Fetal cardiac interventions: an update of therapeutic options

Intervenções cardíacas fetais: atualização de opções terapêuticas

Shi-Min Yuan About the author

Abstracts

Objective:

This article aims to present updated therapeutic options for fetal congenital heart diseases.

Methods:

Data source for the present study was based on comprehensive literature retrieval on fetal cardiac interventions in terms of indications, technical approaches and clinical outcomes.

Results:

About 5% of fetal congenital heart diseases are critical and timely intrauterine intervention may alleviate heart function. Candidates for fetal cardiac interventions are limited. These candidates may include critical aortic valve stenosis with evolving hypoplastic left heart syndrome, pulmonary atresia with an intact ventricular septum and evolving hypoplastic right heart syndrome, and hypoplastic left heart syndrome with an intact or highly restrictive atrial septum as well as fetal heart block. The advocated option are prenatal aortic valvuloplasty, pulmonary valvuloplasty, creation of atrial communication and fetal cardiac pacing.

Conclusion:

Fetal cardiac interventions are feasible at midgestation with gradually improved technical success and fetal/postnatal survival due mainly to a well-trained multidisciplinary team, sophisticated equipment and better postnatal care.

Fetal Heart; Heart Defects, Congenital; Prognosis


Objetivo:

Este artigo tem como objetivo apresentar opções terapêuticas atualizadas para cardiopatias congênitas fetais.

Métodos:

Os dados do presente estudo foram baseados em uma revisão abrangente da literatura a respeito de intervenções cardíacas fetais em termos de indicações, abordagens técnicas e resultados clínicos.

Resultados:

Cerca de 5% das cardiopatias congênitas fetais são críticas e a intervenção intrauterina oportuna pode aliviar a função cardíaca. Os candidatos para intervenções cardíacas fetais são limitados e podem incluir aqueles que são portadores de estenose valvar aórtica crítica com evolução para síndrome de hipoplasia do coração esquerdo, atresia pulmonar com septo ventricular íntegro e com evolução da síndrome de hipoplasia do coração direito e síndrome de hipoplasia do coração esquerdo com septo atrial intacto ou altamente restritivo, bem como bloqueio cardíaco fetal. As opções preconizadas são a valvoplastia aórtica fetal, valvoplastia pulmonar, criação de comunicação interatrial e implante de marca-passos em fetos.

Conclusão:

Intervenções cardíacas fetais são viáveis na fase intermediária da gestação com sucesso técnico e sobrevivência fetal/pós-natal, sendo aprimorados gradualmente, devido, sobretudo, a uma equipe multidisciplinar bem treinada, equipamentos sofisticados e melhores cuidados no pós-natal.

Coração Fetal; Cardiopatias Congênitas; Prognóstico


INTRODUCTION

Cardiac malformations can be a result of intrinsic myocardial disease or a secondary adaptive mechanism of fetal heart during in utero development[1Crispi F, Gratacós E. Fetal cardiac function: technical considerations and potential research and clinical applications. Fetal Diagn Ther. 2012;32(1-2):47-64.]. Pressure and volume stimuli of blood flow through the fetal heart are important determinants of the development of fetal heart and circulation during the second and third trimesters[1Crispi F, Gratacós E. Fetal cardiac function: technical considerations and potential research and clinical applications. Fetal Diagn Ther. 2012;32(1-2):47-64.]. In order to reduce perinatal morbidity and mortality, an early diagnosis of the fetal congenital heart disease (CHD) in the parturients who are at an increased risk of CHD is imperative, particularly for those with a family history of CHD[2Müller MA, Clur SA, Timmerman E, Bilardo CM. Nuchal translucency measurement and congenital heart defects: modest association in low-risk pregnancies. Prenat Diagn. 2007;27(2):164-9.]. About 5% of prenatally diagnosed CHDs including severe aortic stenosis (AS) (1.6%), pulmonary atresia with intact ventricular septum (PA/IVS) (1.9%) and severe pulmonary valve stenosis (1.5%) can be critical and therefore require intrauterine therapeutic interventions[3Simpson JM. Fetal cardiac interventions: worth it? Heart. 2009;95(20):1653-5.]. Early diagnosis of treatable CHDs may improve fetal intervention outcomes[4Acharya G, Sitras V, Maltau JM, Dahl LB, Kaaresen PI, Hanssen TA, et al. Major congenital heart disease in Northern Norway: shortcomings of pre- and postnatal diagnosis. Acta Obstet Gynecol Scand. 2004;83(12):1124-9.], allowing ventricular growth and angiogenesis for fetus with semilunar valve stenosis for successful adaptation to extrauterine life[5Gardiner HM. Response of the fetal heart to changes in load: from hyperplasia to heart failure. Heart. 2005;91(7):871-3.]. Advanced imaging technology and equipment have made an accurate diagnosis of most fetal CHDs possible[6Van Aerschot I, Rosenblatt J, Boudjemline Y. Fetal cardiac interventions: myths and facts. Arch Cardiovasc Dis. 2012;105(6-7):366-72.]. Among them, echocardiography is a reliable means for prenatal diagnosis of a wide spectrum of CHDs[3Simpson JM. Fetal cardiac interventions: worth it? Heart. 2009;95(20):1653-5.]. At present, diagnosis of CHDs at midgestation (18-24-week gestation) has become feasible in almost all situations[7Allan LD, Chita SK, Sharland GK, Fagg NL, Anderson RH, Crawford DC. The accuracy of fetal echocardiography in the diagnosis of congenital heart disease. Int J Cardiol. 1989;25(3):279-88.]. However, minor errors might occur in echocardiographic visualization of a CHD probably due to poor image quality, early (<20 weeks) or late (>34 weeks) gestation, or maternal obesity[7Allan LD, Chita SK, Sharland GK, Fagg NL, Anderson RH, Crawford DC. The accuracy of fetal echocardiography in the diagnosis of congenital heart disease. Int J Cardiol. 1989;25(3):279-88.].

Prenatal interventions for structural CHDs are now plausible with high rates of technical success at midpregnancy[8Pedra SF, Peralta CF, Pedra CAC. Future directions of fetal interventions in congenital heart disease. Interv Cardiol Clin. 2013;2:1-10.]. Boston experiences have confirmed candidates for fetal cardiac interventions, which are critical AS with evolving hypoplastic left heart syndrome (HLHS), PA/IVS and evolving hypoplastic right heart syndrome, and HLHS with an intact or highly restrictive atrial septum[9Dietzel B. Helping families access fetal cardiac intervention to interrupt evolving HLHS and HRHS. Congenit Cardiol Today. 2011;9(8):14-5.]. Moreover, fetuses with hypoplasia of the tricuspid valve annulus seem to be good candidates for pulmonary valve intervention, allowing sufficient right heart growth[6Van Aerschot I, Rosenblatt J, Boudjemline Y. Fetal cardiac interventions: myths and facts. Arch Cardiovasc Dis. 2012;105(6-7):366-72.]. Minimal invasiveness (percutaneous access, only one cardiac puncture, and placental avoidance) and free from complications (fetal bradycardia, effusions and thrombus) are regarded as an ideal procedure[1010 Bacha E. The impact of fetal cardiac intervention on neonatal cardiac surgery [Accessed July 1, 2014]. Available from: http://av.conferencearchives.com/pdfs/100502/09.08.pdf
http://av.conferencearchives.com/pdfs/10...
].

Fetal Cardiac Intervention

Intrauterine balloon aortic valvuloplasty

Severe AS is associated with left ventricular outflow obstruction and may lead to irreversible left ventricular dysfunction secondary to volume overload with right heart failure and hydrops fetalis[1111 Schmider A, Henrich W, Dähnert I, Dudenhausen JW. Prenatal therapy of non-immunologic hydrops fetalis caused by severe aortic stenosis. Ultrasound Obstet Gynecol. 2000;16(3):275-8.]. It may develop into HLHS prenatally and is associated with poor postnatal survival if left untreated in the uterus[1212 Maxwell D, Allan L, Tynan MJ. Balloon dilatation of the aortic valve in the fetus: a report of two cases. Br Heart J. 1991;65(5):256-8.]. Retrograde flow in the transverse aortic arch, severe left ventricular dysfunction, monophasic and short mitral valve inflow and left-to-right flow across the foramen ovale can be determinants of AS progression into HLHS, in which very few chances of left heart growth and function can be available for a biventricular outcome[1313 Mäkikallio K, McElhinney DB, Levine JC, Marx GR, Colan SD, Marshall AC, et al. Fetal aortic valve stenosis and the evolution of hypoplastic left heart syndrome: patient selection for fetal intervention. Circulation. 2006;113(11):1401-5.]. Clinical observations also confirmed pre- and postnatal evolution of HLHS were associated with not only prenatal critical AS, but also endocardial fibroelastosis of the left ventricle[1414 Sharland GK, Chita SK, Fagg NL, Anderson RH, Tynan M, Cook AC, et al. Left ventricular dysfunction in the fetus: relation to aortic valve anomalies and endocardial fibroelastosis. Br Heart J. 1991;66(6):419-24.]. By echocardiography, endocardial fibroelastosis is also implicated in post-interventional outcomes and postnatal heart growth[1515 McElhinney DB, Vogel M, Benson CB, Marshall AC, Wilkins-Haug LE, Silva V, et al. Assessment of left ventricular endocardial fibroelastosis in fetuses with aortic stenosis and evolving hypoplastic left heart syndrome. Am J Cardiol. 2010;106(12):1792-7.].

The entry criteria for prenatal intervention for critical AS have been advocated as severe AS or atresia with severe left ventricular dysfunction and the left ventricular length was not <2 SD below the mean for gestational age at diagnosis. The timing of intervention should be on an urgent basis because of the potential for rapid progression into left ventricular growth failure in fetuses[1616 Tworetzky W, Wilkins-Haug L, Jennings RW, van der Velde ME, Marshall AC, Marx GR, et al. Balloon dilation of severe aortic stenosis in the fetus: potential for prevention of hypoplastic left heart syndrome: candidate selection, technique, and results of successful intervention. Circulation. 2004;110(15):2125-31.].

The first intrauterine balloon aortic valvuloplasty was reported in 1989 for the treatment of critical AS in two fetuses[1212 Maxwell D, Allan L, Tynan MJ. Balloon dilatation of the aortic valve in the fetus: a report of two cases. Br Heart J. 1991;65(5):256-8.]. However, one died intrauterine post-intervention and the other died postnatally. The problem encountered during the maneuver was difficulty of needle withdrawal after the access to the fetal heart, which was afterwards resolved by the utilization of a stillette needle. Tworetzky et al.[1616 Tworetzky W, Wilkins-Haug L, Jennings RW, van der Velde ME, Marshall AC, Marx GR, et al. Balloon dilation of severe aortic stenosis in the fetus: potential for prevention of hypoplastic left heart syndrome: candidate selection, technique, and results of successful intervention. Circulation. 2004;110(15):2125-31.] reported successful aortic valvuloplasty, preventing the evolution of HLHS in fetuses with AS in 2004. Of the 20 pregnancies at 21-29-week gestation, technical success rate was 70% and subsequent postnatal biventricular repair rate was 21%. Further observations by echocardiography revealed left heart growth arrest in unsuccessful or declined cases, but ongoing left heart growth in successful cases. Resumed left heart growth leading to a biventricular circulation at birth was observed in three babies[1616 Tworetzky W, Wilkins-Haug L, Jennings RW, van der Velde ME, Marshall AC, Marx GR, et al. Balloon dilation of severe aortic stenosis in the fetus: potential for prevention of hypoplastic left heart syndrome: candidate selection, technique, and results of successful intervention. Circulation. 2004;110(15):2125-31.]. Arzt et al.[1717 Arzt W, Wertaschnigg D, Veit I, Klement F, Gitter R, Tulzer G. Intrauterine aortic valvuloplasty in fetuses with critical aortic stenosis: experience and results of 24 procedures. Ultrasound Obstet Gynecol. 2011;37(6):689-95.] reported 24 aortic valvuloplasties in 23 fetuses with critical AS at 26 (range, 21-32)-week gestation, both technical success and postnatal biventricular repair rates were 66.7%. Recently, Goldstein et al.[1818 Goldstein BH, Fifer CG, Armstrong AK, Gelehrter SK, Treadwell MC, van de Ven C, et al. Use of a pressure guidewire in fetal cardiac intervention for critical aortic stenosis. Pediatrics. 2011;128(3):e716-9.] introduced a standard 0.014-inch Prime-Wire Prestige coronary guidewire for aortic valvuloplasty. With the aid of a micromanometer pressure sensor 3 cm from the tip, it was directed into the left ventricle and across the severely stenotic aortic valve. Immediate aortic pressure drop was seen after the procedure. This technique allows several potential advantages over conventional procedures in continuous monitoring of pressure waveforms, improvement of intraprocedural fetal hemodynamic monitoring and responsiveness to resuscitation.

Intrauterine aortic valvuloplasty for AS is technically feasible. Success depends on a series of predictive factors, including cardiac structural changes (severe endocardial fibroelastosis), devices available (angle of cannula entry, cannula designs and catheter and wire configurations), fetal positioning, ultrasound imaging, maneuver sophistications and post-interventional care, etc. In addition, quick maneuvers may minimize the progressive fetal bradycardia. A successful procedure was anyway achieved in 81% at 21-26-week gestation fetuses[1616 Tworetzky W, Wilkins-Haug L, Jennings RW, van der Velde ME, Marshall AC, Marx GR, et al. Balloon dilation of severe aortic stenosis in the fetus: potential for prevention of hypoplastic left heart syndrome: candidate selection, technique, and results of successful intervention. Circulation. 2004;110(15):2125-31.]. The mortality and morbidity of fetal AS were mainly due to technical errors and due to the degree of the hemodynamic effects of the stenosis and left ventricular adaptation, development and function during fetal life[1919 Gül A, Saygili A, Kavuncuoglu S, Ceylan Y. Balloon valvuloplasty for critical aortic stenosis in a fetus: a case report. Turk Kardiyol Dern Ars. 2013;41(2):161-5.].

However, fetal aortic valvuloplasty was not a definitive solution for fetal AS. In order to have a biventricular outcome, postnatal interventions are often required, such as repeated aortic valvuloplasty in most cases, temporary left atrial decompression, and frequent surgical interventions, such as coarctation repair, resection of endocardial fibroelastosis, mitral valvuloplasty, etc.[2020 McElhinney DB, Marshall AC, Wilkins-Haug LE, Brown DW, Benson CB, Silva V, et al. Predictors of technical success and postnatal biventricular outcome after in utero aortic valvuloplasty for aortic stenosis with evolving hypoplastic left heart syndrome. Circulation. 2009;120(15):1482-90.].

Intrauterine pulmonary valvuloplasty

PA/IVS is characterized by complete obstruction to right ventricular outflow tract with varying degrees of right ventricular and tricuspid valve hypoplasia[2121 Plunkett MD, Mitropoulos F, Laks H. Pulmonary stenosis and pulmonary atresia with intact ventricular septum [Accessed July 1, 2014]. Available from: http://www.tsda.org/wp-content/uploads/2013/10/Chapter-62-Pulmonary-Stenosis-and-Pulmonary-Atresia-with-Intact-Ventricular-Septum.pdf
http://www.tsda.org/wp-content/uploads/2...
]. Intrauterine pulmonary valvuloplasty in fetuses with PA/IVS allows potential growth and functional improvement of the right heart thereby increasing postnatal survival and biventricular repair[2222 Arzt W, Tulzer G, Aigner M, Mair R, Hafner E. Invasive intrauterine treatment of pulmonary atresia/intact ventricular septum with heart failure. Ultrasound Obstet Gynecol. 2003;21(2):186-8.

23 Galindo A, Gutiérrez-Larraya F, Velasco JM, de la Fuente P. Pulmonary balloon valvuloplasty in a fetus with critical pulmonary stenosis/atresia with intact ventricular septum and heart failure. Fetal Diagn Ther. 2006;21(1):100-4.

24 Tulzer G, Artz W, Franklin RC, Loughna PV, Mair R, Gardiner HM. Fetal pulmonary valvuloplasty for critical pulmonary stenosis/atresia with intact septum. Lancet. 2002;360(9345):1567-8.
-2525 Tworetzky W, McElhinney DB, Marx GR, Benson CB, Brusseau R, Morash D, et al. In utero valvuloplasty for pulmonary atresia with hypoplastic right ventricle: techniques and outcomes. Pediatrics. 2009;124(3):e510-8.]. Prenatal treatment of the lesion may prevent development of non-immune hydrops and intrauterine death[2222 Arzt W, Tulzer G, Aigner M, Mair R, Hafner E. Invasive intrauterine treatment of pulmonary atresia/intact ventricular septum with heart failure. Ultrasound Obstet Gynecol. 2003;21(2):186-8.], however, only limited cases have been reported[2626 National Institute for Health and Clinical Excellence. Percutaneous fetal balloon valvuloplasty for pulmonary atresia with intact ventricular septum [Accessed July 1, 2014]. Available from: http://www.nice.org.uk/ip323overview
http://www.nice.org.uk/ip323overview...
]. Fetal cardiac intervention for PA/IVS is a challenging procedure because of the anatomical features of the right ventricular outflow tract and the difficult access to the pulmonary valve. With advancing gestation, a steady increase of the right ventricle-to-pulmonary artery gradient could lead to a high rate of pregnancy termination (61%) and some intrauterine death (5%) if left untreated[2727 Daubeney PE, Sharland GK, Cook AC, Keeton BR, Anderson RH, Webber SA. Pulmonary atresia with intact ventricular septum: impact of fetal echocardiography on incidence at birth and postnatal outcome. UK and Eire Collaborative Study of Pulmonary Atresia with Intact Ventricular Septum. Circulation. 1998;98(6):562-6.].

It has been shown that pulmonary valvuloplasty in fetal life is also technically feasible in midgestation. With optimal fetal positioning with the aid of adequate echo imaging, a limited maternal laparotomy without uterine exteriorization or incision could be attained. Fetal pulmonary balloon valvuloplasty can be performed at 21-32-week gestation under maternal local anesthesia and sedation by inserting a needle through maternal abdominal wall into the uterine cavity under ultrasound guidance. Fetal analgesic is then injected before advancing the needle through the fetal chest wall into the right ventricular infundibulum of the fetus. A guidewire is inserted through the needle and across the pulmonary valve. A balloon catheter is inserted and then inflated to dilate the stenotic valve. Access to the right ventricular outflow tract is acchieved through direct puncture by using a 19-gauge cannula via a subcostal approach on the fetal chest or an intercostal space next to the sternum, the cannula tip is directed into the right ventricular outflow tract and the atretic pulmonary valve is dilated by inflating a coronary angioplasty balloon. After the final balloon deflation, the wire, balloon and cannula are removed. The catheter and needle are then withdrawn[2626 National Institute for Health and Clinical Excellence. Percutaneous fetal balloon valvuloplasty for pulmonary atresia with intact ventricular septum [Accessed July 1, 2014]. Available from: http://www.nice.org.uk/ip323overview
http://www.nice.org.uk/ip323overview...
].

Since 2002, prenatal intervention for fetal PA/IVS has been performed for membranous pulmonary atresia with identifiable pulmonary valve leaflets or membrane, an intact or highly restrictive ventricular septal defect and right heart hypoplasia with a tricuspid valve annulus z score of <2. Compared with control fetuses with PA/IVS who did not undergo prenatal intervention with postnatal univentricular circulation, the tricuspid valve annulus, right ventricle length and pulmonary valve annulus grew significantly more from mid- to late gestation in the six fetuses that underwent successful interventions[2525 Tworetzky W, McElhinney DB, Marx GR, Benson CB, Brusseau R, Morash D, et al. In utero valvuloplasty for pulmonary atresia with hypoplastic right ventricle: techniques and outcomes. Pediatrics. 2009;124(3):e510-8.]. Gómez Montes et al.[2828 Gómez Montes E, Herraiz I, Mendoza A, Galindo A. Fetal intervention in right outflow tract obstructive disease: selection of candidates and results. Cardiol Res Pract. 2012;2012:592403.] reported fetal intervention was performed for PA/IVS in four fetuses with technical success in all of them and with some improvement of the right heart growth and hemodynamics early after the procedure, thereby increasing the chances for a biventricular repair.

Polat et al.[2929 Polat T, Danisman N. Pulmonary valvulotomy in a fetus with pulmonary atresia with intact ventricular septum: first experience in Turkey. Images Paediatr Cardiol. 2012;14(3):6-11.] also adopted a 0.014-inch floppy tipped coronary guide wire in the maneuver. The wire-catheter assembly was introduced through the needle until the balloon emerged. After deployed in the left pulmonary artery, the balloon was pulled back across the perforated valve with three consecutive inflations. Post-interventional echocardiography showed slight improvement in right ventricular compliance. They performed a successful valvulotomy of the pulmonary valve in a fetus with PA/IVS at 28-week gestation and fetal hemodynamic improvement was observed following the procedure. Galindo et al.[2323 Galindo A, Gutiérrez-Larraya F, Velasco JM, de la Fuente P. Pulmonary balloon valvuloplasty in a fetus with critical pulmonary stenosis/atresia with intact ventricular septum and heart failure. Fetal Diagn Ther. 2006;21(1):100-4.] reported successful valvuloplasty of the pulmonary valve performed in a fetus with critical pulmonary valve stenosis and heart failure at 25-week gestation. It is important to learn that midgestation fetal tricuspid valve z score>-3 and good tricuspid valve growth are the important factors leading to postnatal biventricular repair in fetuses with PA/IVS. According to the Boston experience, a Z-score >-3 is associated with biventricular outcome and a <-3 score with univentricular palliation[3030 Salvin JW, McElhinney DB, Colan SD, Gauvreau K, del Nido PJ, Jenkins KJ, et al. Fetal tricuspid valve size and growth as predictors of outcome in pulmonary atresia with intact ventricular septum. Pediatrics. 2006;118(2):e415-20.].

Prenatal intervention on the atrial septum

Hypoplastic left heart syndrome is potentially detectable in fetuses of 18-22-week gestation with a four-chamber view on echocardiography. With left heart obstruction, the existence of an interatrial communication is important for oxygenated blood to be distributed to the body and to prevent pulmonary congestion[3131 Cester M, Nanhorngue K, Pascoli I, Garofano G, Surico N, Paternoster DM. Hypoplastic left heart syndrome with intact atrial septum: case report. J Prenat Med. 2007;1(2):32-4.]. Prenatal intervention on the atrial septum is indicated for an intact or highly restrictive atrial septum, which promotes profound cyanosis and pulmonary edema after birth, leading to little effective pulmonary blood flow and resulting in chronic pulmonary venous hypertension and lymphatic dilation. This can in turn result in increased perioperative morbidity and mortality with stage I Norwood procedure. Postnatal atrial septotomy, albeit rapid and effective, may not reverse pulmonary vasculature pathologies and further mortality in the first few weeks or months of life. Therefore, midgestation intervention on atrial septum is imperative for preventing pulmonary vasculature changes, reducing the need for additional or urgent procedures and improving the infant's surgical outcome.

The maneuver of prenatal interventions on atrial septum has been described. After acessing the fetal heart, a communication is created by directing the needle across the atrial septum. A wire and small balloon are forwarded into the left atrium and a small atrial communication is enlarged by inflation of the balloon[3232 Balloon atrial septostomy for HLHS [Accessed July 1, 2014]. Available from: http://women.texaschildrens.org/Our-Services/Fetal-Center/Balloon-Atrial-Septostomy-for-HLHS
http://women.texaschildrens.org/Our-Serv...
]. A larger series of intrauterine atrial septoplasty in fetuses with HLHS was reported by Marshall et al.[3333 Marshall AC, Levine J, Morash D, Silva V, Lock JE, Benson CB, et al. Results of in utero atrial septoplasty in fetuses with hypoplastic left heart syndrome. Prenat Diagn. 2008;28(11):1023-8.]. Of 21 fetuses at 24-34-week gestation who received this procedure, there were 19 technical successes and two fetal deaths. An atrial septal defect of at least 3 mm in diameter was confirmed to allow postnatal benefit. However, postnatal outcomes were disappointing with a mortality of 58%. In order to keep septectomy open, a stent can be deployed across the atrial septum. Chaturvedi et al.[3434 Chaturvedi RR, Ryan G, Seed M, van Arsdell G, Jaeggi ET. Fetal stenting of the atrial septum: technique and initial results in cardiac lesions with left atrial hypertension. Int J Cardiol. 2013;168(3):2029-36.] performed percutaneous ultrasound-guided stenting of the atrial septum in 10 fetuses. Two fetuses developed stent stenosis and died postnatally from pulmonary hypertension and sepsis, respectively. Kalish et al.[3535 Kalish BT, Tworetzky W, Benson CB, Wilkins-Haug L, Mizrahi-Arnaud A, McEllhinney DB, et al. Technical challenges of atrial septal stent placement in fetuses with hypoplastic left heart syndrome and intact atrial septum. Catheter Cardiovasc Interv. 2014;84(1):77-85.] reported that nine fetuses at 24-31-week gestation with HLHS/IAS received fetal atrial septal stent placement, with technical success in five and failure in four cases. Stent deployment may decompress the left atrium. Additionally, there were no maternal complications.

Fetal cardiac pacing

Complete heart block can be life-threatening in fetuses. The etiologies were considered to be inflammation and fibrosis at the atrioventricular node associated with the production of antibodies[3636 Hutter D, Silverman ED, Jaeggi ET. The benefits of transplacental treatment of isolated congenital complete heart block associated with maternal anti-Ro/SSA antibodies: a review. Scand J Immunol. 2010;72(3):235-41.]. Heart block can progress during pregnancy and may result in hydrops fetalis and eventual fetal demise[3737 Friedman D, Duncanson Lj, Glickstein J, Buyon J. A review of congenital heart block. Images Paediatr Cardiol. 2003;5(3):36-48.]. There are few effective treatment options for fetal heart block, as side effects of fluorinated steroids (betamethasone or dexamethasone) have been concerned, whereas fetal heart rate and glomerular filtration rate irrespective of the gestational age were not significantly influenced[3838 van den Anker JN, Hop WC, de Groot R, van der Heijden BJ, Broerse HM, Lindemans J, et al. Effects of prenatal exposure to betamethasone and indomethacin on the glomerular filtration rate in the preterm infant. Pediatr Res. 1994;36(5):578-81.,3939 Ville Y, Vincent Y, Tordjman N, Hue MV, Fernandez H, Frydman R. Effect of betamethasone on the fetal heart rate pattern assessed by computerized cardiotocography in normal twin pregnancies. Fetal Diagn Ther. 1995;10(5):301-6.]. Moreover, poor response of congenital fetal heart block to intravenous maternal isoproterenol can be an indication for permanent pacemaker implant before birth[4040 Eghtesady P, Michelfelder EC, Knilans TK, Witte DP, Manning PB, Crombleholme TM. Fetal surgical management of congenital heart block in a hydropic fetus: lessons learned from a clinical experience. J Thorac Cardiovasc Surg. 2011;141(3):835-7.]. In general, a permanent pacemaker is required in about 66% of the cases[4040 Eghtesady P, Michelfelder EC, Knilans TK, Witte DP, Manning PB, Crombleholme TM. Fetal surgical management of congenital heart block in a hydropic fetus: lessons learned from a clinical experience. J Thorac Cardiovasc Surg. 2011;141(3):835-7.].

The first trial of fetal cardiac pacing with a pacemaker implant for complete heart block was reported in 1986[4141 Carpenter RJ Jr, Strasburger JF, Garson A Jr, Smith RT, Deter RL, Engelhardt HT Jr. Fetal ventricular pacing for hydrops secondary to complete atrioventricular block. J Am Coll Cardiol. 1986;8(6):1434-6.,4242 Walkinshaw SA, Welch CR, McCormack J, Walsh K. In utero pacing for fetal congenital heart block. Fetal Diagn Ther. 1994;9(3):183-5.]. Initial attempts of intrauterine percutaneous pacing through a transthoracic approach or an inferior vena cava route resulted in fetal demise shortly after the procedure. Later, Assad et al.[4343 Assad RS, Jatene MB, Moreira LFP, Sales PC, Aiello VD, Costa R, et al. Bloqueio A-V total congênito: novo modelo experimental para avaliação do marca-passo fetal. Rev Bras Cir Cardiovasc. 1994;9(3):133-40.,4444 Assad RS, Jatene MB, Moreira LF, Sales PC, Costa R, Hanley FL, et al. Fetal heart block: a new experimental model to assess fetal pacing. Pacing Clin Electrophysiol. 1994;17(7):1256-63.] designed two modified pacing electrodes: a screw-in lead (11/2 turns) and a stitch-on lead, which were tested in experimental models of fetal heart block induced by cryosurgical ablation of the atrioventricular node. They found that the screw-in electrode was better for fetal pacing.

The initially proposed approach was an epicardial pacing lead on the fetal heart with an extra-uterine pulse generator implanted in the mother. However, a lack of myocardial fixation and dislodgment of the percutaneous lead due to fetal movement were the major limitations of the percutaneous approach. To resolve this problem, an entire single chamber pacing system without exteriorized leads without risk of dislodgement of the pacing system was therefore developed[4545 Loeb GE, Zhou L, Zheng K, Nicholson A, Peck RA, Krishnan A, et al. Design and testing of a percutaneously implantable fetal pacemaker. Ann Biomed Eng. 2013;41(1):17-27.]. Such a design is now possible because of significant advances made in fetal surgery and fetal intervention, allowing the pacing system to be deployed through the maternal abdomen under ultrasound guidance.

Furthermore, Assad et al.[4646 Assad RS, Zielinsky P, Kalil R, Lima G, Aramayo A, Santos A, et al. New lead for in utero pacing for fetal congenital heart block. J Thorac Cardiovasc Surg. 2003;126(1):300-2.] designed a novel prototype T-shaped lead for secure fixation onto the fetal myocardium and prevention from electrode dislodgement, which could be introduced via an 18-gauge needle and therefore an open surgery was not needed. The new lead was tested in fetal goats, suggesting that a gradual increase in the fetal rate, beginning at 80 beats per minute after implantation would be more reliable for an adequate fetal cardiac output[4747 Assad RS, Thomaz PG, Valente AS, Costa R, Barbero-Marcial M, Oliveira SA. Experimental assessment of a new electrode for fetal pacing. Rev Bras Cir Cardiovasc. 2006;21(3):272-82.]. Boudjemline et al.[4848 Boudjemline Y, Rosenblatt J, de La Villeon G, Bénifla JL, Bonnet D, Jouannic JM. Development of a new lead for in utero fetal pacing. Prenat Diagn. 2010;30(2):122-6.] developed an implantable fetal pacing lead, which was made of a flexible quadrifilar coil with outer silicone insulation and a fixed screw on its distal tip. Attempts in 12 pregnant Pre-Alp ewes at 110-112 day gestation were successful for anchoring the lead on the ventricular wall in all 12 and on the atrium in three of them.

DISCUSSION

The reverse remodeling phenomenon should be even more pronounced in fetal life. Thus, fetal cardiac interventions were attempted aiming at promoting ventricular growth and function, decreasing intrauterine death and increasing survival[1010 Bacha E. The impact of fetal cardiac intervention on neonatal cardiac surgery [Accessed July 1, 2014]. Available from: http://av.conferencearchives.com/pdfs/100502/09.08.pdf
http://av.conferencearchives.com/pdfs/10...
]. Fetal cardiac interventions have been advocated for fetuses with semilunar valve stenosis[1616 Tworetzky W, Wilkins-Haug L, Jennings RW, van der Velde ME, Marshall AC, Marx GR, et al. Balloon dilation of severe aortic stenosis in the fetus: potential for prevention of hypoplastic left heart syndrome: candidate selection, technique, and results of successful intervention. Circulation. 2004;110(15):2125-31.,2424 Tulzer G, Artz W, Franklin RC, Loughna PV, Mair R, Gardiner HM. Fetal pulmonary valvuloplasty for critical pulmonary stenosis/atresia with intact septum. Lancet. 2002;360(9345):1567-8.,4949 Kohl T. Foetal cardiac interventions: overview and perspectives in 2012. Eur J Cardiothorac Surg. 2012;42(1):14-6.] or with HLHS with an intact or highly restrictive atrial septum[3333 Marshall AC, Levine J, Morash D, Silva V, Lock JE, Benson CB, et al. Results of in utero atrial septoplasty in fetuses with hypoplastic left heart syndrome. Prenat Diagn. 2008;28(11):1023-8.]. In the early years, fetal cardiac interventions showed poor outcomes, probably related to poor ultrasonographic imaging, limitations of equipment availability and poor fetal conditions[5050 Qureshi SA. Fetal interventions in congenital heart disease [Accessed July 1, 2014]. Available from: http://www.sha-conferences.com/files/presentation2011/090005.pdf
http://www.sha-conferences.com/files/pre...
]. Technical success of fetal cardiac interventions has greatly enhanced postnatal biventricular outcome, thereby avoiding the need for three-stage palliation or cardiac transplant[5151 Emery SP, Kreutzer J, McCaffrey FM, Sherman FS, Simhan HN, Keller BB. The learning curve for a fetal cardiac intervention team. Minim Invasive Surg. 2010;2010:674185.]. Despite the progress made in this field, these fetal cardiac interventions remain controversial in both indications and results[3Simpson JM. Fetal cardiac interventions: worth it? Heart. 2009;95(20):1653-5.,5252 Pavlovic M, Acharya G, Huhta JC. Controversies of fetal cardiac intervention. Early Hum Dev. 2008;84(3):149-53.].

There have been relatively fewer prenatal pulmonary valve interventions comparing with prenatal aortic valve intervention[5353 Matsui H, Gardiner H. Fetal intervention for cardiac disease: the cutting edge of perinatal care. Semin Fetal Neonatal Med. 2007;12(6):482-9.]. On the other hand, prenatal interventions for the management of pulmonary atresia and intact ventricular septum were often associated with increased risks of preterm delivery and neonatal mortality[4949 Kohl T. Foetal cardiac interventions: overview and perspectives in 2012. Eur J Cardiothorac Surg. 2012;42(1):14-6.]. Furthermore, pulmonary valve stenosis may be alleviated with the intrauterine right heart growth and the impact of interventional therapy on the pulmonary circulation does not seem to be as forceful as that on the systemic circulation secondary to fetal aortic valvuloplasty[3Simpson JM. Fetal cardiac interventions: worth it? Heart. 2009;95(20):1653-5.].

Candidates for fetal arrhythmic interventions have been considered supraventricular tachycardia refractory to conventional drug with a potential for progression into hydrops fetalis and fetal demise[5454 Simpson JM, Sharland GK. Fetal tachycardias: management and outcome of 127 consecutive cases. Heart. 1998;79(6):576-81.,5555 Jouannic JM, Delahaye S, Fermont L, Le Bidois J, Villain E, Dumez Y, et al. Fetal supraventricular tachycardia: a role for amiodarone as second-line therapy? Prenat Diagn. 2003;23(2):152-6.]. Immune complete heart block with low ventricular rate may cause significant decrease in fetal cardiac output, cardiac failure and hydrops fetalis[5656 Groves AM, Allan LD, Rosenthal E. Outcome of isolated congenital complete heart block diagnosed in utero. Heart. 1996;75(2):190-4.,5757 Jaeggi ET, Silverman ED, Yoo SJ, Kingdom J. Is immune-mediated complete fetal atrioventricular block reversible by transplacental dexamethasone therapy? Ultrasound Obstet Gynecol. 2004;23(6):602-5.]. The poor prognosis of these fetal arrhythmias has incited the development of alternative therapeutic strategies. Fetal ventricular pacing has been found to improve ventricular output in experimentally induced complete atrioventricular block[5858 Crombleholme TM, Harrison MR, Longaker MT, Langer JC, Adzick NS, Bradley S, et al. Complete heart block in fetal lambs. I. Technique and acute physiological response. J Pediatr Surg. 1990;25(6):587-93.]. However, initial attempts of fetal pacing have failed in human fetuses[4Acharya G, Sitras V, Maltau JM, Dahl LB, Kaaresen PI, Hanssen TA, et al. Major congenital heart disease in Northern Norway: shortcomings of pre- and postnatal diagnosis. Acta Obstet Gynecol Scand. 2004;83(12):1124-9.,4242 Walkinshaw SA, Welch CR, McCormack J, Walsh K. In utero pacing for fetal congenital heart block. Fetal Diagn Ther. 1994;9(3):183-5.,4545 Loeb GE, Zhou L, Zheng K, Nicholson A, Peck RA, Krishnan A, et al. Design and testing of a percutaneously implantable fetal pacemaker. Ann Biomed Eng. 2013;41(1):17-27.]. As open fetal surgery for intrauterine pacemaker insertion has been associated with unacceptable maternal morbidity and fetal demise, minimally invasive approaches using either transcutaneous ultrasound-guided[5959 Dell'Orfano J, Chou HA, Park D, Mirza H, Stys T, Mahan V, et al. The monolithic fetal pacemaker: prototype lead design for closed thorax deployment. Pacing Clin Electrophysiol. 2003;26(4 Pt 1):805-11.] or fetoscopic approaches[4747 Assad RS, Thomaz PG, Valente AS, Costa R, Barbero-Marcial M, Oliveira SA. Experimental assessment of a new electrode for fetal pacing. Rev Bras Cir Cardiovasc. 2006;21(3):272-82.] have been favored. Both endovascular route for intracardiac[4242 Walkinshaw SA, Welch CR, McCormack J, Walsh K. In utero pacing for fetal congenital heart block. Fetal Diagn Ther. 1994;9(3):183-5.] and epicardial lead anchorages[5959 Dell'Orfano J, Chou HA, Park D, Mirza H, Stys T, Mahan V, et al. The monolithic fetal pacemaker: prototype lead design for closed thorax deployment. Pacing Clin Electrophysiol. 2003;26(4 Pt 1):805-11.] were attempted. Adaptations of new leads to the fetal anatomy for a secure anchorage are crucial for obtaining better outcomes of fetal pacing. Fetal cardiac interventions by direct cardiac puncture are associated with significant fetal morbidity. In order to avoid direct cardiac puncture, Nugent et al.[6060 Nugent AW, Kowal RC, Juraszek AL, Ikemba C, Magee K. Model of magnetically guided fetal cardiac intervention: potential to avoid direct cardiac puncture. J Matern Fetal Neonatal Med. 2013;26(18):1778-81.] have employed successfully in an in vitro fetal heart model of approximating a 32-week gestation with magnetically steerable guide wires from the hepatic vein to the descending aorta and balloon to the aortic valve, in between 5 and 10 minutes.

The treatment of critical left ventricular outflow tract obstruction in the neonate and infant remains a significant challenge[6161 Najm HK. Uni-ventricular versus complex biventricular repair for neonates with critical AS [Accessed July 1, 2014]. Available from: http://www.sha-education.com/sites/all/sha23_presentations/30-1-2012/065002.pdf
http://www.sha-education.com/sites/all/s...
]. Postnatal surgical options include biventricular repair (surgical aortic valvotomy, balloon aortic valvotomy, Ross/Konno procedure and arch repair with or without other lesion repair), single ventricular repair (Norwood type), biventricular repair after initial single ventricular repair and cardiac transplantation[6161 Najm HK. Uni-ventricular versus complex biventricular repair for neonates with critical AS [Accessed July 1, 2014]. Available from: http://www.sha-education.com/sites/all/sha23_presentations/30-1-2012/065002.pdf
http://www.sha-education.com/sites/all/s...
]. Biventricular repair presents obvious advantages over univentricular type of repair in terms of better survival and lower hospitalization costs[6262 Copel JA, Tan AS, Kleinman CS. Does a prenatal diagnosis of congenital heart disease alter short-term outcome? Ultrasound Obstet Gynecol. 1997;10(4):237-41.]. Rhodes scores have been taken as reliable indicators for the determination of a biventricular or univentricular repair[6363 Rhodes LA, Colan SD, Perry SB, Jonas RA, Sanders SP. Predictors of survival in neonates with critical aortic stenosis. Circulation. 1991;84(6):2325-35.]. For conditions with no possibility of biventricular repair, the expectant parents may choose, between postnatal palliative management (such as the Norwood procedure for HLHS) or for interruption of pregnancy[6Van Aerschot I, Rosenblatt J, Boudjemline Y. Fetal cardiac interventions: myths and facts. Arch Cardiovasc Dis. 2012;105(6-7):366-72.]. Heart transplantation can be a third option for the parents in saving the baby with life-threatening, critical AS, which fails to other surgical interventions[6464 Heart transplant life-saving in neonatal aortic stenosis [Accessed July 1, 2014]. Available from: http://my.clevelandclinic.org/Documents/Childrens_Hospital/Heart_Boyle_Neonatal_Aortic_Stenosis_Fall_2008.pdf
http://my.clevelandclinic.org/Documents/...
].

At the beginning, the technical success and biventricular repair rates were low, which were now considered to be mostly attributed to postnatal care other than prenatal intervention, while technical failure was only responsible for small parts[4747 Assad RS, Thomaz PG, Valente AS, Costa R, Barbero-Marcial M, Oliveira SA. Experimental assessment of a new electrode for fetal pacing. Rev Bras Cir Cardiovasc. 2006;21(3):272-82.]. Only small part of the mortality could directly correlate with the prenatal intervention; whereas the greater part died postnatally probably due to the limited postnatal surgical and intensive care. The considerably improved survival rates and higher rates of postnatal biventricular repair following fetal dilation of severe semilunar valve obstructions were a result of proficient surgical and intensive care managements[4747 Assad RS, Thomaz PG, Valente AS, Costa R, Barbero-Marcial M, Oliveira SA. Experimental assessment of a new electrode for fetal pacing. Rev Bras Cir Cardiovasc. 2006;21(3):272-82.]. Most recently, with well-established multidisciplinary team and equipments, prenatal intervention success and postnatal biventricular repair rates have been significantly improved[1717 Arzt W, Wertaschnigg D, Veit I, Klement F, Gitter R, Tulzer G. Intrauterine aortic valvuloplasty in fetuses with critical aortic stenosis: experience and results of 24 procedures. Ultrasound Obstet Gynecol. 2011;37(6):689-95.]. In Brazil, fetal interventions for CHDs have achieved a 91% success rate. There were two failures out of the 22 procedures, one was aortic and the other was pulmonary valvuloplasty[6565 Pedra SR, Peralta CF, Crema L, Jatene IB, da Costa RN, Pedra CA. Fetal interventions for congenital heart disease in Brazil. Pediatr Cardiol. 2014;35(3):399-405.].

Technical challenges and poor candidate selection are the two major restrictive factors limiting the development of fetal cardiac interventions. Lee & Comstock[6666 Lee W, Comstock CH. Prenatal diagnosis of congenital heart disease: where are we now? Ultrasound Clin. 2006;1(2):273-91.] emphasized the importance of a well-established practice guidelines and a standardized diagnostic training team for prenatal diagnosis of CHDs. A multidisciplinary team with the incorporation of a pediatric cardiac surgeon with maternal-fetal medicine, interventional cardiologist and fetal echocardiography subspecialists is warranted. Future directions of fetal cardiac interventions lie on technical advancements such as computer-assisted navigation[6666 Lee W, Comstock CH. Prenatal diagnosis of congenital heart disease: where are we now? Ultrasound Clin. 2006;1(2):273-91.], open fetal cardiac surgery and fetoscopic cardiac surgery (Ebsteins' anomaly with hydrops fetalis, tetralogy of Fallot and pulmonary valve atresia).

Open fetal cardiac intervention currently remains stagnant at the stage of animal experiments. It has revealed that midterm ovine fetuses under 30-minute bypass was associated with decreased cardiac output and increased end-diastolic pressure of the right ventricle[6767 Duffy JY, Petrucci O, Baker RS, Lam CT, Reed CA, Everman DJ, et al. Myocardial function after fetal cardiac bypass in an ovine model. J Thorac Cardiovasc Surg. 2011;141(4):961-8, 968.e1.]. Impairment of placental perfusion and respiratory gas exchange have been observed in lamb placenta when the animals were subjected to normothemic or hypothemic CPB with more severe impairment seen under hypothermia[6868 Assad RS, Lee FY, Berger K, Hanley FI. Fetal cardiac surgery: hemodynamic characteristics of placenta during extracorporeal circulation. Rev Bras Cir Cardiovasc. 1991;6(1):38-44.]. Further studies showed right ventricular function of midterm ovine fetuses under 90-minute bypass was better preserved by fibrillatory arrest than by cardioplegia[6969 Petrucci O, Baker RS, Lam CT, Reed CA, Duffy JY, Eghtesady P. Fetal right ventricular myocardial function is better preserved by fibrillatory arrest during fetal cardiac bypass. Ann Thorac Surg. 2010;90(4):1324-31.]. During fetal heart bypass, a volume shift of approximately 100 mL/kg, equivalent to 0.8 mL/kg/min, occurred and this may require volume replacements during bypass and normal physiologic supplements after bypass for maintenance of blood volume[7070 Baker RS, Lam CT, Heeb EA, Eghtesady P. Dynamic fluid shifts induced by fetal bypass. J Thorac Cardiovasc Surg. 2009;137(3):714-22.]. Besides, fetal CPB may lead to a profound, early rise of vasopressin levels, which may in turn impair placental function[7171 Lam CT, Sharma S, Baker RS, Hilshorst J, Lombardi J, Clark KE, et al. Fetal stress response to fetal cardiac surgery. Ann Thorac Surg. 2008;85(5):1719-27.]. These achievements have laid sufficient foundation for future clinical practice of open fetal cardiac interventions in human fetuses.

CONCLUSIONS

Fetal cardiac interventions (intrauterine balloon aortic valvuloplasty, intrauterine pulmonary valvuloplasy, prenatal intervention on the atrial septum and fetal cardiac pacing) for four types of congenital heart defects are feasible during midgestation aiming at improving fetal cardiac function, minimizing loss of fetus and enhancing postnatal biventricular repair. The postnatal deaths are more likely to be a result of candidate selection, effects of improvement of ventricular circulation secondary to fetal cardiac interventions and surgical technical errors and probably a limited intensive care. For improving success rate and post-interventional outcomes, a well-trained team with sophisticated equipment is warranted. With improved patient selection, technical modifications, for example with a robotic interventional approach, promising outcomes may be achieved in future cases. Moreover, with the advances of fetal bypass techniques, it is anticipated that open fetal heart operations would become feasible to facilitate the early treatment of fetal CHDs in the future.

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  • No financial support.
  • This study was carried out at First Hospital of Putian, Teaching Hospital, Fujian Medical University, Putian, Fujian Province, People's Republic of China.

Publication Dates

  • Publication in this collection
    Jul-Sep 2014

History

  • Received
    30 Apr 2014
  • Accepted
    24 July 2014
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