First-Trimester Ultrasound: A Comprehensive Guide

13. Three-Dimensional Ultrasound: A Role in Early Pregnancy?

Luís F. Gonçalves 

(1)

Divisions of Fetal Imaging and Pediatric Radiology, Departments of Obstetrics & Gynecology and Radiology, Oakland University William Beaumont School of Medicine, 3601 W 13 Mile Road, Royal Oak, MI 48073, USA

Luís F. Gonçalves

Email: luis.goncalves@beaumont.edu

Keywords

3D ultrasoundThree-dimensional ultrasound3DUSFirst trimesterFetusEmbryoSTICSpatiotemporal image correlationCongenital anomaliesPrenatal diagnosisFetal anomaliesAnomalies

Introduction

Although the second-trimester “18- to 22-week” scan is the standard of care for fetal anatomical evaluation, technological progress in ultrasound equipment and high-frequency transvaginal transducers made detailed assessment of the first-trimester fetus a reality [19]. High-quality first-trimester ultrasonography represents the first opportunity to identify congenital structural anomalies, usually those at the most severe end of the spectrum [81013]. Parents whose fetus is diagnosed with major and/or lethal anomalies have the benefit of earlier complementary diagnostic workup and counseling and, if pregnancy termination is a consideration, it can performed earlier and safer than if the same diagnosis was made during the second trimester [11].

This chapter reviews the role of three-dimensional ultrasound (3DUS) as an adjunctive imaging modality to two-dimensional ultrasound (2DUS) for first-trimester diagnosis of congenital anomalies. The reader is reminded that knowledge of embryology, natural history of congenital anomalies, as well as operator experience are likely to have a greater impact on the quality of the first-trimester exam than the availability of high-resolution ultrasound systems equipped with state of the art 3D technology.

Instrumentation

3DUS can be performed using mechanical or matrix array transducers. First-trimester prenatal diagnosis of congenital anomalies is ideally performed using high-frequency transvaginal probes. If evaluation of the fetal heart is desired, color Doppler is strongly advised, as its use is associated with increased detection rates for congenital heart disease in the first trimester [111416]. For the examination of the first-trimester heart, volumes are acquired using 4D spatiotemporal image correlation (STIC) technology so that cardiac motion can be analyzed as well [1720].

Ideal Gestational Age to Perform the Exam

Recent studies indicate that extending the NT examination to include a detailed survey for fetal anomalies, in addition to early fetal echocardiography if the NT is increased, results in a high detection rate for congenital anomalies [11121621]. Visualization rates for fetal cardiac structures is higher after 12 weeks compared to 11 weeks, and even better after 13 weeks, when the aortic root can be more consistently demonstrated [22]. The tradeoff is the upper crown-rump length limit of 84 mm to measure the NT [9]. Therefore, careful scheduling of the examination is advised so that both exams can be performed in a single visit.

Please also note that a high detection rate for fetal anomalies, including congenital heart disease, has been reported with the use of transvaginal ultrasonography by expert sonologists performing such exams between 14 and 17 weeks of gestation [1323].

What Can Be Confidently Imaged?

Much of what can be confidently imaged in the first trimester comes from work performed with 2DUS. Table 13.1 provides a list of anatomical structures that may be assessed during the 11–13 6/7 weeks scan [9]. The reader is encouraged to attempt to image structures marked as optional as well, and to push his/her limits beyond the guidelines. For example, with good technique and adequate equipment, the outflow tracts of the fetal heart can be imaged early, and early diagnosis of conotruncal anomalies is possible [5142425].

Table 13.1

Suggested anatomical assessment at 11 to 13 + 6 weeks (ISUOG—International Society of Ultrasound in Obstetrics and Gynecology – guidelines)a

Organ/anatomical area

Present and/or normal?

Head

Present

Cranial bones

Midline falx

Choroid-plexus-filled ventricles

Neck

Normal appearance

Nuchal translucency thickness (if accepted after informed consent and trained/certified operator available)b

Face

Eyes with lensb

Nasal boneb

Normal profile/mandibleb

Intact lipsb

Spine

Vertebrae (longitudinal and axial)b

Intact overlying skinb

Chest

Symmetrical lung fields

No effusions or masses

Heart

Cardiac regular activity

Four symmetrical chambersb

Abdomen

Stomach present in left upper quadrant

Bladderb

Kidneysb

Abdominal wall

Normal cord insertion

No umbilical defects

Extremities

Four limbs each with three segments

Hands and feet with normal orientationb

Placenta

Size and texture

Cord

Three-vessel cordb

aAdapted with permission from ISUOG practice guidelines: performance of first-trimester fetal ultrasound scan. Ultrasound Obstet Gynecol 2013;41:102–113

bOptional structures

Prenatal Diagnosis of Congenital Anomalies by First-Trimester Ultrasound

Since the first reports demonstrating the feasibility of first trimester diagnosis of congenital anomalies in the late 1980s [12627], mounting evidence indicates that accurate prenatal diagnosis of several of the more severe anomalies can be accomplished in the first trimester using high-resolution transvaginal ultrasonography [1282328]. Table 13.2 provides a summary of the studies published until 2014. These studies also provide evidence that, although early and accurate diagnosis of congenital anomalies is possible and allows early decision making, several anomalies may be missed if a second-trimester (or even a third trimester) scan is not performed. Examples of anomalies that can be missed by a first-trimester scan include vermian hypoplasia, agenesis of the corpus callosum, abnormalities of neuronal migration (e.g., lissencephaly, polymicrogyria, gray matter heterotopia), congenital lung anomalies, hypoplastic left heart, aortic and pulmonic valve stenosis, coarctation of the aorta, renal and bladder anomalies, gastrointestinal anomalies, as well as several skeletal anomalies that may manifest only later in pregnancy [7101214252932].

Table 13.2

First-trimester detection rates for congenital anomalies

Author

Country

Year

N

Approach

Detected anomalies N (%)

Additional fetuses with anomalies detected >14 weeks (including second- and third-trimester scans and postnatally) N(%)

First-trimester detection rate (%)

Rottem et al. [1]

Israel

1989

141

TV

3 (2.12)

0

100

Cullen et al. [27]

USA

1990

622

TV

33 (5.31)

NA

NA

Rottem and Bronshtein

Israel

1990

1652

TV

40 (2.42)

4 (0.24)

90.9

Achiron and Tadmor [3]

Israel

1991

800

TA and. TV

8 (1.00)a

6 (0.75)

57.1

Bonilla-Musolles

Spain

1994

834

TV

27 (3.24)

3 (0.36)

90

Yagel et al. [29]

Israel

1995

536

TV

42 (7.8)

13 (2.4)

76.4

D’Ottavio et al. [31]

Italy

1995

4078

TV

54 (1.3)

34 (0.83)

61.4

Hernadi and Torocsik [30]

Hungary

1997

3991

TA and TV

20 (0.41)

29 (0.73)

40.8

Economides et al. [63]

England

1998

1632

TA + TV

11 (0.67)

6 (0.37)

64.7

Whitlow et al. [64]

England

1999

6634

TA + TV

37 (0.56)

55 (0.83)

40.2

Guariglia and Rosatti [10]

Italy

2000

3478

TV

33 (0.95)

31 (0.89)

51.6

Carvalho et al. [65]

Brazil

2002

2853

TA + TV

29 (1.02)

101 (3.54)

22.3

den Hollander et al. [66]

Netherlands

2002

101

TA + TV

9 (9)

2 (2)

81.8

Drysdale et al. [67]

England

2002

984

TA

5 (0.51)

25 (2.54)

16.7

Taipale et al. [68]

Norway

2004

4513

TV

6 (0.13)

27 (0.59)

18.2

Chen et al. [69]

Hong Kong

2004

1609

TA + TV

14 (0.87)

12 (74.6)

53.8

Becker and Wegner [14]

Germany

2006

3094

TA + TV

72 (2.36)

14 (0.45)

83.7

Saltvedt et al. [70]

Sweden

2006

18,053

TA

74 (0.41)

297 (1.64)

20

Cedergren et al. [71]

Sweden

2006

2708

TA

13 (0.48)

19 (0.70)

40.6

Dane et al. [72]

Turkey

2007

1290

TA + TV

17 (1.32)

7 (0.54)

70.8

Chen et al. [69]

Hong Kong

2008

3949

TA + TV

30 (0.76)

33 (0.84)

47.6

Oztekin et al. [73]

Turkey

2009

1085

TA and TV

14 (1.29)

7 (0.65)

66.6

Ebrashy et al. [7]

Egypt

2010

2876

TA + TV

21 (0.73)

10 (0.35)

67.7

Syngelaki et al. [28]

England

2011

44,859

TA + TV

213 (0.48)

275 (0.61)

43.6

Iliescu et al. [11]

Romania and Greece

2013

5472

TA + TV

67 (1.22)

98 (1.05)

41.1

Bromley et al. [12]

USA

2014

9962

TA + TV

50 (0.50)

130 (1.30)

27.7

Goldstein et al. [21]

Israel

2014

4467

TA + TV

33 (0.74)

28 (1.04)b

54.1

TA + TV, transabdominal ultrasonography, followed by transvaginal ultrasonography if adequate views could not be obtained transabdominally; TA and TV, transabdominal followed by transvaginal ultrasonography in all cases; TV, only transvaginal ultrasonography

a4/8 anomalies detected only by transvaginal ultrasonography

bAscertainment available for only 60 % of the scanned pregnancies

What Does 3D Ultrasound Add?

3DUS adds the possibility to obtain multiple planes of an anatomical structure from a 3D volume dataset. The elevation plane, in particular, which is perpendicular to the direction of the sound beam, is impossible to obtain using conventional 2DUS. This capability can be particularly advantageous during the first trimester, when manipulation of the vaginal probe is restricted and, therefore, the obtainable planes of section are limited [33]. Another potential benefit, provided that it can be proved beyond doubt that offline analysis of volume datasets has at least the same level of accuracy as real-time analysis of 2DUS images, is that embryonic exposure to ultrasound can be reduced, since volume acquisition takes only a few seconds and image processing and analysis can be performed offline [34].

Sonoembryology is the term that describes a detailed assessment of the live embryo in vivo by high-resolution transvaginal ultrasonography [333536]. Initial publications on sonoembryology relied on images obtained by 2DUS. Since the original work describing the use of a specially designed high-resolution 3D transvaginal probe for reconstruction of small embryonic structures by Blaas et al. [37] in 1995, several investigators have reported on the use 3DUS for volumetric measurement [3839], assessment of normal embryonic development and early fetal anatomy [344046], as well as early prenatal diagnosis of congenital anomalies [424755].

The best studied organ has been the embryonic brain, with initial studies focusing on volumetry and anatomy of cerebral brain vesicles [373856]. Today, exquisite 3D images of the ventricular system can be obtained using commercially available equipment and inversion mode technology (Fig. 13.1), as reported by Kim et al. [42], who obtained 3DUS volumes of the embryonic and early fetal brain by transvaginal ultrasonography in 46 patients examined between 6 and 13 menstrual weeks. Inversion mode was used to reconstruct the early ventricular system. Appropriate reconstructions were possible only for volumes acquired between 7 and 12 weeks. Based on the experience with that work, the authors correctly diagnosed one case of alobar holoprosencephaly at 10 6/7 weeks and one case of early ventriculomegaly at 12 4/7 weeks.

A328333_1_En_13_Fig1_HTML.jpg

Fig. 13.1

3D rendering of the early cerebral ventricles using inversion mode. P pontine flexure, D diencephalon (future third ventricle), M mesencephalon (future sylvian aqueduct), IR isthmus rhombencephali, RHrhombencephalic cavity

As it is natural to occur with any emerging technologies, several case reports and series have illustrated how 3DUS helped with specific diagnoses, mainly during the embryonic period [48515760]. Among the most interesting are the early detection of a case of spina bifida at 9 weeks with exquisite detail of the defect demonstrated by 3D surface rendered images of the embryonic torso (Fig. 13.2) [495860], confident diagnoses of cyclopia [50] and proboscis [5051] by 3D multiplanar reconstruction at 9 2/7 weeks [50] and 10 6/7 weeks [51] in association with alobar holoprosencephaly, digital casts of the abnormal ventricular system in cases of holoprosencephaly as early as 9 2/7 weeks, conjoined twins at 9 [55] and 10 weeks [57], prune-belly syndrome [58], iniencephaly [45] and frontonasal malformation [61] at 11 weeks, and severe scoliosis associated with omphalocele [58] and encephalocele [45] at 12 weeks.

A328333_1_En_13_Fig2_HTML.jpg

Fig. 13.2

Very early diagnosis of spina bifida by 2DUS and 3DUS at 9 weeks last menstrual period-based gestational weeks. (a) Crown-rump length 22 mm. Left: horizontal section through the embryonic abdomen. Right: three-dimensional geometric reconstruction obtained through manual segmentations; the elevated spinal defect was segmented separately and colored red. The arrows point at the spinal defect; (b) crown-rump length 25 mm. Left: sagittal section through the embryonic spine. Right: three-dimensional surface rendering showing clearly the myelomeningocele at the embryo’s back. The arrows point at the spinal defect. Reprinted from Best Practice & Research Clinical Obstetrics & Gynaecology, 28, Blaas HK, Detection of structural abnormalities in the first trimester using ultrasound, 341–53, Copyright 2014, with permission from Elsevier

More recent research efforts have focused on the role of 4DUS with spatiotemporal image correlation (STIC) technology and color Doppler for evaluation of the first trimester fetal heart (Fig. 13.3). Reported visualization rates for normal fetal echocardiographic landmarks are: situs (61–64 %), four-chambers (86–100 %), left ventricular outflow tract (50–91 %), right ventricular outflow tract (64–100 %), three-vessel and trachea view (75–98 %), and pulmonary veins (32–54 %) [171862]. In studies that have addressed the issue of visualization rates according to gestational age at the time of examination, improved visualization rates for specific structures such as the aortic root and three-vessel view, and a complete examination of the heart were usually possible only after 12 weeks [18]. Improved visualization rates correlate with higher quality volume datasets (based on lack of motion and sharpness of original images) and volume acquisition using a transvaginal probe [19]. Successful early diagnosis of congenital heart disease has been reported in a few studies, including cases of transposition of the great arteries, tricuspid atresia, Ebstein’s anomaly, tetralogy of Fallot, pulmonary atresia with ventricular septal defect, isolated ventricular septal defects, double outlet right ventricle with mitral atresia, hypoplastic left heart syndrome, and atrioventricular septal defects [1820]. Espinoza et al. [20] reported on a multicentric study in which four international centers with expertise in first-trimester 4D fetal echocardiography were asked to examine 4D volume datasets of normal (n = 17) and abnormal fetuses (n = 16) without prior knowledge of clinical indications or results of the 2DUS examination. The median (range) accuracy, sensitivity, and specificity as well as the positive and negative likelihood ratios, for the identification of fetuses with congenital heart defects were 79 % (77–83 %), 90 % (70–96 %), 59 % (58–93 %), 2.35 % (2.05–9.80 %), and 0.18 % (0.08–0.32 %), respectively. The study showed that experienced examiners can use volume datasets to diagnose congenital heart disease with reasonable sensitivity between 11 and 15 weeks; however, the specificity of 59 % was somewhat disappointing. In the only study that compared the effectiveness of 4DUS with STIC against transvaginal 2DUS for diagnosis of congenital heart disease, which included 121 fetuses examined by 2DUS and 115 fetuses examined by 2DUS and 4DUS with STIC, the diagnostic accuracy and area under the receiver-operating characteristics (ROC) curve were significantly higher for 2DUS (diagnostic accuracy: 2DUS 94.2 % vs. 4DUS with STIC 88.7 %; area under the ROC curve: 2DUS 0.912 vs. 4DUS with STIC 0.818, p < 0.05) [18].

A328333_1_En_13_Fig3_HTML.jpg

Fig. 13.3

Tomographic ultrasound image of a volume dataset of the fetal heart obtained using transvaginal ultrasonography with color Doppler and STIC technology at 12 weeks. Images are presented in diastole (a) and systole (b). Note that the aortic root and pulmonary veins are sometimes difficult to visualize in volumes obtained early in pregnancy, as noted in previously published research [171862]. PApulmonary artery, Ao aorta, DA ductus arteriosus, RPA right pulmonary artery, LV left ventricle, RV right ventricle

Summary

3DUS is an attractive technology for early evaluation of the human fetus, with several anomalies, usually major, correctly diagnosed by the method, as illustrated by several case reports, small series, and pictorial assays. At this time, there is no evidence that unequivocally supports that 3DUS is either superior to or that it improves the diagnostic accuracy for early detection of congenital anomalies over 2DUS.

More research is needed, comparing actual diagnostic accuracy of offline analysis of a first-trimester volume dataset, without knowledge of the results of the 2DUS before having access to 2DUS images obtained by a technologist or colleague, or direct real-time examination of the patient [60]. Only in this way will there be unbiased data to support an eventual role for 3DUS in the systematic evaluation of first-trimester pregnancies.

Teaching Points

·               High-resolution images of the embryo and early fetus can be obtained with transvaginal ultrasonography.

·               Several studies demonstrate that early diagnosis of major congenital anomalies is possible by high-resolution transvaginal ultrasonography; however, early ultrasonography is not sufficient to diagnose a significant number of anomalies that may manifest only in the second or third trimesters.

·               High-resolution 3D imaging of the embryo and early fetus can be obtained using transvaginal probes equipped with 3D and 4D technology, facilitating understanding of embryonic anatomy in vivo (sonoembryology).

·               There is currently no evidence that first trimester 3DUS is superior to or that it definitively improves the detection rates for congenital anomalies compared to 2DUS.

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