Urgent neonatal balloon atrial septostomy in simple transposition of the great arteries: predictive value of fetal cardiac parameters

O Patey, J S Carvalho, B Thilaganathan, O Patey, J S Carvalho, B Thilaganathan

Abstract

Objectives: To investigate the impact of abnormal perinatal loading conditions on cardiac geometry and function in term fetuses and neonates with transposition of the great arteries with intact interventricular septum (simple TGA), and to explore the predictive value of fetal cardiac parameters for an urgent balloon atrial septostomy (BAS) after birth.

Methods: This was a prospective longitudinal follow-up study of women delivering at term, including both uncomplicated pregnancies with normal outcome and pregnancies affected by fetal simple TGA. Conventional, spectral-tissue Doppler and speckle-tracking echocardiographic parameters were obtained within 1 week before delivery and within the first few hours after delivery. Neonates with simple TGA that required urgent BAS were assessed after the procedure and before corrective arterial switch surgery. Cardiac parameters were normalized by cardiac cycle length, ventricular end-diastolic length or end-diastolic dimension, as appropriate. Fetal and neonatal cardiac parameters were compared between simple-TGA cases and controls, and perinatal changes in the simple-TGA group were assessed. Receiver-operating-characteristics (ROC)-curve analysis was used to assess the predictive value of fetal cardiac parameters for urgent BAS after birth in the simple-TGA group.

Results: A total of 67 pregnant women delivering at term were included in the study (54 normal pregnancies and 13 with a diagnosis of fetal simple TGA). Compared with normal term fetuses, term fetuses with simple TGA exhibited more globular hypertrophied ventricles, increased biventricular systolic function and diastolic dysfunction (right ventricular (RV) sphericity index (SI), 0.58 vs 0.54; left ventricular (LV)-SI, 0.55 vs 0.49; combined cardiac output (CCO), 483 vs 406 mL/min/kg; LV torsion, 4.3 vs 3.0 deg/cm; RV isovolumetric relaxation time (IVRT'), 127 vs 102 ms; P < 0.01 for all). Compared with normal neonates, neonates with simple TGA demonstrated biventricular hypertrophy, a more spherical right ventricle and altered systolic and diastolic functional parameters (RV-SI, 0.61 vs 0.43; RV myocardial performance index, 0.47 vs 0.34; CCO, 697 vs 486 mL/min/kg; LV-IVRT', 100 vs 79 ms; RV-IVRT', 106 vs 71 ms; P < 0.001 for all). Paired comparison of neonatal and fetal cardiac indices in the simple-TGA group showed persistence of the fetal phenotype, increased biventricular systolic myocardial contractility and CCO, and diastolic dysfunction (RV systolic myocardial velocity (S'), 0.31 vs 0.24 cm/s; LV-S', 0.23 vs 0.18 cm/s; CCO, 697 vs 483 mL/min/kg; LV torsion, 1.1 vs 4.3 deg/cm; P < 0.001 for all). Several fetal cardiac parameters in term fetuses with simple TGA demonstrated high predictive value for an urgent BAS procedure after birth. Our proposed novel fetal cardiac index, LV rotation-to-shortening ratio, as a potential marker of subendocardial dysfunction, for a cut-off value of ≥ 0.23, had an area under the ROC curve (AUC) of 0.94, sensitivity of 100% and specificity of 83%. For RV/LV end-diastolic area ratio ≥ 1.33, pulmonary-valve-to-aortic-valve-dimension ratio ≤ 0.89, RV/LV cardiac output ratio ≥ 1.38 and foramen-ovale-dimension-to-total-interatrial-septal-length ratio ≤ 0.27, AUC was 0.93-0.98, sensitivity was 86% and specificity was 83-100% for all.

Conclusions: Simple-TGA fetuses exhibited cardiac remodeling at term with more profound alterations in these cardiac parameters after birth, suggestive of adaptation to abnormal loading conditions and possible adaptive responses to hypoxemia. Perinatal adaptation in simple TGA might reflect persistence of the abnormal parallel arrangement of cardiovascular circulation and the presence of widely patent fetal shunts imposing volume load on the neonatal heart. The fetal cardiac parameters that showed high predictive value for urgent BAS after birth might reflect the impact of late-gestation pathophysiology and progressive hypoxemia on fetal cardiac geometry and function in simple TGA. If these findings are validated in larger prospective studies, detailed cardiac assessment of fetuses with simple TGA near term could facilitate improvements in perinatal management and refinement of the timing of postnatal intervention strategies to prevent adverse pregnancy outcomes. © 2020 International Society of Ultrasound in Obstetrics and Gynecology.

Keywords: balloon atrial septostomy; echocardiography; fetal heart; left ventricular rotation, twist and torsion; prediction; speckle tracking; tissue Doppler imaging; transposition of the great arteries.

© 2020 International Society of Ultrasound in Obstetrics and Gynecology.

References

REFERENCES

    1. Samanek M. Congenital heart malformations: prevalence, severity, survival, and quality of life. Cardiol Young 2000; 10: 179-185.
    1. Villafane J, Lantin-Hermoso MR, Bhatt AB, Tweddell JS, Geva T, Nathan M, Elliott MJ, Vetter VL, Paridon SM, Kochilas L, Jenkins KJ, Beekman RH 3rd, Wernovsky G, Towbin JA. D-transposition of the great arteries: the current era of the arterial switch operation. J Am Coll Cardiol 2014; 64: 498-511.
    1. Martins P, Castela E. Transposition of the great arteries. Orphanet J Rare Dis 2008; 3: 27.
    1. Maeno YV, Kamenir SA, Sinclair B, van der Velde ME, Smallhorn JF, Hornberger LK. Prenatal features of ductus arteriosus constriction and restrictive foramen ovale in d-transposition of the great arteries. Circulation 1999; 99: 1209-1214.
    1. Jouannic JM, Gavard L, Fermont L, Le Bidois J, Parat S, Vouhe PR, Dumez Y, Sidi D, Bonnet D. Sensitivity and specificity of prenatal features of physiological shunts to predict neonatal clinical status in transposition of the great arteries. Circulation 2004; 110: 1743-1746.
    1. Punn R, Silverman NH. Fetal predictors of urgent balloon atrial septostomy in neonates with complete transposition. J Am Soc Echocardiogr 2011; 24: 425-430.
    1. Porayette P, van Amerom JFP, Yoo S-J, Jaeggi E, Macgowan CK, Seed M. MRI shows limited mixing between systemic and pulmonary circulations in foetal transposition of the great arteries: a potential cause of in utero pulmonary vascular disease. Cardiol Young 2015; 25: 737-744.
    1. Vigneswaran TV, Zidere V, Miller OI, Simpson JM, Sharland GK. Usefulness of the Prenatal Echocardiogram in Fetuses With Isolated Transposition of the Great Arteries to Predict the Need for Balloon Atrial Septostomy. Am J Cardiol 2017; 119: 1463-1467.
    1. Słodki M, Axt-Fliedner R, Zych-Krekora K, Wolter A, Kawecki A, Enzensberger C, Gulczyńska E, Respondek-Liberska M. New method to predict need for Rashkind procedure in fetuses with dextro-transposition of the great arteries. Ultrasound Obstet Gynecol 2018; 51: 531-536.
    1. Buca D, Winberg P, Rizzo G, Khalil A, Liberati M, Makatsariya A, Greco F, Nappi L, Acharya G, D'Antonio F. Prenatal risk factors for urgent atrial septostomy at birth in fetuses with transposition of the great arteries: a systematic review and meta-analysis. J Maternal Fetal Neonatal Med 2020. DOI: 10.1080/14767058.2020.1725883.
    1. Vaujois L, Boucoiran I, Preuss C, Brassard M, Houde C, Fouron JC, Raboisson MJ. Relationship between interatrial communication, ductus arteriosus, and pulmonary flow patterns in fetuses with transposition of the great arteries: prediction of neonatal desaturation. Cardiol Young 2017; 27: 1280-1288.
    1. Tuo G, Paladini D, Montobbio G, Volpe P, Cheli M, Calevo MG, Marasini M. Prenatal Echocardiographic Assessment of Foramen Ovale Appearance in Fetuses with D-Transposition of the Great Arteries and Impact on Neonatal Outcome. Fetal Diagn Ther 2017; 42: 48-56.
    1. Blanc J, Fouron JC, Sonesson SE, Raboisson MJ, Huggon I, Gendron R, Berger A, Brisebois S. Ventricular outputs, central blood flow distribution and flow pattern through the aortic isthmus of fetuses with simple transposition of the great arteries. Acta Obstet Gynecol Scand 2016; 95: 629-634.
    1. Godfrey ME, Friedman KG, Drogosz M, Rudolph AM, Tworetzky W. Cardiac output and blood flow redistribution in the fetus with D-loop transposition of the great arteries and intact ventricular septum: insights into the pathophysiology. Ultrasound Obstet Gynecol 2017; 50: 612-617.
    1. Lachaud M, Dionne A, Brassard M, Charron MA, Birca A, Dehaes M, Raboisson M-J. Cardiac hemodynamics in fetuses with transposition of the great arteries and intact ventricular septum from diagnosis to end of pregnancy: longitudinal follow-up. Ultrasound Obstet Gynecol 2021; 57: 273-281.
    1. Walter C, Soveral I, Bartrons J, Escobar MC, Carretero JM, Quirado L, Gómez O, Sánchez-de-Toledo J. Comprehensive Functional Echocardiographic Assessment of Transposition of the Great Arteries: From Fetus to Newborn. Pediatr Cardiol 2020; 41: 687-694.
    1. Bonnet D, Coltri A, Butera G, Fermont L, Le Bidois J, Kachaner J, Sidi D. Detection of transposition of the great arteries in fetuses reduces neonatal morbidity and mortality. Circulation 1999; 99: 916-918.
    1. Rudolph AM. Aortopulmonary transposition in the fetus: speculation on pathophysiology and therapy. Pediatr Res 2007; 61: 375-380.
    1. Donofrio MT, Skurow-Todd K, Berger JT, McCarter R, Fulgium A, Krishnan A, Sable CA. Risk-Stratified Postnatal Care of Newborns with Congenital Heart Disease Determined by Fetal Echocardiography. J Am Soc Echocardiogr 2015; 28: 1339-1349.
    1. Crispi F, Bijnens B, Sepulveda-Swatson E, Cruz-Lemini M, Rojas-Benavente J, Gonzalez-Tendero A, Garcia-Posada R, Rodriguez-Lopez M, Demicheva E, Sitges M, Gratacos E. Postsystolic shortening by myocardial deformation imaging as a sign of cardiac adaptation to pressure overload in fetal growth restriction. Circ Cardiovasc Imaging 2014; 7: 781-787.
    1. Ingul CB, Loras L, Tegnander E, Eik-Nes SH, Brantberg A. Maternal obesity affects fetal myocardial function as early as in the first trimester. Ultrasound Obstet Gynecol 2016; 47: 433-442.
    1. Crepaz R, Secchieri S, Svaluto G, Milanesi O, Pitscheider W, Gentili L, Rubino M, Stellin G. Echocardiographic evaluation of systolic and diastolic left ventricular function following arterial switch operation in the neonatal period for transposition of the great arteries. Midterm results. G Ital Cardiol 1997; 27: 224-230.
    1. Adhyapak SM, Mahala BK, Pujar SV, Shetty PK, Sharma R. Impact of left ventricular function on early outcomes after arterial switch for D-transposition of great arteries with intact ventricular septum. Indian Heart J 2007; 59: 137-141.
    1. Xie M, Zhang W, Cheng TO, Wang X, Lu X, Hu X. Left ventricular torsion abnormalities in patients after the arterial switch operation for transposition of the great arteries with intact ventricular septum. Int J Cardiol 2013; 168: 4631-4637.
    1. van Doesburg NH, Bierman FZ, Williams RG. Left ventricular geometry in infants with d-transposition of the great arteries and intact interventricular septum. Circulation 1983; 68: 733-739.
    1. Rodriguez-Lopez M, Cruz-Lemini M, Valenzuela-Alcaraz B, Garcia-Otero L, Sitges M, Bijnens B, Gratacos E, Crispi F. Descriptive analysis of the different phenotypes of cardiac remodeling in fetal growth restriction. Ultrasound Obstet Gynecol 2017; 50: 207-221.
    1. Wilson AD, Rao S, Aeschlimann S. Normal fetal foramen flap and transatrial Doppler velocity pattern. J Am Soc Echocardiogr 1990; 3: 491-494.
    1. van Dalen BM, Tzikas A, Soliman OI, Heuvelman HJ, Vletter WB, Ten Cate FJ, Geleijnse ML. Assessment of subendocardial contractile function in aortic stenosis: a study using speckle tracking echocardiography. Echocardiography 2013; 30: 293-300.
    1. Delhaas T, Kotte J, van der Toorn A, Snoep G, Prinzen FW, Arts T. Increase in left ventricular torsion-to-shortening ratio in children with valvular aortic stenosis. Magn Reson Med 2004; 51: 135-139.
    1. Patey O, Carvalho JS, Thilaganathan B. Left ventricular torsional mechanics in term fetuses and neonates. Ultrasound Obstet Gynecol 2020; 55: 233-241.
    1. Patey O, Gatzoulis MA, Thilaganathan B, Carvalho JS. Perinatal Changes in Fetal Ventricular Geometry, Myocardial Performance, and Cardiac Function in Normal Term Pregnancies. J Am Soc Echocardiogr 2017; 30: 485-492.e5.
    1. Patey O, Carvaho JS, Thilaganathan B. Perinatal changes in cardiac geometry and function in growth restricted fetuses at term. Ultrasound Obstet Gynecol 2018; 53: 655-662.
    1. Patey O, Carvalho JS, Thilaganathan B. Perinatal changes in fetal cardiac geometry and function in gestational diabetic pregnancies at term. Ultrasound Obstet Gynecol 2019; 54: 634-642.
    1. Patey O. Re: Differential effect of assisted reproductive technology and small-for-gestational age on fetal cardiac remodeling. B. Valenzuela-Alcaraz, F. Crispi, M. Cruz-Lemini, B. Bijnens, L. García-Otero, M. Sitges, J. Balasch and E. Gratacós. Ultrasound Obstet Gynecol 2017; 50: 63-70. Ultrasound Obstet Gynecol 2017; 50: 17-18.
    1. Patey O, Carvalho JS, Thilaganathan B. Intervendor Discordance of Fetal and Neonatal Myocardial Tissue Doppler and Speckle-Tracking Measurements. J Am Soc Echocardiogr 2019; 32: 1339-1349.
    1. Rudolph AM. Congenital cardiovascular malformations and the fetal circulation. Arch Dis Child Fetal Neonatal Ed 2010; 95: F132-F136.
    1. Konduri GG, Gervasio CT, Theodorou AA. Role of adenosine triphosphate and adenosine in oxygen-induced pulmonary vasodilation in fetal lambs. Pediatr Res 1993; 33: 533-539.
    1. Talemal L, Donofrio MT. Hemodynamic consequences of a restrictive ductus arteriosus and foramen ovale in fetal transposition of the great arteries. J Neonatal Perinatal Med 2016; 9: 317-320.
    1. Rudolph AM. The fetal circulation and its adjustments after birth in congenital heart disease. UCLA Forum Med Sci 1970; 10: 105-118.
    1. McMurphy DM, Heymann MA, Rudolph AM, Melmon KL. Developmental changes in constriction of the ductus arteriosus: responses to oxygen and vasoactive agents in the isolated ductus arteriosus of the fetal lamb. Pediatr Res 1972; 6: 231-238.
    1. Hawkins J, Van Hare GF, Schmidt KG, Rudolph AM. Effects of increasing afterload on left ventricular output in fetal lambs. Circ Res 1989; 65: 127-134.
    1. Gilbert RD. Control of fetal cardiac output during changes in blood volume. Am J Physiol 1980; 238: H80-H86.
    1. Baschat AA, Gembruch U. Development of fetal cardiac and extracardiac Doppler flow in early gestation. In Fetal Cardiology: Embryology, Genetics, Physiology, Echocardiographic Evaluation, Diagnosis and Perinatal Management of Cardiac Diseases (2nd edn), Yagel S, Silverman NH, Gembruch U (eds). Informa Healthcare/CRC Press: Boca Raton, FL, USA, 2009; 152-171.
    1. Brooks PA, Khoo NS, Mackie AS, Hornberger LK. Right ventricular function in fetal hypoplastic left heart syndrome. J Am Soc Echocardiogr 2012; 25: 1068-1074.
    1. Brooks PA, Khoo NS, Hornberger LK. Systolic and diastolic function of the fetal single left ventricle. J Am Soc Echocardiogr 2014; 27: 972-977.
    1. Jonker SS, Giraud MK, Giraud GD, Chattergoon NN, Louey S, Davis LE, Faber JJ, Thornburg KL. Cardiomyocyte enlargement, proliferation and maturation during chronic fetal anaemia in sheep. Exp Physiol 2010; 95: 131-139.
    1. Toischer K, Rokita AG, Unsold B, Zhu W, Kararigas G, Sossalla S, Reuter SP, Becker A, Teucher N, Seidler T, Grebe C, Preuss L, Gupta SN, Schmidt K, Lehnart SE, Kruger M, Linke WA, Backs J, Regitz-Zagrosek V, Schafer K, Field LJ, Maier LS, Hasenfuss G. Differential cardiac remodeling in preload versus afterload. Circulation 2010; 122: 993-1003.
    1. Hauton D, Ousley V. Prenatal hypoxia induces increased cardiac contractility on a background of decreased capillary density. BMC Cardiovasc Disord 2009; 9: 1.
    1. Jonker SS, Giraud GD, Espinoza HM, Davis EN, Crossley DA 2nd. Effects of chronic hypoxia on cardiac function measured by pressure-volume catheter in fetal chickens. Am J Physiol Regul Integr Comp Physiol 2015; 308: R680-R689.
    1. Fulton DR, Fyler DC. D-Transposition of the Great Arteries. In Nadas' Pediatric Cardiology (2nd edn), Keane JF, Lock JE, Fyler DC (eds). Saunders Elsevier: Philadelphia, PA, USA, 2006; 645.
    1. Lalezari S, Hazekamp MG, Bartelings MM, Schoof PH, Gittenberger-De Groot AC. Pulmonary artery remodeling in transposition of the great arteries: relevance for neoaortic root dilatation. J Thorac Cardiovasc Surg 2003; 126: 1053-1060.
    1. Johnson RC, Datar SA, Oishi PE, Bennett S, Maki J, Sun C, Johengen M, He Y, Raff GW, Redington AN, Fineman JR. Adaptive right ventricular performance in response to acutely increased afterload in a lamb model of congenital heart disease: evidence for enhanced Anrep effect. Am J Physiol Heart Circ Physiol 2014; 306: H1222-H1230.
    1. Minegishi S, Kitahori K, Murakami A, Ono M. Mechanism of pressure-overload right ventricular hypertrophy in infant rabbits. Int Heart J 2011; 52: 56-60.
    1. Kameny RJ, He Y, Morris C, Sun C, Johengen M, Gong W, Raff GW, Datar SA, Oishi PE, Fineman JR. Right ventricular nitric oxide signaling in an ovine model of congenital heart disease: a preserved fetal phenotype. Am J Physiol Heart Circ Physiol 2015; 309: H157-H165.
    1. Bogaard HJ, Abe K, Vonk Noordegraaf A, Voelkel NF. The right ventricle under pressure: cellular and molecular mechanisms of right-heart failure in pulmonary hypertension. Chest 2009; 135: 794-804.
    1. Jonker SS, Louey S. Endocrine and other physiologic modulators of perinatal cardiomyocyte endowment. J Endocrinol 2016; 228: R1-R18.
    1. Molina CE, Johnson DM, Mehel H, Spätjens RLHMG, Mika D, Algalarrondo V, Slimane ZH, Lechêne P, Abi-Gerges N, van der Linde HJ, Leroy J, Volders PGA, Fischmeister R, Vandecasteele G. Interventricular differences in β-adrenergic responses in the canine heart: role of phosphodiesterases. J Am Heart Assoc 2014; 3: e000858.
    1. Mital S. Right ventricle in congenital heart disease: is it just a “weaker” left ventricle? Arch Mal Coeur Vaiss 2006; 99: 1244-1251.
    1. Lai CT, Chow PC, Wong SJ, Chan KW, Cheung YF. Circulating annexin A5 levels after atrial switch for transposition of the great arteries: relationship with ventricular deformation and geometry. PLoS One 2012; 7: e52125.
    1. Fisher DJ, Heymann MA, Rudolph AM. Fetal myocardial oxygen and carbohydrate consumption during acutely induced hypoxemia. Am J Physiol 1982; 242: H657-H661.
    1. Chaoui R. Coronary arteries in fetal life: physiology, malformations and the “heart-sparing effect”. Acta Paediatr Suppl 2004; 93: 6-12.
    1. Rudolph AM. Impaired cerebral development in fetuses with congenital cardiovascular malformations: Is it the result of inadequate glucose supply? Pediatr Res 2016; 80: 172-177.
    1. Laser KT, Haas NA, Fisher M, Habash S, Degener F, Prinz C, Körperich H, Sandica E, Kececioglu D. Left ventricular rotation and right-left ventricular interaction in congenital heart disease: the acute effects of interventional closure of patent arterial ducts and atrial septal defects. Cardiol Young 2014; 24: 661-674.

Source: PubMed

3
Suscribir