TIA. Neurohospitalist 1:187–199. https://doi.org/10.1177/1941874411418523

    Article  PubMed  PubMed Central  Google Scholar 

  12. Mlynash M, Olivot JM, Tong DC, Lansberg MG, Eyngorn I, Kemp S, Moseley ME, Albers GW (2009) Yield of combined perfusion and diffusion MR imaging in hemispheric TIA. Neurology 72:1127–1133. https://doi.org/10.1212/01.wnl.0000340983.00152.69

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Petersen ET, Zimine I, Ho YC, Golay X (2006) Non-invasive measurement of perfusion: a critical review of arterial spin labelling techniques. Br J Radiol 79:688–701. https://doi.org/10.1259/bjr/67705974

    Article  CAS  Google Scholar 

  14. Prabhakaran S, Patel SK, Samuels J, McClenathan B, Mohammad Y, Lee VH (2011) Perfusion computed tomography in transient ischemic attack. Arch Neurol 68:85–89. https://doi.org/10.1001/archneurol.2010.320

    Article  PubMed  Google Scholar 

  15. Restrepo L, Jacobs MA, Barker PB, Wityk RJ (2004) Assessment of transient ischemic attack with diffusion- and perfusion-weighted imaging. AJNR Am J Neuroradiol 25:1645–1652

    PubMed  Google Scholar 

  16. Tong T, Yao Z, Feng X (2011) Combined diffusion- and perfusion-weighted imaging: a new way for the assessment of hemispheric transient ischemic attack patients. Int J Dev Neurosci 29:63–69. https://doi.org/10.1016/j.ijdevneu.2010.09.002

    Article  PubMed  Google Scholar 

  17. Grubb RL Jr, Derdeyn CP, Fritsch SM, Carpenter DA, Yundt KD, Videen TO, Spitznagel EL, Powers WJ (1998) Importance of hemodynamic factors in the prognosis of symptomatic carotid occlusion. JAMA 280:1055–1060

    Article  PubMed  Google Scholar 

  18. Alsop DC, Detre JA (1996) Reduced transit-time sensitivity in noninvasive magnetic resonance imaging of human cerebral blood flow. J Cereb Blood Flow Metab 16:1236–1249. https://doi.org/10.1097/00004647-199611000-00019

    Article  CAS  PubMed  Google Scholar 

  19. Kleinman JT, Zaharchuk G, Mlynash M, Ogdie AA, Straka M, Lansberg MG, Schwartz NE, Kemp S, Bammer R, Albers GW, Olivot JM (2012) Automated perfusion imaging for the evaluation of transient ischemic attack. Stroke 43:1556–1560. https://doi.org/10.1161/STROKEAHA.111.644971

    Article  PubMed  PubMed Central  Google Scholar 

  20. MacIntosh BJ, Lindsay AC, Kylintireas I, Kuker W, Gunther M, Robson MD, Kennedy J, Choudhury RP, Jezzard P (2010) Multiple inflow pulsed arterial spin-labeling reveals delays in the arterial arrival time in minor stroke and transient ischemic attack. AJNR Am J Neuroradiol 31:1892–1894. https://doi.org/10.3174/ajnr.A2008

    Article  CAS  PubMed  Google Scholar 

  21. Qiao XJ, Salamon N, Wang DJ, He R, Linetsky M, Ellingson BM, Pope WB (2013) Perfusion deficits detected by arterial spin-labeling in patients with TIA with negative diffusion and vascular imaging. AJNR Am J Neuroradiol 34:2125–2130. https://doi.org/10.3174/ajnr.A3551

    Article  CAS  PubMed  Google Scholar 

  22. Zaharchuk G, Olivot JM, Fischbein NJ, Bammer R, Straka M, Kleinman JT, Albers GW (2012) Arterial spin labeling imaging findings in transient ischemic attack patients: comparison with diffusion- and bolus perfusion-weighted imaging. Cerebrovasc Dis 34:221–228. https://doi.org/10.1159/000339682

    Article  PubMed  Google Scholar 

  23. Derdeyn CP, Grubb RL, Powers WJ (1999) Cerebral hemodynamic impairment: methods of measurement and association with stroke risk. Neurology 53:251–259. https://doi.org/10.1212/WNL.53.2.251

    Article  CAS  PubMed  Google Scholar 

  24. Kroll H, Zaharchuk G, Christen T, Heit JJ, Iv M (2017) Resting-state BOLD MRI for perfusion and ischemia. Top Magn Reson Imaging 26:91–96. https://doi.org/10.1097/RMR.0000000000000119

    Article  PubMed  PubMed Central  Google Scholar 

  25. Khalil AA, Ostwaldt AC, Nierhaus T, Ganeshan R, Audebert HJ, Villringer K, Villringer A, Fiebach JB (2017) Relationship between changes in the temporal dynamics of the blood-oxygen-level-dependent signal and hypoperfusion in acute ischemic stroke. Stroke 48:925–931. https://doi.org/10.1161/STROKEAHA.116.015566

    Article  CAS  PubMed  Google Scholar 

  26. Lv Y, Margulies DS, Cameron Craddock R, Long X, Winter B, Gierhake D, Endres M, Villringer K, Fiebach J, Villringer A (2013) Identifying the perfusion deficit in acute stroke with resting-state functional magnetic resonance imaging. Ann Neurol 73:136–140. https://doi.org/10.1002/ana.23763

    Article  PubMed  Google Scholar 

  27. Ni L, Li J, Li W, Zhou F, Wang F, Schwarz CG, Liu R, Zhao H, Wu W, Zhang X, Li M, Yu H, Zhu B, Villringer A, Zang Y, Zhang B, Lv Y, Xu Y (2017) The value of resting-state functional MRI in subacute ischemic stroke: comparison with dynamic susceptibility contrast-enhanced perfusion MRI. Sci Rep 7:41586. https://doi.org/10.1038/srep41586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Amemiya S, Kunimatsu A, Saito N, Ohtomo K (2014) Cerebral hemodynamic impairment: assessment with resting-state functional MR imaging. Radiology 270:548–555. https://doi.org/10.1148/radiol.13130982

    Article  PubMed  Google Scholar 

  29. Schultz-Larsen K, Lomholt RK, Kreiner S (2007) Mini-mental status examination: a short form of MMSE was as accurate as the original MMSE in predicting dementia. J Clin Epidemiol 60:260–267. https://doi.org/10.1016/j.jclinepi.2006.06.008

    Article  PubMed  Google Scholar 

  30. Biswal B, Hudetz AG, Yetkin FZ, Haughton VM, Hyde JS (1997) Hypercapnia reversibly suppresses low-frequency fluctuations in the human motor cortex during rest using echo-planar MRI. J Cereb Blood Flow Metab 17:301–308. https://doi.org/10.1097/00004647-199703000-00007

    Article  CAS  PubMed  Google Scholar 

  31. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci USA 98:676–682. https://doi.org/10.1073/pnas.98.2.676

    Article  CAS  PubMed  Google Scholar 

  32. Villringer A, Dirnagl U (1995) Coupling of brain activity and cerebral blood flow: basis of functional neuroimaging. Cerebrovasc Brain Metab Rev 7:240–276

    CAS  PubMed  Google Scholar 

  33. Bonakdarpour B, Parrish TB, Thompson CK (2007) Hemodynamic response function in patients with stroke-induced aphasia: implications for fMRI data analysis. Neuroimage 36:322–331. https://doi.org/10.1016/j.neuroimage.2007.02.035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Rossini PM, Altamura C, Ferretti A, Vernieri F, Zappasodi F, Caulo M, Pizzella V, Del Gratta C, Romani GL, Tecchio F (2004) Does cerebrovascular disease affect the coupling between neuronal activity and local haemodynamics? Brain 127:99–110. https://doi.org/10.1093/brain/awh012

    Article  CAS  PubMed  Google Scholar 

  35. Jansen O, Schellinger P, Fiebach J, Hacke W, Sartor K (1999) Early recanalisation in acute ischaemic stroke saves tissue at risk defined by MRI. Lancet 353:2036–2037. https://doi.org/10.1016/S0140-6736(99)01146-0

    Article  CAS  PubMed  Google Scholar 

  36. Ji R, Schwamm LH, Pervez MA, Singhal AB (2013) Ischemic stroke and transient ischemic attack in young adults: risk factors, diagnostic yield, neuroimaging, and thrombolysis. JAMA Neurol 70:51–57. https://doi.org/10.1001/jamaneurol.2013.575

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank two professional radiologists (Ni Ling and Chen Qian) for helping delineate the data. We thank all the patients and volunteers for participating in this study. This work was supported by grants from National Key R&D Program of China (No. 2017YFC1310000), National Natural Science Foundation of China (No. 81771911, 81301210, 81271652, 81520108016, 31471084, 81661148045), Dr. Zang is partly supported by “Qian Jiang Distinguished Professor” program.

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Correspondence to Xiujie Han.

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This study was approved by the Ethics Committee of the Center for Cognition and Brain Disorders, Hangzhou Normal University. Written informed consent was obtained from each participant.

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Lv, Y., Wei, W., Song, Y. et al. Non-invasive evaluation of cerebral perfusion in patients with transient ischemic attack: an fMRI study. J Neurol 266, 157–164 (2019). https://doi.org/10.1007/s00415-018-9113-3

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  • DOI: https://doi.org/10.1007/s00415-018-9113-3

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