(Circulation. 1996;94:67-72.)
© 1996 American Heart Association, Inc.
Articles |
Efficacy of Routine Fetal Ultrasound Screening for Congenital Heart Disease in Normal Pregnancy
From the Department of Paediatrics, Division of Paediatric Cardiology, Sophia Children's Hospital (E.B., I.M.E.F.-M., J.H.); the Department of Epidemiology and Biostatistics, Erasmus University Medical School (E.B., D.E.G.); the Department of Obstetrics and Gynaecology, Division of Prenatal Diagnosis, University Hospital Rotterdam (E.B., P.A.S., J.W.W.); and Rotterdam "Thuiszorg" (Home Care) Foundation (R.E.J.), Rotterdam, Netherlands.
Correspondence to Dr E. Buskens, Division of Paediatric Cardiology, Sophia Children's Hospital, Dr Molewaterplein 60, 3015 GJ Rotterdam, Netherlands. Dr Buskens' current address is Department of Clinical Epidemiology, University Hospital Utrecht, PO Box 85500, 3508 GA Utrecht, Netherlands. E-mail ebuskens{at}rvb.azu.nl
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Abstract |
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Background Second trimester routine ultrasound evaluation of the fetal heart by means of the four-chamber view has been proposed for prenatal detection of cardiac anomalies. The aim of this study was to evaluate the efficacy of this procedure.
Methods and Results A prospective follow-up study on 6922 scanned fetuses was performed. Pregnant women without known risk factors who were scheduled for a routine fetal ultrasound examination between 16 and 24 weeks gestation were invited to participate. Follow-up until 6 months postpartum was available for 5660 subjects (81.8%), of whom 5319 fulfilled all eligibility criteria. By comparing the prenatal diagnosis to the postnatal diagnosis, we obtained sensitivity, specificity, and predictive value (positive and negative). A total of 80 cases of congenital malformations were diagnosed during the study: 44 cases of congenital heart disease, 40 cases of noncardiac malformations, and a combination of the two in 4 cases. The fetal four chamber–view examination was considered abnormal in 7 women who were subsequently referred for extensive fetal ultrasound examination. Two proved to be carrying an affected fetus. Similarly, prenatal referral of 14 women because of suspected noncardiac malformations yielded 12 such cases. The fetal four chamber–view examination had a sensitivity of 4.5% (95% CI, 0.6% to 15%). Sensitivity for noncardiac anomalies was 30% (95% CI, 16.6% to 46.5%). Overall sensitivity of ultrasound examination was 16.3% (95% CI, 2.09% to 48.8%). Specificity and negative predictive value were high (>98%). The positive predictive value was low with wide CIs.
Conclusions These results suggest that the current mode of routine prenatal ultrasound screening for congenital malformations is inefficient, particularly for cardiac anomalies.
Key Words: ultrasonics • diagnosis • heart defects, congenital • echocardiography
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Introduction |
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Congenital heart disease constitutes an important proportion of all major congenital malformations, which are present in 2% to 3% of neonates.1 2 The estimated birth prevalence of cardiac malformations is 8 per 1000.3 Approximately half of the cases of congenital heart disease have only minor consequences or can be corrected easily with surgery, yet 35% of infant deaths due to congenital malformations are related to cardiovascular anomalies.4 5 Hence, congenital heart disease remains an important issue in infant health. In addition, cardiovascular anomalies are strongly associated with other anomalies or chromosomal aberrations.6 7 8
Because the etiology of congenital malformations of the
cardiovascular system is still largely
unknown,7 9 10 primary prevention is not yet possible. The
main options available as methods of secondary prevention are prenatal
detection and subsequent adjustment of the obstetric policy or
termination of the pregnancy if a fatal anomaly is detected. Ultrasound
visualization and interpretation of the fetal four-chamber view at
16 to 24 weeks' gestational age have been advocated as an efficient
and accurate screening test for prenatal detection of the majority of
cardiac malformations.11 12 Accordingly, assessment of the
four-chamber view has been incorporated into routine fetal
ultrasound in many countries, including the Netherlands.13
Despite its popularity, there has been no formal evaluation of a single
routine ultrasound examination of the fetal heart at a gestational age
of 
20 weeks by means of the fetal four-chamber view in a
low-risk population. Therefore, the aim of the present study
was to examine the performance of this screening test in normal
pregnancies and the current, typical clinical setting.
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Methods |
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Source Population
Pregnant women referred for routine fetal ultrasound and who fulfilled the eligibility criteria were invited to participate in the study by the sonographers, ie, ultrasound technicians, midwives, or physicians. Altogether, 15 referring ultrasound units in the Rotterdam metropolitan area participated after approval of their local ethical committees. All participating women gave verbal consent and resided in the southwestern part of the Netherlands. From March 1991 until January 1993, 6922 fetuses were scanned and included in the study. Maternal age was 28.9±4.6 years (mean±SD; range, 14 to 47 years).
Eligibility Criteria
Women were considered eligible if they were scheduled for
routine fetal ultrasound examination between weeks 16 and 24 of
pregnancy. Women referred for determination of gestational age or
growth discrepancy, reassurance because of a preceding miscarriage,
lack of fetal movement, inability to detect a fetal heartbeat, or other
miscellaneous reasons were also considered eligible. All women with
known risk factors for congenital heart disease in their offspring (eg,
a previous child, their partner, or themselves affected with congenital
heart disease), maternal juvenile diabetes, maternal lupus
erythematosus, maternal phenylketonuria, maternal
rubella, or maternal drug or teratogen exposure (for example, use of
anticonvulsants, retinoic acid, or morphine mimetics such as heroin and
methadone) were excluded because these characteristics currently
constitute an acknowledged indication for extensive fetal
echocardiography.14
Personnel and Equipment
In each of the participating ultrasound centers, the majority of
examinations were performed by specific experienced personnel. Of 6922
examinations, 3747 (54%) were performed by technicians, 776 (11%) by
midwives, 1391 (20%) by trainees in obstetrics and gynecology, and
1008 (15%) by consultants. The majority of sonographers
involved in the present study had an ample background in fetal
ultrasound examination, and all had taken an intensive, 2-day
ultrasound training course on the evaluation of the fetal
four-chamber view, including a hands-on tutorial, before
participating in the study. During the study, the ultrasound units were
visited frequently. Also, the sonographers were motivated and supported
by the project supervisor and were informed about the progress of
the study without being told of the findings. Various brands and types
of ultrasound equipment—all state-of-the-art,
two-dimensional appliances (see "Appendix")—were used in the
participating ultrasound units depending on local preference. The aim
was to investigate a setting that resembled current routine practice as
closely as possible with regard to experience and expertise of the
sonographers as well as quality of equipment.
Data Handling
The ultrasound examinations were performed according to the
guidelines issued by the Dutch Society of Obstetrics and
Gynecology,13 which correspond to guidelines issued by the
American Institute for Ultrasound in Medicine. The examinations of the
fetal four-chamber view were evaluated and coded as normal,
abnormal, or impossible to assess, according to standard criteria. The
fetal heart should be located in the middle of the thorax and should
occupy approximately one third of the thorax, display atria and
ventricles of equal size, have an intact ventricular
septum, have a foramen ovale flap demonstrated in the left atrium, and
have offset atrioventricular valves, that is, a more
apical insertion of the tricuspid valve and, potentially, visualization
of the "moderator band" in the right ventricle11 12
(Fig 1
). In addition, data on gestational age, as
determined by biometry, and suspected presence of other congenital
malformation(s) were recorded. Fetal biparietal distance, femur
length, and abdominal circumference were measured. In addition, the
cerebral ventricles, spine, stomach, urinary bladder, kidneys, and
umbilical cord insertion were inspected. Generally, four to five fetal
ultrasound examinations per hour were performed, which took 10 to 15
minutes per patient. Finally, a code for the category of referring
obstetrician (midwife, general practitioner, or
gynecologist), the indication for an ultrasound scan (routine,
determination of gestational age, or other), and whether or not the
pregnant woman was subsequently referred for extended fetal ultrasound
examination were noted. Follow-up data on all women and their
children were collected until 6 months postnatally. In collaboration
with local Child Health Clinics, the required data (date of birth, sex,
and presence of congenital anomalies) were obtained by means of coded
business reply cards for most women. In the Netherlands, Child Health
Clinics routinely offer physical examination of infants and an
interview with their parents within a month after birth and
subsequently at monthly intervals until the infant has reached the age
of 6 months. If no data or incomplete data were available, the woman's
general practitioner was approached for additional
information. Finally, if an anomaly was suspected and the infant had
been referred for expert examination, hospital records, findings on
additional ultrasound examination, and autopsy records, if
applicable, were retrieved and coded.
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Data Analysis
By comparing the prenatal diagnosis (presence or absence of
anomalies) with the postnatal diagnosis, the latter being taken as a
gold standard, we categorized all ultrasound examinations as true
positive in cases when a suspected anomaly was confirmed, false
positive when a suspected anomaly could not be confirmed, false
negative when an anomaly was missed by ultrasound examination, or true
negative when no anomalies were present. Because no consequences
were attached to a four chamber–view examination that was
indeterminable, such cases were considered to have a normal screening
test. Data were subdivided according to the presence of congenital
heart disease and noncardiac congenital anomalies. In addition, by
means of expert consensus, all anomalies were categorized as major
(definitely considered detectable prenatally, eg, disrupting
four-chamber view anatomy), minor (possibility of prenatal
detection is debatable due to size, location, or nature of the
anomaly), or undetectable (excluded from analysis). The last
category consists of anomalies such as patent ductus arteriosus, which
sometimes occurs in combination with secundum-type atrial septal
defect, cryptorchism, and syndactyly. Because there is general
consensus that these anomalies may be considered part of normal fetal
development or cannot be recognized on prenatal ultrasound examination,
such cases were subsequently omitted from
analysis.15 The sensitivity, specificity, positive
predictive value, and negative predictive value were calculated with
corresponding exact 95% binomial CIs.16 In addition, the
prevalence of congenital malformations (the proportion of infants
affected) was calculated.
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Results |
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TopAbstractIntroductionMethodsResultsDiscussionAppendix 1References |
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Subjects and Ultrasound Examinations
Of the 6922 fetuses that were screened, 6571 (95%) underwent a routine ultrasound examination between 16 and 24 weeks' gestational age. Fig 2
shows the distribution of the duration of
pregnancy at which the ultrasound examinations were performed. In 501
(7.2%) of the fetuses, an adequate four-chamber view could not be
obtained. Fig 2 also demonstrates how visualization of the
four-chamber view related to gestational age.
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Follow-up until 6 months postpartum has been completed for 5660 fetuses (81.8%). Of these, 119 appeared to have been included despite known risk factors for congenital heart disease, and 222 were screened outside the 16- to 24-week gestational age range. Consequently, the analysis presented pertains to 5319 routine fetal ultrasound examinations in the gestational age range of 16 to 24 weeks (mean, 19 weeks 5 days), with complete information available on the outcome of pregnancy until 6 months postpartum.
Outcome of Ultrasound
Of all women who were screened prenatally, 7 (0.10%) were
subsequently referred for extended fetal
echocardiography because of the abnormal appearance
of the fetal four-chamber view. Another 14 (0.20%) were referred
because of other suspected congenital anomalies. Two suspected cases of
congenital heart disease that were referred for further examination
were confirmed on subsequent evaluation. Noncardiac anomalies were
detected more accurately; of the 14 cases referred, 12 proved to be
affected.
Outcome of Pregnancy
Eventually, congenital anomalies were recognized in 118 cases
(2.2%; 95% CI, 1.8% to 2.7%). There were 62 cases (1.2%; 95% CI,
0.9% to 1.5%) with congenital heart disease (6 of whom also had other
congenital anomalies). Noncardiac anomalies were detected in 62 cases
(1.2%; 95% CI, 0.9% to 1.5%). Furthermore, 5 cases of congenital
heart disease occurred in combination with chromosomal anomalies. When
evaluated according to category (major, minor, or unrecognizable) of
anomalies, 80 major and minor cases (1.5%; 95% CI, 1.2% to 1.9%)
remained for secondary analysis. These included 44 cases of
congenital heart disease (4 in combination with other malformations)
and 40 cases of noncardiac anomalies. The types of congenital anomalies
(categorized according to total anomalies, ie, minor and major
combined, and major anomalies only) encountered in these 80 cases are
listed in Table 1. Because any one fetus may have had
several anomalies, the sum of anomalies in the "total" row is
>80.
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Performance of Ultrasound
In the categories of cardiac anomalies, noncardiac anomalies, and
all anomalies combined, a distinction has been made between the number
of major and minor anomalies combined and the subsample of major
anomalies likely to have generated an abnormal image at 20 weeks'
gestational age. This is reflected in separate analyses
according to case severity. Table 2 shows the findings
of routine prenatal screening for congenital anomalies of the heart.
Sensitivity for cases of congenital heart disease was low (4.5%; 95%
CI, 0.6% to 15%) even if only major anomalies are considered (16.7%;
95% CI, 2.1% to 48.4%). Sensitivity was somewhat higher for
noncardiac anomalies (30%; 95% CI, 17% to 47%) and higher still for
major anomalies (40%; 95% CI, 23% to 60%). Sensitivity for all
anomalies combined was intermediate (overall: 16%, 95% CI of 9.0% to
26%; major: 33%, 95% CI of 19% to 50%). As expected, specificity
was high (>99%) for both categories of anomalies. Also, the
negative predictive value was high (99%). The positive predictive
value varied considerably over the categories of anomalies and could
not be established accurately, as illustrated by the wide CIs. Test
characteristics and prevalence values are summarized in Table 3.
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Validation
Because we were concerned about the possibility of selective
participation of mothers with children who either have no anomalies or
represent a population with a relatively high number of
anomalies, a random sample of 1500 ultrasound examinations (100 from
each of the participating ultrasound units) was evaluated with regard
to data on gestational age, referring obstetrician, indication for
ultrasound, suspected presence of congenital malformations, and
referral for further evaluation. Because this random sample could not
be selected on the basis of gestational age, a wider gestational age
range was represented. Furthermore, it appeared that
slightly more examinations in the sample were requested by
consultants. However, the small proportion of women referred
because of suspected fetal anomalies was equal to that in the study
population. In addition, we were able to study the database of the
Division of Prenatal Diagnosis of the Department of Obstetrics and
Gynaecology of Dijkzigt University Hospital, which serves the Rotterdam
metropolitan area as a tertiary referral center, and check it for women
not included in the present study who otherwise would have
qualified as participants. Only one woman with a suspected anomaly on
the fetal four-chamber view had been referred during the period of
enrollment in the current study who was not included.
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Discussion |
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The objective of the present study was to evaluate the efficacy of the fetal four-chamber view in routine screening of normal pregnancies to detect congenital heart disease. Our findings indicate that the fetal four-chamber view, as evaluated during routine fetal ultrasound in the second trimester of pregnancy, does not provide an accurate screening test. Even major anomalies that are likely to create an abnormal fetal four-chamber view were not detected prenatally to a satisfactory degree.
Several factors may explain these results. The size of fetal structures
is related to gestational age. Hence, visualization early in the second
trimester, when the fetus is small, will be limited by the resolution
of the ultrasound equipment. However, as is apparent from Fig 2
, the
majority of scans were performed beyond 17 weeks' gestational age, a
time generally deemed appropriate for structural ultrasound
examination. In addition, the proportion of fetal hearts that could not
be assessed remained stable after 17 weeks of gestation; therefore, the
scans appear to have been performed at an appropriate moment.
Furthermore, all participating ultrasound units had
state-of-the-art equipment at their disposal. The scans
were performed by specialized technicians, midwives, or
consultants trained in ultrasound examination in 80% of the
women and by sonographers (trainees) with varying degrees of experience
in the remainder. We feel that this mix adequately reflects the current
ultrasound practice of routine screening and, if anything, the quality
of the procedures was greater than usually encountered. In addition,
because we were aware that trainees who performed ultrasound
examinations tended to be rotated to other locations rather frequently,
all participating ultrasound units were visited regularly. During these
visits, the progress of the study and the demand for additional
training of junior sonographers were assessed. The effect of increasing
experience of the sonographers could be judged by evaluation of the
number of inadequate four-chamber view visualizations during the
study. However, the proportion of adequate ultrasound evaluations of
the fetal heart did not materially fluctuate nor was there any
indication of a particular trend during the period of participation.
Interestingly, the proportion of fetal four-chamber views judged as
indeterminable did not differ among the categories of sonographers.
Also, all sonographers had taken similar additional training in the
fetal four-chamber view examination before they participated in the
study. A comparison of the sensitivities accomplished by each category
of sonographers could have yielded important practical information on
the expertise required. However, in view of the few anomalies actually
detected prenatally, it is not feasible to analyze the data
separately. In summary, it appears unlikely that variations in
experience and skills had a major impact on the efficacy of the
screening procedure.
Rather poor performance was observed for noncardiac congenital anomalies also, with a 30% sensitivity; this resulted in a sensitivity of 16% for all anomalies combined. A discussion analogous to that on the fetal four-chamber view applies to other congenital anomalies as well. Again, the results cannot be readily explained by any of the variables discussed thus far.
The nature of the anomalies encountered in routine screening explains part of the low sensitivity of prenatal detection observed in the present study. Some malformations—for instance, a small ventricular septal defect or an atrial septal defect—may not be visible with current ultrasound equipment or may not be visible by means of the four-chamber view alone. The proportional distribution of congenital anomalies encountered at birth may clarify this argument. Approximately 30% of the cases had ventricular septal defects, 10% had a patent ductus arteriosus, 10% had atrial septal defects, 10% had pulmonary stenosis, and another 25% were cases of tetralogy of Fallot, coarctation of the aorta, aortic stenosis, and transposition of the great arteries.17 As also alluded to by Nelson et al,18 a major proportion of these anomalies is not likely to be diagnosed by means of the fetal four-chamber view, especially in a nonreferral setting. Furthermore, a congenital anomaly may not remain in a steady state. A duodenal or urinary tract obstruction, for instance, may only become visible late in the second trimester. The anatomic substrate may be present already but may not yet have functional (recognizable) consequences at 20 weeks' gestation. This may even apply in some severe cardiac anomalies like hypoplastic left heart.19 Specific conditions of the ultrasound examination may add another explanation for the failure to recognize even gross cardiac pathology. Severe maternal obesity or unfavorable fetal position may considerably hamper possibilities to assess the fetal structures. However, the stable and limited proportion of cases with an indeterminable four-chamber view does not support a major effect of scanning conditions. Apparently, the sensitivity is determined in part by the (im)possibilities of detection by means of prenatal ultrasound and in part by the natural history of the specific anomalies. Nevertheless, even if anomalies for which the possibility for prenatal detection is uncertain were left out of the analysis, low sensitivities were found. The exclusion of "minor" anomalies from evaluation could suggest that one considers these cases irrelevant from an obstetric and pediatric point of view. Yet, minor variants of congenital malformations may have the same cause as major defects and may be associated similarly with other anomalies. In view of this, it would seem irrational to consider such cases irrelevant.
The authors of early reports on routine fetal echocardiography, ie, the four-chamber view, advocated this technique as a useful tool to detect congenital heart disease prenatally.11 12 Our data are not consistent with this view. However, as discussed in a previous review of routine fetal echocardiography,20 it is quite likely that many of the early studies suffered from substantial limitations in design and may have led to overly enthusiastic views. Authors commonly were experts in the field of fetal ultrasound who worked in referral or teaching centers. Accordingly, the study population as well as the ultrasound technique may not have been representative of what is encountered in a general routine ultrasound clinic, where sonographers may be less skilled, face crowded office hours, and have a nonselected population with a low prevalence of anomalies. In addition, case ascertainment has not always been sufficiently complete, eg, retrospective with a short period of follow-up of cases suspected of anomalies. Stillborn fetuses or affected infants may not reach a tertiary hospital or may not be examined routinely. All this may have caused serious bias and overestimated sensitivities. The present prospective cohort study has complete follow-up on the fetuses. The gold standard method of postnatal examination applied in the present study, however, may require some additional comment. Routine physical examination and an interview until 6 months postnatally may have left some minor anomalies undetected. Yet, a prevalence of congenital heart disease in excess of that usually reported was observed.1 2 3 Accordingly, it is likely that ascertainment was virtually complete. Moreover, any cases not detected postnatally would have led to an even lower sensitivity without altering the overall study results. Similarly, any anomalies detected in the 1262 cases for whom follow-up could not be ascertained would not have altered the inference. Assuming a prevalence of congenital heart disease of 0.8%, another 10 cases might have occurred, lowering the estimated sensitivity slightly. Recent reports on ultrasound in second trimester pregnancy that originated from ultrasound units that employ regular personnel and scanning time show an efficacy of routine fetal ultrasound examination for detection of congenital anomalies that is comparable to our findings.21 22 23 24 25 26 27 The recent RADIUS study21 actually demonstrated completely similar reports with regard to scans performed before 24 weeks' gestation.
As discussed, the level of expertise and skills of the sonographers in the present study represent the level of quality in ultrasound examination currently observed in routine screening practice. Suggestions for additional training of the sonographers as well as additional scanning projections have been submitted.28 29 Great effort and substantial resources may be required to establish a level of ultrasound examination skills sufficient to have a major impact on detection rates. Even if achieved, a sizable proportion of cases may remain technically undetectable within the period of gestational age considered optimal for screening. Despite the obvious advantages of prenatal detection in individual cases, we feel that an overall net benefit of routine ultrasound screening has not been established. False-negative and false-positive diagnoses will always occur and have to be taken into account. In addition, it may well be that in a major proportion of the cases that are potentially detectable, prognosis will not improve significantly with early detection.30 31
In conclusion, the findings in the present prospective study indicate that in the setting we have described, routine fetal echocardiography at 20 weeks' gestational age by means of the fetal four-chamber view does not suffice as a prenatal screening test for congenital heart disease.
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Acknowledgments |
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This study was supported by the Netherlands Heart Foundation (grant No. 89.053). We are very much indebted to all the pregnant women, sonographers, obstetricians, child health clinics, general practitioners, pediatricians, and pediatric cardiologists who participated in the study for their willingness to cooperate and provide us with the necessary data. In addition, we thank Andrina Cleveringa, Sharmila Bhikha, and Agnes van der Voorn for their enthusiastic and skillful contribution to the data collection and management and Marcel Eijgermans for his continuous support regarding database handling.
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Appendix 1 |
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TopAbstractIntroductionMethodsResultsDiscussionAppendix 1References |
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The following is a list of hospitals or ultrasound clinics that participated in the study as well as the brand and type of the ultrasound equipment applied locally and its carrier frequency.
Ikazia, Rotterdam: Aloka SSD 620 (3.5 MHz).
St Franciscus Gasthuis, Rotterdam (2 clinics): Hitachi EUB 415 (3.5 MHz). Stichting Trombosedienst & Artsenlaboratorium Rotterdam, Rotterdam: Aloka SSD 650 (3.5 MHz).
University Hospital Rotterdam Dijkzigt, Rotterdam: Hitachi EUB 450 (3.5 MHz).
Zuiderziekenhuis Rotterdam: Toshiba SSA 240A (3.75 MHz).
Westeinde Ziekenhuis, Den Haag: Toshiba SSA 250A (3.5 MHz).
Merwede Ziekenhuis, Dordrecht: Toshiba SSA 240A (3.75 MHz).
Drechtsteden Ziekenhuis Jacobus, Zwijndrecht: Toshiba SSA 90 (3.75 MHz).
Drechtsteden Ziekenhuis Refaja, Dordrecht: Aloka SSD 620 (3.5 MHz).
Reinier de Graaf Gasthuis, Delft: Toshiba SSA 250A (3.75 MHz).
't Lange Land Ziekenhuis, Zoetermeer: Siemens Sonoline SLI (3.5 MHz).
Holy Ziekenhuis, Vlaardingen: Toshiba SSA 250A (3.75 MHz).
IJsselland Ziekenhuis, Capelle a.d. IJssel: Aloka SSD 650CL (3.5 MHz).
Schieland Ziekenhuis, Schiedam: Toshiba SSA 250A (3.75 MHz).
Received September 12, 1995; revision received December 28, 1995; accepted January 2, 1996.
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