Three-dimensional ultrasonography in the first trimester of human pregnancy

Human Reproduction vol.12 no.8 pp.1800–1804, 1997
Three-dimensional ultrasonography in the first trimester
of human pregnancy
Toshiyuki Hata1, Showa Aoki, Atsushi Manabe,
1982). Detailed assessments for the sequential appearance of
Kohkichi Hata and Kohji Miyazaki
embryonic structures by means of transvaginal ultrasonography
have been reported (Warren et al., 1989; Timor-Tritsh et al.,
Department of Obstetrics and Gynecology, Shimane Medical
1988, 1989, 1990, 1991; Dolkart and Reimers, 1991). Recently,
University, Izumo 693, Japan
Fujiwaki et al. (1995) demonstrated that intrauterine ultrasono-
1To whom correspondence should be addressed
graphy could reveal embryonal structures 1–3 weeks earlier
Our purpose was to visualize normal embryonal and fetal
than transvaginal ultrasonography. Images of the embryo’s
surface anatomical structures in the first trimester of
outer configuration might be better with embryoscopy
human pregnancy by use of three-dimensional ultrasono-
(Quintero et al., 1993). However, the latter two techniques are
graphy with a specially developed abdominal three-dimen-
invasive diagnostic procedures and their safety has not been
sional transducer. Four embryos and 31 fetuses of 8–13
established.
weeks gestation were studied with a specially-developed
Three-dimensional (3-D) ultrasonography allows visualiza-
abdominal three-dimensional transducer (3.5 MHz). This
tion of fetal malformations in all three dimensions at the same
imaging system can provide conventional two-dimensional
time, providing an improved overview and a more clearly
ultrasonography images and can also generate, within
defined demonstration of adjusted anatomical planes (Merz
seconds, high-quality three-dimensional images in the sur-
et al., 1995a,b). Experience with the visualization of normal
face and transparent mode with no need for an external
embryonic anatomy by 3-D scanning has now provided some
workstation. The percentage of surface anatomical struc-
authors with the experience and confidence to recognize
tures visualized at each gestational age interval using
fetal malformations in the first and early second trimesters
two-dimensional and three-dimensional ultrasonography is
(Feichtinger, 1993; Bonilla-Musoles et al., 1995; Bonilla-
presented. Head and trunk were depicted in all cases. The
Musoles, 1996). However, to the best of our knowledge, a
number and the clarity of visualization of face, upper and
detailed description of normal embryonal and fetal surface
lower extremities, hand, and foot increased with advancing
structures in the first trimester of pregnancy has not yet been
gestation. The free loop of the umbilical cord was depicted
published. The objective of the current study was to attempt
in most cases. The number of depictions of abdominal cord
a systemic look for normal embryonal and fetal surface anatomy
insertion, midgut herniation, and yolk sac decreased with
in the first-trimester pregnancy by 3-D ultrasonography with
the increase of gestation. Genitals could not be identified
a specially developed abdominal 3-D transducer.
in the first trimester. The ability to view some surface
anatomical structures (face, hand, and foot) was better
with three-dimensional ultrasonography than with two-
Materials and methods
dimensional ultrasonography. Three-dimensional ultra-
Four embryos and 31 fetuses of 8–13 weeks gestation were studied with
sonography provides a novel means for visualization of
specially developed abdominal 3-D ultrasonography transducer (Aloka
surface anatomical structures of the embryo and early
ASU-1000B, 3.5 MHz, Aloka, Tokyo, Japan). This ultrasonic trans-
fetus. These results suggest that three-dimensional ultra-
ducer is connected to an ultrasonography device (Aloka SSD-1700,
sonography can become an important modality in future
Aloka). This imaging system can provide conventional two-dimen-
embryological and early fetal research and in detection of
sional (2-D) ultrasonographic images and can also generate, within
embryonic and fetal developmental disorders in the first
seconds, high-quality 3-D images in the surface and transparent mode
with no need for an external workstation. Subjects with multiple preg-
trimester of pregnancy.
nancies or mole pregnancies were excluded from the study. All subjects
Key words: 2-D ultrasonography/3-D ultrasonography/embryo/
were evaluated in a cross-sectional manner. Gestational age was estim-
fetus/first trimester
ated from the first day of the last menstrual period and confirmed by
first trimester ultrasound examinations. The study was approved by the
local ethics committee of Shimane Medical University, and standard-
ized informed consent was obtained from each mother.
Introduction
A 3-D image is built by selecting a region of interest from a 2-D
The embryonic period, which ranges from 4 to 8 weeks after
image and superimposing on the 2-D image a volume box defined by the
the last menstrual period, is important for human development
examiner. The crystal array of the transducer then sweeps mechanically
because the beginnings of most major anatomical structures
over the 2-D region selected through a 60° angle. Within 5 seconds, the
develop during these 5 weeks. By the end of the embryonic
outlined volume is automatically scanned and a sculpture-like 3-D
period most major organ systems have been formed (Moore,
image is displayed simultaneously on the screen. At present we use a
1800
© European Society for Human Reproduction and Embryology

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3-D ultrasonography in the first trimester of human pregnancy
Figure 1. The whole view of embryo at 8 weeks 5 days. Crown–rump length
1.8 cm. H
head; LLB
lower limb bud; MH
midgut
herniation; ULB
upper limb bud; YS
yolk sac.
Figure 2. Fetus at 9 weeks. Crown–rump length
2.2 cm. (A) Lateral view; (B) lateral view. H
head; LE
lower extremity; MH
midgut herniation; UE
upper extremity. Gestational ages are expressed in weeks and days.
Figure 3. Fetus at 10 weeks. (A) Oblique view, crown–rump length (CRL)
3.3 cm; (B) oblique view, CRL
3.5 cm; (C) lateral view of
head, CRL
3.5 cm; (D) lateral view, CRL
3.5 cm. MH
midgut herniation. Gestational ages are expressed in weeks and days.
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T.Hata et al.
Figure 4. Fetus at 11 weeks. (A) Frontal view, crown–rump length (CRL)
3.8 cm. Both hands are in front of fetal face. (B) Whole view
of fetus, CRL
4.4 cm. Arrow shows the abdominal cord insertion. (C) Lateral view. CRL
4.4 cm. Gestational ages are expressed in
weeks and days.
Figure 5. Fetus at 12 weeks. Biparietal diameter
2.1 cm. (A) Frontal view; (B) frontal view of head. H
head. Gestational ages are
expressed in weeks and days.
128 Mb removable hard disk drive for the permanent storage of 3-
identified but facial structures were not imaged (Figure 1). By
D images.
week 9 upper and lower extremities, and midgut herniation were
For each gestational age interval we recorded the number of cases in
clearly seen, but the face was not yet recognizable (Figure 2).
which a superficial anatomical structure (head, face including eye, nose
Facial structures, hand, and foot could be identified at 10 weeks
and mouth, upper extremities, hand, trunk, abdominal cord insertion,
(Figure 3). At weeks 11 and 12 (Figures 4 and 5) surface struc-
midgut herniation, genitals, lower extremities, foot, free loop of cord,
tures became clearer. At week 13 fingers were depicted clearly
and yolk sac) was visualized, and the percentage of anatomical struc-
and the fetus attained a characteristic human appearance
tures at each interval using 2-D and 3-D ultrasonography was calculated.
Correlation of the detected structures with the appropriate structure
(Figure 6).
in an embryology textbook (Moore, 1982) was attempted for each
Table I shows the anatomical structures distinguished at each
gestational age. Visualization of embryonic structures by 2-D and 3-D
gestational age interval by 2-D and 3-D ultrasonography. Head
ultrasonography was compared using Fisher’s exact test (Siegel and
and trunk were depicted in all cases. The number and the clarity
Castellan, 1988 ). A P value of
0.05 was considered to be statistically
of visualization of face, upper and lower extremities, hand,
significant.
and foot increased with advancing gestation. Free loop of the
umbilical cord was depicted in most cases. The number of occur-
Results
rences of visualization of abdominal cord insertion, midgut her-
Development of the fetus was recorded as 3-D images (Figures
niation, and yolk sac decreased with the advance of gestation.
1–6). By the eighth week the whole embryonal contour could be
Genitals could not be identified in the first trimester. The ability
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3-D ultrasonography in the first trimester of human pregnancy
Figure 6. Fetus at 13 weeks. (A) Oblique view, biparietal diameter
2.4 cm. (B) Lateral view, biparietal diameter
2.4 cm. (C) Lateral
posterior view, biparietal diameter
2.4 cm. (D) Hand and fingers, biparietal diameter
2.6 cm. (E) The whole view of fetus. Free loop
of the cord (arrow) is depicted, biparietal diameter
2.6 cm. Gestational ages are expressed in weeks and days.
Table I. Percentage of cases in which anatomical structures were vizualized at each gestational age by
two-dimensional (2-D) and three dimensional (3-D) ultrasonography
Anatomical structures Gestational age (weeks)
8–9.9 (n
10)
10–11.9 (n
13)
12–13.9 (n
12)
2-D
3-D
2-D
3-D
2-D
3-D
Head
100
100
100
100
100
100
Face
0
0
0
69*
17
58*
Upper extremities
60
50
92
85
100
100
Hand
0
0
15
54*
25
42
Trunk
100
100
100
100
100
100
Addominal cord insertion
70
80
77
92
58
50
Midgut herniation
70
80
50
62
0
0
Genitals
0
0
0
0
0
0
Lower extremities
70
60
100
92
100
92
Foot
0
0
0
38*
8
25
Free loop of cord
90
90
92
85
100
92
Yolk sac
90
90
69
69
0
0
*P
0.05; 2-D versus 3-D at each gestational age.
to view some surface anatomical structures, such as face, hand
transducer, and this imaging system proved capable of providing
and foot, was better with 3-D ultrasonography than with 2-D.
conventional 2-D ultrasonography images, while also possessing
the capacity to generate within, high-quality fine, 3-D images
on the screen with no need for an external workstation (Baba
Discussion
et al., 1996). However, facial structures could not be identified
Potential obstetric applications of 3-D ultrasonography for sys-
at 8–9 weeks gestation, and image quality was slightly impaired.
tematic examination of the developmental stages of the embryo
In the process of embryogenesis, the configuration of embryonic
and early fetus or detection of embryonal and early fetal mal-
facial structure has not been established at this period (Moore,
formations have been reported (Feichtinger, 1993; Bonilla-
1982). Other reasons for these ambiguous visualizations are
Musoles et al., 1995; Steiner et al., 1995; Bonilla-Musoles,
the small embryonal size and the fact that the transabdominal
1996). However, the whole process still takes 5–10 min. In the
transducer frequency (3.5 MHz) is relatively low. Use of a
current study we used a specially developed abdominal 3-D
transvaginal 3-D probe with high-frequency transducer may
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T.Hata et al.
Merz, E., Bahlmann, F. and Weber, G. (1995a) Volume scanning in the
make it possible to obtain finer quality images of very small
evaluation of fetal malformations: a new dimension in prenatal diagnosis.
embryonic structures. However, good quality images of the fetus
Ultrasound Obstet. Gynecol., 5, 222–227.
could be obtained using the transabdominal transducer at 10
Merz, E., Bahlmann, F., Weber, G. and Macchiella, D. (1995b) Three-
dimensional ultrasonography in prenatal diagnosis. J. Perinat. Med., 23,
weeks gestation.
213–222.
The embryonic and early fetal periods are important for human
Moore, K.L. (1982) The Developing Human. 2nd edn. W.B.Saunders,
development because most major organ systems have been
Philadelphia, USA, pp. 227–254.
formed by this time (Moore, 1982). Detailed assessments for
Pretorius, D.H. and Nelson, T.R. (1995) Fetal face visualization using three-
dimensional ultrasonography. J. Ultrasound Med., 14, 349–356.
the sequential appearance of embryonic structures by means of
Quintero, R.A., Romero, R., Mahoney, M.J. et al. (1993) Embryoscopic
transvaginal ultrasonography have been reported (Warren et al.,
demonstration of hemorrhagic lesions on the human embryo after placental
1989; Timor-Tritsh et al., 1988, 1989, 1990, 1991; Dolkart and
trauma. Am. J. Obstet. Gynecol., 168, 756–759.
Reimers, 1991). However, even under optimal conditions, the
Siegel, S. and Castellan, N.J. (1988) Nonparametric Statistics for the
Behavioral Sciences. 2nd edn. McGraw-Hill Book Company, New York,
complex curvature of the embryo makes it difficult to obtain
pp. 103–111.
adequate images with 2-D ultrasonography, and many cross-
Steiner, H., Mertz, E. and Staudach A. (1995) Three-dimensional fetal facing.
sectional images are required to obtain a complete impression
Hum. Reprod. Update, 1, Item 6.
Timor-Tritsh, I.E., Farine, D. and Rosen, M.G. (1988) A close look at early
(Pretorius and Nelson, 1995). Our study demonstrated that 3-D
embryonic development with the high-frequency transvaginal transducer.
ultrasonography could clearly reveal the surface of the entire
Am. J. Obstet. Gynecol., 159, 676–681.
embryo and early fetus in the first trimester. However, in this
Timor-Tritsh, I.E., Warren, W.B., Peisner, D.B. and Pirrone, E. (1989) First-
study, genitals could not be recognized in the first trimester of
trimester midgut herniation: a high-frequency transvaginal sonographic
study. Am. J. Obstet. Gynecol., 161, 831–833.
pregnancy. Bonilla-Musoles et al. (1995) identified male fetal
Timor-Tritsh, I.E., Peisner, D.B. and Raju, S. (1990) Sonoembryology: an
genitals as early as week 12, using a transvaginal approach. Use
organ-oriented approach using a high-frequency vaginal probe. J. Clin.
of a transvaginal 3-D probe with high-frequency transducer
Ultrasound, 18, 286–298.
Timor-Tritsch, I.E., Monteagudo, A. and Warren, W.B. (1991) Transvaginal
should make it possible to obtain finer quality images of very
ultrasonographic definition of central nervous system in first and early
small embryonic structures at an earlier stage than with a transab-
second trimesters. Am. J. Obstet. Gynecol., 164, 497–503.
dominal 3-D probe. Unfortunately, at present we do not have a
Warren, W.B., Timor-Tritsh, I.E., Peisner, D.B. et al. (1989) Dating the early
transvaginal 3-D probe for our new 3-D ultrasonographic device;
pregnancy by sequential appearance of embryonic structures. Am. J. Obstet.
Gynecol., 161, 747–753.
further technical development is awaited.
With respect to limitations associated with 3-D ultrasono-
Received on January 20, 1997; accepted on May 8, 1997
graphy in the first trimester (Bonilla-Musoles et al., 1995), the
most common reason for partial observation was active
embryonal or fetal movement. Another reason was the proximity
of the fetus to the uterine wall or to the placenta. A third barrier
to complete visualization is location of the fetal head deep in the
pelvis in a direct occipito–anterior position. Moreover, strong
curvature of the gestational sac restricted satisfactory visualiza-
tion of the embryo. These problems with 3-D ultrasound fetal
imaging will be resolved as further technical advances are made
(Merz et al., 1995b).
In conclusion, 3-D ultrasonography provides a novel means
for visualizing surface anatomical structures of the embryo and
early fetus. These results suggest that 3-D ultrasonography can
become an important tool in future embryological and early fetal
research and in detection of embryonic and fetal developmental
disorders in the first trimester of pregnancy.
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