Skip to main content
SpringerLink
Log in

Assessment of liver T1 mapping in fontan patients and its correlation with magnetic resonance elastography-derived liver stiffness

  • Hepatobiliary
  • Published:
Abdominal Radiology Aims and scope Submit manuscript

Abstract

Objectives

To explore the utility of liver T1 mapping in Fontan patients and its correlation to magnetic resonance elastography (MRE)-derived liver stiffness.

Background and aims

Liver disease is a major long-term extra cardiac complication in the Fontan population. MRE is frequently used to quantify liver stiffness in Fontan patients; however, it has certain limitations. Native T1 mapping by cardiac magnetic resonance (CMR) is useful in assessment of cardiac fibrosis, but its potential in evaluating liver fibrosis and its correlation to MRE-derived liver stiffness in Fontan patients have not been reported.

Methods

Fontan patients who underwent CMR and MRE were included. Liver Native T1, extracellular volume (ECV) and delta coefficients were measured and correlated with MRE-derived liver stiffness in all Fontan patients. Native liver T1 in Fontan patients were compared to normal controls with biventricular circulation and no known liver disease.

Results

A total of 17 Fontan patients and 7 normal controls were included in this study. Fontan patients had significantly higher liver native T1 (690 ± 41 ms vs 620 ± 35 ms; p < 0.001) as compared to controls. There was strong positive correlation between MRE derived liver stiffness and liver native T1 (r = 0.81, p < 0.001).

Conclusions

Liver native T1 was significantly elevated in Fontan patients compared to controls and strongly correlated with MRE-derived liver stiffness. This technique may prove to be a useful noninvasive imaging biomarker for assessing liver fibrosis in the Fontan population.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Daniels CJ, Bradley EA, Landzberg MJ, et al. Fontan-Associated Liver Disease: Proceedings from the American College of Cardiology Stakeholders Meeting, October 1 to 2, 2015, Washington DC. Journal of the American College of Cardiology. 2017;70(25):3173-94.

    Article  PubMed  Google Scholar 

  2. van Nieuwenhuizen RC, Peters M, Lubbers LJ, Trip MD, Tijssen JG, Mulder BJ. Abnormalities in liver function and coagulation profile following the Fontan procedure. Heart (British Cardiac Society). 1999;82(1):40-6.

    Google Scholar 

  3. Rychik J, Veldtman G, Rand E, et al. The precarious state of the liver after a Fontan operation: summary of a multidisciplinary symposium. Pediatric cardiology. 2012;33(7):1001-12.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Greenway SC, Crossland DS, Hudson M, et al. Fontan-associated liver disease: Implications for heart transplantation. J Heart Lung Transplant. 2016;35(1):26-33.

    Article  PubMed  Google Scholar 

  5. Guha IN, Bokhandi S, Ahmad Z, et al. Structural and functional uncoupling of liver performance in the Fontan circulation. International journal of cardiology. 2013;164(1):77-81.

    Article  PubMed  Google Scholar 

  6. Tomita H, Yamada O, Ohuchi H, et al. Coagulation profile, hepatic function, and hemodynamics following Fontan-type operations. Cardiology in the young. 2001;11(1):62-6.

    Article  CAS  PubMed  Google Scholar 

  7. Fidai A, Dallaire F, Alvarez N, et al. Non-invasive Investigations for the Diagnosis of Fontan-Associated Liver Disease in Pediatric and Adult Fontan Patients. Front Cardiovasc Med. 2017;4:15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Ghaferi AA, Hutchins GM. Progression of liver pathology in patients undergoing the Fontan procedure: Chronic passive congestion, cardiac cirrhosis, hepatic adenoma, and hepatocellular carcinoma. The Journal of thoracic and cardiovascular surgery. 2005;129(6):1348-52.

    Article  PubMed  Google Scholar 

  9. Bryant T, Ahmad Z, Millward-Sadler H, et al. Arterialised hepatic nodules in the Fontan circulation: hepatico-cardiac interactions. International journal of cardiology. 2011;151(3):268-72.

    Article  PubMed  Google Scholar 

  10. Elder RW, McCabe NM, Hebson C, et al. Features of portal hypertension are associated with major adverse events in Fontan patients: the VAST study. International journal of cardiology. 2013;168(4):3764-9.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Assenza GE, Graham DA, Landzberg MJ, et al. MELD-XI score and cardiac mortality or transplantation in patients after Fontan surgery. Heart (British Cardiac Society). 2013;99(7):491-6.

    Google Scholar 

  12. Cromme-Dijkhuis AH, Hess J, Hahlen K, et al. Specific sequelae after Fontan operation at mid- and long-term follow-up. Arrhythmia, liver dysfunction, and coagulation disorders. The Journal of thoracic and cardiovascular surgery. 1993;106(6):1126-32.

  13. Goldberg DJ, Surrey LF, Glatz AC, et al. Hepatic Fibrosis Is Universal Following Fontan Operation, and Severity is Associated With Time From Surgery: A Liver Biopsy and Hemodynamic Study. Journal of the American Heart Association. 2017;6(5).

  14. Wallihan DB, Podberesky DJ, Marino BS, Sticka JS, Serai S. Relationship of MR elastography determined liver stiffness with cardiac function after Fontan palliation. Journal of magnetic resonance imaging : JMRI. 2014;40(6):1328-35.

    Article  PubMed  Google Scholar 

  15. Xanthakos SA, Podberesky DJ, Serai SD, et al. Use of magnetic resonance elastography to assess hepatic fibrosis in children with chronic liver disease. The Journal of pediatrics. 2014;164(1):186-8.

    Article  PubMed  Google Scholar 

  16. Banerjee R, Pavlides M, Tunnicliffe EM, et al. Multiparametric magnetic resonance for the non-invasive diagnosis of liver disease. Journal of hepatology. 2014;60(1):69-77.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Zeng M, Zhang N, He Y, et al. Histological validation of cardiac magnetic resonance T1 mapping for detecting diffuse myocardial fibrosis in diabetic rabbits. Journal of magnetic resonance imaging : JMRI. 2016;44(5):1179-85.

    Article  PubMed  Google Scholar 

  18. Sheng RF, Wang HQ, Yang L, et al. Assessment of liver fibrosis using T1 mapping on Gd-EOB-DTPA-enhanced magnetic resonance. Dig Liver Dis. 2017;49(7):789-95.

    Article  CAS  PubMed  Google Scholar 

  19. Yoon JH, Lee JM, Paek M, Han JK, Choi BI. Quantitative assessment of hepatic function: modified look-locker inversion recovery (MOLLI) sequence for T1 mapping on Gd-EOB-DTPA-enhanced liver MR imaging. Eur Radiol. 2016;26(6):1775-82.

    Article  PubMed  Google Scholar 

  20. Haimerl M, Verloh N, Zeman F, et al. Assessment of clinical signs of liver cirrhosis using T1 mapping on Gd-EOB-DTPA-enhanced 3T MRI. PLoS One. 2013;8(12):e85658.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Messroghli DR, Greiser A, Frohlich M, Dietz R, Schulz-Menger J. Optimization and validation of a fully-integrated pulse sequence for modified look-locker inversion-recovery (MOLLI) T1 mapping of the heart. Journal of magnetic resonance imaging : JMRI. 2007;26(4):1081-6.

    Article  PubMed  Google Scholar 

  22. Messroghli DR, Radjenovic A, Kozerke S, Higgins DM, Sivananthan MU, Ridgway JP. Modified Look-Locker inversion recovery (MOLLI) for high-resolution T1 mapping of the heart. Magn Reson Med. 2004;52(1):141-6.

    Article  PubMed  Google Scholar 

  23. Serai SD, Wallihan DB, Venkatesh SK, et al. Magnetic resonance elastography of the liver in patients status-post fontan procedure: feasibility and preliminary results. Congenital heart disease. 2014;9(1):7-14.

    Article  PubMed  Google Scholar 

  24. Poterucha JT, Johnson JN, Qureshi MY, et al. Magnetic Resonance Elastography: A Novel Technique for the Detection of Hepatic Fibrosis and Hepatocellular Carcinoma After the Fontan Operation. Mayo Clin Proc. 2015;90(7):882-94.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Serai SD, Trout AT, Miethke A, Diaz E, Xanthakos SA, Dillman JR. Putting it all together: established and emerging MRI techniques for detecting and measuring liver fibrosis. Pediatric radiology. 2018;48(9):1256-72.

    Article  PubMed  Google Scholar 

  26. Serai SD, Trout AT, Sirlin CB. Elastography to assess the stage of liver fibrosis in children: Concepts, opportunities, and challenges. Clinical Liver Disease. 2017;9(1):5-10.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Serai SD, Towbin AJ, Podberesky DJ. Pediatric liver MR elastography. Digestive diseases and sciences. 2012;57(10):2713-9.

    Article  PubMed  Google Scholar 

  28. Messroghli DR, Moon JC, Ferreira VM, et al. Clinical recommendations for cardiovascular magnetic resonance mapping of T1, T2, T2* and extracellular volume: A consensus statement by the Society for Cardiovascular Magnetic Resonance (SCMR) endorsed by the European Association for Cardiovascular Imaging (EACVI). Journal of cardiovascular magnetic resonance : official journal of the Society for Cardiovascular Magnetic Resonance. 2017;19(1):75.

    Article  Google Scholar 

  29. Moon JC, Messroghli DR, Kellman P, et al. Myocardial T1 mapping and extracellular volume quantification: a Society for Cardiovascular Magnetic Resonance (SCMR) and CMR Working Group of the European Society of Cardiology consensus statement. Journal of cardiovascular magnetic resonance : official journal of the Society for Cardiovascular Magnetic Resonance. 2013;15:92.

    Article  Google Scholar 

  30. Li Z, Sun J, Hu X, et al. Assessment of liver fibrosis by variable flip angle T1 mapping at 3.0T. Journal of magnetic resonance imaging : JMRI. 2016;43(3):698-703.

  31. Kutty SS, Zhang M, Danford DA, et al. Hepatic stiffness in the bidirectional cavopulmonary circulation: The Liver Adult-Pediatric-Congenital-Heart-Disease Dysfunction Study group. The Journal of thoracic and cardiovascular surgery. 2016;151(3):678-84.

    Article  PubMed  Google Scholar 

Download references

Author information

Author notes

    Authors and Affiliations

    1. Division of Pediatric Cardiology, University of Kentucky, Lexington, KY, 40506, USA

      Preeti Ramachandran

    2. Department of Radiology, Children’s Hospital of Philadelphia, 3401 Civic Center Blvd, Philadelphia, PA, 19104, USA

      Suraj D. Serai

    3. Pediatric Cardiology, Cincinnati Children’s Hospital, 3333 Burnet Avenue, Cincinnati, OH, 45229, USA

      Gruschen R. Veldtman, Sean M. Lang, Tarek Alsaied & Ryan A. Moore

    4. Department of Cardiology, The Christ Hospital, 2123 Auburn Ave, Cincinnati, OH, 45219, USA

      Wojciech Mazur

    5. Department of Radiology, Cincinnati Children’s Hospital, 3333 Burnet Avenue, Cincinnati, OH, 45229, USA

      Andrew T. Trout, Jonathan R. Dillman & Robert J. Fleck

    6. Pediatric Cardiology, Children’s Healthcare of Atlanta, 1405 Clifton Rd. NE, Atlanta, GA, 30322, USA

      Michael D. Taylor

    Authors
    1. Preeti Ramachandran
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Suraj D. Serai
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Gruschen R. Veldtman
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Sean M. Lang
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Wojciech Mazur
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Andrew T. Trout
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Jonathan R. Dillman
      View author publications

      You can also search for this author in PubMed Google Scholar

    8. Robert J. Fleck
      View author publications

      You can also search for this author in PubMed Google Scholar

    9. Michael D. Taylor
      View author publications

      You can also search for this author in PubMed Google Scholar

    10. Tarek Alsaied
      View author publications

      You can also search for this author in PubMed Google Scholar

    11. Ryan A. Moore
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Suraj D. Serai.

    Additional information

    Publisher's Note

    Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

    Preeti Ramachandran and Suraj D. Serai have contributed equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Ramachandran, P., Serai, S.D., Veldtman, G.R. et al. Assessment of liver T1 mapping in fontan patients and its correlation with magnetic resonance elastography-derived liver stiffness. Abdom Radiol 44, 2403–2408 (2019). https://doi.org/10.1007/s00261-019-01990-9

    Download citation

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00261-019-01990-9

    Keywords

    Search

    Navigation