Skip to main content
Log in

T1 mapping of the myocardium and liver in the single ventricle population

  • Original Article
  • Published:
Pediatric Radiology Aims and scope Submit manuscript

Abstract

Background

Fontan associated liver disease (FALD) is an increasingly recognized complication of the single ventricle circulation characterized by hepatic venous congestion leading to hepatic fibrosis. Within the Fontan myocardium, fibrotic myocardial remodeling may occur and lead to ventricular dysfunction. Magnetic resonance imaging (MRI) T1 mapping can characterize both myocardial and liver properties.

Objective

The aim of this study was to compare myocardial and liver T1 between single ventricle patients with and without a Fontan and biventricular controls.

Materials and methods

A retrospective study of 3 groups of patients: 16 single ventricle patients before Fontan (SVpre 2 newborns, 9 pre-Glenn, 5 pre-Fontan, 31% single right ventricle [SRV]), 16 Fontans (56% SRV) and 10 repaired d-transposition of the great arteries (TGA). Native modified Look-Locker inversion T1 times were measured in the myocardium and liver. Cardiac MRI parameters, myocardial and liver T1 values were compared in the three groups. Correlations were assessed between liver T1 and cardiac parameters.

Results

Myocardial T1 was higher in SVpre (1,056 ± 48 ms) and Fontans (1,047 ± 41 ms) compared to TGA (1,012 ± 48 ms, P < 0.05). Increased liver T1 was found in both SVpre (683 ± 82 ms) and Fontan (727 ± 49 ms) patients compared to TGA patients (587 ± 58 ms, P < 0.001). There was no difference between single left ventricle (SLV) versus SRV myocardial or liver T1. Liver T1 showed moderate correlations with myocardial T1 (r = 0.48, confidence interval [CI] 0.26–0.72) and ejection fraction (r = -0.36, CI -0.66–0.95) but not with other volumetric parameters.

Conclusion

Increased liver T1 at both pre- and post-Fontan stages suggests there are intrinsic liver abnormalities early in the course of single ventricle palliation. Increased myocardial T1 and its relationship to liver T1 suggest a combination of edema from passive venous congestion and/or myocardial fibrosis occurring in this population. Liver T1 may provide an earlier marker of liver disease warranting further study.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Cetta F, Driscoll DJ (1997) The Fontan operation: what is it and what is its future? Cardiol Rev 5:98–104

    Article  Google Scholar 

  2. Pudi KN, Johnson JN, Dearani JA et al (2015) 40-year follow-up after the Fontan operation: long-term outcomes of 1,052 patients. J Am Coll Cardiol 66:1700–1710

    Article  Google Scholar 

  3. Daniels CJ, Bradley EA, Landzberg MJ et al (2017) Fontan-associated liver disease: proceedings from the American College of Cardiology Stakeholders Meeting, October 1 to 2, 2015, Washington DC. J Am Coll Cardiol 70:3173–3194

    Article  PubMed  Google Scholar 

  4. Hilscher MB, Wells ML, Venkatesh SK et al (2022) Fontan-associated liver disease. Hepatology 75:1300–1321

    Article  PubMed  Google Scholar 

  5. Camposilvan S, Milanesi O, Stellin G et al (2008) Liver and cardiac function in the long term after Fontan operation. Ann Thorac Surg 86:177–182

    Article  PubMed  Google Scholar 

  6. Ghaferi AA, Hutchins GM (2005) Progression of liver pathology in patients undergoing the Fontan procedure: chronic passive congestion, cardiac cirrhosis, hepatic adenoma, and hepatocellular carcinoma. J Thorac Cardiovasc Surg 129:1348–1352

    Article  PubMed  Google Scholar 

  7. Wallihan DB, Podberesky DJ, Marino BS et al (2014) Relationship of MR elastography determined liver stiffness with cardiac function after Fontan palliation. J Magn Reson Imaging 40:1328–1335

    Article  PubMed  Google Scholar 

  8. Rychik J, Veldtman G, Rand E et al (2012) The precarious state of the liver after a Fontan operation: summary of a multidisciplinary symposium. Pediatr Cardiol 33:1001–1012

    Article  PubMed  PubMed Central  Google Scholar 

  9. Friedrich-Rust M, Koch C, Rentzsch A et al (2008) Noninvasive assessment of liver fibrosis in patients with Fontan circulation using transient elastography and biochemical fibrosis markers. J Thorac Cardiovasc Surg 135:560–567

    Article  PubMed  Google Scholar 

  10. Serai SD, Towbin AJ, Podberesky DJ (2012) Pediatric liver MR elastography. Dig Dis Sci 57:2713–2719

    Article  PubMed  Google Scholar 

  11. Child N, Suna G, Dabir D et al (2016) T1 mapping in characterizing myocardial disease: a comprehensive review. Circ Res 119:277–299

    Article  Google Scholar 

  12. Child N, Suna G, Dabir D et al (2018) Comparison of MOLLI, shMOLLLI, and SASHA in discrimination between health and disease and relationship with histologically derived collagen volume fraction. Eur Heart J Cardiovasc Imaging 19:768–776

    Article  PubMed  Google Scholar 

  13. Chow AM, Gao DS, Fan SJ et al (2012) Measurement of liver T(1) and T(2) relaxation times in an experimental mouse model of liver fibrosis. J Magn Reson Imaging 36:152–158

    Article  PubMed  Google Scholar 

  14. Kazour I, Serai SD, Xanthakos SA, Fleck RJ (2018) Using T1 mapping in cardiovascular magnetic resonance to assess congestive hepatopathy. Abdom Radiol (NY) 43:2679–2685

    Article  PubMed  Google Scholar 

  15. Gilligan LA, Dillman JR, Tkach JA et al (2019) Magnetic resonance imaging T1 relaxation times for the liver, pancreas and spleen in healthy children at 1.5 and 3 Tesla. Pediatr Radiol 49:1018–1024

    Article  PubMed  Google Scholar 

  16. Hoffman DH, Ayoola A, Nickel D et al (2020) T1 mapping, T2 mapping and MR elastography of the liver for detection and staging of liver fibrosis. Abdom Radiol (NY) 45:692–700

    Article  PubMed  Google Scholar 

  17. Pagano JJ, Yim D, Lam CZ et al (2020) Normative data for myocardial native T1 and extracellular volume fraction in children. Radiol Cardiothorac Imaging 2:e190234

    Article  PubMed  PubMed Central  Google Scholar 

  18. de Lange C, Reichert MJE, Pagano JJ et al (2019) Increased extracellular volume in the liver of pediatric Fontan patients. J Cardiovasc Magn Reson 21:39

    Article  PubMed  PubMed Central  Google Scholar 

  19. Ramachandran P, Serai SD, Veldtman GR et al (2019) Assessment of liver T1 mapping in Fontan patients and its correlation with magnetic resonance elastography-derived liver stiffness. Abdom Radiol (NY) 44:2403–2408

    Article  PubMed  Google Scholar 

  20. Shiina Y, Inai K, Ohashi R, Nagao M (2021) Potential of liver T1 mapping for the detection of Fontan-associated liver disease in adults. Magn Reson Med Sci 20:295–302

    Article  CAS  PubMed  Google Scholar 

  21. Schwartz MC, Glatz AC, Daniels K et al (2015) Hepatic abnormalities are present before and early after the Fontan operation. Ann Thorac Surg 100:2298–2304

    Article  PubMed  Google Scholar 

  22. Kutty SS, Zhang M, Danford DA et al (2016) Hepatic stiffness in the bidirectional cavopulmonary circulation: The Liver Adult-Pediatric-Congenital-Heart-Disease Dysfunction Study group. J Thorac Cardiovasc Surg 151:678–684

    Article  PubMed  Google Scholar 

  23. DiPaola FW, Schumacher KR, Goldberg CS et al (2017) Effect of Fontan operation on liver stiffness in children with single ventricle physiology. Eur Radiol 27:2434–2442

    Article  PubMed  Google Scholar 

  24. Khoo NS, Smallhorn JF, Kaneko S et al (2011) Novel insights into RV adaptation and function in hypoplastic left heart syndrome between the first 2 stages of surgical palliation. JACC Cardiovasc Imaging 4:128–137

    Article  PubMed  Google Scholar 

  25. Tham EB, Smallhorn JF, Kaneko S et al (2014) Insights into the evolution of myocardial dysfunction in the functionally single right ventricle between staged palliations using speckle-tracking echocardiography. J Am Soc Echocardiogr 27:314–322

    Article  PubMed  Google Scholar 

  26. Bulut OP, Romero R, Mahle WT et al (2013) Magnetic resonance imaging identifies unsuspected liver abnormalities in patients after the Fontan procedure. J Pediatr 163:201–206

    Article  PubMed  Google Scholar 

  27. Kiesewetter CH, Sheron N, Vettukattill JJ et al (2007) Hepatic changes in the failing Fontan circulation. Heart 93:579–584

    Article  PubMed  Google Scholar 

  28. Haaf P, Garg P, Messroghli DR et al (2016) Cardiac T1 mapping and extracellular volume (ECV) in clinical practice: a comprehensive review. J Cardiovasc Magn Reson 18:89

    Article  PubMed  PubMed Central  Google Scholar 

  29. Kutty SS, Peng Q, Danford DA et al (2014) Increased hepatic stiffness as consequence of high hepatic afterload in the Fontan circulation: a vascular Doppler and elastography study. Hepatology 59:251–260

    Article  PubMed  Google Scholar 

  30. Serai SD, Wallihan DB, Venkatesh SK et al (2014) Magnetic resonance elastography of the liver in patients status-post fontan procedure: feasibility and preliminary results. Congenit Heart Dis 9:7–14

    Article  PubMed  Google Scholar 

  31. Poterucha JT, Johnson JN, Qureshi MY et al (2015) magnetic resonance elastography: a novel technique for the detection of hepatic fibrosis and hepatocellular carcinoma after the Fontan operation. Mayo Clin Proc 90:882–894

    Article  PubMed  Google Scholar 

  32. Ackerman T, Geerts A, Van Vlierberghe H et al (2018) Hepatic changes in the Fontan circulation: identification of liver dysfunction and an attempt to streamline follow-up screening. Pediatr Cardiol 39:1604–1613

    Article  CAS  PubMed  Google Scholar 

  33. Egbe A, Miranda WR, Connolly HM et al (2018) Temporal changes in liver stiffness after Fontan operation: results of serial magnetic resonance elastography. Int J Cardiol 258:299–304

    Article  PubMed  Google Scholar 

  34. Melero-Ferrer JL, Osa-Sáez A, Buendía-Fuentes F et al (2014) Fontan circulation in adult patients: acoustic radiation force impulse elastography as a useful tool for liver assessment. World J Pediatr Congenit Heart Surg 5:365–371

    Article  PubMed  Google Scholar 

  35. Mak KM, Png CYM (2020) The hepatic central vein: structure, fibrosis, and role in liver biology. Anat Rec (Hoboken) 303:1747–1767

    Article  CAS  PubMed  Google Scholar 

  36. Paris J, Henderson NC (2022) Liver zonation, revisited. Hepatology 76:1219–1230

    Article  PubMed  Google Scholar 

  37. Alsaied T, Moore RA, Lang SM et al (2020) Myocardial fibrosis, diastolic dysfunction and elevated liver stiffness in the Fontan circulation. Open Heart 7:e001434

    Article  PubMed  PubMed Central  Google Scholar 

  38. Padalino MA, Castellani C, Toffoli S et al (2008) Pathological changes and myocardial remodelling related to the mode of shunting following surgical palliation for hypoplastic left heart syndrome. Cardiol Young 18:415–422

    Article  PubMed  Google Scholar 

  39. Ho SY, Jackson M, Kilpatrick L et al (1996) Fibrous matrix of ventricular myocardium in tricuspid atresia compared with normal heart. A quantitative analysis. Circulation 94:1642–1646

    Article  CAS  PubMed  Google Scholar 

  40. Rathod RH, Prakash A, Powell AJ, Geva T (2010) Myocardial fibrosis identified by cardiac magnetic resonance late gadolinium enhancement is associated with adverse ventricular mechanics and ventricular tachycardia late after Fontan operation. J Am Coll Cardiol 55:1721–1728

    Article  PubMed  PubMed Central  Google Scholar 

  41. Diaz ES, Dillman JR, Veldtman GR, Trout AT (2019) MRI measured liver stiffness does not predict focal liver lesions after the Fontan operation. Pediatr Radiol 49:99–104

    Article  PubMed  Google Scholar 

  42. Tang A, Cloutier G, Szeverenyi NM, Sirlin CB (2015) Ultrasound elastography and MR elastography for assessing liver fibrosis: part 2, diagnostic performance, confounders, and future directions. AJR Am J Roentgenol 205:33–40

    Article  PubMed  PubMed Central  Google Scholar 

  43. Kato A, Riesenkampff E, Yim D et al (2017) Pediatric Fontan patients are at risk for myocardial fibrotic remodeling and dysfunction. Int J Cardiol 240:172–177

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Authors Mirza V. R. Beigh and Kiera B. E. Pajunen contributed equally to the manuscript. We wish to thank the following people for their support and assistance in this project: research coordinators Charlene Cars and Dory Sample and our cardiac MRI techs Wendy Chu, Rebecca Gray, Melissa Grzeszczak, Kelley Justice, Kam Ma and Justine Muller.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Edythe B. Tham.

Ethics declarations

Conflicts of interest

None

Additional information

Publisher's note

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

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Beigh, M.V.R., Pajunen, K.B.E., Pagano, J.J. et al. T1 mapping of the myocardium and liver in the single ventricle population. Pediatr Radiol 53, 1092–1099 (2023). https://doi.org/10.1007/s00247-022-05560-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00247-022-05560-y

Keywords

Navigation