Abstract
Objectives
Evaluation of liver stiffness (LS) by magnetic resonance elastography (MRE) is useful for estimating right atrial pressure (RAP) in patients with heart failure (HF). However, its prognostic implications are unclear. We sought to investigate whether LS measured by MRE (LS-MRE) could predict clinical outcomes in patients with HF.
Methods
We prospectively examined 207 consecutive HF patients between April 2018 and May 2021 after excluding those with organic liver disease. All patients underwent 3.0-T MRE. The primary outcome of interest was the composite of all-cause death and hospitalisation for HF.
Results
During a median follow-up period of 720 (interquartile range [IQR] 434–1013) days, the primary outcome occurred in 44 patients (21%), including 15 (7%) all-cause deaths and 29 (14%) hospitalisations for HF. The patients were divided into two groups according to median LS-MRE of 2.54 (IQR 2.34–2.82) kPa. Patients with higher LS-MRE showed a higher incidence of the primary outcome compared to those with lower LS-MRE (p < 0.001). Multivariable Cox regression analyses revealed that LS-MRE value was independently associated with the risk of adverse events (hazard ratio 2.49, 95% confidence interval 1.46–4.24). In multivariable linear regression, RAP showed a stronger correlation with LS-MRE (β coefficient = 0.31, p < 0.001) compared to markers related to liver fibrosis.
Conclusions
In patients without chronic liver disease and presenting with HF, elevated LS-MRE was independently associated with worse clinical outcomes. Elevated LS-MRE may be useful for risk stratification in patients with HF and without chronic liver disease.
Key Points
• Magnetic resonance elastography (MRE) is an emerging non-invasive imaging technique for evaluating liver stiffness (LS) which can estimate right atrial pressure.
• Elevated LS-MRE, which mainly reflects liver congestion, was independently associated with worse clinical outcomes in patients with heart failure.
• The assessment of LS-MRE would be useful for stratifying the risk of adverse events in heart failure patients without chronic liver disease.
Similar content being viewed by others
Abbreviations
- APRI:
-
Aspartate aminotransferase to platelet ratio index
- BSA:
-
Body surface area
- C.I.:
-
Cardiac index
- CO:
-
Cardiac output
- CRT:
-
Cardiac resynchronisation therapy
- FIB-4:
-
Fibrosis 4 index
- GGT:
-
Gamma-glutamyl transpeptidase
- HF:
-
Heart failure
- ICD:
-
Implantable cardioverter defibrillator
- IQR:
-
Interquartile range
- IVC:
-
Inferior vena cava
- LA:
-
Left atrial
- LAVA:
-
Liver acquisition with volume acceleration
- LS:
-
Liver stiffness
- M2BPGi:
-
Mac-2 binding protein glycosylation isomer
- MEG:
-
Motion encoding gradient
- MRE:
-
Magnetic resonance elastography
- PA:
-
Pulmonary artery
- PCWP:
-
Pulmonary capillary wedge pressure
- P-III-P:
-
Type III procollagen N-terminal peptide
- RAP:
-
Right atrial pressure
- RHC:
-
Right heart catheterisation
- RV:
-
Right ventricular
- RVFAC:
-
Right ventricular fractional area change
- TAPSE:
-
Tricuspid annular plane systolic excursion
- VAD:
-
Ventricular assist device
- VCTE:
-
Vibration-controlled transient elastography
- VTQ:
-
Virtual touch quantification
References
Braunwald E (2013) Heart failure. JACC Heart Fail 1:1–20. https://doi.org/10.1016/j.jchf.2012.10.002
Shimokawa H, Miura M, Nochioka K, Sakata Y (2015) Heart failure as a general pandemic in Asia. Eur J Heart Fail 17:884–892. https://doi.org/10.1002/ejhf.319
Harjola VP, Mullens W, Banaszewski M et al (2017) Organ dysfunction, injury and failure in acute heart failure: from pathophysiology to diagnosis and management. A review on behalf of the Acute Heart Failure Committee of the Heart Failure Association (HFA) of the European Society of Cardiology (ESC). Eur J Heart Fail 19:821–836. https://doi.org/10.1002/ejhf.872
Damman K, van Deursen VM, Navis G, Voors AA, van Veldhuisen DJ, Hillege HL (2009) Increased central venous pressure is associated with impaired renal function and mortality in a broad spectrum of patients with cardiovascular disease. J Am Coll Cardiol 53:582–588. https://doi.org/10.1016/j.jacc.2008.08.080
Mullens W, Abrahams Z, Francis GS et al (2009) Importance of venous congestion for worsening of renal function in advanced decompensated heart failure. J Am Coll Cardiol 53:589–596. https://doi.org/10.1016/j.jacc.2008.05.068
Uthoff H, Thalhammer C, Potocki M et al (2010) Central venous pressure at emergency room presentation predicts cardiac rehospitalization in patients with decompensated heart failure. Eur J Heart Fail 12:469–476. https://doi.org/10.1093/eurjhf/hfq024
Fuster V, Steele PM, Edwards WD, Gersh BJ, McGoon MD, Frye RL (1984) Primary pulmonary hypertension: natural history and the importance of thrombosis. Circulation 70:580–587. https://doi.org/10.1161/01.cir.70.4.580
Hoeper MM, Lee SH, Voswinckel R et al (2006) Complications of right heart catheterization procedures in patients with pulmonary hypertension in experienced centers. J Am Coll Cardiol 48:2546–2552. https://doi.org/10.1016/j.jacc.2006.07.061
Merrer J, De Jonghe B, Golliot F et al (2001) Complications of femoral and subclavian venous catheterization in critically ill patients: a randomized controlled trial. JAMA 286:700–707. https://doi.org/10.1001/jama.286.6.700
Jalal Z, Iriart X, De Ledinghen V et al (2015) Liver stiffness measurements for evaluation of central venous pressure in congenital heart diseases. Heart 101:1499–1504. https://doi.org/10.1136/heartjnl-2014-307385
Castera L, Le Bail B, Roudot-Thoraval F et al (2009) Early detection in routine clinical practice of cirrhosis and oesophageal varices in chronic hepatitis C: comparison of transient elastography (FibroScan) with standard laboratory tests and non-invasive scores. J Hepatol 50:59–68. https://doi.org/10.1016/j.jhep.2008.08.018
Nightingale K, Soo MS, Nightingale R, Trahey G (2002) Acoustic radiation force impulse imaging: in vivo demonstration of clinical feasibility. Ultrasound Med Biol 28:227–235. https://doi.org/10.1016/s0301-5629(01)00499-9
Colli A, Pozzoni P, Berzuini A et al (2010) Decompensated chronic heart failure: increased liver stiffness measured by means of transient elastography. Radiology 257:872–878. https://doi.org/10.1148/radiol.10100013
Omote K, Nagai T, Asakawa N et al (2019) Impact of admission liver stiffness on long-term clinical outcomes in patients with acute decompensated heart failure. Heart Vessels 34:984–991. https://doi.org/10.1007/s00380-018-1318-y
Taniguchi T, Ohtani T, Kioka H et al (2019) Liver stiffness reflecting right-sided filling pressure can predict adverse outcomes in patients with heart failure. JACC Cardiovasc Imaging 12:955–964. https://doi.org/10.1016/j.jcmg.2017.10.022
Taniguchi T, Sakata Y, Ohtani T et al (2014) Usefulness of transient elastography for noninvasive and reliable estimation of right-sided filling pressure in heart failure. Am J Cardiol 113:552–558. https://doi.org/10.1016/j.amjcard.2013.10.018
Yoshitani T, Asakawa N, Sakakibara M et al (2016) Value of virtual touch quantification elastography for assessing liver congestion in patients with heart failure. Circ J 80:1187–1195. https://doi.org/10.1253/circj.CJ-15-1200
Bota S, Sporea I, Sirli R et al (2014) Factors associated with the impossibility to obtain reliable liver stiffness measurements by means of Acoustic Radiation Force Impulse (ARFI) elastography--analysis of a cohort of 1,031 subjects. Eur J Radiol 83:268–272. https://doi.org/10.1016/j.ejrad.2013.11.019
Castera L, Foucher J, Bernard PH et al (2010) Pitfalls of liver stiffness measurement: a 5-year prospective study of 13,369 examinations. Hepatology 51:828–835. https://doi.org/10.1002/hep.23425
Motosugi U, Ichikawa T, Sano K et al (2010) Magnetic resonance elastography of the liver: preliminary results and estimation of inter-rater reliability. Jpn J Radiol 28:623–627. https://doi.org/10.1007/s11604-010-0478-1
Singh S, Venkatesh SK, Wang Z et al (2015) Diagnostic performance of magnetic resonance elastography in staging liver fibrosis: a systematic review and meta-analysis of individual participant data. Clin Gastroenterol Hepatol 13(440-451):e446. https://doi.org/10.1016/j.cgh.2014.09.046
Wells ML, Fenstad ER, Poterucha JT et al (2016) Imaging findings of congestive hepatopathy. Radiographics 36:1024–1037. https://doi.org/10.1148/rg.2016150207
Tang A, Dzyubak B, Yin M et al (2022) MR elastography in nonalcoholic fatty liver disease: inter-center and inter-analysis-method measurement reproducibility and accuracy at 3T. Eur Radiol 32:2937–2948. https://doi.org/10.1007/s00330-021-08381-z
Zhang YN, Fowler KJ, Boehringer AS et al (2022) Comparative diagnostic performance of ultrasound shear wave elastography and magnetic resonance elastography for classifying fibrosis stage in adults with biopsy-proven nonalcoholic fatty liver disease. Eur Radiol 32:2457–2469. https://doi.org/10.1007/s00330-021-08369-9
Kato Y, Nagai T, Oyama-Manabe N et al (2020) Usefulness of liver magnetic resonance elastography for estimating right-atrial pressure in heart failure patients. JACC Cardiovasc Imaging 13:2050–2052. https://doi.org/10.1016/j.jcmg.2020.03.015
Ponikowski P, Voors AA, Anker SD et al (2016) 2016 ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure: the Task Force for the diagnosis and treatment of acute and chronic heart failure of the European Society of Cardiology (ESC)Developed with the special contribution of the Heart Failure Association (HFA) of the ESC. Eur Heart J 37:2129–2200. https://doi.org/10.1093/eurheartj/ehw128
Yancy CW, Jessup M, Bozkurt B et al (2017) 2017 ACC/AHA/HFSA Focused update of the 2013 ACCF/AHA guideline for the management of heart failure: a report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines and the Heart Failure Society of America. Circulation 136:e137–e161. https://doi.org/10.1161/CIR.0000000000000509
Lang RM, Badano LP, Mor-Avi V et al (2015) Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr 28(1-39):e14. https://doi.org/10.1016/j.echo.2014.10.003
Koda M, Matunaga Y, Kawakami M, Kishimoto Y, Suou T, Murawaki Y (2007) FibroIndex, a practical index for predicting significant fibrosis in patients with chronic hepatitis C. Hepatology 45:297–306. https://doi.org/10.1002/hep.21520
Wai CT, Greenson JK, Fontana RJ et al (2003) A simple noninvasive index can predict both significant fibrosis and cirrhosis in patients with chronic hepatitis C. Hepatology 38:518–526. https://doi.org/10.1053/jhep.2003.50346
Xiao G, Yang J, Yan L (2015) Comparison of diagnostic accuracy of aspartate aminotransferase to platelet ratio index and fibrosis-4 index for detecting liver fibrosis in adult patients with chronic hepatitis B virus infection: a systemic review and meta-analysis. Hepatology 61:292–302. https://doi.org/10.1002/hep.27382
Xu H, Kong W, Liu L et al (2017) Accuracy of M2BPGi, compared with Fibro Scan(R), in analysis of liver fibrosis in patients with hepatitis C. BMC Gastroenterol 17:62. https://doi.org/10.1186/s12876-017-0618-5
Yoneda M, Mawatari H, Fujita K et al (2007) Type IV collagen 7s domain is an independent clinical marker of the severity of fibrosis in patients with nonalcoholic steatohepatitis before the cirrhotic stage. J Gastroenterol 42:375–381. https://doi.org/10.1007/s00535-007-2014-3
Bekheirnia MR, Schrier RW (2006) Pathophysiology of water and sodium retention: edematous states with normal kidney function. Curr Opin Pharmacol 6:202–207. https://doi.org/10.1016/j.coph.2005.09.008
Millonig G, Friedrich S, Adolf S et al (2010) Liver stiffness is directly influenced by central venous pressure. J Hepatol 52:206–210. https://doi.org/10.1016/j.jhep.2009.11.018
Lemmer A, VanWagner LB, Ganger D (2018) Assessment of advanced liver fibrosis and the risk for hepatic decompensation in patients with congestive hepatopathy. Hepatology 68:1633–1641. https://doi.org/10.1002/hep.30048
Bedossa P (1994) Intraobserver and interobserver variations in liver biopsy interpretation in patients with chronic hepatitis C. The French METAVIR Cooperative Study Group. Hepatology 20:15–20. https://doi.org/10.1002/hep.1840200104
Bedossa P, Poynard T (1996) An algorithm for the grading of activity in chronic hepatitis C. The METAVIR Cooperative Study Group. Hepatology 24:289–293. https://doi.org/10.1002/hep.510240201
Yoshimitsu K, Mitsufuji T, Shinagawa Y et al (2016) MR elastography of the liver at 3.0 T in diagnosing liver fibrosis grades; preliminary clinical experience. Eur Radiol 26:656–663. https://doi.org/10.1007/s00330-015-3863-4
Ichikawa S, Motosugi U, Morisaka H et al (2015) Comparison of the diagnostic accuracies of magnetic resonance elastography and transient elastography for hepatic fibrosis. Magn Reson Imaging 33:26–30. https://doi.org/10.1016/j.mri.2014.10.003
Acknowledgements
The authors are grateful to Kinya Ishizaka for his support with analysis of MRE imaging findings.
Funding
This study has received funding from grants from the Japan Society for the Promotion of Science, Tokyo, Japan (KAKENHI no. 18K08122, Dr. Nagai), the Takeda Science Foundation (Dr. Nagai), and a Bayer Scholarship for Cardiovascular Research, the Japan Cardiovascular Research Foundation (Dr. Nagai).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Guarantor
The scientific guarantor of this publication is Toshiyuki Nagai.
Conflict of interest
The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.
Statistics and biometry
Michikazu Nakai kindly provided statistical advice for this manuscript.
Informed consent
Written informed consent was obtained from all subjects (patients) in this study.
Ethical approval
Institutional Review Board approval was obtained.
Methodology
• prospective
• observational
• performed at one institution
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 67 kb)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Tada, A., Nagai, T., Kato, Y. et al. Liver stiffness assessed by magnetic resonance elastography predicts clinical outcomes in patients with heart failure and without chronic liver disease. Eur Radiol 33, 2062–2074 (2023). https://doi.org/10.1007/s00330-022-09209-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00330-022-09209-0