Skip to main content
SpringerLink
Log in

Blood flow and perfusion lateralization in border zone infarct using 4D flow and arterial spin labeling

  • Functional Neuroradiology
  • Published:
Neuroradiology Aims and scope Submit manuscript

Abstract

Purpose

Hemodynamics may play an important role in border zone infarct (BZI), but macroscopic and microscopic hemodynamics of BZI still remain unclear. This study aims to investigate arterial flow and tissue perfusion differences between BZI and non-BZI in patients with unilateral middle cerebral artery (MCA) territory infarcts.

Methods

Subacute ischemic stroke patients with unilateral infarcts at MCA territory were included. Imaging protocols included 4D flow, ASL (arterial spin labeling), and routine clinical brain MRI scan. A total of 56 patients (56.1 ± 11.9 years, 39 male) were included and divided as BZI (n = 26) and non-BZI (n = 30). BZI was further subdivided as cortical BZI (CBZI, n = 9), internal BZI (IBZI, n = 11), and mixed BZI (n = 6). Average blood flow (Flowavg), regional average cerebral blood flow (CBFavg) were compared between infarct and contralateral sides to test hemodynamic lateralization. Flow-index and CBF-index (infarct sides/contralateral sides) were compared between groups and subgroups.

Results

Flowavg and CBFavg showed significant lateralization in both BZI and non-BZI as well as CBZI and IBZI. Flow-index (0.51 ± 0.37 vs. 0.87 ± 0.36, p < 0.01) and CBF-index (0.70 ± 0.21 vs. 0.90 ± 0.19, p < 0.01) were significantly different between BZI and non-BZI but were not significantly different between CBZI and IBZI.

Conclusion

In summary, hemodynamic lateralization can occur in subacute stroke patients with BZI and non-BZI and the one that occurs in BZI tends to be more severe in view of arterial flow and tissue perfusion.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Availability of data and material

Data supporting the findings of this study are available from the corresponding author on reasonable request.

Code availability

Code supporting the findings of this study are available from the corresponding author on reasonable request.

References

  1. Tatu L, Moulin T, Bogousslavsky J, Duvernoy H (1998) Arterial territories of the human brain: ccerebral hemispheres. Neurology 50:1699–1708. https://doi.org/10.1212/wnl.50.6.1699

    Article  PubMed  CAS  Google Scholar 

  2. Lee DK, Kim JS, Kwon SU, Yoo SH, Kang DW (2005) Lesion patterns and stroke mechanism in atherosclerotic middle cerebral artery disease: early diffusion-weighted imaging study. Stroke 36:2583–2588. https://doi.org/10.1161/01.STR.0000189999.19948.14

    Article  PubMed  Google Scholar 

  3. Torvik A (1984) The pathogenesis of watershed infarcts in the brain. Stroke 15:221–223. https://doi.org/10.1161/01.STR.15.2.221

    Article  PubMed  CAS  Google Scholar 

  4. Yaghi S, Grory BM, Prabhakaran S, Yeatts SD, Cutting S, Jayaraman M, Sacchetti D, Furie K, Zaidat OO, Liebeskind DS, Khatri P (2019) Infarct pattern, perfusion mismatch thresholds, and recurrent cerebrovascular events in symptomatic intracranial stenosis. J Neuroimaging 29:640–644. https://doi.org/10.1111/jon.12630

    Article  PubMed  Google Scholar 

  5. Schaafsma JD, Silver FL, Kasner SE, Caplan LR, Rose-Finnell L, Charbel FT, Pandey DK, Amin-Hanjani S, for the VSG (2019) Infarct patterns in patients with atherosclerotic vertebrobasilar disease in relation to hemodynamics. Cerebrovasc Dis Extra 9:123–128. https://doi.org/10.1159/000503091

    Article  PubMed  PubMed Central  Google Scholar 

  6. Del Sette M, Eliasziw M, Streifler JY, Hachinski VC, Fox AJ, Barnett HJ (2000) Internal borderzone infarction: a marker for severe stenosis in patients with symptomatic internal carotid artery disease. For the North American Symptomatic Carotid Endarterectomy (NASCET) Group. Stroke 31:631–636. https://doi.org/10.1161/01.str.31.3.631

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  8. Chaves CJ, Silver B, Schlaug G, Dashe J, Caplan LR, Warach S (2000) Diffusion- and perfusion-weighted MRI patterns in borderzone infarcts. Stroke 31:1090–1096. https://doi.org/10.1161/01.str.31.5.1090

    Article  PubMed  CAS  Google Scholar 

  9. Bisschops RH, Klijn CJ, Kappelle LJ, van Huffelen AC, van der Grond J (2003) Association between impaired carbon dioxide reactivity and ischemic lesions in arterial border zone territories in patients with unilateral internal carotid artery occlusion. Arch Neurol 60:229–233. https://doi.org/10.1001/archneur.60.2.229

    Article  PubMed  Google Scholar 

  10. Markl M, Frydrychowicz A, Kozerke S, Hope M, Wieben O (2012) 4D flow MRI. J Magn Reson Imaging 36:1015–1036. https://doi.org/10.1002/jmri.23632

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  12. Song X, Zhao X, Liebeskind DS, Wang L, Xu W, Xu Y, Hou D, Zheng Z, Wu J (2020) Incremental value of plaque enhancement in predicting stroke recurrence in symptomatic intracranial atherosclerosis. Neuroradiology 62:1123–1131. https://doi.org/10.1007/s00234-020-02418-8

    Article  PubMed  Google Scholar 

  13. van Osch MJ, Teeuwisse WM, van Walderveen MA, Hendrikse J, Kies DA, van Buchem MA (2009) Can arterial spin labeling detect white matter perfusion signal? Magn Reson Med 62:165–173. https://doi.org/10.1002/mrm.22002

    Article  PubMed  Google Scholar 

  14. Mangla R, Kolar B, Almast J, Ekholm SE (2011) Border zone infarcts: pathophysiologic and imaging characteristics. Radiographics 31:1201–1214. https://doi.org/10.1148/rg.315105014

    Article  PubMed  Google Scholar 

  15. Yamauchi H, Nishii R, Higashi T, Kagawa S, Fukuyama H (2009) Hemodynamic compromise as a cause of internal border-zone infarction and cortical neuronal damage in atherosclerotic middle cerebral artery disease. Stroke 40:3730–3735. https://doi.org/10.1161/STROKEAHA.109.560011

    Article  PubMed  Google Scholar 

  16. Li Y, Chen H, He L, Cao X, Wang X, Chen S, Li R, Yuan C (2018) Hemodynamic assessments of venous pulsatile tinnitus using 4D-flow MRI. Neurology 91:e586–e593. https://doi.org/10.1212/WNL.0000000000005948

    Article  PubMed  Google Scholar 

  17. Amukotuwa S, Straka M, Aksoy D, Fischbein N, Desmond P, Albers G, Bammer R (2019) Cerebral blood flow predicts the infarct core: new insights from contemporaneous diffusion and perfusion imaging. Stroke 50:2783–2789. https://doi.org/10.1161/STROKEAHA.119.026640

    Article  PubMed  PubMed Central  Google Scholar 

  18. Bang OY, Lee PH, Heo KG, Joo US, Yoon SR, Kim SY (2005) Specific DWI lesion patterns predict prognosis after acute ischaemic stroke within the MCA territory. J Neurol Neurosurg Psychiatry 76:1222–1228. https://doi.org/10.1136/jnnp.2004.059998

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Mutsaerts HJ, Petr J, Vaclavu L, van Dalen JW, Robertson AD, Caan MW, Masellis M, Nederveen AJ, Richard E, MacIntosh BJ (2017) The spatial coefficient of variation in arterial spin labeling cerebral blood flow images. J Cereb Blood Flow Metab 37:3184–3192. https://doi.org/10.1177/0271678X16683690

    Article  PubMed  PubMed Central  Google Scholar 

  20. Ibaraki M, Nakamura K, Toyoshima H, Takahashi K, Matsubara K, Umetsu A, Pfeuffer J, Kuribayashi H, Kinoshita T (2019) Spatial coefficient of variation in pseudo-continuous arterial spin labeling cerebral blood flow images as a hemodynamic measure for cerebrovascular steno-occlusive disease: a comparative 15O positron emission tomography study. J Cereb Blood Flow Metab 39:173–181. https://doi.org/10.1177/0271678X18781667

    Article  PubMed  Google Scholar 

  21. ElSadek A, Gaber A, Afifi H, Farag S, Salaheldien N (2019) Microemboli versus hypoperfusion as an etiology of acute ischemic stroke in Egyptian patients with watershed zone infarction. Egypt J Neurol Psychiatr Neurosurg 55:2. https://doi.org/10.1186/s41983-018-0045-8

    Article  PubMed  PubMed Central  Google Scholar 

  22. van Gelderen P, de Zwart JA, Duyn JH (2008) Pittfalls of MRI measurement of white matter perfusion based on arterial spin labeling. Magn Reson Med 59:788–795. https://doi.org/10.1002/mrm.21515

    Article  PubMed  Google Scholar 

  23. Wong KS, Gao S, Chan YL, Hansberg T, Lam WW, Droste DW, Kay R, Ringelstein EB (2002) Mechanisms of acute cerebral infarctions in patients with middle cerebral artery stenosis: a diffusion-weighted imaging and microemboli monitoring study. Ann Neurol 52:74–81. https://doi.org/10.1002/ana.10250

    Article  PubMed  Google Scholar 

  24. Mutsaerts H, Petr J, Bokkers RPH, Lazar RM, Marshall RS, Asllani I (2020) Spatial coefficient of variation of arterial spin labeling MRI as a cerebrovascular correlate of carotid occlusive disease. PLoS ONE 15:e0229444. https://doi.org/10.1371/journal.pone.0229444

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Funding

This study is supported by the Beijing Municipal Science & Technology Commission (Z171100001017019), Tsinghua University initiative scientific research program (20219990033).

Author information

Author notes

  1. Wenwen Chen and Xiaowei Song equally contributed to this work.

Authors and Affiliations

  1. Center for Biomedical Imaging Research, Department of Biomedical Engineering, School of Medicine, Tsinghua University, Beijing, China

    Wenwen Chen, Shuo Chen, Mingzhu Fu & Rui Li

  2. Department of Neurology, Beijing Tsinghua Changgung Hospital, Beijing, 102218, China

    Xiaowei Song, Chenming Wei & Jian Wu

  3. Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China

    Zhensen Chen

  4. Department of Radiology, Beijing Tsinghua Changgung Hospital, Beijing, 102218, China

    Zhuozhao Zheng

Authors
  1. Wenwen Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaowei Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shuo Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhensen Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mingzhu Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chenming Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhuozhao Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jian Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Rui Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Wenwen Chen: study design, data acquisition, data analysis, interpretation of the results, article writing; Xiaowei Song: study design, data acquisition, interpretation of the results, article editing; Zhensen Chen: data analysis, interpretation of the results, article editing; Shuo Chen: study design, interpretation of the results, article editing; Mingzhu Fu: data analysis, proofreading; Chenming Wei: interpretation of the results, proofreading; Zhuozhao Zheng: data acquisition, interpretation of the results; Jian Wu: data acquisition, interpretation of the results, article editing; Rui Li: study design, study supervision, interpretation of the results, article editing.

Corresponding authors

Correspondence to Jian Wu or Rui Li.

Ethics declarations

Ethics approval

The Ethical Review Board of the Beijing Changguang Hospital approved the study, and it was performed in accordance with the guidelines of the Declaration of Helsinki.

Consent to participate

Informed consent from participants was obtained from each patient or their family members.

Consent for publication

Patients signed informed consent regarding publishing their data and photographs.

Conflict of interest

The authors declare that there is no conflict of interest.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 16 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, W., Song, X., Chen, S. et al. Blood flow and perfusion lateralization in border zone infarct using 4D flow and arterial spin labeling. Neuroradiology 64, 2145–2152 (2022). https://doi.org/10.1007/s00234-022-02967-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00234-022-02967-0

Keywords

Search

Navigation