The diagnosis of foetal anomalies relies almost invariably, at least as a first step, on ultrasound examination. Since the 1980s, increasing quality of ultrasound machines and increasing insights in anatomy and pathophysiology of the foetal heart have led to a vast body of knowledge and even a subspecialty in foetal cardiology. Development of the embryonic and foetal heart and circulation, both normal and abnormal, has been studied in animals and humans extensively. Although some limitations still remain related to obviously lower-resolution scanning, which has to be performed through the maternal tissues, and impracticality of obtaining a reliable real-time foetal electrocardiogram, the majority of structural heart defects can now be diagnosed correctly well before birth.
Clear advantages have been shown in timely prenatal detection of heart defects. How to develop effective and cost-effective general screening programmes, however, remains a matter of sometimes hot debate.Reference Bull1–Reference Tegnander, Williams, Johansen, Blaas and Eik-Nes3 In particular, those specialists working in tertiary referral centres, confronted repeatedly with undiagnosed, incorrectly diagnosed, or incompletely diagnosed very sick neonates requiring emergency care, often advocate implementation of high-quality, routine screening in pregnancy for foetal heart defects. Definite progress has been made in detection rates of foetal cardiac anomalies in many countries, with incorporation of not only the four-chamber view but also outflow tracts and the three-vessel view into the routine 20-week scan protocol. Unfortunately, however, cardiac anomalies are still on top of the list of missed prenatal diagnoses.Reference Garne, Stoll and Clementi2 New ideas such as screening newborns using pulse oximetry may improve outcomes, although adaptation of time and place of birth, one of the benefits of prenatal diagnosis, is impossible.
One of the often-heard solutions to the issue of missed cardiac diagnoses is to promote early and unrestricted referral of pregnant women with an increased risk or the slightest hint of a foetal cardiac problem directly to a specialised foetal/paediatric cardiologist. The risk of missing essential foetal heart defects undoubtedly can be reduced in that way. These experts most often work in an environment where multidisciplinary consultation of foetal medicine subspecialists, geneticists, and paediatric cardiac surgeons can easily be arranged. Proper and early counselling can then be provided, and optimal place and time of delivery organised with the appropriate caregivers ready to help the neonate immediately after birth.
In this paper, we suggest a patient-centred path of care following the suspected diagnosis of a foetal cardiac anomaly, with emphasis on, first, rapid detection of all possible foetal anomalies, both structural, functional, and genetic, supervised by the maternal–foetal medicine specialist in close multidisciplinary teamwork.
Detection of foetal anomalies
The question is whether such a model is an effective way of helping pregnant women who carry a foetus with anomalies. The above situation may sound logical. However, it does not take into consideration the quite high likelihood that the cardiac defect is not an isolated anomaly. Prognosis and management options radically alter if the cardiac defect is not isolated. Second, foetal cardiac malformations, in general, carry a high risk of chromosomal alterations. A not uncommon example is a referral for detailed foetal echocardiography followed by expert in-depth counselling on the surgical management of the diagnosed heart defect, to find out that 2 days later the foetus has a trisomy.
A foetus may be recognised as a patient through several distinct pathways. A family history or specific risk factors in the mother’s health, such as diabetes, epilepsy, and use of certain drugs, are well-established indications for detailed ultrasound evaluation of foetal anatomy. Second, clinical signs such as a large or small-for-dates uterus, or decreased movements, may trigger further evaluation including a full foetal anatomical and functional examination. Finally, most countries have adopted universal, routine screening programmes including foetal anatomy scans, most often scheduled around 18–20 weeks’ gestation.
In all these situations, the foetal ultrasound examination is conducted by a sonographer supervised by an obstetrician or by a radiologist, or the scan is performed by the obstetrician himself/herself. In vast majority (>90%) of these cases, no foetal anatomic defects are found.
The first step to discuss is how to refer women whose foetuses are suspected to have an anomaly based on one of the above-mentioned evaluations.
Here, it is important to realise that the first survey with, in general, a “low index of suspicion”, a limited examination time, and by non-expert sonographers is a type of triage. Repeated training of these first-level sonographers, especially how to obtain basic views such as the four-chamber view and the three-vessel view is necessary to ascertain an optimal level of triage. Most foetuses are labelled “likely normal”, whereas others are “possibly abnormal” and require referral for further evaluation. We believe that the specialist these women are best referred to is the Maternal–Foetal Medicine specialist, in a tertiary care centre, who has, apart from his own expertise, full and direct access to advanced diagnostic methods, such as invasive procedures, genetic testing, and MRI, and ability to contact paediatric and other subspecialists.
One possible exception is the pregnant woman with a previous child with a heart defect, or who has a congenital heart defect herself. She may be scheduled for “primary” detailed foetal echocardiography by an expert, to reliably rule out a recurring heart defect in the foetus. As recurrence risks even in such cases are still low, care should be taken to avoid the “pitfall” of just looking at the heart. The complete foetal anatomy needs to be evaluated, which means that either the woman is scanned by both a paediatric cardiologist and an obstetric sonographer, or, which seems preferable to us, a Maternal–Foetal Medicine specialist with a high level of expertise in foetal cardiac evaluation, who can combine the two scans.
Referral to a tertiary care centre, and then what?
The two main groups of patients we are discussing here are: pregnancies with a foetus with multiple congenital anomalies, possibly, including a heart defect; and pregnancies with a foetal cardiac anomaly, in which additional extracardiac anomalies are not, yet, ruled out. It is known for decades that these two clinical presentations are very common.
Copel et alReference Copel, Pilu and Kleinman4 reviewed the literature and came up with a list of prenatally detectable non-cardiac anomalies highly associated with the presence of a heart defect as well; thus, as they advocated, it should warrant expert echocardiography. Their list included hydrocephalus, microcephaly, holoprosencephaly, agenesis of the corpus callosum, Meckel–Gruber syndrome, oesophageal atresia, duodenal atresia, diaphragmatic hernia, omphalocele, or renal dysplasia. In a large autopsy study from Finland, almost half of the neonates with CHD had extracardiac anomalies. In one-third of the deaths, the extracardiac anomalies were thought to be the main cause of demise.Reference Wallgren, Landtman and Rapola5
Chromosomal anomalies are very common too. In an Italian study, echocardiography was performed on 469 foetuses at risk for heart disease. A heart defect was found in 31 (7%) foetuses, of which 15 (48%) were subsequently found to have an abnormality in the karyotype, most often trisomies. In this group, 29% of the foetuses had an isolated chromosomal abnormality, and 71% had additional defects on ultrasound.Reference Paladini, Calabrò, Palmieri and D’Andrea6
Here is where the controversies start. Who should be involved in what stage of the care process? In cases with suspected multiple congenital anomalies, there is little doubt that the preferred route is referral to a Maternal–Foetal Medicine specialist for first detailed evaluation. Advanced diagnostic evaluation will then be performed first, followed by multidisciplinary team discussions on further testing and management. Paediatric cardiology may be part of this team. In cases where the pregnancy will be continued, and a foetal cardiac defect is part of the syndrome, the paediatric cardiologist can subsequently be more closely involved in further diagnosis and counselling.
Although it is important to optimise the ultrasound evaluation including detailed assessment of cardiac structures to have the most accurate diagnosis, we assume most would agree that involving a subspecialist for a certain organ system very early, in cases where it is still possible that a lethal or non-curable syndrome such as trisomy 18 and 13 is present, may be less efficient. Parents may be put on the wrong track if they are already counselled on postnatal interventions such as keeping the ductus open or heart operations, only to hear later that their foetus has a lethal trisomy, or another syndrome considered a contraindication for neonatal heart surgery or completely altering long-term expectations.
Obviously, time is of great importance, putting the responsibility in the hands of the Maternal–Foetal Medicine specialist to make sure that all essential information, including chromosomal analysis, is done urgently.
It becomes more complicated if the patient is referred to a tertiary care centre based on a suspected diagnosis of an isolated cardiac problem. Should these women be seen primarily by a paediatric cardiologist? For rapid and optimal evaluation of the foetal heart, this might be a logical choice. However, there are several other issues to reconsider such a route. The first and foremost is the distinct possibility that the cardiac anomaly is not truly isolated.
The capabilities of the referring centre may be variable, and no tertiary care centre would like to totally rely on another doctor’s ultrasound report. The patient has a right to a full foetal anatomic assessment, as well as a full evaluation of the other issues, that may play a role in further managing the pregnancy, such as obstetric and general history and maternal characteristics. In practically all cases, genetic testing using amniocentesis is part of the early diagnostic work-up. Thus, a Maternal–Foetal Medicine specialist both for performing the detailed general anatomy ultrasound as well as counselling for and performing of the amniocentesis is required anyway. And again, as argued above, a final diagnosis involving more abnormalities than just the heart may be encountered. A paediatric cardiologist is unlikely to be very fond of only performing the echocardiography, while refraining from giving any information and counselling on the foetal cardiac anomaly diagnosis. Again, the parents may in some cases become confused when the final diagnosis involves more than the heart problem and its management described to them first. Waiting a couple of days until more certainty on the presence or absence of associated anomalies is available will make the job of the paediatric cardiologist much more rewarding.
The effective team approach
Intake and first evaluation
A tertiary care centre striving to put the patient’s best interests at the centre of their path of care offers a team approach to pregnant women referred with foetal anomalies. Rapid access to the foetal care unit is essential. For most cases, and for the parents who often do not expect detection of foetal anomalies, we believe they should be observed within 48 hours after first suspicion. A full general, obstetric, and family history is an integral part of evaluating any new patient in an obstetric service. In addition, a physical obstetric examination is conducted. Then, a detailed, complete ultrasound evaluation of the foetus, amniotic fluid, and placenta needs to be performed by an experienced obstetric sonographer using state-of-the-art equipment.
Whether the background of the sonographer is in obstetrics or radiology is not particularly relevant. The sonographer ideally not only produces all required images, planes, and video clips, he or she actually interprets the findings in real time, obviously storing ample material for offline evaluation and sharing with others. In most units where the sonographer is supervised by a Maternal–Foetal Medicine specialist, the supervisor joins the scanning session or conducts the examination himself/herself. In some cultures, sonographers are supervised by radiologists who obviously need to have sufficient training and knowledge of foetal ultrasound. We do believe, however, that assessment of foetal anatomy and function only by offline analysis of stored images and clips has limited value, and therefore radiologists should be able to perform tertiary care-level obstetric ultrasound. We do recognise that some of the best foetal ultrasound specialists are indeed radiologists.
Following the intake and first ultrasound evaluation, the parents are, in our view, entitled to a first counselling session by the responsible Maternal–Foetal Medicine specialist. They are informed, most often, that the examination thus far confirms the suspicion of the referring doctor that their foetus has a health problem. The parents are informed about the path of care they can expect from there on, that they will receive the best possible care by a multidisciplinary team of specialists.
Almost invariably, further diagnostic testing is required or at least offered. Taking an amniotic fluid sample is often done during the first visit to avoid losing precious time. However, this should be preceded by full communication on what tests will be conducted with this material, and what results could be expected. In the new era of microarrays, including taking parental blood samples for comparison, this is quite a challenge for the average Maternal–Foetal Medicine specialist, and may require assistance from genetic counsellors or geneticists.
The next step in the process often is a team discussion, such as on weekly foetal rounds, evaluating images, all information gathered up till then, and producing a differential diagnosis list. In a multidisciplinary setting, involving at least the responsible Maternal–Foetal Medicine specialist as primary caregiver, neonatology, genetics, and social work, and ideally representatives of paediatric subspecialists such as cardiology, nephrology, neurology, and surgery. Such a team is able to quickly draft an individual plan for each patient for further diagnostic steps, followed by counselling, and then, together with the patient plan, the interventions and the process around the delivery.
In case the foetus has a heart defect, one of the parts of this individual diagnostic plan would be performance of foetal echocardiography. Depending on the skills of the team members, this can be performed by a sonographer, a Maternal–Foetal Medicine specialist, or a paediatric cardiologist, where we actually prefer to really do this as a team, with all three present to interpret the imaging in real time. Preferably, this team should also do the subsequent counselling together. This way, tertiary care obstetric sonographers and Maternal–Foetal Medicine specialists can learn a lot from their paediatric cardiology colleagues, greatly improving the value of team discussions on diagnostic testing, management options, and prognosis.
Although it is great that we now have genetic testing options available with high-resolution chromosome analysis, this technology at present still takes quite some time. Waiting for 2 weeks for a microarray result is quite common. In practice, most centres elect to continue the diagnostic imaging process and subsequent counselling, for foetal heart defects, while awaiting these genetic results. The presence or absence of deletions or duplications in the foetal DNA may make a huge difference in the severity of a foetal condition, a fact that needs to be emphasised during counselling. Hopefully, these techniques can be performed faster in the near future. In that event, we do believe that the most efficient order of diagnostic testing, counselling, and further planning is going to be the Maternal–Foetal Medicine specialist evaluation first, including amniocentesis or hopefully free foetal DNA testing from maternal plasma, and then multidisciplinary team rounds, followed by more detailed assessment involving the appropriate paediatric subspecialists, depending on the preliminary findings.
Conclusion
In conclusion, we would like to promote a system of tertiary care for the pregnant woman with a foetus with anomalies truly centred around the patient, with a network of specialists closely collaborating to provide a logical and rapid sequence of diagnostic testing, counselling, and individualised planning of the care process. In addition, we know from experience that the team performance, including job satisfaction for all, can be greatly enhanced by more interaction between Maternal–Foetal Medicine specialists and paediatric subspecialists, such as cardiologists.
Acknowledgements
None.
Conflict of Interest
The authors have no conflicts of interest to declare.
