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Ultrasound Obstet Gynecol 2021; 57: 38–42

Published online in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/uog.23551

Opinion

Evolution of fetal cardiac imaging a long-lasting friendship and close collaboration that
crystallized in the publication of three books. In 2009, I
in 30 years of ISUOG was elected Chair of the Education Committee of ISUOG,
which took me all over the world, from India to Brazil,
R. CHAOUI from Egypt to Singapore and Moscow, to disseminate
Center for Prenatal Diagnosis and Human Genetics, Berlin,
ultrasound knowledge and help achieve ISUOG’s mission.
Germany I also had my fair share of UOG publications. What an
(e-mail: chaoui@feindiagnostik.de) honor it was when, almost 30 years later, in 2018, I was
presented with the Stuart Campbell Award for Education
and, together with Kurt Hecher, in 2019, invited to host
the 29th ISUOG World Congress in Berlin.
My personal journey with ISUOG and UOG
Although, theoretically, history is objective with clear Color and spectral Doppler
landmarks, the telling of historical events is invariably
distorted by the perception of the observer. I should The ultrasound unit in East Berlin, in which I started
emphasize at the outset that the following account, which my residency specializing in ObGyn in 1986, did not
reflects mainly my personal experience and contribution have sophisticated equipment, but I was lucky to have
to ISUOG and the White Journal, is biased. I apologize the chance, sporadically, to scan my patients in the
for this and also that space constraints prevent me from departments of radiology and cardiology. From early on,
citing, thanking and honoring the many individuals who I could scan for a few hours each week on a brand-new
I have met over the years and who have contributed machine with color Doppler capability and taught myself
tremendously to the development of ultrasound in fetal how to use this new technology with which very few
medicine. had experience. In Paris, in 1989, at a fetal cardiology
When I started, in 1986, to perform fetal ultrasound, the symposium, I met pioneering experts such as Lindsey
only learning resources available were a handful of books Allan, Laurent Fermont, Greg DeVore and Jim Huhta,
and a few articles scattered amongst numerous journals. and heard them report on the novel application of color
It is to the credit of Stuart Campbell, and a few fellow Doppler in imaging of the fetal heart. I knew that I
pioneers, that he agreed to found a platform dedicated was on the right track and could see how, in addition
to ultrasound in obstetrics and gynecology. As he told to elucidating numerous known anomalies of the fetal
me later, choosing the American spelling ‘gynecology’ heart, technologies such as pulsed and color Doppler
instead of the British ‘gynaecology’ was intended to could be key to new research and knowledge. Color
show openness to the world and to attract American and Doppler has evolved enormously since that time, as shown
other international scientists. The new platform had three in Figure 1, which illustrates imaging of hypoplastic left
components, namely, a new global Society, ISUOG, an heart syndrome from the 1980s to today.
annual world congress where specialists and enthusiasts I was fascinated by the detail that could be revealed
could meet and exchange experiences, and a new journal, by fine-tuning color Doppler. With this approach, it
Ultrasound in Obstetrics & Gynecology (UOG), that was possible to visualize, in some circumstances, the
would be accessible to prospective authors based on fetal coronary arteries and, in an international meeting
the quality of their research and images rather than on organized by Ulrich Gembruch in Lübeck, Germany, in
their country of origin. A bonus was that publication of 1995, I gave an overview of the coronary arterial system,
color images was, from the very start, free of charge. its regulation and visualization on ultrasound. I was then
From my first ISUOG World Congress – the second, approached by Stuart Campbell to write an editorial for
organized by Manfred Hansmann in 1992, in Bonn, UOG1 , which turned out to be my first paper in the
Germany – I felt like a member of a family, even though White Journal! My experience with tiny vessels extended
I was to meet famous people, such as Stuart Campbell, to the pulmonary and venous systems and later, focusing
Kypros Nicolaides, Mark Evans, Sturla Eik-Nes, Juriy on miniscule vessels around the heart, I came across an
Wladimiroff and others, and be inspired by them. I made aberrant right subclavian artery (ARSA) in a fetus with
my way in the ISUOG community, becoming a member Down syndrome, which ultimately led to the discovery
of both the Editorial Board of UOG (1998–2005) and the of a new sign2,3 . ARSA has since been adopted as a soft
Board of ISUOG (2004–2013). During these years, I made marker of aneuploidy.
many new friends and worked with many extraordinary From the mid 90s, I started to focus on new,
ultrasound teachers, including Gianluigi Pilu, Roberto high-resolution imaging tools. Along with my partners,
Romero, the late Philippe Jeanty, Dario Paladini, Yves Karim Kalache and Kai-Sven Heling, I worked with
Ville and Alfred Abuhamad. Alfred and I developed new technologies, including color Doppler4 , power

© 2021 International Society of Ultrasound in Obstetrics and Gynecology OPINION


Opinion 39

Figure 1 Evolution of color Doppler resolution from 1988 until now: visualization of hypoplastic left heart syndrome. (a) My first case using
color Doppler, in 1988, and (b–d) subsequent examples from 1996 (b), 2008 (c) and 2020 (d).

Doppler5 , dynamic or HD flow and three-dimensional published over the years, including ISUOG Guidelines on
(3D) ultrasound6,7 , to examine the fetal thymus8,9 , cardiac screening16 which have been adapted in many
intracranial translucency10 and maxillary gap11 , among countries as standards to be followed. Figure 2 shows
other signs and structures. Most of these novel findings some of the techniques available today.
were published in UOG and some of the images even
found their way onto the cover of the Journal3,12–15 . Fetal cardiac examination beyond detecting anomalies
Over the last 30 years, there have been incredible
advances in fetal cardiac imaging. The increased quality In the mid 80s, fetal echocardiographic examination
and sensitivity of color Doppler imaging has opened was introduced by, among others, pediatric cardiologists,
the door to fetal echocardiographic examination at such as Lindsey Allan, Laurent Fermont and Charlie
11–13 weeks’ gestation. Detection of cardiac anomalies Kleinman, with the main aim of detecting or ruling out, in
in many centers has shifted into the first trimester high-risk pregnancies, complex cardiac abnormality that
and, today, the heart can be assessed even earlier would impact the neonatal period. With the increasingly
than 11 weeks. The evolution of technology has not widespread use of spectral and color Doppler ultrasound
only improved the resolution of grayscale imaging in many perinatology units in the early 90s, many
and color Doppler, but also enriched the arsenal of centers started to integrate cardiac examination into the
fetal cardiology with tools such as power Doppler, evaluation of pregnancies with suspected fetal or maternal
sensitive bidirectional power Doppler, M-mode, color disease or risk factors. Today, a fetal echocardiographic
Doppler M-mode, anatomical M-mode, spatiotemporal examination may be performed for many reasons,
image correlation (STIC) M-mode, spectral flow Doppler, including as part of genetic screening (to detect conditions
color and spectral tissue Doppler, speckle tracking, 3D such as echogenic focus, ARSA, pericardial effusion,
ultrasound, STIC and 4D ultrasound, cardiac strain linear insertion of the atrioventricular valves, small
evaluation and magnetic resonance imaging (MRI) of thymus), in the workup of severe growth restriction
the fetal heart. The Society has played a huge part in (assessment of cardiac function, pulmonary vascular
the progression of cardiac imaging, with many articles Doppler), in assessing fetal anemia (in Rhesus disease,

© 2021 International Society of Ultrasound in Obstetrics and Gynecology Ultrasound Obstet Gynecol 2021; 57: 38–42.
40 Chaoui

Figure 2 Examples of various tools for fetal heart examination. Fetal heart is generally examined with grayscale 2D ultrasound (a), but, in
last 30 years, numerous imaging tools have been introduced to provide additional information on, among other things, flow events and
function. These include: (b) color Doppler, (c) bidirectional sensitive power Doppler, (d) spectral Doppler of valves and tissue, (e) M-mode
of valves and cardiac walls, (f) M-mode in combination with color Doppler, (g) 3D/4D rendering of intracardiac flow using spatiotemporal
image correlation (STIC), (h) assessment of cardiac wall movements with speckle tracking and (i) magnetic resonance imaging (MRI).

parvovirus infection, monochorionic twins) and volume acquisition. Initially, the calculation of data took hours,
overload (in recipient in twin–twin transfusion syndrome, and later minutes. With advances in computer science
arteriovenous fistula), in evaluating maternal disease (e.g. in the late 90s and, in particular, with the advent of
diabetes mellitus, systemic lupus erythematosus) and rapid processors, the time required for the calculation
effects of maternal drug intake (e.g. indomethacin) and was reduced to a matter of seconds. The combination of
in the monitoring of fetal therapy (arrhythmia, cardiac 3D technology with grayscale and color or power Doppler
intervention, intrauterine diaphragmatic hernia surgery). opened a new door to assessment of the cardiovascular
Knowledge of the assessment of cardiac function has
system.
expanded dramatically in recent years.
The invention of STIC and the development of matrix
transducers enabled the first steps to be taken into the new
Three-dimensional ultrasound, from the face to the
field of 3D cardiac imaging. It was again at the ISUOG
heart
World Congresses and in UOG that new data were pre-
Thirty years ago, the first steps in the journey of 3D sented and published18 . The modern approach, inspired
ultrasound were taken, with offline reconstruction of a largely by ultrasound specialist and artist, Bernard Benoit,
fetal face following acquisition of adjacent slices of the considers 3D not as a gimmick, to view the baby’s face,
regions of interest with a special mechanical transducer17 . but as technology that enables the acquisition and storage
Another approach was proposed soon after, in the mid of information in the form of raw volume data for later
90s, with a sensor attached to a regular transducer and the offline analysis. The acquisition of a fetal heart volume
data being analyzed by remote computer after free-hand can be achieved today as static 3D, or with STIC or live

© 2021 International Society of Ultrasound in Obstetrics and Gynecology Ultrasound Obstet Gynecol 2021; 57: 38–42.
Opinion 41

Figure 3 Variation on a theme of three dimensions (3D): examples in single fetus with diagnosis of transposition of the great arteries,
showing different 3D displays that may be applied to visualize abnormal course of great vessels: (a) tomography multiplanar mode,
(b) orthogonal biplane mode, (c) OmniView combined with color Doppler, (d) surface rendering mode, (e) inversion mode, (f) minimum
mode, (g) volume contrast imaging (VCI) of A-plane in combination with inversion mode, (h) color Doppler with glass-body mode using
spatiotemporal image correlation (STIC) and (i) STIC with transparent silhouette mode and color Doppler.

4D with an electronic probe, with the display of informa- was fighting against the Internet and digitalization at the
tion varying depending on the acquisition technique and beginning of the millennium. It is our role, as specialists,
the combination with grayscale or color Doppler19 . The to define how AI can improve our daily work, helping us
tools used for the different displays resemble smartphone to acquire the best images and achieve accurate diagnosis.
or tablet applications and enable different extraction and UOG will, as always, be the best venue for documenting
use of information. Figure 3 illustrates, in a fetus with the resultant innovations and exchanging opinions.
a diagnosis of transposition of the great arteries, how
data may be variously displayed in different modes. It Conclusion
is likely that the huge potential of 3D technology will
lie in the ability to standardize the cardiac volume, with Since its conception, ISUOG has stood witness, through
automatic reconstruction of the typical planes, pioneered its congresses and members’ contributions, to the many
by Alfred Abuhamad and his team20 and examined by outstanding developments in fetal ultrasound. UOG has
others since21 . In an era in which artificial intelligence become the main forum in which, in thousands of articles,
(AI) has started to infiltrate medicine, volume ultrasound these innovations are documented. I can only conclude by
is potentially the best enabler of its application in fetal saying ‘Happy Birthday, ISUOG and UOG’, and thanking
imaging. The background assessment of structures during you for all the fulfilling years. I look forward with great
scanning22 or the offline analysis of raw data enables excitement and optimism to the 40th anniversary and
the comparison of acquired images with ‘learned’ images beyond!
of normal and abnormal cases. Recent use of MRI
technology in the fetal heart, alone or in combination REFERENCES
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© 2021 International Society of Ultrasound in Obstetrics and Gynecology Ultrasound Obstet Gynecol 2021; 57: 38–42.

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