Quantitative liver MRI combining phase contrast imaging, elastography, and DWI: assessment of reproducibility and postprandial effect at 3.0 T

Guido H Jajamovich, Hadrien Dyvorne, Claudia Donnerhack, Bachir Taouli, Guido H Jajamovich, Hadrien Dyvorne, Claudia Donnerhack, Bachir Taouli

Abstract

Purpose: To quantify short-term reproducibility (in fasting conditions) and postprandial changes after a meal in portal vein (PV) flow parameters measured with phase contrast (PC) imaging, liver diffusion parameters measured with multiple b value diffusion-weighted imaging (DWI) and liver stiffness (LS) measured with MR elastography (MRE) in healthy volunteers and patients with liver disease at 3.0 T.

Materials and methods: In this IRB-approved prospective study, 30 subjects (11 healthy volunteers and 19 liver disease patients; 23 males, 7 females; mean age 46.5 y) were enrolled. Imaging included 2D PC imaging, multiple b value DWI and MRE. Subjects were initially scanned twice in fasting state to assess short-term parameter reproducibility, and then scanned 20 min. after a liquid meal. PV flow/velocity, LS, liver true diffusion coefficient (D), pseudodiffusion coefficient (D*), perfusion fraction (PF) and apparent diffusion coefficient (ADC) were measured in fasting and postprandial conditions. Short-term reproducibility was assessed in fasting conditions by measuring coefficients of variation (CV) and Bland-Altman limits of agreement. Differences in MR metrics before and after caloric intake and between healthy volunteers and liver disease patients were assessed.

Results: PV flow parameters, D, ADC and LS showed good to excellent short-term reproducibility in fasting state (CV <16%), while PF and D* showed acceptable and poor reproducibility (CV = 20.4% and 51.6%, respectively). PV flow parameters and LS were significantly higher (p<0.04) in postprandial state while liver diffusion parameters showed no significant change (p>0.2). LS was significantly higher in liver disease patients compared to healthy volunteers both in fasting and postprandial conditions (p<0.001). Changes in LS were significantly correlated with changes in PV flow (Spearman rho = 0.48, p = 0.013).

Conclusions: Caloric intake had no/minimal/large impact on diffusion/stiffness/portal vein flow, respectively. PC MRI and MRE but not DWI should be performed in controlled fasting state.

Conflict of interest statement

Competing Interests: GE Healthcare provided funding toward this study. There are no patents, products in development, or marketed products to declare. This does not alter our adherence to all PLOS ONE policies on sharing data and materials.

Figures

Figure 1. Study design.
Figure 1. Study design.
All subjects were scanned twice after 6 hours of fasting to assess short-term reproducibility of MRI metrics (subjects were removed from the MRI system and re-imaged). Subjects were then scanned again in postprandial conditions, 20 min. after a 700 kcal liquid meal.
Figure 2. Image processing demonstrated in a…
Figure 2. Image processing demonstrated in a 30 year-old healthy volunteer.
Top row demonstrates the region of interest placement in the portal vein (PV) on the phase contrast magnitude and phase images obtained in fasting and postprandial conditions. PV flow and velocity values were 21.15 ml/s/2.7 cm/s (fasting) and 31.1 ml/s/17.8 cm/s (postprandial). Middle row demonstrates the region of interest placement in the right hepatic lobe on the diffusion images (for b = 15) and plots for bi-exponential fitting in fasting (true diffusion coefficient D, pseudodiffusion coefficient D* and perfusion fraction PF of 1.3×10−3 mm2/s, 57×10−3 mm2/s and 22%) and postprandial conditions (1.1×10−3 mm2/s, 171×10−3 mm2/s, 19%). Bottom row shows the gradient echo MRE reference image (left) and liver stiffness (LS) maps in fasting and postprandial conditions (LS was 1.9 and 1.9 kPa in fasting and postprandial conditions, respectively).
Figure 3. Changes in portal vein (PV)…
Figure 3. Changes in portal vein (PV) flow (A), PV velocity (B), liver stiffness LS measured with MRE (C), liver true diffusion coefficient D (D), pseudodiffusion coefficient D* (E), perfusion fraction PF (F), and apparent diffusion coefficient ADC (G) in fasting (1st exam) and postprandial conditions in 11 healthy volunteers (solid black lines) and 19 patients (dashed red lines).
LS shows a clear separation between healthy volunteers and patients. PV: portal vein, PV flow (ml/s), PV velocity (cm/s), LS (liver stiffness, kPa), D (true diffusion coefficient, ×10−3 mm2/s), D* (pseudodiffusion coefficient, ×10−3 mm2/s), PF (perfusion fraction, %), ADC (apparent diffusion coefficient, ×10−3 mm2/s). *LS was calculated for 27 subjects.
Figure 4. Changes in liver stiffness after…
Figure 4. Changes in liver stiffness after a liquid meal (ΔLS*) correlated to changes in portal vein flow (ΔPV Flow*) in healthy volunteers (blue diamonds) and patients (red squares).
There was a significant correlation between ΔLS vs. ΔPV Flow (Spearman rho = 0.48, p = 0.013 for all subjects; rho = 0.51 p = 0.05 for fibrosis patients, and rho = 0.41, p = 0.21 for healthy volunteers). *Δ computed as 100*(postprandial-fasting)/fasting.

References

    1. Castera L, Vergniol J, Foucher J, Le Bail B, Chanteloup E, et al. (2005) Prospective comparison of transient elastography, Fibrotest, APRI, and liver biopsy for the assessment of fibrosis in chronic hepatitis C. Gastroenterology. 128: 343–350.
    1. Foucher J, Chanteloup E, Vergniol J, Castera L, Le Bail B, et al. (2006) Diagnosis of cirrhosis by transient elastography (FibroScan): a prospective study. Gut 55: 403–408.
    1. Friedrich-Rust M, Rosenberg W, Parkes J, Herrmann E, Zeuzem S, et al. (2010) Comparison of ELF, FibroTest and FibroScan for the non-invasive assessment of liver fibrosis. BMC Gastroenterol 10: 103.
    1. Ganne-Carrie N, Ziol M, de Ledinghen V, Douvin C, Marcellin P, et al. (2006) Accuracy of liver stiffness measurement for the diagnosis of cirrhosis in patients with chronic liver diseases. Hepatology 44: 1511–1517.
    1. Lucidarme D, Foucher J, Le Bail B, Vergniol J, Castera L, et al. (2009) Factors of accuracy of transient elastography (fibroscan) for the diagnosis of liver fibrosis in chronic hepatitis C. Hepatology. 49: 1083–1089.
    1. Bureau C, Metivier S, Peron JM, Selves J, Robic MA, et al. (2008) Transient elastography accurately predicts presence of significant portal hypertension in patients with chronic liver disease. Aliment Pharmacol Ther 27: 1261–1268.
    1. Yin M, Talwalkar JA, Glaser KJ, Manduca A, Grimm RC, et al... (2007) Assessment of hepatic fibrosis with magnetic resonance elastography. Clin Gastroenterol Hepatol 5: 1207–1213 e1202.
    1. Huwart L, Sempoux C, Salameh N, Jamart J, Annet L, et al. (2007) Liver fibrosis: noninvasive assessment with MR elastography versus aspartate aminotransferase-to-platelet ratio index. Radiology 245: 458–466.
    1. Huwart L, Sempoux C, Vicaut E, Salameh N, Annet L, et al. (2008) Magnetic resonance elastography for the noninvasive staging of liver fibrosis. Gastroenterology 135: 32–40.
    1. Wang Y, Ganger DR, Levitsky J, Sternick LA, McCarthy RJ, et al. (2011) Assessment of chronic hepatitis and fibrosis: comparison of MR elastography and diffusion-weighted imaging. AJR Am J Roentgenol 196: 553–561.
    1. Taouli B, Tolia AJ, Losada M, Babb JS, Chan ES, et al. (2007) Diffusion-weighted MRI for quantification of liver fibrosis: preliminary experience. AJR Am J Roentgenol 189: 799–806.
    1. Taouli B, Chouli M, Martin AJ, Qayyum A, Coakley FV, et al. (2008) Chronic hepatitis: role of diffusion-weighted imaging and diffusion tensor imaging for the diagnosis of liver fibrosis and inflammation. J Magn Reson Imaging 28: 89–95.
    1. Girometti R, Furlan A, Bazzocchi M, Soldano F, Isola M, et al. (2007) Diffusion-weighted MRI in evaluating liver fibrosis: a feasibility study in cirrhotic patients. Radiol Med (Torino) 112: 394–408.
    1. Lewin M, Poujol-Robert A, Boelle PY, Wendum D, Lasnier E, et al. (2007) Diffusion-weighted magnetic resonance imaging for the assessment of fibrosis in chronic hepatitis C. Hepatology. 46: 658–665.
    1. Dyvorne HA, Galea N, Nevers T, Fiel MI, Carpenter D, et al. (2013) Diffusion-weighted imaging of the liver with multiple b values: effect of diffusion gradient polarity and breathing acquisition on image quality and intravoxel incoherent motion parameters–a pilot study. Radiology 266: 920–929.
    1. Van Beers BE, Materne R, Annet L, Hermoye L, Sempoux C, et al. (2003) Capillarization of the sinusoids in liver fibrosis: Noninvasive assessment with contrast-enhanced MRI in the rabbit. Magn Reson Med 49: 692–699.
    1. Annet L, Materne R, Danse E, Jamart J, Horsmans Y, et al. (2003) Hepatic flow parameters measured with MR imaging and Doppler US: correlations with degree of cirrhosis and portal hypertension. Radiology 229: 409–414.
    1. Hagiwara M, Rusinek H, Lee VS, Losada M, Bannan MA, et al. (2008) Advanced liver fibrosis: diagnosis with 3D whole-liver perfusion MR imaging–initial experience. Radiology 246: 926–934.
    1. Patel J, Sigmund EE, Rusinek H, Oei M, Babb JS, et al. (2010) Diagnosis of cirrhosis with intravoxel incoherent motion diffusion MRI and dynamic contrast-enhanced MRI alone and in combination: preliminary experience. J Magn Reson Imaging 31: 589–600.
    1. Gallavan RH Jr, Chou CC (1985) Possible mechanisms for the initiation and maintenance of postprandial intestinal hyperemia. Am J Physiol 249: G301–308.
    1. Lee SS, Hadengue A, Moreau R, Sayegh R, Hillon P, et al. (1988) Postprandial hemodynamic responses in patients with cirrhosis. Hepatology 8: 647–651.
    1. O’Brien S, Keogan M, Patchett S, McCormick PA, Afdhal N, et al. (1992) Postprandial changes in portal haemodynamics in patients with cirrhosis. Gut 33: 364–367.
    1. Ludwig D, Schwarting K, Korbel CM, Bruning A (1998) Schiefer B, et al (1998) The postprandial portal flow is related to the severity of portal hypertension and liver cirrhosis. J Hepatol 28: 631–638.
    1. Dauzat M, Lafortune M, Patriquin H, Pomier-Layrargues G (1994) Meal induced changes in hepatic and splanchnic circulation: a noninvasive Doppler study in normal humans. Eur J Appl Physiol Occup Physiol 68: 373–380.
    1. Ozdogan O, Atalay H, Cimsit C, Tahan V, Tokay S, et al. (2008) Role of echo Doppler ultrasonography in the evaluation of postprandial hyperemia in cirrhotic patients. World J Gastroenterol 14: 260–264.
    1. Berzigotti A, De Gottardi A, Vukotic R, Siramolpiwat S, Abraldes JG, et al. (2013) Effect of meal ingestion on liver stiffness in patients with cirrhosis and portal hypertension. PLoS One 8: e58742.
    1. Koinuma M, Ohashi I, Hanafusa K, Shibuya H (2005) Apparent diffusion coefficient measurements with diffusion-weighted magnetic resonance imaging for evaluation of hepatic fibrosis. J Magn Reson Imaging 22: 80–85.
    1. Lewin M, Poujol-Robert A, Boëlle PY, Wendum D, Lasnier E, et al. (2007) Diffusion - weighted magnetic resonance imaging for the assessment of fibrosis in chronic hepatitis C. Hepatology. 46: 658–665.
    1. Le Bihan D (1995) Molecular diffusion, tissue microdynamics and microstructure. NMR Biomed 8: 375–386.
    1. Hollingsworth KG, Lomas DJ (2006) Influence of perfusion on hepatic MR diffusion measurement. NMR Biomed 19: 231–235.
    1. Le Bihan D, Breton E, Lallemand D, Aubin ML, Vignaud J, et al. (1988) Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology 168: 497–505.
    1. Luciani A, Vignaud A, Cavet M, Nhieu JT, Mallat A, et al. (2008) Liver cirrhosis: intravoxel incoherent motion MR imaging–pilot study. Radiology 249: 891–899.
    1. Muthupillai R, Lomas DJ, Rossman PJ, Greenleaf JF, Manduca A, et al. (1995) Magnetic resonance elastography by direct visualization of propagating acoustic strain waves. Science 269: 1854–1857.
    1. Shire NJ, Yin M, Chen J, Railkar RA, Fox-Bosetti S, et al. (2011) Test-retest repeatability of MR elastography for noninvasive liver fibrosis assessment in hepatitis C. J Magn Reson Imaging. 34: 947–955.
    1. Lee YJ, Lee JM, Lee JE, Lee KB, Lee ES, et al... (2013) MR elastography for noninvasive assessment of hepatic fibrosis: Reproducibility of the examination and reproducibility and repeatability of the liver stiffness value measurement. J Magn Reson Imaging.
    1. Hines CD, Bley TA, Lindstrom MJ, Reeder SB (2010) Repeatability of magnetic resonance elastography for quantification of hepatic stiffness. J Magn Reson Imaging 31: 725–731.
    1. Asbach P, Klatt D, Hamhaber U, Braun J, Somasundaram R, et al. (2008) Assessment of liver viscoelasticity using multifrequency MR elastography. Magn Reson Med 60: 373–379.
    1. Huwart L, van Beers BE (2008) MR elastography. Gastroenterol Clin Biol 32: 68–72.
    1. Lupsor M, Badea R, Stefanescu H, Grigorescu M, Sparchez Z, et al. (2008) Analysis of histopathological changes that influence liver stiffness in chronic hepatitis C. Results from a cohort of 324 patients. J Gastrointestin Liver Dis 17: 155–163.
    1. Yin M, Talwalkar JA, Glaser KJ, Venkatesh SK, Chen J, et al. (2011) Dynamic postprandial hepatic stiffness augmentation assessed with MR elastography in patients with chronic liver disease. AJR Am J Roentgenol 197: 64–70.
    1. Hara AK, Burkart DJ, Johnson CD, Felmlee JP, Ehman RL, et al. (1996) Variability of consecutive in vivo MR flow measurements in the main portal vein. AJR Am J Roentgenol 166: 1311–1315.
    1. Yzet T, Bouzerar R, Allart J-D, Demuynck F, Legallais C, et al. (2010) Hepatic vascular flow measurements by phase contrast MRI and doppler echography: a comparative and reproducibility study. Journal of magnetic resonance imaging: JMRI 31: 579–588.
    1. Gouya H, Vignaux O, Sogni P, Mallet V, Oudjit A, et al. (2011) Chronic liver disease: systemic and splanchnic venous flow mapping with optimized cine phase-contrast MR imaging validated in a phantom model and prospectively evaluated in patients. Radiology 261: 144–155.
    1. Kashitani N, Kimoto S, Tsunoda M, Ito T, Tsuji T, et al. (1995) Portal blood flow in the presence or absence of diffuse liver disease: measurement by phase contrast MR imaging. Abdominal imaging 20: 197–200.
    1. Sadek AG, Mohamed FB, Outwater EK, El-Essawy SS, Mitchell DG (1996) Respiratory and postprandial changes in portal flow rate: assessment by phase contrast MR imaging. J Magn Reson Imaging 6: 90–93.
    1. Burkart DJ, Johnson CD, Reading CC, Ehman RL (1995) MR measurements of mesenteric venous flow: prospective evaluation in healthy volunteers and patients with suspected chronic mesenteric ischemia. Radiology 194: 801–806.
    1. Bellis L, Berzigotti A, Abraldes JG, Moitinho E, Garcia-Pagan JC, et al. (2003) Low doses of isosorbide mononitrate attenuate the postprandial increase in portal pressure in patients with cirrhosis. Hepatology 37: 378–384.
    1. Pazahr S, Nanz D, Rossi C, Chuck N, Stenger I, et al... (2013) Magnetic Resonance Imaging of the Liver: Apparent Diffusion Coefficients From Multiexponential Analysis of b Values Greater Than 50 s/mm2 Do Not Respond to Caloric Intake Despite Increased Portal-Venous Blood Flow. Invest Radiol.
    1. Hines CD, Lindstrom MJ, Varma AK, Reeder SB (2011) Effects of postprandial state and mesenteric blood flow on the repeatability of MR elastography in asymptomatic subjects. J Magn Reson Imaging 33: 239–244.

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