Published online February 29, 2008
PEDIATRICS Vol. 121 No. 3 March 2008, pp. e660-e665 (doi:10.1542/peds.2007-1493)
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ARTICLE

Incremental Diagnostic Yield of Pediatric Cardiac Assessment After Fetal Echocardiography in the Offspring of Women With Congenital Heart Disease: A Prospective Study

Molly Thangaroopan, MD, Rachel M. Wald, MD, Candice K. Silversides, MD, SM, Jennifer Mason, RN, Jeffrey F. Smallhorn, MD, Mathew Sermer, MD, Jack M. Colman, MD and Samuel C. Siu, MD, SM

University of Toronto Pregnancy and Heart Disease Research Program, Mount Sinai Hospital, Toronto General Hospital, Hospital for Sick Children, University of Toronto, Toronto, Ontario, Canada


   ABSTRACT
TOP
 ABSTRACT
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
OBJECTIVE. We sought to determine the incremental diagnostic utility of pediatric cardiac assessment in the offspring of women with congenital heart disease who have had previous fetal echocardiography.

PATIENTS AND METHODS. We prospectively followed pregnant women with congenital heart disease who were receiving care at 2 obstetric and cardiac centers and identified 276 infants who underwent both fetal echocardiography and pediatric cardiac assessment. All of the infants with abnormal fetal echocardiography findings or abnormal pediatric cardiac assessments underwent subsequent confirmatory pediatric echocardiography.

RESULTS. In this cohort, congenital heart disease was detected in 22 (8%) of 276 offspring born to women with congenital heart disease. There was concordance between the results of fetal echocardiography and pediatric cardiac assessment in 235 (85%) of 276 offspring (231, both normal; 4, both abnormal) and discordance between the results of fetal echocardiography and pediatric cardiac assessment in 41 (15%) of 276 infants. In the 41 subjects with discordant results, there were normal fetal echocardiography findings but abnormal pediatric cardiac assessments in 35 of 41 (pediatric echocardiography revealed congenital heart disease in 18 of 35 and normal anatomy in 17 of 35) and abnormal fetal echocardiography findings but normal pediatric cardiac assessments in 6 of 41 (pediatric echocardiography findings normal in all 6 of the infants). Fetal echocardiography detected all of the major forms of congenital heart disease. Lesions missed by fetal echocardiography but detected on pediatric cardiac assessment included shunt lesions and minor valvular abnormalities.

CONCLUSIONS. Although fetal echocardiography can reliably exclude major forms of congenital heart disease, minor congenital heart disease lesions can be missed on fetal echocardiography; however, these can be diagnosed with careful pediatric cardiac assessment. Postnatal pediatric cardiac assessment has incremental diagnostic utility for the detection of congenital heart disease in the offspring of women with congenital heart disease and previous fetal echocardiography.

Key Words: fetal • pediatrics • diagnosis • congenital heart defects • echocardiography • pregnancy

Abbreviations: CHD—congenital heart disease • FE—fetal echocardiography • CA—pediatric cardiac assessment • PE—pediatric echocardiography • PDA—patent ductus arteriosus • VSD—ventricular septal defect

The incidence of congenital heart disease (CHD) is increased in children born to women with CHD (4.0%–8.0%) as compared with the normal population (0.8%–1.0%).1–4 Antenatal diagnosis of CHD with transabdominal fetal echocardiography (FE) is now accepted clinical practice in cases where an increased risk of CHD in the fetus has been established.5 The rationale for the performance of FE includes early counseling and decision-making for the expectant parents. In addition, in some forms of CHD, the outcome of a fetus with an antenatal diagnosis of CHD is improved relative to an infant diagnosed postnatally with the same cardiac lesion.6,7 Although the accuracy of FE for the diagnosis of major intracardiac pathology is excellent,8 milder forms of CHD (specifically, shunt lesions and minor valvular abnormalities) can often go undetected in fetal life. Nevertheless, even knowledge pertaining to less severe forms of CHD is of relevance and often necessitates postnatal surveillance to determine the need for and timing of possible intervention over the course of a lifetime.

The optimal strategy for the postnatal follow-up of children born to women with CHD is unclear. Despite the theoretical advantage of combining FE and pediatric cardiac assessment (CA) to maximize diagnostic yield for the detection of recurrent CHD, this approach has not been studied previously in a large population of pregnant women with CHD. Although current clinical guidelines recommend FE in this high-risk population of women,5 postnatal screening of infants at increased risk of CHD has not been formally evaluated. The aim of this study was to examine the additional utility of CA for the detection of CHD in the offspring of a large population of pregnant women with CHD who have had previous FE.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Consecutive pregnant women referred to the Toronto General or Mount Sinai hospitals in Toronto from October 1994 onward were prospectively enrolled if they had CHD and were included if they had completed 1 year of postpartum follow-up by January 2005. Excluded were women with acquired heart disease, isolated arrhythmia, hypertrophic cardiomyopathy, Marfan syndrome, and known genetic syndromes associated with CHD.

Referral for FE was made after 15 weeks gestation. FE was performed with an ATL 5000 ultrasound machine (ATL Ultrasound, Bothell, WA) and appropriately sized curved-array transducers (3.5–7.5 MHz). All of the fetuses were scanned using a sequential segmental anatomic approach.9–11 Expert fetal echocardiographers at the Hospital for Sick Children in Toronto interpreted all of the FE.

Comprehensive CA was performed on all of the children within the first year of life and included a thorough history obtained from the caregiver, detailed physical examination (including measurements of growth, oxygen saturation, 4-limb blood pressure evaluation, and detailed cardiovascular assessment), and the performance of a 15-lead electrocardiogram. Pediatric cardiologists affiliated with the Hospital for Sick Children performed each screening CA (with the exception of 4 patients for whom CA was performed by a local pediatrician). CA was considered abnormal if findings on the physical examination suggested cardiac disease (ie, tachypnea, cyanosis in the absence of pulmonary disease, abnormal 4-limb blood pressure, poor peripheral circulation, or pathologic murmur on auscultation, etc) or electrocardiographic anomalies consistent with CHD (ie, abnormalities in cardiac axis, chamber size, etc).

When pediatric cardiac disease was suspected, or if FE findings were abnormal, a postnatal confirmatory pediatric echocardiogram (PE) was obtained by using state-of-the-art echocardiography and high-frequency transducers. PE was performed by dedicated pediatric sonographers and reviewed by experienced pediatric echocardiographers at the Hospital for Sick Children. Research ethics approval was obtained at all of the participating institutions.

Baseline and pregnancy outcome data were prospectively collected and entered into the University of Toronto Pregnancy and Heart Disease Research Program database after extensive validity checks.12 Prospective postpartum data collection was continued for a 6-month minimum (longer if the first pediatric assessment occurred later than 6 months of age). For those infants with findings of CHD at birth, extended follow-up was obtained.

Data analysis was performed by using SPSS for Windows 14.0.01. (SPSS Inc, Chicago, IL). Means and SD were calculated for continuous data; median and ranges were also provided if data were not normally distributed. Categorical data were expressed as absolute counts and percentages. For the purpose of analysis, the data unit was individual fetus or infant (not woman or pregnancy). Agreement between FE and CA regarding the presence or absence of CHD in infants who had both assessments was the principal outcome of interest.


   RESULTS
TOP
 ABSTRACT
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Characteristics of the Study Population
A total of 353 fetuses (349 pregnancies with 2 twin gestations and 1 triplet gestation) in 318 women with CHD were eligible for inclusion in this study (see Fig 1). Of these, 194 pregnancies in 172 women had been included in previous studies evaluating maternal and neonatal outcomes in women with heart disease.12,13 The present study population was composed of 276 fetuses (274 singleton and 1 twin pregnancy) with antenatal FE and postnatal CA.


Figure 1
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  		FIGURE 1 The outcome of fetuses included in the study group. a Terminations of pregnancy: maternal cardiovascular reasons (n = 7), fetal genetic abnormality (n = 2), and psychological (n = 3). b CHD: pulmonary atresia and intact ventricular septum (n = 1), atrioventricular septal defect (n = 1), and complete transposition of the great arteries (n = 1).

 
The mean maternal age in the study group was 28 ± 6 years; maternal age of <20 or >35 years was present in 60 pregnancies (21%). Maternal comorbid conditions were present in 75 women (27%) and included hypertension, anemia, pulmonary disease, and thyroid disorders. In 8 pregnancies (3%), fetal CHD had complicated a previous pregnancy. Mean gestational age at FE was 21 weeks gestation (range: 16–37 weeks) with 63% of the scans performed before 21 weeks' gestation. The mean gestational age in the earlier half of the study era did not differ from the latter half (21.6 ± 4.3 vs 21.1 ± 4.6 weeks; P = .28); there was no temporal trend toward earlier FE in the later years of the study. Mean gestational age at delivery was 38 ± 2 weeks. Mean age at pediatric assessment was 6 ± 2 months (range: 1–28 months). The various forms of maternal CHD are shown in Table 1. In 183 (66%) of 276 pregnancies, the mother had undergone ≥1 cardiac surgery before pregnancy, including valvuloplasty or valvotomy, valve replacement, closure of shunts, coarctation repair, reimplantation of anomalous coronary arteries, or "complex" repairs (ie, Mustard procedure, Fontan palliation, correction of tetralogy of Fallot, and palliation for pulmonary atresia).


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  		TABLE 1 Nature of Maternal Congenital Heart Lesions

 
Diagnosis of CHD
In 22 (8.3%) of 276 infants, CHD was confirmed on PE after birth. Infants with a patent foramen ovale (based on the typical echocardiographic appearance of an interatrial shunt across the flap valve of the fossa ovalis) were not considered to have CHD, because this is a common finding in young infants. A patent ductus arteriosus (PDA) was not designated as a lesion that was missed by FE, because the PDA is a normal fetal structure. A diagnosis of PDA was established in 6 term infants at the time of CA examination, all of whom were diagnosed after 1 month of age.

Table 2 compares the FE and CA for diagnosis of CHD. There was agreement between FE and CA in 235 (85%) of 276 infants. Four had both abnormal FE and abnormal CA findings (truncus arteriosus: n = 1; ventricular septal defect(s) [VSD]: n = 2; and anterior deviation of the aorta suggesting tetralogy of Fallot: n = 1), and PE confirmed the presence of CHD suspected on FE in each of the 4 aforementioned patients. In all of the patients with discordance between CA and FE, subsequent confirmatory PE was performed.


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  		TABLE 2 Concordance Between FE and CA

 
In 41 (15%) of 276 patients, there was discordance between the results of CA and FE. Of the 35 of 41 infants with abnormal CA findings and normal FE findings, subsequent PE diagnosed CHD in 18 of 35 (normal anatomy was documented on PE in 17). Abnormalities on CA included abnormal cardiovascular examination (n = 28), failure to thrive (n = 1), and abnormal electrocardiogram findings (n = 14; not mutually exclusive). Electrocardiographic abnormalities included left ventricular hypertrophy (n = 6), right ventricular hypertrophy (n = 1), incomplete right bundle branch block (n = 5), extreme right axis deviation (n = 1), and extreme left axis deviation (n = 1). On subsequent confirmatory PE in the 14 patients with abnormal electrocardiography findings, 9 had normal anatomy. Of the 5 with abnormal anatomy (atrial septal defect: n = 2; VSD: n = 1; pulmonary stenosis: n = 1; coronary fistula: n = 1), the corresponding electrocardiographic abnormalities were incomplete right bundle branch block (n = 2), left ventricular hypertrophy (n = 2), and extreme right axis deviation (n = 1).

Diagnoses on PE in the aforementioned 18 patients (performed at a mean age of 6 ± 2 months) are detailed in Table 3 and consisted primarily of left-to-right shunts (n = 17) and valvular abnormalities (n = 5; diagnoses are not mutually exclusive). Follow-up data were available for 13 of 18 infants with abnormal CA and PE findings despite normal FE findings (follow-up duration: 30 ± 29 months; median follow-up: 18 months of age; range: 4–96 months). Outcomes in these children included surgical correction (n = 4), device closure of atrial septal defect (n = 1), persistence of hemodynamically noncompromising shunts (n = 5), and spontaneous closure of shunt lesions (n = 3). In the 6 infants with normal CA findings but previously abnormal FE findings, PE did not detect any evidence of CHD; the lesions diagnosed on FE were muscular VSD (n = 5) and bicuspid aortic valve (n = 1).


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  		TABLE 3 Additional Lesions Detected by CA and Confirmed by PE

 
Of the 4 infants evaluated by a general pediatrician (rather than a pediatric cardiologist), 2 had normal FE findings and normal CA findings. In the other 2 patients, FE findings were normal but CA findings were abnormal; subsequent PE documented normal anatomy in 1 and a VSD in 1.


   DISCUSSION
TOP
 ABSTRACT
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
To the best of our knowledge, this is the first study to prospectively demonstrate the incremental diagnostic value of postnatal CA after FE in women with CHD. In keeping with the published literature, we found that FE detected all of the major forms of CHD. However, we demonstrate that postnatal CA is important for the diagnosis of simpler forms of CHD that can go undetected even after detailed FE.

Prenatal Diagnosis of CHD in Fetuses of Women With CHD
Although FE is widely recognized as a highly sensitive and specific diagnostic modality for the detection of major structural and/or functional cardiac abnormalities in the fetus, noncomplex lesions can still be missed. The lesions that were undetected by FE in our series were in keeping with accepted shortcomings of this modality and could be classified into 1 of the following categories: (1) characteristics of normal fetal circulation (ie, presence of patent foramen ovale and PDA); (2) limitations imposed by circulations in parallel with relative equality between right and left heart pressures (thereby rendering color flow mapping generally unreliable for the assessment of a VSD); (3) findings present during normal cardiac morphogenesis (ie, muscular VSDs); and (4) the inherent limitations of present ultrasound technology for the detection of certain lesions, such as the bicuspid aortic valve in the young fetus.

Postnatal Pediatric Assessment of Infants With Previous FE
Although minor forms of CHD can be missed on FE, and these generally do not have an impact on the early management of an infant or child, some of these lesions do require timely postnatal follow-up for monitoring of disease progression and evolution, which may then necessitate surgical or catheter intervention over the long term. For example, the detection of a persistent shunt lesion may require percutaneous or surgical closure later in life. Similarly, a bicuspid aortic valve will require regular lifetime surveillance for valve integrity.14 Furthermore, the presence of CHD would have important implications for genetic counseling when this cohort reaches adulthood and faces decisions regarding family planning.15

To maximize diagnostic yield of postnatal CA, appropriate timing is crucial. Newborn infants with CHD are often asymptomatic initially, and routine predischarge neonatal examination fails to detect more than half of infants with heart disease.16 Although complex CHD may be reliably detected with FE or with detailed CA after birth, less severe defects may not be manifest while the pulmonary vascular resistance and pulmonary arterial pressures are elevated. Pulmonary pressures are elevated in the neonate, reflecting the "transitional circulation" and do not decrease to adult levels until 2 to 6 weeks of age17; therefore, CA performed before pulmonary pressures have normalized may not detect some shunt lesions and certain valvular lesions (ie, pulmonary stenosis). In our study, CA was performed at ≥1 month of age, when neonatal pulmonary pressures should have normalized, and with this strategy, CA detected lesions in 18 (6.5%) of 276 infants who were not diagnosed on FE.

Although there is some literature to suggest that the diagnostic yield of CA performed by an academic general pediatrician is similar to that of a pediatric cardiologist,18 our study was not designed to compare CA between general pediatricians and pediatric cardiologists. Because CA was performed by a general pediatrician in <2% (4 of 276) of the infants, we cannot address whether the diagnosis utility and/or outcome in these children differs from the remainder of the study population.

The Role of Targeted PE
The indications for PE in this study were abnormal FE or CA findings. Although routine screening PE has been advocated by some, screening PE was not performed in all of the infants born to women with CHD in this study, because we believe that this approach is neither practical nor cost-effective and, importantly, is not supported by recent practice guidelines.19,20 It is not feasible for all infants to undergo both CA and confirmatory PE for the following reasons. Echocardiography in infants or children may require administration of sedation to obtain a comprehensive study. In addition, Bayesian principles dictate that if there is a low pretest probability of CHD based on a normal CA, PE will incur cost but will have minimal yield. Finally, screening PE performed early in life may detect small shunts with a high chance of spontaneous closure during early childhood. Therefore, screening PE will necessitate further follow-up PE at an escalating cost to document resolution of a lesion, which could be excluded by well-timed CA. We suggest that selective performance of PE should be based on suspected CHD and would be deemed unnecessary if a detailed and appropriately timed CA findings were determined to be normal by an experienced pediatric examiner.21

Limitations
In this study, routine screening PE was not performed in all of the infants; therefore, the sensitivity and specificity of CA could not be evaluated. In addition, the excellent quality of FE and the high standards of CA in this study may not be generalizable to centers where access to experts in fetal and pediatric cardiology may be limited.


   CONCLUSIONS
TOP
 ABSTRACT
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
This study demonstrates that there is incremental diagnostic value in the performance-detailed postnatal CA in children of women with CHD who have already undergone FE. Although FE can reliably exclude major forms of CHD, less complex lesions can be missed. These minor forms of CHD can be diagnosed on appropriately timed and performed postnatal CA. Routine PE in all children born to women with CHD may not be necessary. Our approach is to combine FE and postnatal CA, with confirmatory PE if either of the aforementioned is abnormal.


   ACKNOWLEDGMENTS
 
Dr Thangaroopan was supported in part by a University of Toronto Department of Medicine Fellowship Award. This study was supported by an operating grant from Canadian Institutes of Health Research grant MOP 53130 and the Division of Cardiology, Mount Sinai Hospital and University Health Network.


   FOOTNOTES
 
Accepted Aug 20, 2007.

Address correspondence to Rachel M. Wald, MD, North Wing, 5N-519, Toronto General Hospital, 585 University St, Toronto, Ontario, Canada M5G 2N2. E-mail: rachel.wald{at}uhn.on.ca

The authors have indicated they have no financial relationships relevant to this article to disclose.


   REFERENCES
TOP
 ABSTRACT
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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PEDIATRICS (ISSN 1098-4275). ©2008 by the American Academy of Pediatrics




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