Skip to main content

Advertisement

Log in

Right atrial function early after tetralogy of Fallot repair

  • Original Paper
  • Published:
The International Journal of Cardiovascular Imaging Aims and scope Submit manuscript

Abstract

Diastolic dysfunction after repair for Tetralogy of Fallot (TOF) is associated with adverse long-term outcomes. Right atrial (RA) mechanics as a proxy of right ventricular (RV) diastolic function in the early post-operative period after surgical repair for TOF has not been reported. We sought to evaluate RA and RV strain prior to hospital discharge after TOF repair and to identify important patient factors associated with strain using a machine learning method. Single center retrospective cohort study of TOF patients undergoing surgical repair, with analysis of RA and RV strain from pre-and post-operative echocardiograms. RA function was assessed by the peak RA strain, systolic RA strain rate, early diastolic RA strain rate and RA emptying fraction. RV systolic function was measured by global longitudinal strain. Pre- and post-operative values were compared using Wilcoxon rank sum test. Gradient boosted machine (GBM) models were used to identify the most important predictors of post-operative strain. In total, 153 patients were enrolled, median age at TOF repair 3.5 months (25th-75th percentile: 2.2- 5.2), mostly male (67%), and White (64.1%). From pre-to post-operative period, there was significant worsening in all RA parameters and in RV strain. GBM models identified patient, anatomic, and surgical factors that were strong predictors of post-operative RA and RV strain. These factors included pulmonary valve and branch pulmonary artery Z scores, birth weight, gestational age and age at surgery, pre-operative RV fractional area change and oxygen saturation, type of outflow tract repair, duration of cardiopulmonary bypass, and early post-operative partial arterial pressure of oxygen. There is significant worsening in RA and RV strain early after TOF repair, indicating early alteration in diastolic and systolic function after surgery. Several patient and operative factors influence post-operative RV function. Most of the factors described are not readily modifiable, however they may inform pre-operative risk-stratification. The clinical application of RA strain and the prognostic implication of these early changes merit 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
Fig. 5

Similar content being viewed by others

Abbreviations

RA:

Right atrium/ right atrial

RV:

Right ventricle/ right ventricular

GBM:

Gradient boosted quantile regression models

TOF:

Tetralogy of Fallot

References

  1. Maskatia SA, Morris SA, Spinner JA, Krishnamurthy R, Altman CA (2015) Echocardiographic parameters of right ventricular diastolic function in repaired tetralogy of Fallot are associated with important findings on magnetic resonance imaging. Congenit Heart Dis 10:E113–E122

    Article  PubMed  Google Scholar 

  2. Aboulhosn JA, Lluri G, Gurvitz MZ, Khairy P, Mongeon FP, Kay J, Valente AM, Earing MG, Opotowsky AR, Lui G, Gersony DR, Cook S, Child J, Ting J, Webb G, Landzberg M, Alliance for Adult Research in Congenital C (2013) Broberg CS Left and right ventricular diastolic function in adults with surgically repaired tetralogy of Fallot: a multi-institutional study. Can J Cardiol. 29:866–72

    Article  PubMed  Google Scholar 

  3. Hope KD, Calderon Anyosa RJC, Wang Y, Montero AE, Sato T, Hanna BD, Banerjee A (2018) Right atrial mechanics provide useful insight in pediatric pulmonary hypertension. Pulm Circ 8:2045893218754852

    Article  PubMed  PubMed Central  Google Scholar 

  4. Jone PN, Schafer M, Li L, Craft M, Ivy DD, Kutty S (2017) Right atrial deformation in predicting outcomes in pediatric pulmonary hypertension. Circ Cardiovasc Imaging. 10(12):e006250

    Article  PubMed  PubMed Central  Google Scholar 

  5. Kutty S, Padiyath A, Li L, Peng Q, Rangamani S, Schuster A, Danford DA (2013) Functional maturation of left and right atrial systolic and diastolic performance in infants, children, and adolescents. J Am Soc Echocardiogr 26(398–409):e2

    Google Scholar 

  6. Badano LP, Kolias TJ, Muraru D, Abraham TP, Aurigemma G, Edvardsen T, D’Hooge J, Donal E, Fraser AG, Marwick T, Mertens L, Popescu BA, Sengupta PP, Lancellotti P, Thomas JD, Voigt JU, Industry r and Reviewers: This document was reviewed by members of the ESDC (2018) Standardization of left atrial, right ventricular, and right atrial deformation imaging using two-dimensional speckle tracking echocardiography: a consensus document of the EACVI/ASE/Industry Task Force to standardize deformation imaging Standardization of left atrial, right ventricular, and right atrial deformation imaging using two-dimensional speckle tracking echocardiography: a consensus document of the EACVI/ASE/Industry Task Force to standardize deformation imaging. Eur Heart J Cardiovasc Imaging 19:591–600

    Article  PubMed  Google Scholar 

  7. Hou J, Yu HK, Wong SJ, Cheung YF (2015) Atrial mechanics after surgical repair of tetralogy of Fallot. Echocardiography 32:126–134

    Article  PubMed  Google Scholar 

  8. Gaynor SL, Maniar HS, Bloch JB, Steendijk P, Moon MR (2005) Right atrial and ventricular adaptation to chronic right ventricular pressure overload. Circulation 112:I212–I218

    Article  PubMed  Google Scholar 

  9. Gaynor SL, Maniar HS, Prasad SM, Steendijk P, Moon MR (2005) Reservoir and conduit function of right atrium: impact on right ventricular filling and cardiac output. Am J Physiol Heart Circ Physiol 288:H2140–H2145

    Article  CAS  PubMed  Google Scholar 

  10. Rai AB, Lima E, Munir F, Faisal Khan A, Waqas A, Bughio S, ul Haq E, Attique HB, Rahman ZU (2015) Speckle tracking echocardiography of the right atrium: the neglected chamber. Clin Cardiol 38:692–7

    Article  PubMed  PubMed Central  Google Scholar 

  11. Riesenkampff E, Mengelkamp L, Mueller M, Kropf S, Abdul-Khaliq H, Sarikouch S, Beerbaum P, Hetzer R, Steendijk P, Berger F, Kuehne T (2010) Integrated analysis of atrioventricular interactions in tetralogy of Fallot. Am J Physiol Heart Circ Physiol 299:H364–H371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Mercer-Rosa L, Elci OU, DeCost G, Woyciechowski S, Edman SM, Ravishankar C, Mascio CE, Kawut SM, Goldmuntz E (2018) Predictors of length of hospital stay after complete repair for tetralogy of Fallot: a prospective cohort study. J Am Heart Assoc 7(11):e008719

    Article  PubMed  PubMed Central  Google Scholar 

  13. DiLorenzo MP, Elci OU, Wang Y, Banerjee A, Sato T, Ky B, Goldmuntz E, Mercer-Rosa L (2018) Longitudinal changes in right ventricular function in tetralogy of Fallot in the initial years after surgical repair. J Am Soc Echocardiogr 31:816–821

    Article  PubMed  PubMed Central  Google Scholar 

  14. Bhat M, Goldmuntz E, Fogel MA, Rychik J, Mercer-Rosa L (2017) Longitudinal validation of the diastolic to systolic time-velocity integral ratio as a doppler-derived measure of pulmonary regurgitation in patients with repaired tetralogy of Fallot. Pediatr Cardiol 38:240–246

    Article  PubMed  Google Scholar 

  15. Mercer-Rosa L, Yang W, Kutty S, Rychik J, Fogel M, Goldmuntz E (2012) Quantifying pulmonary regurgitation and right ventricular function in surgically repaired tetralogy of Fallot: a comparative analysis of echocardiography and magnetic resonance imaging. Circ Cardiovasc Imaging 5:637–643

    Article  PubMed  PubMed Central  Google Scholar 

  16. Hopper RK, Wang Y, DeMatteo V, Santo A, Kawut SM, Elci OU, Hanna BD, Mercer-Rosa L (2018) Right ventricular function mirrors clinical improvement with use of prostacyclin analogues in pediatric pulmonary hypertension. Pulm Circ 8:2045894018759247

    Article  PubMed  PubMed Central  Google Scholar 

  17. R Core Team (2017). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/

  18. Hui W, Abd El Rahman MY, Dsebissowa F, Rentzsch A, Gutberlet M, Alexi-Meskishvili V, Hetzer R, Lange PE, Abdul-Khaliq H (2004) Quantitative analysis of right atrial performance after surgical repair of tetralogy of Fallot. Cardiol Young 14:520–6

    Article  PubMed  Google Scholar 

  19. Riesenkampff E, Luining W, Seed M, Chungsomprasong P, Manlhiot C, Elders B, McCrindle BW, Yoo SJ, Grosse-Wortmann L (2016) Increased left ventricular myocardial extracellular volume is associated with longer cardiopulmonary bypass times, biventricular enlargement and reduced exercise tolerance in children after repair of tetralogy of Fallot. J Cardiovasc Magn Reson 18:75

    Article  PubMed  PubMed Central  Google Scholar 

  20. Sareban M, Perz T, Macholz F, Reich B, Schmidt P, Fried S, Mairbaurl H, Berger MM, Niebauer J (2020) Preserved right ventricular function but increased right atrial contractile demand in altitude-induced pulmonary hypertension. Int J Cardiovasc Imaging 36:1069–1076

    Article  PubMed  PubMed Central  Google Scholar 

  21. Alenezi F, Mandawat A, Il’Giovine ZJ, Shaw LK, Siddiqui I, Tapson VF, Arges K, Rivera D, Romano MMD, Velazquez EJ, Douglas PS, Samad Z, Rajagopal S (2018) Clinical utility and prognostic value of right atrial function in pulmonary hypertension. Circ Cardiovasc Imaging 11:e006984

    Article  PubMed  PubMed Central  Google Scholar 

  22. D’Alto M, D’Andrea A, Di Salvo G, Scognamiglio G, Argiento P, Romeo E, Di Marco GM, Mattera Iacono A, Bossone E, Sarubbi B, Russo MG (2017) Right atrial function and prognosis in idiopathic pulmonary arterial hypertension. Int J Cardiol 248:320–325

    Article  PubMed  Google Scholar 

  23. Sakata K, Uesugi Y, Isaka A, Minamishima T, Matsushita K, Satoh T, Yoshino H (2016) Evaluation of right atrial function using right atrial speckle tracking analysis in patients with pulmonary artery hypertension. J Echocardiogr 14:30–38

    Article  PubMed  Google Scholar 

  24. Watanabe K, Schafer M, Cassidy C, Miyamoto SD, Jone PN (2019) Right atrial function in pediatric heart transplant patients by echocardiographic strain measurements. Pediatr Transplant 23:e13383

    Article  PubMed  Google Scholar 

  25. Gatzoulis MA, Clark AL, Cullen S, Newman CG, Redington AN (1995) Right ventricular diastolic function 15 to 35 years after repair of tetralogy of Fallot. Restrictive physiology predicts superior exercise performance. Circulation 91:1775–81

    Article  CAS  PubMed  Google Scholar 

  26. Norgard G, Gatzoulis MA, Moraes F, Lincoln C, Shore DF, Shinebourne EA, Redington AN (1996) Relationship between type of outflow tract repair and postoperative right ventricular diastolic physiology in tetralogy of Fallot implications for long-term outcome. Circulation 94:3276–3280

    Article  CAS  PubMed  Google Scholar 

  27. Norgard G, Gatzoulis MA, Josen M, Cullen S, Redington AN (1998) Does restrictive right ventricular physiology in the early postoperative period predict subsequent right ventricular restriction after repair of tetralogy of Fallot? Heart 79:481–484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Cullen S, Shore D, Redington A (1995) Characterization of right ventricular diastolic performance after complete repair of tetralogy of Fallot. Restrictive physiology predicts slow postoperative recovery. Circulation 91:1782–9

    Article  CAS  PubMed  Google Scholar 

  29. Rathore KS, Gupta N, Kapoor A, Modi N, Singh PK, Tewari P, Sinha N (2004) Assessment of right ventricular diastolic function: does it predict post-operative course in tetralogy of Fallot. Indian Heart J 56:220–224

    PubMed  Google Scholar 

  30. Ye JJ, Shu Q, Liu XW, Gu WZ, Yu J, Jiang GP (2014) Noninvasive perioperative evaluation of right ventricular function in children with tetralogy of Fallot. Artif Organs 38:41–47

    Article  CAS  PubMed  Google Scholar 

  31. Kutty S, Shang Q, Joseph N, Kowallick JT, Schuster A, Steinmetz M, Danford DA, Beerbaum P, Sarikouch S (2017) Abnormal right atrial performance in repaired tetralogy of Fallot: A CMR feature tracking analysis. Int J Cardiol 248:136–142

    Article  PubMed  Google Scholar 

  32. DiLorenzo M, Hwang WT, Goldmuntz E, Ky B, Mercer-Rosa L (2018) Diastolic dysfunction in tetralogy of Fallot: comparison of echocardiography with catheterization. Echocardiography 35:1641–1648

    Article  PubMed  PubMed Central  Google Scholar 

  33. Abd El Rahman M, Raedle-Hurst T, Rentzsch A, Schafers HJ, Abdul-Khaliq H (2015) Assessment of inter-atrial, inter-ventricular, and atrio-ventricular interactions in tetralogy of Fallot patients after surgical correction. Insights from two-dimensional speckle tracking and three-dimensional echocardiography. Cardiol Young 25:1254–62

    Article  PubMed  Google Scholar 

  34. Riesenkampff E, Al-Wakeel N, Kropf S, Stamm C, Alexi-Meskishvili V, Berger F, Kuehne T (2014) Surgery impacts right atrial function in tetralogy of Fallot. J Thorac Cardiovasc Surg 147:1306–1311

    Article  PubMed  Google Scholar 

  35. DiLorenzo MP, Goldmuntz E, Nicolson SC, Fogel MA, Mercer-Rosa L (2018) Early postoperative remodelling following repair of tetralogy of Fallot utilising unsedated cardiac magnetic resonance: a pilot study. Cardiol Young 28:697–701

    Article  PubMed  PubMed Central  Google Scholar 

  36. Laudito A, Graham EM, Stroud MR, Bandisode V, Bhat AN, Crawford FA Jr, Atz AM, Bradley SM (2006) Complete repair of conotruncal defects with an interatrial communication: oxygenation, hemodynamic status, and early outcome. Ann Thorac Surg 82:1286–1291 (discussion 1291)

    Article  PubMed  Google Scholar 

  37. Munkhammar P, Cullen S, Jogi P, de Leval M, Elliott M, Norgard G (1998) Early age at repair prevents restrictive right ventricular (RV) physiology after surgery for tetralogy of Fallot (TOF): diastolic RV function after TOF repair in infancy. J Am Coll Cardiol 32:1083–1087

    Article  CAS  PubMed  Google Scholar 

  38. Ruiz VM, Saenz L, Lopez-Magallon A, Shields A, Ogoe HA, Suresh S, Munoz R, Tsui FR (2019) Early prediction of critical events for infants with single-ventricle physiology in critical care using routinely collected data. J Thorac Cardiovasc Surg 158:234-243.e3

    Article  PubMed  Google Scholar 

  39. Knuf M, Kuroczynski W, Schone F, Martin C, Huth R, Rhein M, Vahl CF, Kampann C (2010) Significance of patient categorization for perioperative management of children with tetralogy of Fallot, with special regard to co-existing malformations. Cardiol J 17:20–28

    PubMed  Google Scholar 

Download references

Funding

This work was supported by Grant NIH K01HL125521 (Mercer-Rosa), and Pulmonary Hypertension Association Supplement to K01HL125521.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. The authors would like to thank Sharon Edman, MS, for data management. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Laura Mercer-Rosa.

Ethics declarations

Conflict of interests

The authors have no relevant financial or non-financial interests to disclose.

Ethical approval

The study protocol was approved by the Institutional Review Board for the Protection of Human Subjects at Children’s Hospital of Philadelphia, and parents of subjects gave informed consent to participating in the study.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ekhomu, O., Faerber, J.A., Wang, Y. et al. Right atrial function early after tetralogy of Fallot repair. Int J Cardiovasc Imaging 38, 1961–1972 (2022). https://doi.org/10.1007/s10554-022-02595-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10554-022-02595-y

Keywords

Navigation