Advertisement

Relation of Magnetic Resonance Elastography to Fontan Failure and Portal Hypertension

      Fontan associated liver disease is associated with morbidity and mortality in palliated single-ventricle congenital heart disease patients. Magnetic resonance elastography (MRE) provides a quantitative assessment of liver stiffness in Fontan patients. We hypothesized that MRE liver stiffness correlates with liver enzymes, hemodynamics, portal hypertension, and Fontan failure (FF). All adult Fontan patients who had MRE between 2011 and 2018 were included. Radiologic portal hypertension was defined as splenomegaly, ascites, and/or varices. FF was defined as death, transplantation, or heart failure symptoms requiring escalation of diuretics. Seventy patients with a median age of 24.7 years and a median follow-up from MRE of 3.9 years were included. The median liver stiffness was 4.3 kPa (interquartile range [IQR]: 3.8 to 5.0 kPa). There was a weak, positive correlation between liver stiffness and Fontan pathway pressure (r = 0.34, p = 0.03). There was a moderate negative correlation of liver stiffness with ventricular ejection fraction (r = −0.52, p = 0.03). Liver stiffness was weakly positively correlated with liver transaminases and gamma glutamyl transferase. Patients with portal hypertension had higher liver stiffness compared to patients without (5.2 ± 1.3 vs 4.2 ± 0.8 kPa, p = 0.03). At MRE or during follow-up, 13 patients (19%) met definition of FF and had significantly higher liver stiffness compared to patients without FF (5.1 [IQR: 4.3 to 6.3] vs 4.2 [IQR: 3.7 to 4.7] kPa, p = 0.01). Liver stiffness above 4.5 kPa differentiated FF with a sensitivity of 77% and specificity of 77%. In conclusion, elevated MRE-derived liver stiffness is associated with worse hemodynamics, liver enzymes and clinical outcomes in Fontan patients. This measure may serve as a global imaging biomarker of Fontan health.
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to American Journal of Cardiology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Daniels CJ
        • Bradley EA
        • Landzberg MJ
        • Aboulhosn J
        • Beekman RH
        • 3rd Book W
        • Gurvitz M
        • John A
        • John B
        • Marelli A
        • Marino BS
        • Minich LL
        • Poterucha JJ
        • Rand EB
        • Veldtman GR
        Fontan-associated liver disease: proceedings from the American College of Cardiology stakeholders meeting, October 1 to 2, 2015, Washington DC.
        J Am Coll Cardiol. 2017; 70: 3173-3194
        • Alsaied T
        • Bokma JP
        • Engel ME
        • Kuijpers JM
        • Hanke SP
        • Zuhlke L
        • Zhang B
        • Veldtman GR
        Factors associated with long-term mortality after Fontan procedures: a systematic review.
        Heart. 2017; 103: 104-110
        • Book WM
        • Gerardin J
        • Saraf A
        • Marie Valente A
        • Rodriguez 3rd., F
        Clinical phenotypes of Fontan failure: implications for management.
        Congenit Heart Dis. 2016; 11: 296-308
        • Gordon-Walker TT
        • Bove K
        • Veldtman G
        Fontan-associated liver disease: a review.
        J Cardiol. 2019; 74: 223-232https://doi.org/10.1016/j.jjcc.2019.02.016
        • Kiesewetter CH
        • Sheron N
        • Vettukattill JJ
        • Hacking N
        • Stedman B
        • Millward-Sadler H
        • Haw M
        • Cope R
        • Salmon AP
        • Sivaprakasam MC
        • Kendall T
        • Keeton BR
        • Iredale JP
        • Veldtman GR
        Hepatic changes in the failing Fontan circulation.
        Heart (British Cardiac Society). 2007; 93: 579-584
        • Bradley E
        • Hendrickson B
        • Daniels C
        Fontan liver disease: review of an emerging epidemic and management options.
        Curr Treat Options Cardiovasc Med. 2015; 17: 51
        • Rychik J
        • Goldberg D
        • Rand E
        • Semeao E
        • Russo P
        • Dori Y
        • Dodds K
        End-organ consequences of the Fontan operation: liver fibrosis, protein-losing enteropathy and plastic bronchitis.
        Cardiol Young. 2013; 23: 831-840
        • Munsterman ID
        • Duijnhouwer AL
        • Kendall TJ
        • Bronkhorst CM
        • Ronot M
        • van Wettere M
        • van Dijk APJ
        • Drenth JPH
        • Tjwa E
        • Nijmegen Fontan I
        The clinical spectrum of Fontan-associated liver disease: results from a prospective multimodality screening cohort.
        Eur Heart J. 2019; 40: 1057-1068
        • Silva-Sepulveda JA
        • Fonseca Y
        • Vodkin I
        • Vaughn G
        • Newbury R
        • Vavinskaya V
        • Dwek J
        • Perry JC
        • Reshamwala P
        • Baehling C
        • Lyon J
        • Davis C
        • Lee JW
        • El-Sabrout H
        • Shahbah D
        • Alshawabkeh L
        • Moore JW
        • El-Said H
        Evaluation of Fontan liver disease: correlation of transjugular liver biopsy with magnetic resonance and hemodynamics.
        Cong Heart Dis. 2019; 14: 600-608https://doi.org/10.1111/chd.1277
        • Srinivasan A
        • Guzman AK
        • Rand EB
        • Rychik J
        • Goldberg DJ
        • Russo PA
        • Cahill AM
        Percutaneous liver biopsy in Fontan patients.
        Pediatr Radiol. 2019; 49: 342-350
        • Ramachandran P
        • Serai SD
        • Veldtman GR
        • Lang SM
        • Mazur W
        • Trout AT
        • Dillman JR
        • Fleck RJ
        • Taylor MD
        • Alsaied T
        • Moore RA
        Assessment of liver T1 mapping in fontan patients and its correlation with magnetic resonance elastography-derived liver stiffness.
        Abdom Radiol (NY). 2019;
        • Evans WN
        • Acherman RJ
        • Ciccolo ML
        • Carrillo SA
        • Galindo A
        • Rothman A
        • Mayman GA
        • Adams EA
        • Reardon LC
        • Winn BJ
        • Yumiaco NS
        • Shimuizu L
        • Inanaga Y
        • Deleon RJ
        • Restrepo H
        A composite noninvasive index correlates with liver fibrosis scores in post-Fontan patients: preliminary findings.
        Cong Heart Dis. 2018; 13: 38-45
        • Surrey LF
        • Russo P
        • Rychik J
        • Goldberg DJ
        • Dodds K
        • O'Byrne ML
        • Glatz AC
        • Rand EB
        • Lin HC
        Defining the role of liver biopsy in the assessment of liver fibrosis in patients with Fontan circulation-reply.
        Human Path. 2017; 69: 141
        • Wallihan DB
        • Podberesky DJ
        • Marino BS
        • Sticka JS
        • Serai S
        Relationship of MR elastography determined liver stiffness with cardiac function after Fontan palliation.
        J Magn Reson Imaging. 2014; 40: 1328-1335
        • Ackerman T
        • Geerts A
        • Van Vlierberghe H
        • De Backer J
        • Francois K
        Hepatic changes in the Fontan circulation: identification of liver dysfunction and an attempt to streamline follow-up screening.
        Pediatr Cardiol. 2018; 39: 1604-1613
        • Egbe AC
        • Connolly HM
        • Miranda WR
        • Ammash NM
        • Hagler DJ
        • Veldtman GR
        • Borlaug BA
        Hemodynamics of Fontan failure: the role of pulmonary vascular disease.
        Circ Heart Fail. 2017; : 10
        • Jahangiri M
        • Kreutzer J
        • Zurakowski D
        • Bacha E
        • Jonas RA
        Evaluation of hemostatic and coagulation factor abnormalities in patients undergoing the Fontan operation.
        J Thoracic Cardiovasc Surg. 2000; 120: 778-782
        • Wagener G
        • Diaz G
        • Guarrera JV
        • Minhaz M
        • Renz JF
        • Sladen RN
        Protein C activity and postoperative metabolic liver function after liver transplantation.
        Transplant Proc. 2012; 44: 1336-1340
        • Kim YS
        • Jang YN
        • Song JS
        Comparison of gradient-recalled echo and spin-echo echo-planar imaging MR elastography in staging liver fibrosis: a meta-analysis.
        Eur Radiol. 2018; 28: 1709-1718
        • Diaz ES
        • Dillman JR
        • Veldtman GR
        • Trout AT
        MRI measured liver stiffness does not predict focal liver lesions after the Fontan operation.
        Pediatr Radiol. 2019; 49: 99-104
        • Serai SD
        • Dillman JR
        • Trout AT
        Spin-echo echo-planar imaging MR elastography versus gradient-echo MR elastography for assessment of liver stiffness in children and young adults suspected of having liver disease.
        Radiology. 2017; 282: 761-770
        • Egbe A
        • Miranda WR
        • Connolly HM
        • Khan AR
        • Al-Otaibi M
        • Venkatesh SK
        • Simonetto D
        • Kamath P
        • Warnes C
        Temporal changes in liver stiffness after Fontan operation: results of serial magnetic resonance elastography.
        Int J Cardiol. 2018; 258: 299-304
        • Wu FM
        • Opotowsky AR
        • Raza R
        • Harney S
        • Ukomadu C
        • Landzberg MJ
        • Valente AM
        • Breitbart RE
        • Singh MN
        • Gauvreau K
        • Jonas MM
        Transient elastography may identify Fontan patients with unfavorable hemodynamics and advanced hepatic fibrosis.
        Cong Heart Dis. 2014; 9: 438-447
        • Pundi K
        • Pundi KN
        • Kamath PS
        • Cetta F
        • Li Z
        • Poterucha JT
        • Driscoll DJ
        • Johnson JN
        Liver disease in patients after the Fontan operation.
        Am J Cardiol. 2016; 117: 456-460
        • Talwalkar JA
        • Kurtz DM
        • Schoenleber SJ
        • West CP
        • Montori VM
        Ultrasound-based transient elastography for the detection of hepatic fibrosis: systematic review and meta-analysis.
        Clin Gastroenterol Hepatol. 2007; 5: 1214-1220
        • Schachter JL
        • Patel M
        • Horton SR
        • Mike Devane A
        • Ewing A
        • Abrams GA
        FibroSURE and elastography poorly predict the severity of liver fibrosis in Fontan-associated liver disease.
        Cong Heart Dis. 2018; 13: 764-770
        • Shimizu M
        • Miyamoto K
        • Nishihara Y
        • Izumi G
        • Sakai S
        • Inai K
        • Nishikawa T
        • Nakanishi T
        Risk factors and serological markers of liver cirrhosis after Fontan procedure.
        Heart Vessels. 2016; 31: 1514-1521
        • Venkatesh SK
        • Yin M
        • Ehman RL
        Magnetic resonance elastography of liver: clinical applications.
        J Comput Assist Tomogr. 2013; 37: 887-896