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Journal of Cardiovascular Magnetic Resonance

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Open Access 01-12-2017 | Technical notes

Bayesian intravoxel incoherent motion parameter mapping in the human heart

Authors: Georg R. Spinner, Constantin von Deuster, Kerem C. Tezcan, Christian T. Stoeck, Sebastian Kozerke

Published in: Journal of Cardiovascular Magnetic Resonance | Issue 1/2017

Abstract

Background

Intravoxel incoherent motion (IVIM) imaging of diffusion and perfusion in the heart suffers from high parameter estimation error. The purpose of this work is to improve cardiac IVIM parameter mapping using Bayesian inference.

Methods

A second-order motion-compensated diffusion weighted spin-echo sequence with navigator-based slice tracking was implemented to collect cardiac IVIM data in early systole in eight healthy subjects on a clinical 1.5 T CMR system. IVIM data were encoded along six gradient optimized directions with b-values of 0–300 s/mm². Subjects were scanned twice in two scan sessions one week apart to assess intra-subject reproducibility. Bayesian shrinkage prior (BSP) inference was implemented to determine IVIM parameters (diffusion D, perfusion fraction F and pseudo-diffusion D*). Results were compared to least-squares (LSQ) parameter estimation. Signal-to-noise ratio (SNR) requirements for a given fitting error were assessed for the two methods using simulated data. Reproducibility analysis of parameter estimation in-vivo using BSP and LSQ was performed.

Results

BSP resulted in reduced SNR requirements when compared to LSQ in simulations. In-vivo, BSP analysis yielded IVIM parameter maps with smaller intra-myocardial variability and higher estimation certainty relative to LSQ. Mean IVIM parameter estimates in eight healthy subjects were (LSQ/BSP): 1.63 ± 0.28/1.51 ± 0.14·10⁻³ mm²/s for D, 13.13 ± 19.81/13.11 ± 5.95% for F and 201.45 ± 313.23/13.11 ± 14.53·10⁻³ mm²/s for D ^∗. Parameter variation across all volunteers and measurements was lower with BSP compared to LSQ (coefficient of variation BSP vs. LSQ: 9% vs. 17% for D, 45% vs. 151% for F and 111% vs. 155% for D ^∗). In addition, reproducibility of the IVIM parameter estimates was higher with BSP compared to LSQ (Bland-Altman coefficients of repeatability BSP vs. LSQ: 0.21 vs. 0.26·10⁻³ mm²/s for D, 5.55 vs. 6.91% for F and 15.06 vs. 422.80·10⁻³ mm²/s for D*).

Conclusion

Robust free-breathing cardiac IVIM data acquisition in early systole is possible with the proposed method. BSP analysis yields improved IVIM parameter maps relative to conventional LSQ fitting with fewer outliers, improved estimation certainty and higher reproducibility. IVIM parameter mapping holds promise for myocardial perfusion measurements without the need for contrast agents.

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Le Bihan D. Intravoxel incoherent motion imaging using steady-state free precession. Magn Reson Med. 1988;7:346–51.CrossRefPubMed

Le Bihan D. Intravoxel incoherent motion perfusion MR imaging: a wake-up call. Radiology. 2008;249:748–52. https://doi.org/10.1148/radiol.2493081301. CrossRefPubMed

Le Bihan D, Breton E, Lallemand D, Aubin ML, Vignaud J, Laval-Jeantet M. Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology. 1988;168:497–505. https://doi.org/10.1148/radiology.168.2.3393671. CrossRefPubMed

Le Bihan D, Turner R. The capillary network: a link between IVIM and classical perfusion. Magn Reson Med. 1992;27:171–8.CrossRefPubMed

Yamada I, Aung W, Himeno Y, Nakagawa T, Shibuya H. Diffusion coefficients in abdominal organs and hepatic lesions: evaluation with intravoxel incoherent motion echo-planar MR imaging. Radiology. 1999;210:617–23. https://doi.org/10.1148/radiology.210.3.r99fe17617. CrossRefPubMed

Notohamiprodjo M, Chandarana H, Mikheev A, Rusinek H, Grinstead J, Feiweier T, Raya JG, Lee VS, Sigmund EE. Combined intravoxel incoherent motion and diffusion tensor imaging of renal diffusion and flow anisotropy. Magn Reson Med. 2015;73:1526–32. https://doi.org/10.1002/mrm.25245. CrossRefPubMed

Lemke A, Laun FB, Klau M, Re TJ, Simon D, Delorme S, Schad LR, Stieltjes B. Differentiation of pancreas carcinoma from healthy pancreatic tissue using multiple b-values. Investig Radiol. 2009;44:769–75. https://doi.org/10.1097/RLI.0b013e3181b62271. CrossRef

Luciani A, Vignaud A, Cavet M, et al. Liver cirrhosis: intravoxel incoherent motion MR imaging—pilot study. Radiology. 2008;249:891–9. https://doi.org/10.1148/radiol.2493080080. CrossRefPubMed

Patel J, Sigmund EE, Rusinek H, Oei M, Babb JS, Taouli B. Diagnosis of cirrhosis with intravoxel incoherent motion diffusion MRI and dynamic contrast-enhanced MRI alone and in combination: preliminary experience. J Magn Reson Imaging. 2010;31:589–600. https://doi.org/10.1002/jmri.22081. CrossRefPubMedPubMedCentral

10.

Froeling M, Strijkers GJ, Nederveen AJ, Chamuleau SA, Luijten PR. Feasibility of in vivo whole heart DTI and IVIM with a 15 minute acquisition protocol. J Cardiovasc Magn Reson. 2014;16:O15. https://doi.org/10.1186/1532-429X-16-S1-O15.CrossRefPubMedCentral

11.

Moulin KK, Croisille P, Feiweier T, Delattre BMA, Wei H, Robert B, Beuf O, Viallon M. In vivo free-breathing DTI and IVIM of the whole human heart using a real-time slice-followed SE-EPI navigator-based sequence: a reproducibility study in healthy volunteers. Magn Reson Med. 2016;76:70–82. https://doi.org/10.1002/mrm.25852. CrossRefPubMed

12.

Deux J-F, Maatouk M, Vignaud A, Luciani A, Lenczner G, Mayer J, Lim P, Dubois-Randé J-L, Kobeiter H, Rahmouni A. Diffusion-weighted echo planar imaging in patients with recent myocardial infarction. Eur Radiol. 2011;21:46–53. https://doi.org/10.1007/s00330-010-1912-6. CrossRefPubMed

13.

Laissy J-P, Gaxotte V, Ironde-laissy E, Klein I, Ribet A, Bendriss A, Chillon S, Schouman-Claeys E, Steg PG, Serfaty J-M. Cardiac diffusion-weighted MR imaging in recent, subacute, and chronic myocardial infarction: a pilot study. J Magn Reson Imaging. 2013;38:1377–87. https://doi.org/10.1002/jmri.24125. CrossRefPubMed

14.

Deuster C Von, Stoeck CT, Wissmann L, Spinner G, Fleischmann T, Emmert MY, Cesarovic N, Kozerke S. Verification of the intra-voxel incoherent motion (IVIM) model in the porcine heart. In: Proc Intl Soc Mag Reson Med. 2015;23.

15.

Ismail TF, Hsu L-Y, Greve AM, et al. Coronary microvascular ischemia in hypertrophic cardiomyopathy - a pixel-wise quantitative cardiovascular magnetic resonance perfusion study. J Cardiovasc Magn Reson. 2014;16:1–10. https://doi.org/10.1186/s12968-014-0049-1. CrossRef

16.

Gamper U, Boesiger P, Kozerke S. Diffusion imaging of the in vivo heart using spin echoes--considerations on bulk motion sensitivity. Magn Reson Med. 2007;57:331–7. https://doi.org/10.1002/mrm.21127. CrossRefPubMed

17.

Stoeck CT, von Deuster C, Genet M, Atkinson D, Kozerke S. Second-order motion-compensated spin echo diffusion tensor imaging of the human heart. Magn Reson Med. 2016;75:1669–76. https://doi.org/10.1002/mrm.25784. CrossRefPubMed

18.

Welsh CL, DiBella EVR, Hsu EW. Higher-order motion-compensation for in vivo cardiac diffusion tensor imaging in rats. IEEE Trans Med Imaging. 2015;34:1843–53. https://doi.org/10.1109/TMI.2015.2411571. CrossRefPubMedPubMedCentral

19.

Nguyen C, Fan Z, Sharif B, He Y, Dharmakumar R, Berman DS, Li D. In vivo three-dimensional high resolution cardiac diffusion-weighted MRI: a motion compensated diffusion-prepared balanced steady-state free precession approach. Magn Reson Med. 2014;72:1257–67. https://doi.org/10.1002/mrm.25038. CrossRefPubMed

20.

21.

Pai VM, Rapacchi S, Kellman P, Croisille P, Wen HPCATMIP. Enhancing signal intensity in diffusion-weighted magnetic resonance imaging. Magn Reson Med. 2011;65:1611–9. https://doi.org/10.1002/mrm.22748. CrossRefPubMed

22.

Rapacchi S, Wen H, Viallon M, Grenier D, Kellman P, Croisille P, Pai VM. Low b-value diffusion-weighted cardiac magnetic resonance imaging: initial results in humans using an optimal time-window imaging approach. Investig Radiol. 2011;46:751–8. https://doi.org/10.1097/RLI.0b013e31822438e8. CrossRef

23.

Delattre BM, Viallon M, Wei H, Zhu Y, Pai VM, Wen H, Croisille P. Intravoxel incoherent motion applied to cardiac diffusion weighted MRI using breath-hold acquisitions in healthy volunteers. J Cardiovasc Magn Reson. 2012;14:P261. https://doi.org/10.1186/1532-429X-14-S1-P261.CrossRefPubMedCentral

24.

Callot V, Bennett E, Decking UKM, Balaban RS, Wen H. Vivo study of microcirculation in canine myocardium using the IVIM method. Magn Reson Med. 2003;50:531–40. https://doi.org/10.1002/mrm.10568. CrossRefPubMedPubMedCentral

25.

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. https://doi.org/10.1002/jmri.24195. CrossRefPubMed

26.

W-C W, Chen Y-F, Tseng H-M, Yang S-C, My P-C. Caveat of measuring perfusion indexes using intravoxel incoherent motion magnetic resonance imaging in the human brain. Eur Radiol. 2015;25:2485–92. https://doi.org/10.1007/s00330-015-3655-x. CrossRef

27.

Federau C, O’Brien K, Birbaumer A, et al. Functional mapping of the human visual cortex with intravoxel incoherent motion MRI Zochowski M. PLoS One. 2015;10:1–11. https://doi.org/10.1371/journal.pone.0117706. CrossRef

28.

Huang H-M, Shih Y-Y, Lin C. Formation of parametric images using mixed-effects models: a feasibility study. NMR Biomed. 2016;29:239–47. https://doi.org/10.1002/nbm.3453. CrossRefPubMed

29.

Rheinheimer S, Stieltjes B, Schneider F, Simon D, Pahernik S, Kauczor HU, Hallscheidt P. Investigation of renal lesions by diffusion-weighted magnetic resonance imaging applying intravoxel incoherent motion-derived parameters--initial experience. Eur J Radiol. 2012;81:e310–6. https://doi.org/10.1016/j.ejrad.2011.10.016. CrossRefPubMed

30.

Orton MR, Collins DJ, Koh D-M, Leach MO. Improved intravoxel incoherent motion analysis of diffusion weighted imaging by data driven Bayesian modeling. Magn Reson Med. 2014;71:411–20. https://doi.org/10.1002/mrm.24649. CrossRefPubMed

31.

Jeffreys H. An invariant form for the prior probability in estimation problems. Proc R Soc Lond A Math Phys Sci. 1946;186:453–61.CrossRefPubMed

32.

Feinberg DA, Hoenninger JC, Crooks LE, Kaufman L, Watts JC, Arakawa M. Inner volume MR imaging: technical concepts and their application. Radiology. 1985;156:743–7. https://doi.org/10.1148/radiology.156.3.4023236. CrossRefPubMed

33.

Meyer CH, Pauly JM, Macovski A, Nishimura DG. Simultaneous spatial and spectral selective excitation. Magn Reson Med. 1990;15:287–304.CrossRefPubMed

34.

Ernst RR. Application of Fourier transform spectroscopy to magnetic resonance. Rev Sci Instrum. 1966;37:93–102. https://doi.org/10.1063/1.1719961. CrossRef

35.

Nordmeyer-Massner J A, De Zanche N, Pruessmann KP. Mechanically adjustable coil array for wrist MRI. Magn Reson Med. 2009;61:429–438. doi: https://doi.org/10.1002/mrm.21868.

36.

Vishnevskiy V, Gass T, Szekely G, Tanner C, Goksel O. Isotropic total variation regularization of displacements in parametric image registration. IEEE Trans Med Imaging. 2016;62:1–1. https://doi.org/10.1109/TMI.2016.2610583.

37.

Huizinga W, Poot DHJ, Guyader J-M, et al. PCA-based groupwise image registration for quantitative MRI. Med Image Anal. 2015; https://doi.org/10.1016/j.media.2015.12.004.

38.

Scott AD, Nielles-Vallespin S, Ferreira PF, McGill L-A, Pennell DJ, Firmin DN. The effects of noise in cardiac diffusion tensor imaging and the benefits of averaging complex data. NMR Biomed. 2016;29:588–99. https://doi.org/10.1002/nbm.3500. CrossRefPubMed

39.

Messroghli DR, Plein S, Higgins DM, Walters K, Jones TR, Ridgway JP, Sivananthan MU. Human myocardium: single-breath-hold MR T1 mapping with high spatial resolution--reproducibility study. Radiology. 2006;238:1004–12. https://doi.org/10.1148/radiol.2382041903. CrossRefPubMed

40.

von Deuster C, Stoeck CT, Genet M, Atkinson D, Kozerke S. Spin echo versus stimulated echo diffusion tensor imaging of the in vivo human heart. Magn Reson Med. 2016;76:862–72. https://doi.org/10.1002/mrm.25998. CrossRefPubMed

41.

Wetscherek A, Stieltjes B, Laun FB. Flow-compensated intravoxel incoherent motion diffusion imaging. Magn Reson Med. 2015;74:410–9. https://doi.org/10.1002/mrm.25410. CrossRefPubMed

42.

While PT. A comparative simulation study of Bayesian fitting approaches to intravoxel incoherent motion modeling in diffusion-weighted MRI. Magn Reson Med. 2017;77 https://doi.org/10.1002/mrm.26598.

43.

Freiman M, Perez-Rossello JM, Callahan MJ, Voss SD, Ecklund K, Mulkern RV, Warfield SK. Reliable estimation of incoherent motion parametric maps from diffusion-weighted MRI using fusion bootstrap moves. Med Image Anal. 2013;17:325–36. https://doi.org/10.1016/j.media.2012.12.001. CrossRefPubMedPubMedCentral

44.

Stoneking CJ. Bayesian inference of Gaussian mixture models with noninformative priors; 2014. https://arxiv.org/abs/1405.4895.

45.

Stoeck CT, von Deuster C, van Gorkum R, Kozerke S. Impact of eddy-currents and cardiac motion in DTI of the in-vivo heart - a comparison of second-order motion compensated SE versus STEAM. In: Proc Intl Soc Mag Reson Med. 2017.

46.

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. https://doi.org/10.1016/j.mri.2011.03.004. CrossRefPubMed

47.

Fang ZY, Prins JB, Marwick TH. Diabetic cardiomyopathy: evidence, mechanisms, and therapeutic implications. Endocr Rev. 2004;25:543–67. https://doi.org/10.1210/er.2003-0012. CrossRefPubMed

48.

Jones DK, Horsfield MA, Simmons A. Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging. Magn Reson Med. 1999;42:515–25.CrossRefPubMed

Title: Bayesian intravoxel incoherent motion parameter mapping in the human heart
Authors: Georg R. Spinner
Constantin von Deuster
Kerem C. Tezcan
Christian T. Stoeck
Sebastian Kozerke
Publication date: 01-12-2017
Publisher: BioMed Central
Published in: Journal of Cardiovascular Magnetic Resonance / Issue 1/2017
Electronic ISSN: 1532-429X
DOI: https://doi.org/10.1186/s12968-017-0391-1

At a glance: The STEP trials

Springer Medicine

Bayesian intravoxel incoherent motion parameter mapping in the human heart

Abstract

Background

Methods

Results

Conclusion

At a glance: The STEP trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

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