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Effect of breath hold mode on the storage modulus of the liver in healthy individuals studied with a gravitational transducer at magnetic resonance elastography
Philippe Garteiser1, Gwenael Page1, Aimé-Pacifique Manzi2, Valérie Vilgrain2, Ralph Sinkus3,4, and Bernard E Van Beers1,2

1Center for Research on Inflammation, Inserm UMR1149, Paris, France, 2Radiology department, Beaujon hospital, AP-HP, Clichy, France, 3King's College London, London, United Kingdom, 4LVTS, Inserm U1149, Paris, France

Synopsis

Although MR elastography (MRE) is a preferred diagnostic tool for hepatic fibrosis, MRE-derived mechanical properties are affected by factors such as portal pressure. Since portal pressure is modulated across the breathing cycle, we sought to evaluate the effect of breathing condition by acquiring MRE in end expiration and end inspiration in 19 healthy volunteers. A gravitational transducer operating at 50Hz was used, which yielded a satisfactory repeatability. Storage modulus values were significantly higher at end inspiration than at end expiration, and the amplitude of the difference was significantly correlated to the end inspiration storage modulus values.

Background

Although magnetic resonance elastography (MRE) is widely accepted as useful in the diagnosis of liver fibrosis, the mechanical properties of the liver are known to be influenced by a variety of factors besides the collagen content of the tissue. Portal hypertension and chronic hepatic congestion are known to increase the apparent stiffness[1-3]. Post-prandial stiffness has been reported to increase relative to normal state[4]. Finally, the effect of breathing conditions at MRE is not extensively studied. However, the change in position of the diaphragm and visceral organs that occurs between the two extreme positions of end inspiration and end expiration, and more importantly the corresponding effect on hepatic venous blood flow could potentially modify the mechanical properties of the liver[5]. In this work, we propose to evaluate the repeatability of a novel type of mechanical actuation in MRE, and to apply this mode of actuation for studying the variation in mechanical properties between inspiration and expiration breath hold mode in volunteers with healthy livers.

Methods

This investigational clinical study was approved by the appropriate ethics committee, and informed consent was obtained from each participant. Recruitment was done on the basis of prescription of an MRI examination with absence of known hepatic disease. Acquisition was performed on a 3.0T Philips Ingenia system equipped with 80mT/m gradients. MR elastography data were acquired with the “eXpresso” sequence, consisting of a fractionally encoded gradient echo sequence[6]. Mechanical actuation was performed at a frequency of 50Hz with a gravitational transducer [7]. Acquisitions were carried out at an isotropic spatial resolution of 4mm. An echo time of 6.91ms (third in phase condition between water and fat) was chosen to maximize signal and prevent water-fat shift artifacts. Repetition time was 85ms, and flip angle was 20°. Eight slices were acquired with 4 temporal steps along the mechanical cycle in a single breath hold. Encoding was performed sequentially in three orthogonal directions, followed by an acquisition without motion encoding (unbalanced four-points encoding)[8], for a total scan duration of 4 breath holds. Storage modulus was calculated by inverting the Helmholtz wave equation using the rotational of the unwrapped phase images. Patients were instructed to hold their breath either at end inspiration or end expiration. The acquisition in inspiration was repeated twice for a repeatability assessment. Additionally in two patients the acquisition at expiration could also be acquired twice, in which cases the datasets were also added in the repeatability study.

Results

Seventeen patients were recruited. An average storage modulus (G’) of 1.80 ± 0.28kPa was obtained during the first repeatability scan, and the average value was 1.86 ± 0.33 during the second repeatability scan. No significant difference was found between the two repeatability scans with the Mann-Whitney test. Bland-Altman analysis of the repeatability study indicated a 95% limits of agreement interval of [-15% -9%], with a negligible bias of -2.7 ± 6.3%. Mechanical properties were found to increase from expiration to inspiration. Indeed, average expiration G’ values were 1.47 ± 0.27kPa, while in inspiration those reached 1.94 ± 0.41 kPa (Mann-Whitney p=0.0002), amounting to a difference of 0.49 ± 0.35 kPa between expiration and inspiration (significantly different from zero, p < 0.0001). The extent of the difference between inspiration and expiration breath hold storage moduli was found to be significantly correlated with the the storage modulus at inspiration (Spearman r = 0.64, p = 0.0035).

Conclusions

These results indicate that the storage modulus at MRE can precisely be estimated in the liver using a gravitational transducer. We observed a significant effect of respiration on the storage modulus of the liver. Mechanical properties were higher at end inspiration than at end expiration, and the increase in storage modulus was higher in individuals with high storage modulus at inspiration. This effect could potentially be caused by decreased liver congestion in blocked expiration, similar to the observation during Valsalva maneuver[9]. The use of breath hold mode may be useful in manipulating the mechanical properties via a modulation in intrahepatic pressure.

Acknowledgements

This project has received funding from the European Union’s Horizon 2020 research and Innovation programme under grant agreement No 668039

References

1. Sun, H.Y., et al., Usefulness of MR elastography for predicting esophageal varices in cirrhotic patients. J Magn Reson Imaging, 2014. 39(3): p. 559-66.

2. Gharib, A.M., et al., Magnetic Resonance Elastography Shear Wave Velocity Correlates with Liver Fibrosis and Hepatic Venous Pressure Gradient in Adults with Advanced Liver Disease. Biomed Res Int, 2017. 2017: p. 2067479.

3. Simonetto, D.A., et al., Chronic passive venous congestion drives hepatic fibrogenesis via sinusoidal thrombosis and mechanical forces. Hepatology, 2015. 61(2): p. 648-59.

4. Jajamovich, G.H., et al., Quantitative liver MRI combining phase contrast imaging, elastography, and DWI: assessment of reproducibility and postprandial effect at 3.0 T. PLoS One, 2014. 9(5): p. e97355.

5. Ipek-Ugay, S., et al., Physiologic Reduction of Hepatic Venous Blood Flow by the Valsalva Maneuver Decreases Liver Stiffness. J Ultrasound Med, 2017. 36(7): p. 1305-1311.

6. Garteiser, P., et al., Rapid acquisition of multifrequency, multislice and multidirectional MR elastography data with a fractionally encoded gradient echo sequence. NMR Biomed, 2013. 26(10): p. 1326-35.

7. Runge, J., et al. Abstract 1369: A novel MR Elastography transducer concept based on a rotational eccentric mass: the gravitational transducer. in Proceedings of the 2017 International Society of Magnetic Resonance in Medicine conference. 2017. Honolulu, USA.

8. Guenthner, C., et al., Analysis and improvement of motion encoding in magnetic resonance elastography. NMR Biomed, 2018. 31(5): p. e3908.

9. Bang, D.H., et al., Doppler ultrasonography measurement of hepatic hemodynamics during Valsalva maneuver: healthy volunteer study. Ultrasonography, 2015. 34(1): p. 32-8.


Figures

Bland-Altman plot for the measurement of storage modulus using the gravitational transducer. No important bias was found, and the agreement between both measurements was good overall.

Plot of the storage modulus values, paired by volunteer, in end inspiration (left) or end expiration (right). A significantly higher value is obtained in end-inspiration.

Correlation between the difference in storage modulus (storage modulus at end inspiration - storage modulus at end expiration) and the end inspiration value of the storage modulus. A significant correlation is observed.

Proc. Intl. Soc. Mag. Reson. Med. 27 (2019)
3970