fetal echocardiography in three and four dimensions

ELSEVIER

@Original Contribution

Ultrasound in Med. & Biol.. Vo. 32. No. X, pp. 97Y-YXh. iYYh Copyright Q 1996 World Federation for Ultrasound in Medicine & Biology

Printed in the USA. All right\ rehervrd 03ObS6291Y6 $15.00 + .IJO

PII: SO301-5629(96)00119-6

FETAL ECHOCARDIOGRAPHY IN THREE AND FOUR DIMENSIONS

JING DENG,+’ JOHN E. GARDENER,~ CHARLES H. RODECK* and WILLIAM R. LEES+ “Department of Medical Imaging, ‘Department of Medical Physics;

and *Department of Obstetrics and Gynaecology, University College, London. UK

(Received 22 December 1995; in final ,form 8 May 1996)

Abstract-A three-dimensional (3D) acquisition system using an electromagnetic position sensor attached to a standard transducer on an unmodified ultrasound scanner was developed to capture two-dimensional (2D) fetal echocardiograms at various positions and orientations. Operating in real-time directed M-mode allowed recording of 2D structural images and cardiac motion curves, from which the fetal cardiac phase could be determined. By digitising over 100 image frames for each scanning sequence, and by selecting frames at particular phases, 3D views of the fetal heart were reconstructed for each phase. Of 20 sequences of six fetuses scanned, 13 sequences successfully demonstrated usable 3D fetal heart structures, including four cardiac chambers, ventricular and atria1 septa, foramen ovale and some of the cardiac valves and great vessels. Rearrangement of those phased 3D images into a cyclic sequence could generate dynamic 3D views of a beating fetal heart. We believe that, with further technical development, this new approach will be of use in the diagnosis of prenatal cardiac malformations and malfunctions, in in utero cardiac surgery and in fetal cardiology teaching. Copyright 0 1996 World Federation for Ultrasound in Medicine & Biology

Key Words: Echocardiography, Ultrasonography, Three-dimensional, Dynamic three-dimensional (four- dimensional), Fetal heart, kedical imaging. - -

INTRODUCTION

Echocardiography has been developed as the best non- invasive technique in prenatal diagnosis of fetal cardiac abnormalities (Kleinman et al. 1980; Maulik et al. 1986; Wang and Xiao 1964; Winsberg 1972). Al- though standardised scanning planes have been intro- duced (Allan et al. 1980), normal measurements have been provided (De Vore et al. 1984) and some easily obtainable views (e.g., 4-chamber view) have been included into routine pregnancy screening (Cope1 et al. 1987), fetal echocardiography is still a procedure demanding great expertise. It requires collaboration between the paediatric cardiologist with a special interest in fetal cardiology and fetal medicine specialists to make precise diagnosis and to plan management (Allan 1994). This is due not only to the small size, rapid beating and constant development of the fetal heart, but also to the limitations of conventional real-time B- mode and colour Doppler echocardiography, which

Address correspondence to: Jing Deng c/o W. R. Lees, Imaging Department, Middlesex Hospital, Mortimer Street, London W 1 N 8AA. UK, E-mail: [email protected]

can only display two-dimensional (2D) structural images of the intricate three-dimensional (3D) fetal heart.

Over the past two decades, researchers have been investigating 3D sonographic visualisation of the adult and paediatric heart (Dekker et al. 1974; Geiser et al. 1982; Schwartz et al. 1994; Vogel and Losch 1994; Wang et al. 1994). In those studies, electrocardiography (ECG ) has played a key role in phasing the cardiac cycle.

More recently, attempts have been made three- dimensionally to reconstruct fetal echocardiograms without using cardiac gating ( Kuo et al. 1992; Merz et al. 1995). Obviously, these nongated 3D pictures are of little clinical usefulness. An area of current interest has been to investigate the feasibility of producing gated 3D fetal cardiac images. However, due to the relative weakness of fetal cardiac electric activities compared with the maternal ECG and other noise sources ( Wakai et al. 1994)) conventional ECG gating is impractical in the fetus.

The aim of this study was to develop a new gating method for 3D and dynamic 3D (4D) reconstruction of clinically useful fetal cardiac images. We have used the simultaneous real-time directed M-mode facility, available on most standard ultrasound machines, to

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Fetal echocardiography 0 J. Dw(, v/ cti. 'Ml

record the cardiac phases. This produces a cardiac motion tracing when the M-mode sampling line passes through suitable moving structures. This has provided a means for demonstrating the possibility of using sonographic gating.

PATIENTS AND METHODS

Ultrasound settirlg

A standard Acuson 128 XP/lO (Acuson Corp., Mountainview, CA. USA) was used in this study with a 4.0- or 5.0-MHz real-time directed M-mode transducer.

The acquisition system came from the Medical Graphics & Imaging Group (MGI; University College, London, UK) (Gardener 1991) . It attaches to most clinical scanners and operates by recording the 2D frame output from the scanner in conjunction with sensing probe position and orientation. The probe is otherwise free and is moved nianually, allowing 3D acquisitions to be interspersed with routine scanning.

The position sensing is effected by using an electromagnetic remote localiser (Polhemus Corp., Col- Chester. VT, USA). It consists of an electromagnetic source and sensor pair together with electronics capa- ble of determining three position and three angle coor-

dinates with acceptable accuracy over the range required for scanning. The sensor and source were mounted, respectively. to the probe ;lnd to ;I tixtxi tri- pod. Conductive metallic objects. which can distort the sensing field, were excluded from the region of the

field linking the source and sensor. The system can record up to 250 frames from a

region of interest up to 256 X 256 within 20 s, although the actual sample rate is determined by the selected triggering, mainly depending on the size and depth of the region of interest to be scanned. Detailed tech- niques were as described previously ( Kelly et al. 1994: Lees et al. 1991).

To obtain cardiac cycle information as well as cardiac structure data, the real-time 2D images and M-

mode curves of the fetal heart were simultaneously displayed on the screen. Both were included in the region of interest to be captured by the acquisition system (Fig. 1) . The brightness of M-mode sampling lines through the 2D structures was adjusted to be lower than the echogenic intensity of the myocardium. Thus, it would be below the threshold used during later 3D reconstruction of the grabbed video images. causing no artifacts. The sample rate was preset between about 8 and 12 frames/s. Each scan sequence acquired about 120 frames. This setting provided about

Fig. 1. Cardiac phasing. Only 15 of 110 frames from a sequence are shown here. The M-mode sampling lines through the 2D structural images in the upper part of each frame were intentionaIIy dimmed and may only be visible in the fifth frame of this figure (see text). The cardiac phase of each structural image is determined by the position of the white bar (( ) on the M-mode cardiac curves in the lower part of each corresponding frame. These frames were not necessarily acquired in cardiac cyclic order. ED, end-diastole; ES, end-systole; MD. mid-

diastole; MS, mid-systole.

Fetal echocardiography 0 J. DENG et al. 981

Fig. 2. Surface display of an end-diastolic phased volume of the fetal heart inside the thorax at 19 weeks gestational age, showing: ( 1) 3D four-chamber view; (2) right ventricular outlet tract (RVOT) and pulmonary artery (PA) view. View (2) was generated from view (I ) by cutting in the plane (pl) and rotating. RV and LV, right and left ventricles; RA and LA, right and left atria; DAO. descending aorta; SP, spine; PV, pulmonary valve. Anatomical directions of 3D objects in all the figures are approximately

indicated by letters on or around the blue cubes: S, superior; I, inferior; A, anterior; P, posterior: R. right; L, left.

four to five fetal cardiac phases per cardiac cycle and 20-40 frames per phased fetal cardiac volume, which was sufficient for most gated 3D reconstructions in this preliminary study (see Problems in the Discussion section).

The system allows immediate online review of stored images. If the image sequence is unacceptable due to poor quality or fetal movement, acquisition can restart immediately.

Graphics workstation The MGI (University College, London, UK)

graphics workstation provides a great variety of 3D offline display options, as previously described (Tan and Richards 199 1) , such as thresholding, image surgery, surface and volume rendering, multiplanar reformatting, movie display and volumetric measuring. When dynamic sequences are prepared, all phased volumes of the same sequence have identical editing parameters to achieve consistent morphometry.

Patients and scanning procedure Six pregnant volunteers were examined after ap-

propriate informed consent had been obtained. The gestational age of the six fetuses was between 19 and

Fig. 3. A 3D fetal cardiac image similar to the conventional 2D aortic-root four-chamber view, but providing better spatial perception of cardiac structures. However, the finest structures, such as cardiac valves, could not be reconstructed.

AO, aorta. For other abbreviations, see Figs. I and 2.

Fig. 1. Two end-systolic phased 3D views of the atria from different sequences from one fetus: ( 1 ) inferioi- ww~

cava (WC) returning to the right atrium toward the foramen ovale (FO) and left atrium; ( 2 ) superior vena cava ( SVC) returning to the right atrium, showing the anatomical basis of fetal circulation ( red arrows I. FOV. F!) valve: MV. mitral valve: TV. tricuspid valve. For other abbreviations. bee Figs. l-3.

29 weeks. Fetal echocardiograms to be used for 3D/ 4D reconstruction were acquired by the following steps: ( 1 ) Moving the transducer on the maternal abdomen and confining scans to an area where good-quality real-time 2D images of the fetal heart could be obtained. (2) Initiating the machine’s real-time directed M-mode function and positioning the M-mode sampling line through the cardiac structures until clear cardiac motion curves appear. (3) Performing a preliminary volumetric scan to make sure that the M- mode curves and 2D images are both distinct in most parts of the scan. (4) Rescanning the same volume and capturing frames in the acquisition system. The transducer was kept immobile at each individual position of the volume for about 1 s before moving to the next position to cover different phases of a cardiac cycle. The interval between two neighbouring sections is about 1 mm. Depending on the cardiac size, about I5 -25 sections were used in each sequence. Fetal body movement is monitored by real-time 2D imaging and M-mode waveforms. One to five sequences were tried in each of the patients, and each scan of’ a sequence only lasted up to 30 s, so the time the fetus was required to remain immobile was 15-30 s.

Fig. 5. Hollow cardiac chambers are displayed as solid objects by inverting the intensity range of the volume in Fig.

2. For abbreviations, see Figs. 1-4.

Fetal echocardiography 0 J. DENC er al. 9x3

Cardiac phase selection Phases of individual frames in the cardiac cycle

were decided from the sweeping bar position on the M-mode curves (Fig. 1). Frames at constant phases (e.g., end-diastole, end-systole and other phases when possible), were manually selected offline and reorga- nised into corresponding phased files, each of which consisted of about 20-40 frames that made up a phased volume during 3D computer processing.

RESULTS

The actual time for 3D acquisitions was about 2-5 min per patient. This included the time for the preliminary scan and one to four recorded scans.

A total of 20 sequences of fetal echocardiograms were recorded and digitised for 3D/4D imaging from the six patients. Significant fetal body movements oc- curred in five of the sequences, and the corresponding records were immediately discarded.

Fifteen sequences were analyzed offline. Two 3D reconstructed images presented distorted views of the fetal heart because some parts of the M-mode curves were rather blurred and unable to provide sufficient phased frames to form a 3D volume. Another sequence had excessive acoustic shadowing artifacts that made the 3D reconstructed object unrecognisable.

The remaining 12 sequences successfully demonstrated some or most parts of cardiac structures, including four chambers, atria1 and ventricular septa, foramen ovale and its valve, some other cardiac valves, parts of the pulmonary artery and veins and parts of the aorta (Figs. 2-7). Much better perception of the 3D structures can be obtained by rotating these images on an interactive video display.

In these images, the displayed fetal thorax has been edited to some extent by post-scan image surgery in order to show internal detail. Three-dimensional reconstructed objects are generally depicted by surface display [Figs. 2-4, 6(o), 71. Yellow colour within the thorax is used for natural surfaces, representing the boundaries between low echogenic (translucent) regions such as the blood pool (cardiac chambers) and amniotic fluid, and high echogenic regions such as the cardiac walls, septa and other thoracic organs. Where an artificial cut is seen, the recorded gray scale pattern is shown. Because the echogenic difference between the outer border of the cardiac walls and surrounding tissues is not as distinct as that between its inner border and the blood pool on 2D echocardiograms, reconstructed 3D images have so far been unable to depict definitely the outer surface of the heart distinct from its surroundings.

In order to view internal surfaces, some parts of the 3D objects needed to be cut away, resulting an incomplete chamber view. Otherwise, by inverting the intensity range of the images, the entire sizes and shapes of cardiac chambers could be visualized in solid (Fig. 5).

Conventional 2D cardiac planes were correctly recreated from phased 3D objects by multiplanar reformatting technique (Fig. 6). By orientating a 3D object in any desired direction, this technique was also used to generate an unlimited number of 2D planes, obtainable or unobtainable at the time of on-patient scanning.

Three sequences had well-defined 2D structural images and M-mode cardiac cycle waveforms. These were then used to build up adequate 3D images at different stages of the cardiac cycle, i.e., end-diastole, end-systole, mid-diastole and mid-systole. Arrange- ments of these different phased 3D images in cardiac cyclic order can generate dynamic 3D images of the heart beating, i.e., fetal 4D echocardiograms (Fig. 7 ), which can be best reviewed as a movie sequence (Deng et al. 1995 [available on the Internet with URL address: http://www.ucl.ac.ukmedphys/3dfoetal.html] )

DISCUSSION

Phasing the fetal cardiac cycle This study has shown the feasibility of using real-

time directed M-mode to grab and gate the fetal cardiac cycle for 3D/4D fetal cardiac reconstruction. The ad- vantages are: (1) Relative timing accuracy: real-time directed M-mode echocardiography is able to provide clear cardiac phase information by depicting both systolic and diastolic motions of both atria1 and ventricular structures of the fetal heart. It has clinically proven to be the best technique in prenatal diagnosis of fetal arrhythmias (Silverman et al. 1985). Current fetal ECG, obtained through the maternal abdominal wall, can only provide approximate cardiac phase information by demonstrating the QRS-complex of the ventricular systole, which is interfered with by strong maternal ECG signals, and there would be further intet-fer- ence from other sources, including 3D ultrasound scanning. (2) Simplicity and economy of scanning : just one commercially available real-time directed M- mode transducer is required. (3) Monitoring fetal movements: either real-time images or M-mode curves can be used for this purpose. (4) Safety: unlike Dopp- ler, the acoustic power output of real-time and M- mode is quite low and safe for the developing fetus. However, the principle of this phasing method is also applicable to 3D/4D colour Doppler reconstruction of the fetal cardiovascular system.

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Fig. 6. Interactive multiplanar reformatting of the 3D object with different orientations-( o ). and ( I ) and (2) in Fig. 2- providing unlimited sets of three orthogonal 2D planes by using only one scan data set. Shown here are: (a) long axis view of left heart, (b) cardiac base short axis view and (c) biventricular view. The positions of planes ( a), (b) and (c) are indicated

by section lines a, b and c. For abbreviations. see Figs. 1-4.

Fig. 7. Dynamic 3D (4D) display of the fetal heart beating. Only eight frames in cardiac cyclic order from a movie sequence are shown here. Except for cardiac beating, the object is being rotated to provide different 4D views. Compare to Fig. 1.

Fetal echocardiography l J. DENG et al. 985

Compared with conventional 2D fetal echocardiography, 3D scanning time is much reduced (2-5 min rather than 20 min or more), and the scanning skill required is relatively reduced as well. In contrast, off- patient processing was complicated and time-consum- ing. For a 3D acquisition, the transducer had to be moved from one place to another to provide a volume with sufficient cardiac 2D images. Consequently, the M-mode waveforms of one sequence were formed from different cardiac structures and appeared nonuni- form. This nonuniformity hindered automatic phasing programming, and manual editing was used in this preliminary study.

ments. For example, by cutting off connected atria and vessels and calculating the ventricular volumetric difference between end-diastole and end-systole, cardiac output can be obtained. The fetal cardiac index can then be derived from the cardiac output divided by fetal surface area, also obtainable from 3D reconstruction and relative measurement.

To make cardiac phasing easier and more precise, several approaches are being tried. These include developing autophasing programmes and using new transducer combinations or even new transducers. The latter may involve: (1) The use of two transducers, working simultaneously: one for real-time 2D and one for M-mode/spectral Doppler. (2) The use of one transducer that rotates about its M-mode/Doppler sampling line axis to obtain structural information as well as uniform M-mode/Doppler waveforms. The development of a high-resolution real-time 2D array transducer or a real-time volumetric transducer (Smith et al. 1992) may be a much better solution and may allow online real-time 4D echocardiography of the fetus.

Multiplanar reformatting can not only display conventional cardiac views obtainable by 2D echocardiography but it can also create clinically useful images that are difficult or impossible to obtain from 2D imaging or are difficult to obtain at the time of scanning due to nonideal fetal position. This technique can provide an unlimited number of fetal cardiac images from different points of view using one scan data set (Fig. 6), which reduces the time for one scan and the times for repeated scans. It can also be used to guide image surgery.

Interactive generation of 4D fetal cardiac images provides a more realistic presentation that is of great value not only for cardiologists detecting, prenatally, cardiac abnormalities but also for surgeons simulating future in utero heart operations and for students study- ing, noninvasively, fetal cardiology.

Problems

Freehand scanning The electromagnetic remote localiser used here

provided the freedom of moving the transducer to cover different volumes required by individual scans. This is of importance in fetal heart examination, because the fetal heart almost triples in size from 16 weeks gestational age to term (De Vore et al. 1984) and because it can be located in quite different sites inside the maternal abdomen. However, without digital access to image control settings such as zoom and pan, integration of the acquisition system with different commercial scanners is currently not ideal.

Admittedly, problems remain in processing useful 3D/4D images for routine use. These problems are due not only to inadequate quality of 2D imaging at acquisition in some patients but also to the limitations of 3D image segmentation.

For instance, a threshold is currently applied to all the area of a frame. Therefore, a selected setting may be suitable for one part of the frame but not for another part of the same frame. Hence, when the echogenicity of the membranous septum is lower than the threshold intensity suitable to render most other parts of the fetal heart, the membranous septum visible on 2D images may become invisible after 3D reconstruction.

Workstation processing Surface display (Figs. 2-4) can provide better un-

derstanding of the spatial relationship of cardiac structures visible on conventional 2D echocardiograms and of the orientations and connections of the fetal heart and great vessels invisible on 2D images. These features will help clinicians make more reliable diagnosis of spatially complex cardiovascular malformations.

Another difficulty arises when a 4D image is to be created. The necessity for applying identical segmentation and other editing parameters to all phased volumes in order to obtain a uniform dynamic sequence will sometimes sacrifice local details. In addi- tion, the present sample rate of 8- 12 frames/s due to instrumental limitation does not meet the requirement of at Ieast lo- 12 phases per cardiac cycle (equivalent to 25 frames/s) for visualising a real, dynamic 3D fetal heart.

Inverting the intensity range of the images (Fig. In fact, this study failed to disclose some fine 5) can allow better visualisation of the cardiac cham- structures, such as some cardiac valves and thin parts bers and connected great vessels, allowing easier selec- of atria1 and ventricular septa. It also distorted some tion of a region of interest for volumetric measure- tiny structures, such as atrioventricular valves and

Ultrasound in Medicine and Biology Volume 22, Number X, 1996

great vessels. Overcoming these segmentation problems will require more sophisticated technical develop- ments. which are currently being pursued.

Using the 3D acquisition technique and the real- time directed M-mode gating method, this initial study has successfully demonstrated 3D and 4D fetal cardiac images requiring much less scanning time than the conventional 2D procedure. Although further technical development is needed, the method has shown consid- erable potential for more reliable evaluation of fetal cardiac volumes and their dynamic changes, and for more precise detection of spatially complex cardiac malformations in utero.

Achnowlrdyenzenrs- We are grateful to the staff of Medical Graph- ics and Imaging Group. University College, London (UCL), for development of the 3D graphic display workstation. JD was a visiting fellow with UCL from Wuhan First Hospital, China, supported by a TCT Award from the British-Chinese governments.

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fetal echocardiography in three and four dimensions

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