Volume 55, Issue 5 pp. 1478-1488

Research Article

Diverse Right Ventricular Remodeling Evaluated by MRI and Prognosis in Eisenmenger Syndrome With Different Shunt Locations

Chao Gong MD,

Chao Gong MD

Department of Cardiology, West China Hospital, Sichuan University, Chengdu, PR China

Search for more papers by this author

Shuai He BMSci,

Shuai He BMSci

Department of Radiology, West China Hospital, Sichuan University, Chengdu, PR China

Search for more papers by this author

Xiaoling Chen BMSci,

Xiaoling Chen BMSci

Department of Cardiology, West China Hospital, Sichuan University, Chengdu, PR China

Search for more papers by this author

Lili Wang BMSci,

Lili Wang BMSci

Department of Cardiology, West China Hospital, Sichuan University, Chengdu, PR China

Search for more papers by this author

Jiajuan Guo BMSci,

Jiajuan Guo BMSci

Department of Cardiology, West China Hospital, Sichuan University, Chengdu, PR China

Search for more papers by this author

Juan He BMSci,

Juan He BMSci

Department of Cardiology, West China Hospital, Sichuan University, Chengdu, PR China

Search for more papers by this author

Lidan Yin BMSci,

Lidan Yin BMSci

Department of Cardiology, West China Hospital, Sichuan University, Chengdu, PR China

Search for more papers by this author

Chen Chen MD,

Chen Chen MD

Department of Cardiology, West China Hospital, Sichuan University, Chengdu, PR China

Search for more papers by this author

Yuchi Han PhD,

Yuchi Han PhD

Department of Medicine (Cardiovascular Division), University of Pennsylvania, Philadelphia, Pennsylvania, USA

Search for more papers by this author

Yucheng Chen MD,

Corresponding Author

Yucheng Chen MD

[email protected]

orcid.org/0000-0002-0601-8039

Department of Cardiology, West China Hospital, Sichuan University, Chengdu, PR China

Address reprint requests to: Y.C., Guoxue Xiang No. 37, Chengdu, Sichuan Province 610041, PR China. E-mail: [email protected]

Search for more papers by this author

Chao Gong MD,

Chao Gong MD

Department of Cardiology, West China Hospital, Sichuan University, Chengdu, PR China

Search for more papers by this author

Shuai He BMSci,

Shuai He BMSci

Department of Radiology, West China Hospital, Sichuan University, Chengdu, PR China

Search for more papers by this author

Xiaoling Chen BMSci,

Xiaoling Chen BMSci

Department of Cardiology, West China Hospital, Sichuan University, Chengdu, PR China

Search for more papers by this author

Lili Wang BMSci,

Lili Wang BMSci

Department of Cardiology, West China Hospital, Sichuan University, Chengdu, PR China

Search for more papers by this author

Jiajuan Guo BMSci,

Jiajuan Guo BMSci

Department of Cardiology, West China Hospital, Sichuan University, Chengdu, PR China

Search for more papers by this author

Juan He BMSci,

Juan He BMSci

Department of Cardiology, West China Hospital, Sichuan University, Chengdu, PR China

Search for more papers by this author

Lidan Yin BMSci,

Lidan Yin BMSci

Department of Cardiology, West China Hospital, Sichuan University, Chengdu, PR China

Search for more papers by this author

Chen Chen MD,

Chen Chen MD

Department of Cardiology, West China Hospital, Sichuan University, Chengdu, PR China

Search for more papers by this author

Yuchi Han PhD,

Yuchi Han PhD

Department of Medicine (Cardiovascular Division), University of Pennsylvania, Philadelphia, Pennsylvania, USA

Search for more papers by this author

Yucheng Chen MD,

Corresponding Author

Yucheng Chen MD

[email protected]

orcid.org/0000-0002-0601-8039

Department of Cardiology, West China Hospital, Sichuan University, Chengdu, PR China

Address reprint requests to: Y.C., Guoxue Xiang No. 37, Chengdu, Sichuan Province 610041, PR China. E-mail: [email protected]

Search for more papers by this author

First published: 21 June 2021

https://doi.org/10.1002/jmri.27791

Citations: 6

Chao Gong and Shuai He contributed equally to this work.

Contract grant sponsor: 1.3.5 project for disciplines of excellence, West China Hospital, Sichuan University (ZYJC18013).

Share a link

Email
Wechat
Bluesky

Abstract

Background

Congenital shunt location is related to Eisenmenger syndrome (ES) survival. Moreover, right ventricular (RV) remodeling is associated with poor survival in pulmonary hypertension.

Purpose

To investigate RV remodeling using comprehensive magnetic resonance imaging (MRI) techniques and identify its relationship with prognosis in ES subgroups classified by shunt location.

Study Type

Prospective observational study.

Population

Fifty-four adults with ES (16 with pre-tricuspid shunt and 38 with post-tricuspid shunt).

Field Strength/Sequence

3.0 T/cine MRI with balanced steady-state free precession sequence, late gadolinium enhancement with inversion recovery segmented gradient echo sequence and phase-sensitive reconstruction, and T1 mapping with modified Look-Locker inversion recovery sequence.

Assessment

Demographics, clinical characteristics, hemodynamics, RV remodeling features (morphology, systolic function, RV–pulmonary artery (PA) coupling and myocardial fibrosis), and prognosis were compared between ES subgroups. The adverse endpoint was all-cause mortality or readmission for heart failure.

Statistical Tests

The independent samples t-test, Fisher's exact test or Chi-squared test, and the Kaplan–Meier method were used. P < 0.05 was considered significant.

Results

Compared to patients with post-tricuspid shunt, patients with pre-tricuspid shunt were significantly older and had higher N-terminal pro-B-type natriuretic peptide concentrations and poorer exercise tolerance. Pre-tricuspid shunt showed significantly larger RV dimensions (end-diastolic volume index: 185.81 ± 37.49 vs. 98.20 ± 36.26 mL/m²), worse RV ejection fraction (23.54% ± 12.35% vs. 40.82% ± 10.77%), and RV–PA decoupling (0.35 ± 0.31 vs. 0.72 ± 0.29). Biventricular myocardial fibrosis was significantly more severe in pre-tricuspid shunt than post-tricuspid shunt (extracellular volume, left ventricle: 35.85% ± 2.58% vs. 29.10% ± 5.20%; RV free wall: 30.93% ± 5.65% vs. 26.75% ± 5.15%). In addition, pre-tricuspid shunt demonstrated a significantly increased risk of adverse endpoint (hazard ratio: 2.938, 95% confidence interval: 1.204–7.172).

Data Conclusion

ES with pre-tricuspid shunt might be a unique subtype with worse clinically decompensated RV remodeling and poor prognosis.

Level of Evidence: 2

Technical Efficacy Stage: 5

Supporting Information

References

1Galie N, Humbert M, Vachiery JL, et al. 2015 ESC/ERS guidelines for the diagnosis and treatment of pulmonary hypertension: The joint task force for the diagnosis and treatment of pulmonary hypertension of the European Society of Cardiology (ESC) and the European Respiratory Society (ERS): Endorsed by: Association for European Paediatric and Congenital Cardiology (AEPC), International Society for Heart and Lung Transplantation (ISHLT). Eur Respir J 2015; 46(4): 903-975.
10.1183/13993003.01032-2015
CAS PubMed Web of Science® Google Scholar
2Moons P, Bovijn L, Budts W, Belmans A, Gewillig M. Temporal trends in survival to adulthood among patients born with congenital heart disease from 1970 to 1992 in Belgium. Circulation 2010; 122(22): 2264-2272.
10.1161/CIRCULATIONAHA.110.946343
PubMed Web of Science® Google Scholar
3Baumgartner H, De Backer J, Babu-Narayan SV, et al. ESC guidelines for the management of adult congenital heart disease. Eur Heart J 2021; 42(6): 563-645.
10.1093/eurheartj/ehaa554
CAS PubMed Web of Science® Google Scholar
4Jiang X, Jing ZC. Epidemiology of pulmonary arterial hypertension. Curr Hypertens Rep 2013; 15(6): 638-649.
10.1007/s11906-013-0397-5
CAS PubMed Web of Science® Google Scholar
5Manes A, Palazzini M, Leci E, Bacchi Reggiani ML, Branzi A, Galie N. Current era survival of patients with pulmonary arterial hypertension associated with congenital heart disease: A comparison between clinical subgroups. Eur Heart J 2014; 35(11): 716-724.
10.1093/eurheartj/eht072
PubMed Web of Science® Google Scholar
6Kempny A, Hjortshoj CS, Gu H, et al. Predictors of death in contemporary adult patients with Eisenmenger syndrome: A multicenter study. Circulation 2017; 135(15): 1432-1440.
10.1161/CIRCULATIONAHA.116.023033
PubMed Web of Science® Google Scholar
7Jensen AS, Broberg CS, Rydman R, et al. Impaired right, left, or biventricular function and resting oxygen saturation are associated with mortality in Eisenmenger syndrome: A clinical and cardiovascular magnetic resonance study. Circ Cardiovasc Imaging 2015; 8(12):e003596.
10.1161/CIRCIMAGING.115.003596
PubMed Web of Science® Google Scholar
8Dong Y, Pan Z, Wang D, et al. Prognostic value of cardiac magnetic resonance-derived right ventricular remodeling parameters in pulmonary hypertension: A systematic review and meta-analysis. Circ Cardiovasc Imaging 2020; 13(7):e010568.
10.1161/CIRCIMAGING.120.010568
PubMed Web of Science® Google Scholar
9de Siqueira ME, Pozo E, Fernandes VR, et al. Characterization and clinical significance of right ventricular mechanics in pulmonary hypertension evaluated with cardiovascular magnetic resonance feature tracking. J Cardiovasc Magn Reson 2016; 18(1): 39.
10.1186/s12968-016-0258-x
PubMed Web of Science® Google Scholar
10Moceri P, Kempny A, Liodakis E, et al. Physiological differences between various types of Eisenmenger syndrome and relation to outcome. Int J Cardiol 2015; 179: 455-460.
10.1016/j.ijcard.2014.11.100
PubMed Web of Science® Google Scholar
11Alonso-Gonzalez R, Lopez-Guarch CJ, Subirana-Domenech MT, et al. Pulmonary hypertension and congenital heart disease: An insight from the REHAP National Registry. Int J Cardiol 2015; 184: 717-723.
10.1016/j.ijcard.2015.02.031
PubMed Web of Science® Google Scholar
12Badagliacca R, Poscia R, Pezzuto B, et al. Right ventricular concentric hypertrophy and clinical worsening in idiopathic pulmonary arterial hypertension. J Heart Lung Transplant 2016; 35(11): 1321-1329.
10.1016/j.healun.2016.04.006
PubMed Web of Science® Google Scholar
13Badagliacca R, Poscia R, Pezzuto B, et al. Right ventricular remodeling in idiopathic pulmonary arterial hypertension: Adaptive versus maladaptive morphology. J Heart Lung Transplant 2015; 34(3): 395-403.
10.1016/j.healun.2014.11.002
PubMed Web of Science® Google Scholar
14Andersen S, Nielsen-Kudsk JE, Vonk Noordegraaf A, de Man FS. Right ventricular fibrosis. Circulation 2019; 139(2): 269-285.
10.1161/CIRCULATIONAHA.118.035326
CAS PubMed Web of Science® Google Scholar
15Broberg CS, Prasad SK, Carr C, Babu-Narayan SV, Dimopoulos K, Gatzoulis MA. Myocardial fibrosis in Eisenmenger syndrome: A descriptive cohort study exploring associations of late gadolinium enhancement with clinical status and survival. J Cardiovasc Magn Reson 2014; 16: 32.
10.1186/1532-429X-16-32
PubMed Web of Science® Google Scholar
16Peacock AJ, Vonk NA. Cardiac magnetic resonance imaging in pulmonary arterial hypertension. Eur Respir Rev 2013; 22(130): 526-534.
10.1183/09059180.00006313
PubMed Google Scholar
17Alassas K, Mergo P, Ibrahim ES, et al. Cardiac MRI as a diagnostic tool in pulmonary hypertension. Future Cardiol 2014; 10(1): 117-130.
10.2217/fca.13.97
CAS PubMed Google Scholar
18Aus Dem Siepen F, Buss SJ, Messroghli D, et al. T1 mapping in dilated cardiomyopathy with cardiac magnetic resonance: Quantification of diffuse myocardial fibrosis and comparison with endomyocardial biopsy. Eur Heart J Cardiovasc Imaging 2015; 16(2): 210-216.
10.1093/ehjci/jeu183
PubMed Web of Science® Google Scholar
19Fontana M, White SK, Banypersad SM, et al. Comparison of T1 mapping techniques for ECV quantification. Histological validation and reproducibility of ShMOLLI versus multibreath-hold T1 quantification equilibrium contrast CMR. J Cardiovasc Magn Reson 2012; 14: 88.
10.1186/1532-429X-14-88
PubMed Web of Science® Google Scholar
20Broberg CS, Ujita M, Prasad S, et al. Pulmonary arterial thrombosis in eisenmenger syndrome is associated with biventricular dysfunction and decreased pulmonary flow velocity. J Am Coll Cardiol 2007; 50(7): 634-642.
10.1016/j.jacc.2007.04.056
PubMed Web of Science® Google Scholar
21Galie N, Beghetti M, Gatzoulis MA, et al. Bosentan therapy in patients with Eisenmenger syndrome: A multicenter, double-blind, randomized, placebo-controlled study. Circulation 2006; 114(1): 48-54.
10.1161/CIRCULATIONAHA.106.630715
CAS PubMed Web of Science® Google Scholar
22Gatzoulis MA, Landzberg M, Beghetti M, et al. Evaluation of Macitentan in patients with Eisenmenger syndrome. Circulation 2019; 139(1): 51-63.
10.1161/CIRCULATIONAHA.118.033575
CAS PubMed Web of Science® Google Scholar
23 Laboratories ATSCoPSfCPF. ATS statement: Guidelines for the six-minute walk test. Am J Respir Crit Care Med 2002; 166(1): 111-117.
10.1164/ajrccm.166.1.at1102
PubMed Web of Science® Google Scholar
24Schulz-Menger J, Bluemke DA, Bremerich J, et al. Standardized image interpretation and post processing in cardiovascular magnetic resonance: Society for Cardiovascular Magnetic Resonance (SCMR) board of trustees task force on standardized post processing. J Cardiovasc Magn Reson 2013; 15: 35.
10.1186/1532-429X-15-35
PubMed Web of Science® Google Scholar
25Sievers B, Addo M, Breuckmann F, Barkhausen J, Erbel R. Reference right atrial function determined by steady-state free precession cardiovascular magnetic resonance. J Cardiovasc Magn Reson 2007; 9(5): 807-814.
10.1080/10976640701545552
PubMed Web of Science® Google Scholar
26Zhan Y, Debs D, Khan MA, Nguyen DT, Graviss EA, Shah DJ. Normal reference values and reproducibility of tricuspid annulus dimensions using cardiovascular magnetic resonance. Am J Cardiol 2019; 124(4): 594-598.
10.1016/j.amjcard.2019.05.019
PubMed Web of Science® Google Scholar
27Van De Bruaene A, De Meester P, Voigt JU, et al. Right ventricular function in patients with Eisenmenger syndrome. Am J Cardiol 2012; 109(8): 1206-1211.
10.1016/j.amjcard.2011.12.003
PubMed Web of Science® Google Scholar
28Moceri P, Bouvier P, Baudouy D, et al. Cardiac remodelling amongst adults with various aetiologies of pulmonary arterial hypertension including Eisenmenger syndrome-implications on survival and the role of right ventricular transverse strain. Eur Heart J Cardiovasc Imaging 2017; 18(11): 1262-1270.
10.1093/ehjci/jew277
PubMed Web of Science® Google Scholar
29Berger RM, Beghetti M, Galie N, et al. Atrial septal defects versus ventricular septal defects in BREATHE-5, a placebo-controlled study of pulmonary arterial hypertension related to Eisenmenger's syndrome: A subgroup analysis. Int J Cardiol 2010; 144(3): 373-378.
10.1016/j.ijcard.2009.04.037
PubMed Web of Science® Google Scholar
30Lahm T, Douglas IS, Archer SL, et al. Assessment of right ventricular function in the research setting: Knowledge gaps and pathways forward. An official American Thoracic Society research statement. Am J Respir Crit Care Med 2018; 198(4): e15-e43.
10.1164/rccm.201806-1160ST
PubMed Web of Science® Google Scholar
31Bossone E, D'Andrea A, D'Alto M, et al. Echocardiography in pulmonary arterial hypertension: From diagnosis to prognosis. J Am Soc Echocardiogr 2013; 26(1): 1-14.
10.1016/j.echo.2012.10.009
PubMed Web of Science® Google Scholar
32Vonk Noordegraaf A, Westerhof BE, Westerhof N. The relationship between the right ventricle and its load in pulmonary hypertension. J Am Coll Cardiol 2017; 69(2): 236-243.
10.1016/j.jacc.2016.10.047
PubMed Web of Science® Google Scholar
33Nochioka K, Querejeta Roca G, Claggett B, et al. Right ventricular function, right ventricular-pulmonary artery coupling, and heart failure risk in 4 US communities: The atherosclerosis risk in communities (ARIC) study. JAMA Cardiol 2018; 3(10): 939-948.
10.1001/jamacardio.2018.2454
PubMed Web of Science® Google Scholar
34Vanderpool RR, Pinsky MR, Naeije R, et al. RV-pulmonary arterial coupling predicts outcome in patients referred for pulmonary hypertension. Heart 2015; 101(1): 37-43.
10.1136/heartjnl-2014-306142
PubMed Web of Science® Google Scholar
35Reiter U, Reiter G, Kovacs G, et al. Native myocardial T1 mapping in pulmonary hypertension: Correlations with cardiac function and hemodynamics. Eur Radiol 2017; 27(1): 157-166.
10.1007/s00330-016-4360-0
PubMed Web of Science® Google Scholar
36Roller FC, Wiedenroth C, Breithecker A, et al. Native T1 mapping and extracellular volume fraction measurement for assessment of right ventricular insertion point and septal fibrosis in chronic thromboembolic pulmonary hypertension. Eur Radiol 2017; 27(5): 1980-1991.
10.1007/s00330-016-4585-y
PubMed Web of Science® Google Scholar
37Homsi R, Luetkens JA, Skowasch D, et al. Left ventricular myocardial fibrosis, atrophy, and impaired contractility in patients with pulmonary arterial hypertension and a preserved left ventricular function: A cardiac magnetic resonance study. J Thorac Imaging 2017; 32(1): 36-42.
10.1097/RTI.0000000000000248
PubMed Web of Science® Google Scholar
38Friedberg MK, Redington AN. Right versus left ventricular failure: Differences, similarities, and interactions. Circulation 2014; 129(9): 1033-1044.
10.1161/CIRCULATIONAHA.113.001375
PubMed Web of Science® Google Scholar
39Marcus JT, Gan CT, Zwanenburg JJ, et al. Interventricular mechanical asynchrony in pulmonary arterial hypertension: Left-to-right delay in peak shortening is related to right ventricular overload and left ventricular underfilling. J Am Coll Cardiol 2008; 51(7): 750-757.
10.1016/j.jacc.2007.10.041
PubMed Web of Science® Google Scholar
40Lancellotti P, Moura L, Pierard LA, et al. European Association of Echocardiography recommendations for the assessment of valvular regurgitation. Part 2: Mitral and tricuspid regurgitation (native valve disease). Eur J Echocardiogr 2010; 11(4): 307-332.
10.1093/ejechocard/jeq031
PubMed Web of Science® Google Scholar

Citing Literature

Volume55, Issue5

May 2022

Pages 1478-1488

Diverse Right Ventricular Remodeling Evaluated by MRI and Prognosis in Eisenmenger Syndrome With Different Shunt Locations

Abstract

Background

Purpose

Study Type

Population

Field Strength/Sequence

Assessment

Statistical Tests

Results

Data Conclusion

Supporting Information

References

Citing Literature

References

Information

About Wiley Online Library

Help & Support

Opportunities

Connect with Wiley

Diverse Right Ventricular Remodeling Evaluated by MRI and Prognosis in Eisenmenger Syndrome With Different Shunt Locations

Abstract

Background

Purpose

Study Type

Population

Field Strength/Sequence

Assessment

Statistical Tests

Results

Data Conclusion

Supporting Information

References

Citing Literature

References

Related

Information