Skip to main content
SpringerLink
Log in

Hemodynamic Evaluation of Paradoxical Blood Oxygenation Level-Dependent Cerebrovascular Reactivity with Transcranial Doppler and MR Perfusion in Patients with Symptomatic Cerebrovascular Steno-occlusive Disease

  • Protocol
  • First Online:
Cerebrovascular Reactivity

Part of the book series: Neuromethods ((NM,volume 175))

  • 463 Accesses

Abstract

Background and Purpose: In patients with steno-occlusive disease, paradoxical blood oxygenation level-dependent fMRI cerebrovascular reactivity (BOLD-CVR) is a feasible surrogate marker for hemodynamic impairment. BOLD-CVR, however, does not measure hemodynamic changes directly; hence, we study complementary hemodynamic features in brain areas exhibiting paradoxical BOLD-CVR using perfusion-weighted MRI (PW-MRI) and transcranial Doppler (TCD).

Methods: Twenty participants with unilateral symptomatic chronic cerebrovascular steno-occlusive disease and ipsilateral paradoxical BOLD-CVR were studied. The region with paradoxical BOLD-CVR was used as a region of interest for the PW-MRI-weighted images. As a comparison, a contralateral analysis was done. Ipsilateral and contralateral TCD flow velocities of the posterior circulation were compared as an indicator of collateral supply.

Results: Brain tissue exhibiting paradoxical BOLD-CVR showed prolonged mean transit time and time-to-peak with increased cerebral blood volume. CBF followed a post-stroke time evolution. The ipsilateral posterior cerebral artery (PCA)-P2 segment flow velocity was significantly increased compared to the contralateral side, correlating strongly with the paradoxical BOLD-CVR brain tissue volume.

Conclusions: In symptomatic steno-occlusive patients, brain areas with ipsilateral paradoxical BOLD-CVR show clear hemodynamic changes, i.e., prolonged mean transit time and time-to-peak and increased cerebral blood volume. Moreover, increased flow velocities in the ipsilateral PCA-P2 segment indicate increased hemodynamic efforts due to increased need for collateral supply from the posterior circulation. This further supports the premise that paradoxical BOLD-CVR within the symptomatic hemisphere is a reliable surrogate for exhausted perfusion reserve and should be studied in an independent study cohort to determine its value for predicting stroke risk.

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

Access this chapter

Log in via an institution
Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 109.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 139.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Esposito G, Amin-Hanjani S, Regli L (2016) Role of and indications for bypass surgery after carotid occlusion surgery study (coss)? Stroke 47:282–290

    Article  Google Scholar 

  2. Fierstra J, van Niftrik C, Warnock G, Wegener S, Piccirelli M, Pangalu A et al (2018) Staging hemodynamic failure with blood oxygen-level–dependent functional magnetic resonance imaging cerebrovascular reactivity. Stroke 49:621

    Article  Google Scholar 

  3. Derdeyn CP, Grubb RL Jr, Powers WJ (1999) Cerebral hemodynamic impairment: methods of measurement and association with stroke risk. Neurology 53:251–259

    Article  CAS  Google Scholar 

  4. Powers WJ, Press GA, Grubb RL Jr, Gado M, Raichle ME (1987) The effect of hemodynamically significant carotid artery disease on the hemodynamic status of the cerebral circulation. Ann Intern Med 106:27–34

    Article  CAS  Google Scholar 

  5. Powers WJ (2008) Imaging preventable infarction in patients with acute ischemic stroke. AJNR. Am J Neuroradiol 29:1823–1825

    Article  CAS  Google Scholar 

  6. Derdeyn CP, Videen TO, Fritsch SM, Carpenter DA, Grubb RL Jr, Powers WJ (1999) Compensatory mechanisms for chronic cerebral hypoperfusion in patients with carotid occlusion. Stroke 30:1019–1024

    Article  CAS  Google Scholar 

  7. Derdeyn CP, Shaibani A, Moran CJ, Cross DT III, Grubb RL Jr, Powers WJ (1999) Lack of correlation between pattern of collateralization and misery perfusion in patients with carotid occlusion. Stroke 30:1025–1032

    Article  CAS  Google Scholar 

  8. Schneider J, Sick B, Luft AR, Wegener S (2015) Ultrasound and clinical predictors of recurrent ischemia in symptomatic internal carotid artery occlusion. Stroke 46:3274–3276

    Article  Google Scholar 

  9. Sobczyk O, Battisti-Charbonney A, Fierstra J, Mandell DM, Poublanc J, Crawley AP et al (2014) A conceptual model for co(2)-induced redistribution of cerebral blood flow with experimental confirmation using bold mri. NeuroImage 92:56–68

    Article  CAS  Google Scholar 

  10. Arteaga DF, Strother MK, Faraco CC, Jordan LC, Ladner TR, Dethrage LM et al (2014) The vascular steal phenomenon is an incomplete contributor to negative cerebrovascular reactivity in patients with symptomatic intracranial stenosis. J Cereb Blood Flow Metab 34:1453–1462

    Article  CAS  Google Scholar 

  11. Slessarev M, Han J, Mardimae A, Prisman E, Preiss D, Volgyesi G et al (2007) Prospective targeting and control of end-tidal co2 and o2 concentrations. J Physiol 581:1207–1219

    Article  CAS  Google Scholar 

  12. van Niftrik CHB, Piccirelli M, Bozinov O, Maldaner N, Strittmatter C, Pangalu A et al (2018) Impact of baseline co2 on blood-oxygenation-level-dependent mri measurements of cerebrovascular reactivity and task-evoked signal activation. Magn Reson Imaging 49:123

    Article  Google Scholar 

  13. van Niftrik CHB, Piccirelli M, Bozinov O, Pangalu A, Fisher JA, Valavanis A et al (2017) Iterative analysis of cerebrovascular reactivity dynamic response by temporal decomposition. Brain Behav 7:e00705

    Article  Google Scholar 

  14. Sebok M, van Niftrik CHB, Piccirelli M, Bozinov O, Wegener S, Esposito G et al (2018) Bold cerebrovascular reactivity as a novel marker for crossed cerebellar diaschisis. Neurology 91:e1328

    Article  Google Scholar 

  15. van Niftrik CHB, Sebok M, Muscas G, Piccirelli M, Serra C, Krayenbuhl N et al (2020) Characterizing ipsilateral thalamic diaschisis in symptomatic cerebrovascular steno-occlusive patients. J Cereb Blood Flow Metab 40:563

    Article  Google Scholar 

  16. Sobczyk O, Crawley AP, Poublanc J, Sam K, Mandell DM, Mikulis DJ et al (2016) Identifying significant changes in cerebrovascular reactivity to carbon dioxide. AJNR Am J Neuroradiol 37:818–824

    Article  CAS  Google Scholar 

  17. Powers WJ, Zazulia AR (2010) Pet in cerebrovascular disease. PET Clin 5:83106

    Article  Google Scholar 

  18. Derdeyn CP, Videen TO, Yundt KD, Fritsch SM, Carpenter DA, Grubb RL et al (2002) Variability of cerebral blood volume and oxygen extraction: stages of cerebral haemodynamic impairment revisited. Brain 125:595–607

    Article  Google Scholar 

  19. Rapela CE, Green HD (1964) Autoregulation of canine cerebral blood flow. Circ Res 15(Suppl):205–212

    CAS  Google Scholar 

  20. Hill MA, Davis MJ, Meininger GA, Potocnik SJ, Murphy TV (2006) Arteriolar myogenic signalling mechanisms: implications for local vascular function. Clin Hemorheol Microcirc 34:67–79

    PubMed  Google Scholar 

  21. Lucas SJ, Tzeng YC, Galvin SD, Thomas KN, Ogoh S, Ainslie PN (2010) Influence of changes in blood pressure on cerebral perfusion and oxygenation. Hypertension 55:698–705

    Article  CAS  Google Scholar 

  22. Yonas H, Smith HA, Durham SR, Pentheny SL, Johnson DW (1993) Increased stroke risk predicted by compromised cerebral blood flow reactivity. J Neurosurg 79:483–489

    Article  CAS  Google Scholar 

  23. Fisher JA, Venkatraghavan L, Mikulis DJ (2018) Magnetic resonance imaging-based cerebrovascular reactivity and hemodynamic reserve: a review of method optimization and data interpretation. Stroke 49:2011

    Article  Google Scholar 

  24. Webster MW, Makaroun MS, Steed DL, Smith HA, Johnson DW, Yonas H (1995) Compromised cerebral blood flow reactivity is a predictor of stroke in patients with symptomatic carotid artery occlusive disease. J Vasc Surg 21:338–344. discussion 344–335

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  26. Derdeyn CP, Powers WJ, Grubb RL Jr (1998) Hemodynamic effects of middle cerebral artery stenosis and occlusion. AJNR Am J Neuroradiol 19:1463–1469

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Kuhn FP, Warnock G, Schweingruber T, Sommerauer M, Buck A, Khan N (2015) Quantitative h[o]-pet in pediatric moyamoya disease: evaluating perfusion before and after cerebral revascularization. J Stroke Cerebrovasc Dis 24:965–971

    Article  Google Scholar 

  28. Derdeyn CP, Yundt KD, Videen TO, Carpenter DA, Grubb RL Jr, Powers WJ (1998) Increased oxygen extraction fraction is associated with prior ischemic events in patients with carotid occlusion. Stroke 29:754–758

    Article  CAS  Google Scholar 

  29. Mandell DM, Han JS, Poublanc J, Crawley AP, Stainsby JA, Fisher JA et al (2008) Mapping cerebrovascular reactivity using blood oxygen level-dependent MRI in patients with arterial steno-occlusive disease: comparison with arterial spin labeling MRI. Stroke 39:2021–2028

    Article  Google Scholar 

  30. Kassner A, Winter JD, Poublanc J, Mikulis DJ, Crawley AP (2010) Blood-oxygen level dependent mri measures of cerebrovascular reactivity using a controlled respiratory challenge: reproducibility and gender differences. J Magn Reson Imaging 31:298–304

    Article  Google Scholar 

  31. Heyn C, Poublanc J, Crawley A, Mandell D, Han JS, Tymianski M et al (2010) Quantification of cerebrovascular reactivity by blood oxygen level-dependent mr imaging and correlation with conventional angiography in patients with moyamoya disease. AJNR Am J Neuroradiol 31:862–867

    Article  CAS  Google Scholar 

  32. Watchmaker JM, Frederick BD, Fusco MR, Davis LT, Juttukonda MR (2018) Lants SK, et al. Clinical use of cerebrovascular compliance imaging to evaluate revascularization in patients with moyamoya. Neurosurgery 84:261

    Article  Google Scholar 

  33. Hauser TK, Seeger A, Bender B, Klose U, Thurow J, Ernemann U et al (2019) Hypercapnic bold mri compared to h2(15)o pet/ct for the hemodynamic evaluation of patients with moyamoya disease. NeuroImage Clin 22:101713

    Article  Google Scholar 

  34. Davis TL, Kwong KK, Weisskoff RM, Rosen BR (1998) Calibrated functional MRI: mapping the dynamics of oxidative metabolism. Proc Natl Acad Sci U S A 95:1834–1839

    Article  CAS  Google Scholar 

  35. Bright MG, Croal PL, Blockley NP, Bulte DP (2019) Multiparametric measurement of cerebral physiology using calibrated fmri. NeuroImage 187:128–144

    Article  Google Scholar 

  36. Sebök M, Van Niftrik B, Piccirelli M, Bozinov O, Wegener S, Esposito G et al (2018) Bold cerebrovascular reactivity as a novel marker for crossed cerebellar diaschisis. Neurology 91:1–10

    Article  Google Scholar 

  37. Jussen D, Zdunczyk A, Schmidt S, Rösler J, Buchert R, Julkunen P et al (2016) Motor plasticity after extra–intracranial bypass surgery in occlusive cerebrovascular disease. Neurology 87(1):27–35

    Article  Google Scholar 

  38. Jiang TT, Videen TO, Grubb RL Jr, Powers WJ, Derdeyn CP (2010) Cerebellum as the normal reference for the detection of increased cerebral oxygen extraction. J Cereb Blood Flow Metab 30:1767–1776

    Article  CAS  Google Scholar 

  39. Goetti R, Warnock G, Kuhn FP, Guggenberger R, O’Gorman R, Buck A et al (2014) Quantitative cerebral perfusion imaging in children and young adults with moyamoya disease: comparison of arterial spin-labeling-mri and h(2)[(15)o]-pet. AJNR Am J Neuroradiol 35:1022–1028

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Forschungskredit, Postdoc Initiative 2016, from the University of Zurich (FK-16–040) and the Swiss Cancer League (KFS-3975-08-2016-R), both allocated to Dr. Jorn Fierstra.

Author information

Authors and Affiliations

  1. Department of Neurosurgery, University Hospital Zurich, University of Zurich, Zurich, Switzerland

    Christiaan Hendrik Bas van Niftrik, Martina Sebök, Giovanni Muscas, Aimée Hiller, Matthias Halter, Luca Regli & Jorn Fierstra

  2. Clinical Neuroscience Center, University Hospital Zurich, University of Zurich, Zurich, Switzerland

    Christiaan Hendrik Bas van Niftrik, Martina Sebök, Giovanni Muscas, Aimée Hiller, Matthias Halter, Susanne Wegener, Luca Regli & Jorn Fierstra

  3. Department of Neurosurgery, Careggi University Hospital, University of Florence, Florence, Italy

    Giovanni Muscas

  4. Department of Neurology, University Hospital Zurich, University of Zurich, Zurich, Switzerland

    Susanne Wegener

Authors
  1. Christiaan Hendrik Bas van Niftrik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Martina Sebök
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Giovanni Muscas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Aimée Hiller
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Matthias Halter
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Susanne Wegener
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Luca Regli
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jorn Fierstra
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christiaan Hendrik Bas van Niftrik .

Editor information

Editors and Affiliations

  1. Baycrest Centre for Geriatric Care, University of Toronto, Toronto, ON, Canada

    Jean Chen

  2. Department of Neurosurgery, University Hospital Zurich, Zürich, Zürich, Switzerland

    Jorn Fierstra

Rights and permissions

Reprints and permissions

Copyright information

© 2022 Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

van Niftrik, C.H.B. et al. (2022). Hemodynamic Evaluation of Paradoxical Blood Oxygenation Level-Dependent Cerebrovascular Reactivity with Transcranial Doppler and MR Perfusion in Patients with Symptomatic Cerebrovascular Steno-occlusive Disease. In: Chen, J., Fierstra, J. (eds) Cerebrovascular Reactivity. Neuromethods, vol 175. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-1763-2_6

Download citation

  • DOI: https://doi.org/10.1007/978-1-0716-1763-2_6

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-0716-1762-5

  • Online ISBN: 978-1-0716-1763-2

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation