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Optimized Combination of b‑values for IVIM Perfusion Imaging in Acute Ischemic Stroke Patients

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Abstract

Purpose

To determine the optimal combination of low b‑values to generate perfusion information from intravoxel incoherent motion (IVIM) in patients with acute ischemic stroke (AIS) considering the time constraints for these patients.

Methods

A retrospective cohort study of AIS patients with IVIM MRI was performed. A two-step voxel-by-voxel postprocessing was used to derive IVIM perfusion fraction maps with different combinations of b values. Signal values within regions of ischemic core, non-infarcted ischemic hemisphere, and contralateral hemisphere were measured on IVIM (f, D*, fD*, D) parameter maps. Bland-Altman analysis and the Dice similarity coefficient were used to determine quantitative and spatial agreements between the reference standard IVIM (IVIM with 6 b values of 0, 50, 100, 150, 200, 1000 s/mm2) and other combinations of b values. Significance level was set at p < 0.05.

Results

There were 58 patients (36 males, 61.3%; mean age 70.2 ± 13.4 years) included. Considering all IVIM parameters, the combination of b values of 0, 50, 200, 1000 was the most consistent with our reference standard on Bland-Altman analysis. The best voxel-based overlaps of ischemic regions were on IVIM D, while there were good voxel-based overlaps on IVIM f.

Conclusion

The IVIM with these four b values collects diffusion and perfusion information from a single short MRI sequence, which may have important implications for the imaging of AIS patients.

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Abbreviations

ADC:

Apparent diffusion coefficient

AIS:

Acute ischemic stroke

ANOVA:

Analysis of variance

CBF:

Cerebral blood flow

CBV:

Cerebral blood volume

CTA:

Computed tomography angiography

D:

Molecular diffusion coefficient

D* :

Pseudodiffusion coefficient

DWI:

Diffusion-weighted imaging

f:

Flowing blood volume fraction

FLAIR:

Fluid-attenuated inversion recovery

GRE:

Gradient echo

IVIM:

Intravoxel incoherent motion

LVO:

Large vessel occlusion

MRA:

Magnetic resonance angiography

MRI:

Magnetic resonance imaging

MTT:

Mean transit time

NIHSS:

National Institutes of Health Stroke Scale

PWI:

Perfusion-weighted imaging

ROI:

Regions of interest

Tmax:

Time-to-Maximum

References

  1. Rydhög AS, Szczepankiewicz F, Wirestam R, Ahlgren A, Westin CF, Knutsson L, Pasternak O. Separating blood and water: perfusion and free water elimination from diffusion MRI in the human brain. Neuroimage. 2016;156:423–34.

    Article  Google Scholar 

  2. Gao QQ, Lu SS, Xu XQ, Wu CJ, Liu XL, Liu S, Shi HB. Quantitative assessment of hyperacute cerebral infarction with intravoxel incoherent motion MR imaging: initial experience in a canine stroke model. J Magn Reson Imaging. 2017;46:550–6.

    Article  Google Scholar 

  3. Hu LB, Hong N, Zhu WZ. Quantitative measurement of cerebral perfusion with Intravoxel incoherent motion in acute Ischemia stroke: initial clinical experience. Chin Med J (Engl). 2015;128:2565–9.

    Article  Google Scholar 

  4. Suo S, Cao M, Zhu W, Li L, Li J, Shen F, Zu J, Zhou Z, Zhuang Z, Qu J, Chen Z, Xu J. Stroke assessment with intravoxel incoherent motion diffusion-weighted MRI. NMR Biomed. 2016;29:320–8.

    Article  Google Scholar 

  5. Federau C, Sumer S, Becce F, Maeder P, O’Brien K, Meuli R, Wintermark M. Intravoxel incoherent motion perfusion imaging in acute stroke: Initial clinical experience. Neuroradiology. 2014;56:629–35.

    Article  CAS  Google Scholar 

  6. Federau C, O’Brien K, Meuli R, Hagmann P, Maeder P. Measuring brain perfusion with intravoxel incoherent motion (IVIM): initial clinical experience. J Magn Reson Imaging. 2014;39:624–32.

    Article  Google Scholar 

  7. Iima M, Le Bihan D. Clinical Intravoxel incoherent motion and diffusion MR imaging: past, present, and future. Radiology. 2016;278:13–32.

    Article  Google Scholar 

  8. Lemke A, Stieltjes B, Schad LR, Laun FB. Toward an optimal distribution of b values for intravoxel incoherent motion imaging. Magn Reson Imaging. 2011;29:766–76.

    Article  Google Scholar 

  9. Federau C, Maeder P, O’Brien K, Browaeys P, Meuli R, Hagmann P. Quantitative measurement of brain perfusion with intravoxel incoherent motion MR imaging. Radiology. 2012;265:874–81.

    Article  Google Scholar 

  10. Straka M, Albers GW, Bammer R. Real-time diffusion-perfusion mismatch analysis in acute stroke. J Magn Reson Imaging. 2010;32:1024–37.

    Article  Google Scholar 

  11. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9:671–5.

    Article  CAS  Google Scholar 

  12. Keil VC, Mädler B, Gielen GH, Pintea B, Hiththetiya K, Gaspranova AR, Gieseke J, Simon M, Schild HH, Hadizadeh DR. Intravoxel incoherent motion MRI in the brain: Impact of the fitting model on perfusion fraction and lesion differentiability. J Magn Reson Imaging. 2017;46:1187–99.

    Article  Google Scholar 

  13. Heit JJ, Wintermark M. Imaging selection for reperfusion therapy in acute Ischemic stroke. Curr Treat Options Neurol. 2015;17:332.

    PubMed  Google Scholar 

  14. Albers GW, Marks MP, Kemp S, Christensen S, Tsai JP, Ortega-Gutierrez S, McTaggart RA, Torbey MT, Kim-Tenser M, Leslie-Mazwi T, Sarraj A, Kasner SE, Ansari SA, Yeatts SD, Hamilton S, Mlynash M, Heit JJ, Zaharchuk G, Kim S, Carrozzella J, Palesch YY, Demchuk AM, Bammer R, Lavori PW, Broderick JP, Lansberg MG; DEFUSE 3 Investigators. Thrombectomy for stroke at 6 to 16 hours with selection by perfusion imaging. N Engl J Med. 2018;378:708–18.

    Article  Google Scholar 

  15. Berkhemer OA, Fransen PS, Beumer D, van den Berg LA, Lingsma HF, Yoo AJ, Schonewille WJ, Vos JA, Nederkoorn PJ, Wermer MJ, van Walderveen MA, Staals J, Hofmeijer J, van Oostayen JA, Lycklama à Nijeholt GJ, Boiten J, Brouwer PA, Emmer BJ, de Bruijn SF, van Dijk LC, Kappelle LJ, Lo RH, van Dijk EJ, de Vries J, de Kort PL, van Rooij WJ, van den Berg JS, van Hasselt BA, Aerden LA, Dallinga RJ, Visser MC, Bot JC, Vroomen PC, Eshghi O, Schreuder TH, Heijboer RJ, Keizer K, Tielbeek AV, den Hertog HM, Gerrits DG, van den Berg-Vos RM, Karas GB, Steyerberg EW, Flach HZ, Marquering HA, Sprengers ME, Jenniskens SF, Beenen LF, van den Berg R, Koudstaal PJ, van Zwam WH, Roos YB, van der Lugt A, van Oostenbrugge RJ, Majoie CB, Dippel DW; MR CLEAN Investigators. A randomized trial of Intraarterial treatment for acute Ischemic stroke. N Engl J Med. 2015;372:11–20.

    Article  Google Scholar 

  16. Campbell BC, Mitchell PJ, Kleinig TJ, Dewey HM, Churilov L, Yassi N, Yan B, Dowling RJ, Parsons MW, Oxley TJ, Wu TY, Brooks M, Simpson MA, Miteff F, Levi CR, Krause M, Harrington TJ, Faulder KC, Steinfort BS, Priglinger M, Ang T, Scroop R, Barber PA, McGuinness B, Wijeratne T, Phan TG, Chong W, Chandra RV, Bladin CF, Badve M, Rice H, de Villiers L, Ma H, Desmond PM, Donnan GA, Davis SM; EXTEND-IA Investigators. Endovascular therapy for Ischemic stroke with perfusion-imaging selection. N Engl J Med. 2015;372:1009–18.

    Article  CAS  Google Scholar 

  17. Jovin TG, Chamorro A, Cobo E, de Miquel MA, Molina CA, Rovira A, San Román L, Serena J, Abilleira S, Ribó M, Millán M, Urra X, Cardona P, López-Cancio E, Tomasello A, Castaño C, Blasco J, Aja L, Dorado L, Quesada H, Rubiera M, Hernandez-Pérez M, Goyal M, Demchuk AM, von Kummer R, Gallofré M, Dávalos A; REVASCAT Trial Investigators. Thrombectomy within 8 hours after symptom onset in Ischemic stroke. N Engl J Med. 2015;372:2296–306.

    Article  CAS  Google Scholar 

  18. Goyal M, Demchuk AM, Menon BK, Eesa M, Rempel JL, Thornton J, Roy D, Jovin TG, Willinsky RA, Sapkota BL, Dowlatshahi D, Frei DF, Kamal NR, Montanera WJ, Poppe AY, Ryckborst KJ, Silver FL, Shuaib A, Tampieri D, Williams D, Bang OY, Baxter BW, Burns PA, Choe H, Heo JH, Holmstedt CA, Jankowitz B, Kelly M, Linares G, Mandzia JL, Shankar J, Sohn SI, Swartz RH, Barber PA, Coutts SB, Smith EE, Morrish WF, Weill A, Subramaniam S, Mitha AP, Wong JH, Lowerison MW, Sajobi TT, Hill MD; ESCAPE Trial Investigators. Randomized assessment of rapid Endovascular treatment of Ischemic stroke. N Engl J Med. 2015;372:1019–30.

    Article  CAS  Google Scholar 

  19. Nogueira RG, Jadhav AP, Haussen DC, Bonafe A, Budzik RF, Bhuva P, Yavagal DR, Ribo M, Cognard C, Hanel RA, Sila CA, Hassan AE, Millan M, Levy EI, Mitchell P, Chen M, English JD, Shah QA, Silver FL, Pereira VM, Mehta BP, Baxter BW, Abraham MG, Cardona P, Veznedaroglu E, Hellinger FR, Feng L, Kirmani JF, Lopes DK, Jankowitz BT, Frankel MR, Costalat V, Vora NA, Yoo AJ, Malik AM, Furlan AJ, Rubiera M, Aghaebrahim A, Olivot JM, Tekle WG, Shields R, Graves T, Lewis RJ, Smith WS, Liebeskind DS, Saver JL, Jovin TG; DAWN Trial Investigators. Thrombectomy 6 to 24 hours after stroke with a mismatch between deficit and infarct. N Engl J Med. 2018;378:11–21.

    Article  Google Scholar 

  20. Saver JL, Goyal M, Bonafe A, Diener HC, Levy EI, Pereira VM, Albers GW, Cognard C, Cohen DJ, Hacke W, Jansen O, Jovin TG, Mattle HP, Nogueira RG, Siddiqui AH, Yavagal DR, Baxter BW, Devlin TG, Lopes DK, Reddy VK, du Mesnil de Rochemont R, Singer OC, Jahan R; SWIFT PRIME Investigators. Stent-retriever Thrombectomy after intravenous t‑PA vs. t‑PA alone in stroke. N Engl J Med. 2015;372:2285–95.

    Article  CAS  Google Scholar 

  21. Saver JL, Goyal M, van der Lugt A, Menon BK, Majoie CB, Dippel DW, Campbell BC, Nogueira RG, Demchuk AM, Tomasello A, Cardona P, Devlin TG, Frei DF, du Mesnil de Rochemont R, Berkhemer OA, Jovin TG, Siddiqui AH, van Zwam WH, Davis SM, Castaño C, Sapkota BL, Fransen PS, Molina C, van Oostenbrugge RJ, Chamorro Á, Lingsma H, Silver FL, Donnan GA, Shuaib A, Brown S, Stouch B, Mitchell PJ, Davalos A, Roos YB, Hill MD; HERMES Collaborators. Time to treatment with endovascular thrombectomy and outcomes from ischemic stroke: Ameta-analysis. JAMA. 2016;316:1279–88.

    Article  Google Scholar 

  22. Zhu G, Federau C, Wintermark M, Marcellus DG, Martin BW, Heit JJ. Comparison of MRI IVIM and MR perfusion imaging in acute ischemic stroke due to large vessel occlusion. Int J Stroke. 2019. Accepted.

  23. Le Bihan D. What can we see with IVIM MRI? Neuroimage. 2018;187:56–67.

    Article  Google Scholar 

  24. Le Bihan D. Diffusion, confusion and functional MRI. Neuroimage. 2012;62:1131–6.

    Article  Google Scholar 

  25. Meeus EM, Novak J, Dehghani H, Peet AC. Rapid measurement of intravoxel incoherent motion (IVIM) derived perfusion fraction for clinical magnetic resonance imaging. MAGMA. 2018;31:269–83.

    Article  Google Scholar 

  26. Conklin XJ, Heyn XC, Roux XM, Cerny XM, Wintermark XM, Federau XC. Validation of a simplified model for Intravoxel Incoherent Motion Perfusion Imaging of the brain. AJNR Am J Neuroradiol. 2016;37:2251–7.

    Article  CAS  Google Scholar 

  27. Fournet G, Li JR, Cerjanic AM, Sutton BP, Ciobanu L, Le Bihan D. A two-pool model to describe the IVIM cerebral perfusion. J Cereb Blood Flow Metab. 2017;37:2987–3000.

    Article  Google Scholar 

  28. Heit JJ, Wintermark M, Martin BW, Zhu G, Marks MP, Zaharchuk G, Dodd RL, Do HM, Steinberg GK, Lansberg MG, Albers GW, Federau C. Reduced intravoxel incoherent motion microvascular perfusion predicts delayed cerebral ischemia and vasospasm after aneurysm rupture. Stroke. 2018;49:741–5.

    Article  Google Scholar 

  29. Pavilla A, Arrigo A, Mejdoubi M, Duvauferrier R, Gambarota G, Saint-Jalmes H. Measuring cerebral Hypoperfusion induced by hyperventilation challenge with Intravoxel incoherent motion magnetic resonance imaging in healthy volunteers. J Comput Assist Tomogr. 2018;42:85–91.

    Article  Google Scholar 

  30. Nelander M, Hannsberger D, Sundström-Poromaa I, Bergman L, Weis J, Åkerud H, Wikström J, Wikström AK. Assessment of cerebral perfusion and edema in preeclampsia with intravoxel incoherent motion MRI. Acta Obstet Gynecol Scand. 2018;97:1212–8.

    Article  CAS  Google Scholar 

  31. Zhang CE, Wong SM, Uiterwijk R, Staals J, Backes WH, Hoff EI, Schreuder T, Jeukens CR, Jansen JF, van Oostenbrugge RJ. Intravoxel incoherent motion imaging in small vessel disease: microstructural integrity and Microvascular perfusion related to cognition. Stroke. 2017;48:658–63.

    Article  Google Scholar 

  32. Detsky JS, Keith J, Conklin J, Symons S, Myrehaug S,Sahgal A, Heyn CC, Soliman H. Differentiating radiation necrosis from tumor progression in brain metastases treated with stereotactic radiotherapy: utility of intravoxel incoherent motion perfusion MRI and correlation with histopathology. J Neurooncol. 2017;134(2):433–41.

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Radiology, Neuroradiology Section, Stanford Healthcare, 300 Pasteur Drive – S047, 94305, Stanford, CA, USA

    Guangming Zhu, Jeremy J. Heit, Blake W. Martin, David G. Marcellus & Max Wintermark

  2. Institute for Biomedical Engineering, ETH Zürich, Gloriastrasse 35, 8092, Zürich, Switzerland

    Christian Federau

  3. Department of Radiology, Diagnostic and Interventional Neuroradiology, University of Basel, Petersgraben, 4031, Basel, Switzerland

    Christian Federau

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  1. Guangming Zhu
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  2. Jeremy J. Heit
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  4. David G. Marcellus
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  5. Christian Federau
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Contributions

G. Zhu: drafting the article, analysis and interpretation; J. J. Heit: study conception and design, interpretation, revising the article; B. W. Martin: data acquisition and analysis; D. G. Marcellus: data acquisition and analysis; C. Federau: interpretation and revising the article; M. Wintermark: study conception and design, interpretation, revising the article.

Corresponding author

Correspondence to Max Wintermark.

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Conflict of interest

G. Zhu, J.J. Heit, B.W. Martin, D.G. Marcellus, C. Federau and M. Wintermark declare no relationships with any companies, whose products or services may be related to the subject matter of the article.

Ethical standards

For this article no studies with human participants or animals were performed by any of the authors. Written informed consent was waived by the Institutional Review Board. Institutional Review Board approval was obtained.

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Guarantor

The scientific guarantor of this publication is Dr. Max Wintermark.

Caption Electronic Supplementary Material

62_2019_817_MOESM1_ESM.docx

Supplemental Table. Differences in IVIM values between our reference standard with six b values and the other combinations of b values

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Zhu, G., Heit, J.J., Martin, B.W. et al. Optimized Combination of b‑values for IVIM Perfusion Imaging in Acute Ischemic Stroke Patients. Clin Neuroradiol 30, 535–544 (2020). https://doi.org/10.1007/s00062-019-00817-w

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  • DOI: https://doi.org/10.1007/s00062-019-00817-w

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