Abstract
Objectives
The objectives were to investigate the diffusional kurtosis imaging (DKI) incorporation into the intravoxel incoherent motion (IVIM) model for measurements of cerebral hypoperfusion in healthy subjects.
Materials and methods
Eight healthy subjects underwent a hyperventilation challenge with a 4-min diffusion weighted imaging protocol, using 8 b values chosen with the Cramer-Rao Lower Bound optimization approach. Four regions of interest in gray matter (GM) were analyzed with the DKI–IVIM model and the bi-exponential IVIM model, for normoventilation and hyperventilation conditions.
Results
A significant reduction in the perfusion fraction (f) and in the product fD* of the perfusion fraction with the pseudodiffusion coefficient (D*) was found with the DKI–IVIM model, during the hyperventilation challenge. In the cerebellum GM, the percentage changes were f: −43.7 ± 40.1, p = 0.011 and fD*: −50.6 ± 32.1, p = 0.011; in thalamus GM, f: −47.7 ± 34.7, p = 0.012 and fD*: −47.2 ± 48.7, p = 0.040. In comparison, using the bi-exponential IVIM model, only a significant decrease in the parameter fD* was observed for the same regions of interest. In frontal-GM and posterior-GM, the reduction in f and fD* did not reach statistical significance, either with DKI–IVIM or the bi-exponential IVIM model.
Conclusion
When compared to the bi-exponential IVIM model, the DKI–IVIM model displays a higher sensitivity to detect changes in perfusion induced by the hyperventilation condition.
Similar content being viewed by others
References
Le Bihan D, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeantet M (1986) MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 161:401–407
Le Bihan D, Breton E, Lallemand D, Aubin ML, Vignaud J, Laval-Jeantet M (1988) Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology 168:497–505
Koh D-M, Collins DJ, Orton MR (2011) Intravoxel incoherent motion in body diffusion-weighted MRI: reality and challenges. AJR Am J Roentgenol 196:1351–1361
Luciani A, Vignaud A, Cavet M, Nhieu JTV, Mallat A, Ruel L, Laurent A, Deux J-F, Brugieres P, Rahmouni A (2008) Liver cirrhosis: intravoxel incoherent motion MR imaging—pilot study. Radiology 249:891–899
Le Bihan D (2008) Intravoxel incoherent motion perfusion MR imaging: a wake-up call 1. Radiology 249:748–752
Le Bihan D, Turner R (1992) The capillary network: a link between IVIM and classical perfusion. Magn Reson Med 27:171–178
Wirestam R, Borg M, Brockstedt S, Lindgren A, Holtås S, Ståhlberg F (2001) Perfusion-related parameters in intravoxel incoherent motion MR imaging compared with CBV and CBF measured by dynamic susceptibility-contrast MR technique. Acta Radiol Stockh Swed 1987 42:123–128
Federau C, O’Brien K, Meuli R, Hagmann P, Maeder P (2014) Measuring brain perfusion with intravoxel incoherent motion (IVIM): initial clinical experience: brain IVIM: initial clinical experience. J Magn Reson Imaging 39:624–632
Wu W-C, Chen Y-F, Tseng H-M, Yang S-C, My P-C (2015) Caveat of measuring perfusion indexes using intravoxel incoherent motion magnetic resonance imaging in the human brain. Eur Radiol 25:2485–2492
Mulkern RV, Haker SJ, Maier SE (2009) On high b diffusion imaging in the human brain: ruminations and experimental insights. Magn Reson Imaging 27:1151–1162
Clark CA, Le Bihan D (2000) Water diffusion compartmentation and anisotropy at high b values in the human brain. Magn Reson Med 44:852–859
Sehy JV, Ackerman JJH, Neil JJ (2002) Evidence that both fast and slow water ADC components arise from intracellular space. Magn Reson Med 48:765–770
Bennett KM, Schmainda KM, Bennett RT, Rowe DB, Lu H, Hyde JS (2003) Characterization of continuously distributed cortical water diffusion rates with a stretched-exponential model. Magn Reson Med 50:727–734
Jensen JH, Helpern JA (2010) MRI quantification of non-Gaussian water diffusion by kurtosis analysis. NMR Biomed 23:698–710
Rosenkrantz AB, Padhani AR, Chenevert TL, Koh D-M, De Keyzer F, Taouli B, Le Bihan D (2015) Body diffusion kurtosis imaging: basic principles, applications, and considerations for clinical practice. J Magn Reson Imaging 42:1190–1202
Weber RA, Hui ES, Jensen JH, Nie X, Falangola MF, Helpern JA, Adkins DL (2015) Diffusional kurtosis and diffusion tensor imaging reveal different time-sensitive stroke-induced microstructural changes. Stroke 46:545–550
Zhu J, Zhuo C, Qin W, Wang D, Ma X, Zhou Y, Yu C (2015) Performances of diffusion kurtosis imaging and diffusion tensor imaging in detecting white matter abnormality in schizophrenia. NeuroImage Clin 7:170–176
Bai Y, Lin Y, Tian J, Shi D, Cheng J, Haacke EM, Hong X, Ma B, Zhou J, Wang M (2016) Grading of gliomas by using monoexponential, biexponential, and stretched exponential diffusion-weighted MR imaging and diffusion kurtosis MR imaging. Radiology 278:496–504
Lu Y, Jansen JFA, Mazaheri Y, Stambuk HE, Koutcher JA, Shukla-Dave A (2012) Extension of the intravoxel incoherent motion model to non-Gaussian diffusion in head and neck cancer. J Magn Reson Imaging 36:1088–1096
Wu W-C, Yang S-C, Chen Y-F, Tseng H-M, My P-C (2016) Simultaneous assessment of cerebral blood volume and diffusion heterogeneity using hybrid IVIM and DK MR imaging: initial experience with brain tumors. Eur Radiol. doi:10.1007/s00330-016-4272-z
De Luca A, Bertoldo A, Froeling M (2016) Effects of perfusion on DTI and DKI estimates in the skeletal muscle: effects of perfusion on DTI and DKI in muscle. Magn Reson Med. doi:10.1002/mrm.26373
Kety SS, Schmidt CF (1946) The effects of active and passive hyperventilation on cerebral blood flow, cerebral oxygen consumption, cardiac output, and blood pressure of normal young men. J Clin Invest 25:107–119
Moreton FC, Dani KA, Goutcher C, O’Hare K, Muir KW (2016) Respiratory challenge MRI: practical aspects. NeuroImage Clin 11:667–677
Zhang J, Zhou D, Nguyen TD, Spincemaille P, Gupta A, Wang Y (2016) Cerebral metabolic rate of oxygen (CMRO2) mapping with hyperventilation challenge using quantitative susceptibility mapping (QSM). Magn Reson Med. doi:10.1002/mrm.26253
Federau C, Maeder P, O’Brien K, Browaeys P, Meuli R, Hagmann P (2012) Quantitative measurement of brain perfusion with intravoxel incoherent motion MR imaging. Radiology 265:874–881
Leporq B, Saint-Jalmes H, Rabrait C, Pilleul F, Guillaud O, Dumortier J, Scoazec J-Y, Beuf O (2015) Optimization of intra-voxel incoherent motion imaging at 3.0 tesla for fast liver examination: optimization of liver motion imaging at 3.0 T. J Magn Reson Imaging 41:1209–1217
Federau C, Sumer S, Becce F, Maeder P, O’Brien K, Meuli R, Wintermark M (2014) Intravoxel incoherent motion perfusion imaging in acute stroke: initial clinical experience. Neuroradiology 56:629–635
Tancredi FB, Hoge RD (2013) Comparison of cerebral vascular reactivity measures obtained using breath-holding and CO2 inhalation. J Cereb Blood Flow Metab 33:1066–1074
Suo S, Cao M, Zhu W, Li L, Li J, Shen F, Zu J, Zhou Z, Zhuang Z, Qu J, Chen Z, Xu J (2016) Stroke assessment with intravoxel incoherent motion diffusion-weighted MRI: IVIM diffusion-weighted MRI for human stroke. NMR Biomed 29:320–328
Suo S, Lin N, Wang H, Zhang L, Wang R, Zhang S, Hua J, Xu J (2015) Intravoxel incoherent motion diffusion-weighted MR imaging of breast cancer at 3.0 tesla: comparison of different curve-fitting methods: different IVIM analyses in breast cancer. J Magn Reson Imaging 42:362–370
Barbieri S, Donati OF, Froehlich JM, Thoeny HC (2016) Impact of the calculation algorithm on biexponential fitting of diffusion-weighted MRI in upper abdominal organs. Magn Reson Med 75:2175–2184
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723
Yuan J, Yeung DKW, Mok GSP, Bhatia KS, Wang Y-XJ, Ahuja AT, King AD (2014) Non-gaussian analysis of diffusion weighted imaging in head and neck at 3T: a pilot study in patients with nasopharyngeal carcinoma. PLoS One 9:e87024
Le Bihan D (2013) Apparent diffusion coefficient and beyond: what diffusion MR imaging can tell us about tissue structure. Radiology 268:318–322
Grinberg F, Farrher E, Ciobanu L, Geffroy F, Le Bihan D, Shah NJ (2014) Non-gaussian diffusion imaging for enhanced contrast of brain tissue affected by ischemic stroke. PLoS One 9:e89225
Federau C, Meuli R, O’Brien K, Maeder P, Hagmann P (2014) Perfusion measurement in brain gliomas with intravoxel incoherent motion MRI. Am J Neuroradiol 35:256–262
Federau C, O’Brien K, Birbaumer A, Meuli R, Hagmann P, Maeder P (2015) Functional mapping of the human visual cortex with intravoxel incoherent motion MRI. PLoS One 10:e0117706
Bisdas S, Braun C, Skardelly M, Schittenhelm J, Teo TH, Thng CH, Klose U, Koh TS (2014) Correlative assessment of tumor microcirculation using contrast-enhanced perfusion MRI and intravoxel incoherent motion diffusion-weighted MRI: is there a link between them? NMR Biomed 27:1184–1191
Acknowledgements
This study was supported by the Conseil Scientifique et Méthodologique (CSM) of the University Hospital of Martinique (CHU).
Author information
Authors and Affiliations
Contributions
Pavilla: protocol/data collection/data analysis; Gambarota: protocol/data analysis/project development; Arrigo: protocol/data collection management/project development; Mejdoubi: Protocol/project development; Duvauferrier: protocol/project development; Saint-Jalmes: protocol/data analysis/project development
Corresponding author
Ethics declarations
Conflict of interest
The authors each declare that they have no conflict of interest.
Ethical approval
All procedures performed in studies involving human participants were approved by the appropriate ethics committee and were therefore performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Pavilla, A., Gambarota, G., Arrigo, A. et al. Diffusional kurtosis imaging (DKI) incorporation into an intravoxel incoherent motion (IVIM) MR model to measure cerebral hypoperfusion induced by hyperventilation challenge in healthy subjects. Magn Reson Mater Phy 30, 545–554 (2017). https://doi.org/10.1007/s10334-017-0629-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10334-017-0629-9