fetal interventions for congenital heart disease in brazil

ORIGINAL ARTICLE

Fetal Interventions for Congenital Heart Disease in Brazil

Simone Rolim Fernandes Fontes Pedra • Cleisson Fabio Andrioli Peralta •

Luciana Crema • Ieda Bosisio Jatene • Rodrigo Nieckel da Costa •

Carlos Augusto Cardoso Pedra

Received: 14 May 2013 / Accepted: 28 August 2013 / Published online: 13 September 2013

� Springer Science+Business Media New York 2013

Abstract Fetal interventions have been performed for

some congenital heart diseases. However, these procedures

have not gained wide acceptance due to concerns about

their efficacy and safety. The aim of this study was to

report on a preliminary experience with fetal cardiac

interventions in Brazil. Twenty-two cardiac interventions

were performed in 21 fetuses. Thirteen fetuses had critical

aortic stenosis (CAS), 4 had hypoplastic left heart syn-

drome (HLHS) and intact interatrial septum or small patent

foramen ovale, 1 had pulmonary atresia with intact ven-

tricular septum (IVS), and 3 had critical pulmonary ste-

nosis (CPS). The main outcome variables evaluated were

technical success and procedural complications as well as

pregnancy and postnatal outcomes. Success was achieved

in 20 of 22 procedures (91 %) with 1 failed aortic and 1

failed pulmonary valvuloplasties. There was 1 fetal death.

No maternal complications occurred. One patient with

CAS, severe mitral regurgitation, and hydrops died post-

natally within 5 months of age. All patients with HLHS

and restrictive atrial septum died after interventional or

surgical procedures and prolonged hospitalizations. All

patients with CPS/IVS survived and achieved a biventric-

ular (BV) circulation after neonatal valvuloplasty and

ductal stenting. A BV circulation was achieved in 4 of 8

patients with CAS and evolving HLHS (one still in utero),

including 2 with initial borderline left ventricles (LV) in

whom surgical LV overhaul was performed at 9 months of

age. In this preliminary experience, the feasibility of fetal

cardiac interventions and their outcomes were similar to

those previously reported.

Keywords Congenital heart disease � Fetal

intervention � Fetal surgery � Fetal therapy

Introduction

Since first reported by Maxwell et al. [10] in 1991, fetal

interventions have been performed for some congenital

heart diseases, such as critical aortic stenosis (CAS),

hypoplastic left heart syndrome (HLHS), and pulmonary

atresia (PA) or critical pulmonary stenosis (CPS) with

hypoplastic right heart syndrome (HRHS) [1, 6–9, 11–13,

15–18]. The rationale behind these procedures is the pos-

sibility of improvement of cardiac morphology and func-

tion, which may help to change the natural intrauterine

history of these diseases. However, these interventions

have not gained wide acceptance due to concerns about

their efficacy and safety [4, 5].

The aim of this study was to describe our preliminary

experience with fetal cardiac intervention in the context of

an established cardiology program at a referral institution

in Brazil.

Materials and Methods

Case Selection

Records of all patients who underwent fetal cardiac inter-

ventions from July 2007 through December 2012 per-

formed by a multidisciplinary team were reviewed. The

parents provided written consent after they were informed

S. R. F. F. Pedra � C. F. A. Peralta (&) � L. Crema �I. B. Jatene � R. N. da Costa � C. A. C. Pedra

Fetal Cardiology Unit, Heart Hospital, Rua Desembargador

Eliseu Guilherme, 123, Sao Paulo, SP CEP 05675-120, Brazil

e-mail: [email protected]

123

Pediatr Cardiol (2014) 35:399–405

DOI 10.1007/s00246-013-0792-3

about the risks and potential benefits of these procedures.

The Ethics Committee for Clinical Investigation approved

this study.

The inclusion criteria for fetal intervention consisted of

isolated cardiac defects (i.e., absence of any other struc-

tural abnormality or marker for chromosomal aberration)

with the following echocardiographic findings:

1. CAS and evolving HLHS: The presence of thickened,

immobile aortic valve with turbulent or decreased

color Doppler flow; left-ventricular (LV) diastolic

length above the lower limit of normal (z-score[-2);

reversed blood flow in the transverse aortic arch; left-

to-right flow across the interatrial septum (IAS);

monophasic mitral valve inflow; and severe LV

dysfunction. In cases with smaller left ventricles (LV

diastolic length z-score \-2), valvuloplasty was

performed in an effort to ameliorate LV function [1,

6, 8, 11, 12].

2. CAS, massive mitral regurgitation (MR), giant left

atrium (GLA), and hydrops: Presence of dilated LV

and reversed flow in the transverse aortic arch [18].

3. HLHS and intact IAS or small patent foramen ovale

(PFO): The presence of unequivocal HLHS with either

an intact IAS or a small (B1 mm) PFO, dilated left

atrium, and pulmonary veins. The pulmonary vein flow

Doppler tracing was bidirectional with the systolic

component having the same velocity as the ‘‘a’’ wave

reversal and tiny or no forward flow in early diastole

[7, 9].

4. PA with intact ventricular septum (PA/IVS) or CPS

with impending HRHS: The presence of membranous

PA with identifiable pulmonary valve (PV) leaflets or

membrane; no/minimal systolic PV opening; no/min-

imal color Doppler ultrasound flow across the PV;

reversed flow in a patent ductus arteriosus; and right

heart hypoplasia with a tricuspid valve (TV) annulus

z-score \2 and an identifiable but qualitatively small

right ventricle (RV) [2, 15, 17].

Technique

Table 1 lists the standard technique used for the proce-

dures, which were all monitored solely by fetal echocar-

diography. A technically successful aortic or pulmonary

valvuloplasty was defined as a case where antegrade flow

and/or new aortic/pulmonary regurgitation were detected

by color Doppler. A technically successful atrial septo-

plasty was defined as a case where there was evidence of a

newly created atrial septal defect (ASD) with significant

improvement on the left-to-right shunt, which was associ-

ated with a decrease in LA size and improvement in the

pulmonary vein Doppler pattern.

Follow-up and Postnatal Management

Follow-up and delivery occurred at our center or at the

referring institution. Mothers had elective cesarean sections

(C-section), and the neonates were transferred to the

intensive care unit to receive prostaglandin.

Postnatal management varied according to the cardiac

defect and the institution providing care and consisted of

percutaneous aortic valvuloplasty through the carotid

artery; branch pulmonary artery banding and ductal stent-

ing through a median sternotomy (hybrid approach); atrial

septostomy; surgical aortic valvuloplasty; surgical mitral

replacement; surgical resection of endocardial fibroelasto-

sis (LV overhaul); and percutaneous pulmonary valvulo-

plasty plus ductal stenting.

Main Outcome Variables

The main outcome variables evaluated in this study were

technical success and procedural complications as well as

pregnancy and postnatal outcomes. Among the surviving

neonates, postnatal outcomes were characterized as (1)

having biventricular (BV) circulation from birth, (2) having

BV circulation (at the time of cross-sectional follow-up)

after an initial staging procedure, or (3) having univen-

tricular (UV) circulation (i.e., a definitive UV circulation

from birth or at the time of cross-sectional follow-up) or (4)

a temporary intermediate (mixed) circulation in which one

or both ventricles contributed to the systemic and pul-

monary output. Z-scores were calculated according to GA

on the basis of unpublished fetal norms derived from data

collected at The Children’s Hospital of Boston and used in

their previous publications [6–9, 11, 12, 17].

Results

Twenty-one fetuses with a median GA of 29 weeks (range

23–34) and a median estimated weight of 1,200 g (range

500–2,500) underwent cardiac interventions. Thirteen

fetuses had CAS (9 had evolving HLHS, of whom 3 had

LV diastolic length z-score \-2 and 4 had dilated LVs,

severe MR, GLA, and hydrops, respectively); 4 had HLHS

and intact IAS or small PFO; 1 had PA/IVS; and 3 had

CPS.

Technical Success and Procedural Complications

(Table 2)

Twenty of 22 interventions (91 %) were performed suc-

cessfully (case no. 17 underwent atrial septostomy and aortic

valvuloplasty). Significant pericardial effusion requiring

drainage (1–3 ml) for recovery and hemodynamic instability

400 Pediatr Cardiol (2014) 35:399–405

123

requiring epinephrine administration to resume the heart rate

were observed in 9 (45 %) and 8 (40 %) of the 20 technically

successful cases, respectively. No maternal complications

occurred.

Pregnancy and Postnatal Outcomes

CAS and Evolving HLHS (Fig. 1; Tables 2, 3)

Median GA at the procedure was 28 weeks (range 23–30).

One patient is still in utero (case no. 21), and one patient

(case no. 9) was born prematurely (34 weeks of gestation)

due to maternal pre-eclampsia.

Among those who had successful AV dilation and who

were born at term (n = 6), the survival rate was 50 %.

Three of four patients (75 %) who were delivered at our

center survived: one child (case no. 8) had a BV circulation

from birth, underwent a successful aortic valvuloplasty at

3 weeks of age, is doing well, and has normal LV size and

function. The other two patients (cases no. 13 and 14) had

borderline LVs at birth, underwent hybrid procedures, and,

at age 9 months, were changed to BV circulation after LV

rehabilitation and aortic valvotomy. One fetus (case no. 15)

had a severely dilated, dysfunctional thin-walled LV and

hydrops. No improvement in the size and function of the

left heart structures was observed. Because he was deemed

to have a functionally UV heart, the parents opted for

supportive care after delivery.

Both patients born at other centers had borderline LVs at

birth. One patient (case no. 5) died after bidirectional

cavopulmonary anastomosis at age 6 months. The other

patient (case no. 7) died after a hybrid procedure due to

complications related to central venous line insertion.

CAS, MR, GLA, and Hydrops (Tables 2, 3)

Four fetuses presented with this condition and underwent

successful aortic valvuloplasty at 25, 30 (two cases), and

34 weeks’ gestation. Postnatal survival rate was 25 %.

Two patients (cases no. 2 and 10) were born prematurely

(at 33 and 35 weeks of gestation, respectively) in other

institutions while still severely hydropic, and each died a

couple of hours after birth. The third patient (case no. 12)

was born at our institution and underwent aortic valvulo-

plasty with no improvement of mitral valve regurgitation.

She underwent surgical replacement of the mitral valve and

aortic valvuloplasty. At 5 months of age, she had severe

prosthesis stenosis, which was treated percutaneously, with

immediate severe MR followed by death. The fourth fetus

(case no. 19) had a successful valvuloplasty followed by

complete in utero resolution of the hydrops. After birth at

our institution, she underwent balloon septostomy and

aortic valvuloplasty, which resulted in a significant

improvement of her hemodynamic status. Due to mild LV

hypoplasia, a hybrid procedure was performed, and she was

discharge home at age 4 months.

HLHS and Intact IAS or Small PFO (Tables 2, 3)

There was no postnatal survival in this group. Our first

patient (case no. 1) had successful creation of a 3-mm ASD

at 32 weeks’ gestation. Delivery was at term at another

institution. The neonate underwent a successful hybrid

procedure on the day of life 4 followed by atrial stenting on

the postoperative day 14. She subsequently underwent

Norwood–Glenn surgery at age 5 months and died on the

operating room probably due to pulmonary hypertension.

The second patient (case no. 3) underwent a hybrid pro-

cedure and died from sepsis after a prolonged period under

Table 1 Technique for fetal cardiac intervention

Uterine contraction prevention

Nifedipine 20 mg PO TID starting 8 h before and 2 more doses

afterward

Maternal anesthesia

Conscious sedation and spinal blockade

Polydramnious evacuation (if needed)

Fetal external version (if needed) to obtain optimal angle of needle

entry

Fetal anesthesia (chordal or muscular)

Fentanyl ? pancuronium ? atropine (usual anesthetic doses)

Maternal access

Percutaneous transabdominal and transuterine

Fetal access

Transthoracic or subcostal

Valvuloplasties, apical access

Septostomy, right atrial wall access

Needles

Chiba 15 mm long, 17G, 18G, and 19G

Balloons

Coronary balloons premounted on 0.01400 guidewire (floppy tip)

3.0–4.0 mm diameter, 6–10 mm length

System marked and secured with sterile tapes

Septostomy

4.0 mm diameter balloons inflated B 4.7 mm

Aortic and pulmonary valvuloplasties

10–30 % greater than valve annulus

System (wire ? balloon ? needle) withdrawn as a unit

Pericardial effusion drainage

20G Chiba needle

Fetal resuscitation if needed

Epinephrine and/or atropine in pericardial space (small doses)

Pediatr Cardiol (2014) 35:399–405 401

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difficult mechanical ventilation. One fetal death (case no.

4) occurred the day after successful and uneventful atrial

septoplasty (transplacental approach).

In our last case (no. 17), atrial septostomy was performed

successfully and was followed by aortic valvuloplasty with

significant improvement of antegrade aortic flow. The

neonate underwent an atrial septostomy immediately after

birth followed by a hybrid procedure. A complicated post-

operative course ensued, and the patient died at age

4 months.

Table 2 Indications and results of 22 interventions for congenital heart disease performed in 21 fetuses

Case no. GA (weeks) Disease/indication Procedure Result

1 32 HLHS ? small PFO AS Successful

2 30 CAS ? MR ? GLA ? hydrops AoV Successful

3 29 HLHS ? intact IAS AS Successful

4 32 HLHS ? small PFO AS Successful

5 29 CAS ? evolving HLHS AoV Successful

6 28 PA/IVS PuV Unsuccessful





11 29 4/7 CPS PuV Successful



14 27 5/7 CAS ? evolving HLHSa AoV Successful

15 25 4/7 CAS ? evolving HLHS ? hydrops AoV Successful

16 23 CAS ? evolving HLHSa AoV Unsuccessful

17 26 HLHS ? small PFO AS ? AoV Successful

18 29 CPS PuV Successful


20 27 CPS PuV Successful

21 29 CAS ? evolving HLHSa AoV Successful

GA gestational age, HLHS hypoplastic left heart syndrome, PFO patent foramen ovale, AS atrial septostomy, CAS critical aortic stenosis, MR

mitral regurgitation, GLA giant left atrium, AoV aortic valvuloplasty, IAS inter-atrial septum, PA/IVS pulmonary atresia and intact ventricular

septum, PuV pulmonary valvuloplasty, CPS critical pulmonary stenosisa Small LV = diastolic length Z-score \-2

Fig. 1 Serial echocardiograms of a fetus who underwent aortic

valvuloplasty (case no. 13, Tables 1 and 2). a Four-chamber view at

27 weeks of gestation before fetal intervention. The LV is dysfunc-

tional and small (long-axis z-value -4). There are patchy areas of

endocardial fibroelastosis and hypertrophic papillary muscle. The

mitral valve annulus is smaller than normal (z-value -3). b At birth,

the LV showed important growth (long-axis z-value -2.5) and

normal function. This neonate underwent a hybrid procedure as a

bridge to definitive repair. c At the age of 9 months, the LV was of

normal size (long-axis z-value -0.1). Patchy areas of endocardial

fibroelastosis are seen on the septum. The infant underwent successful

LV overhaul and surgical aortic valvuloplasty after the ductal stent

and pulmonary artery bands were removed

402 Pediatr Cardiol (2014) 35:399–405

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PA/IVS and CPS with Impending HRHS (Fig. 2; Tables 2,

3)

Our first valvuloplasty attempt (case 6) was unsuccessful

due to a high point of needle entry in the infundibulum.

This child died from sepsis at age 8 weeks after successful

radiofrequency-assisted PV dilation and ductal stenting.

The second fetus (case no. 11) was born at term with PV

stenosis. The neonate underwent successful pulmonary

valvuloplasty on day of life 2 followed by ductal stenting.

The child is now 5 months old and doing well.

The third and fourth fetuses, each with moderate to

severe RV hypoplasia (cases no. 18 and 20), had significant

increase in their RV sizes after pulmonary valvuloplasty.

Both were born at our institution and underwent percuta-

neous pulmonary valvuloplasties and ductal stenting.

Discussion

In this preliminary experience, we have shown that fetal

cardiac interventions were feasible in our hands and that

the outcomes were comparable with those of other insti-

tutions. Several aspects of these interventions merit

discussion.

Older GA at intervention was observed in our series

when compared with those seen in previous reports, par-

ticularly for aortic and pulmonary valvuloplasties [7, 16,

17]. This probably results from late prenatal diagnosis and

referrals in our environment and perhaps some reluctance

to accept fetal cardiac intervention as a feasible treatment

modality.

The indications for fetal interventions were similar to

those encountered in previously published experiences,

with the exception of intervening in fetuses with CAS and

smaller LVs (z-value -2 to -3). Acknowledging that fetal

CAS with evolving HLHS is intrinsically a disease of the

LV myocardium, we agree that only a subset of patients

would eventually achieve BV circulation [11, 12]. In our

series, BV circulation was observed in 50 % of patients

with CAS and evolving HLHS who underwent successful

AV dilation and who were born at term. However, we still

believe that there are other reasons to intervene in fetuses

with smaller and borderline LVs. This group may theo-

retically benefit from the procedure due to improved cor-

onary flow and preservation of myocardial function, which

may have a positive impact on neonatal outcomes regard-

less of the initial strategy (Norwood vs. hybrid). Because

the classic and modified neonatal Norwood procedures are

associated with disappointing outcomes in our institution,

the so-called hybrid approach has been widely adopted

with improved results in the last 5 years (unpublished

data). In such palliated patients, it is our impression that

antegrade aortic flow results in a more stable and predict-

able postoperative course. In addition, promoting forward

flow across the aortic valve in utero may theoretically help

minimize the neurodevelopmental abnormalities secondary

to retrograde transverse aortic arch perfusion observed in

Table 3 Postnatal procedures

and outcomes of 20 fetuses who

underwent prenatal

interventions for congenital

heart disease

HLHS hypoplastic left heart

syndrome, CAS critical aortic

stenosis, GLA giant left atrium,

PA/IVS pulmonary atresia and

intact ventricular septum, PuV

pulmonary valvuloplasty, AoV

aortic valvuloplasty, BV

biventricular, MV mitral valve,

LVRH left-ventricle

rehabilitation, UV

univentricular, BAS balloon

atrial septostomy

Case no. Disease Postnatal procedure Outcome

1 HLHS Hybrid–Norwood/Glenn Death at stage II

2 CAS ? GLA None Death soon after birth

3 HLHS Hybrid Death after hybrid procedure

4 HLHS None Death after fetal intervention

5 CAS Norwood I and II Death at stage II

6 PA/IVS PuV ? stent Death at 8 weeks of sepsis

7 CAS Hybrid Death after hybrid procedure

8 CAS AoV BV; survived

9 CAS AoV BV; prematurity; died

10 CAS ? GLA None Death soon after birth

11 CPS PuV ? stent BV; survived

12 CAS ? GLA MV replacement ? AoV BV; died at 5 months

13 CAS AoV ? hybrid ? LVRH BV; survived

14 CAS Hybrid ? LVRH BV; survived

15 CAS None Supportive care provided

16 CAS Hybrid UV; interstage death

17 HLHS BAS ? hybrid UV; interstage death


19 CAS ? GLA AoV ? hybrid Probable BV; survived


Pediatr Cardiol (2014) 35:399–405 403

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fetuses with established HLHS. Moreover, progressive

growth of the left heart structures during fetal life and

during infancy, resulting in an eventual BV repair, was

observed in two patients in this study.

Indications for interventions in fetuses with HLHS and

intact IAS or small PFO and PA/IVS were the same as

those found in the literature [7, 9]. Fetuses with CAS and

severe MR associated with hydrops have dismal outcomes

no matter what strategy employed was employed [18].

Perhaps in those patients, ASD creation, or enlargement of

PFO to decompress the GLA, should be assigned the same

importance as aortic valvuloplasty [18].

In this series, we employed techniques that had been

described before and which helped to optimize our learning

curve. Avoiding maternal general anesthesia most likely

facilitated fetal positioning and minimized the need for

laparotomy, which is eschewed in our practice.

Fetal hemodynamic instability due to bradycardia and

hemopericardium were common complications in this and

other series [8, 13, 15–17]. Therefore, prophylactic atro-

pine administration during fetal anesthesia, occasional

intracardiac or pericardial injection of epinephrine and

atropine, and prompt pericardial drainage should be con-

sidered as part of the standard of care in such interventions.

Although any fetal intervention may incite premature

labor, this complication was not observed in this series.

Nonetheless, three of our neonates were born preterm: two

had CAS, severe MR, and hydrops, and one had CAS and

evolving HLHS (prematurity was associated with maternal

pre-eclampsia). The observation that three of the remaining

six fetuses with CAS and evolving HLHS who were born

near term in this series achieved a BV circulation is

encouraging and in line with previously reported experi-

ences [1, 16].

It remains unclear whether our three patients with CPS

really benefited from fetal pulmonary valvuloplasty.

According to a previously published scoring system with

morphological and functional predictors of eventual BV

circulation, their PV and TV/MV ratio were already greater

than the cut-off values for UV circulation at 29–30 weeks

of gestation [2]. However, despite being more challenging

from a technical standpoint, procedural feasibility was

confirmed and thus may be useful for future cases.

Although we were able to create ASDs in fetuses with

HLHS and intact IAS or small PFO, postnatal outcomes

were disappointing. In two fetuses, the IAS was highly

restrictive at birth. In the other patient, despite an initially

favorable clinical course, death occurred due to pulmonary

hypertension. This raises the question of procedural effi-

cacy in late gestation in terms of preventing the develop-

ment of secondary pulmonary vascular and parenchymal

changes.

Although a fetal intervention may place the mother at

risk, previous experiences with cardiac and noncardiac

fetal interventions performed by our group and other

groups have shown excellent safety profile with limited

morbidity and no mortality to the mother [1, 3, 6–18].

Although we acknowledge that an elective C-section may

theoretically add some more risk to this equation and that

most centers advocate vaginal delivery for fetuses with

congenital heart disease, we believe that this delivery route

poses much less cardiovascular stress to such fragile

patients, especially those with CAS and ventricular dys-

function as well as those with HLHS and near-intact IAS.

In addition, an elective C-section facilitates postnatal care

and planning for subsequent invasive procedures. Finally,

assessment and perception of maternal and fetal risks

should take into consideration each individual’s value

system. What is a tolerable risk for some parents may differ

from others with a different culture, socioeconomic class,

religious background, or personal family situation. Proper

parental counseling with more than one individual and

Fig. 2 Serial echocardiograms of a fetus who underwent pulmonary

valvuloplasty (case no. 11, Tables 1 and 2). a Four-chamber view at

29 weeks of gestation before fetal intervention. The RV (long-axis

z-value -4.1) and the TV (z-value -2.7) are small. b The balloon is

inflated at the PV level. The neonate underwent pulmonary

valvuloplasty and ductal stenting. c Four-chamber view at age

5 months. The RV is of normal size (z-value TV -1.3). There is

predominant left-to-right shunting across a PFO. The ductal stent

closed spontaneously, and the RV outflow tract is unobstructed

404 Pediatr Cardiol (2014) 35:399–405

123

institutional surveillance are crucial to ensure that parents

are aware of the current state of knowledge and possible

alternatives to fetal catheter intervention. This highlights

the importance of establishing a complete fetal cardiac

program with its own peculiarities from diagnostic to

prenatal and postnatal cardiologic and neonatal treatment

capabilities and parental support [4, 5].

This study has obvious limitations, including its

descriptive nature, small number of patients, and nonuni-

form postnatal care. However, we believe that none of

these limitations affects the take-home message of this

report.

The feasibility of fetal cardiac interventions and their

outcomes in this preliminary experience were similar to

those previously reported. Although we believe that the

data presented herein justify expanding the availability of

fetal catheter intervention as a treatment option to centers

with the infrastructure and commitment to perform these

procedures, they should still be restricted to referral centers

that can amass a critical volume of experience to ensure

clinical competence.

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fetal interventions for congenital heart disease in brazil

Art & Photos

abstract fetal interventions

fetal death

fetal cardiac inter

congenital heart diseases

heart syndrome hlhs

critical aortic stenosis

heart syn drome hlhs

preliminary experience