DOI: 10.1148/rg.241035027
(Radiographics. 2004;24:157-174.)
© RSNA, 2004
Detection of Fetal Structural Abnormalities with US during Early Pregnancy1
Katherine W. Fong, MB, BS, FRCPC,
Ants Toi, MD, FRCPC,
Shia Salem, MD, FRCPC,
Lisa K. Hornberger, MD, FRCPC,
David Chitayat, MD, FRCPC,
Sarah J. Keating, MD, FRCPC,
Fionnuala McAuliffe, MD, MRCOG, MRCPI and
Jo-Ann Johnson, MD, FRCSC
1 From the Department of Medical Imaging (K.W.F., A.T., S.S.), Prenatal Diagnosis and Medical Genetics Program (D.C.), Department of Pathology and Laboratory Medicine (S.J.K.), and Department of Obstetrics and Gynecology (F.M., J.J.), Mount Sinai Hospital and University of Toronto, 600 University Ave, Rm 570, Toronto, ON, Canada M5G 1X5; and the Department of Pediatrics, Hospital for Sick Children and University of Toronto (L.K.H.). Presented as an education exhibit at the 2002 RSNA scientific assembly. Received February 4, 2003; revision requested April 9 and received June 19; accepted June 19. All authors have no financial relationships to disclose. Address correspondence to K.W.F. (e-mail: katherine.fong@sympatico.ca).
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Abstract
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Ultrasonography (US) is performed during early pregnancy for dating, determination of the number of fetuses, assessment of early complications, and increasingly for evaluation of the fetus, including measurement of the thickness of the nuchal translucency (NT). Measurement of NT thickness between 11 and 14 weeks gestation, combined with maternal age and maternal serum biochemistry, can be an effective method of screening for trisomy 21 and other chromosomal abnormalities. Furthermore, an increased NT thickness in the presence of a normal karyotype is associated with an increased frequency of structural defects and genetic syndromes. Therefore, this finding is an indication for a more detailed anatomic survey of the fetus. Besides nuchal abnormalities, a wide range of other congenital anomalies can be diagnosed with US at 11–14 weeks gestation, including defects of the central nervous system, heart, anterior abdominal wall, urinary tract, and skeleton. The anatomic survey can be performed with a standardized protocol by using transabdominal US and, when necessary, transvaginal US. A thorough knowledge of the US features of normal fetal development is necessary to avoid potential diagnostic pitfalls.
© RSNA, 2004
Index Terms: Fetus, abnormalities, 856.87 • Fetus, US, 856.1298 • Pregnancy, abnormalities, 856.87 • Pregnancy, US, 856.1298
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LEARNING OBJECTIVES
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After reading this article and taking the test, the reader will be able to:
- Identify fetal structural abnormalities that can be detected with US during the first 14 weeks of pregnancy.
- Discuss nuchal translucency screening for chromosomal abnormalities, structural defects, and genetic syndromes.
- Describe the potential diagnostic pitfalls and limitations of fetal US due to early fetal development.
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Introduction
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Ultrasonography (US) is usually performed in the first trimester (up to 13 weeks 6 days gestation) for dating, determination of the number of fetuses, and assessment for early pregnancy complications. Recently, fetal nuchal translucency (NT) measurement between 11 and 14 weeks gestation, combined with maternal age, has provided an effective method of screening for trisomy 21 and other chromosome abnormalities (1). The detection rate of fetuses with trisomy 21 is further increased by combining maternal age, fetal NT thickness, and maternal serum biochemistry (free ß–human chorionic gonadotropin and pregnancy-associated plasma protein-A) (2). In addi-tion, increased NT thickness in the presence of a normal karyotype is associated with an increased frequency of structural defects and genetic syndromes (3,4) and is an indication for more detailed scanning of the fetus.
Besides nuchal abnormalities, a wide range of other congenital anomalies can be diagnosed at 11–14-week US (5), including defects of the central nervous system, heart, anterior abdominal wall, urinary tract, and skeleton. However, in some conditions, such as anencephaly, the early US features differ from those observed in the second and third trimesters (6). It is also important not to mistake normal embryonic findings such as physiologic midgut herniation for anomalies (7).
In this article, our objectives are as follows: (a) to review nuchal and structural abnormalities detected before or at 14 weeks gestation and (b) to discuss potential diagnostic pitfalls and limitations due to early fetal development.
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Materials and Methods
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We retrospectively reviewed cases of abnormal US findings in fetuses scanned before or at 14 weeks gestation during the period July 1, 2000, to October 30, 2002. The study was approved by the Research Ethics Committees of the participating hospitals. All women underwent transabdominal US and, when necessary, transvaginal US, which were performed with an ATL-HDI 5000 unit (Philips Medical Systems, Bothell, Wash). The US findings were correlated with the results of autopsy, chromosome analysis, further US studies performed in the second and third trimesters, and fetal echocardiography, as well as results of postnatal follow-up, when available. Termination with dilation and curettage precluded detailed pathologic examination in some cases.
Since this was not a prospective study, we did not have the total number of US studies performed during the specified period or a record of the outcome for all cases. However, among the group of 8,537 women scanned at 11–14 weeks gestation (crown-rump length, 45–84 mm), there were 175 fetuses with an increased NT (NT measurement > 95th percentile for crown-rump length when normative data for our population were used). Chromosomal abnormality was present in 33 of 124 fetuses karyotyped. Out-comes were available in 59% of fetuses (103 of 175). Some of the examples for this pictorial essay were chosen from this group.
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Fetal Head, Spine, and Face
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The early embryo (<10 weeks) is best examined with transvaginal US. The cephalic pole or end is identified by about 7 weeks. The echo-free space behind the hindbrain is the rhombencephalic cavity (the developing fourth ventricle), which decreases in size as the cerebellum forms (8) (Fig 1). It should not be mistaken for an abnormality.
By 10 or 11 weeks gestation, the echogenic choroid plexuses are the most prominent intracranial structures and fill the (relatively large) lateral ventricles (Fig 2a). The brain parenchyma at this age is very thin and is seen as a relatively hypoechoic peripheral rind that is best appreciated in the frontal region. The thalamus and midbrain are visible more caudally (Fig 2b). Ossified frontal and parietal bones are visible by 11 weeks (Fig 2).
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Figure 2a. Normal head at 12 weeks gestation. (a) Axial transabdominal US image of the fetal head shows ossified frontal and parietal bones (arrows) and echogenic choroid plexuses (C) filling the lateral ventricles. (b) Axial US image obtained caudad to a shows the thalamus (T). (c) Coronal US image shows the ossified frontal bone (arrow) and orbits.
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Figure 2b. Normal head at 12 weeks gestation. (a) Axial transabdominal US image of the fetal head shows ossified frontal and parietal bones (arrows) and echogenic choroid plexuses (C) filling the lateral ventricles. (b) Axial US image obtained caudad to a shows the thalamus (T). (c) Coronal US image shows the ossified frontal bone (arrow) and orbits.
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Figure 2c. Normal head at 12 weeks gestation. (a) Axial transabdominal US image of the fetal head shows ossified frontal and parietal bones (arrows) and echogenic choroid plexuses (C) filling the lateral ventricles. (b) Axial US image obtained caudad to a shows the thalamus (T). (c) Coronal US image shows the ossified frontal bone (arrow) and orbits.
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Acrania, Exencephaly, Anencephaly
Anencephaly is the most common anomaly affecting the central nervous system and results from failure of closure of the rostral portion of the neural tube. Typically, there is progression in utero from a relatively normal-appearing brain to an amorphous brain mass to no recognizable brain tissue (which is the usual US appearance of anencephaly in the second and third trimesters). In the first trimester, the brain of affected fetuses may appear relatively normal (Fig 3a) or may demonstrate varying degrees of distortion and disruption (exencephaly). However, the important US feature is an absent cranium, which allows diagnosis from 11 weeks onward (9). At 11–14 weeks gestation, the majority of cranial ossification is in the lateral aspects of the frontal bones and lower parietal bones, and no vault ossification is visible in the midline on a perfect midsagittal image. Hence, misdiagnosis may occur if only midsagittal views of the fetus are obtained, such as those for NT measurement and nasal bone assessment. The absence of cranial ossification may not be noted, and the head may appear relatively normal (Fig 3b). It is important to look specifically for frontal bone ossification in the axial and coronal planes.
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Figure 3a. Acrania and exencephaly at 12 weeks gestation. Coronal (a) and sagittal (b) transvaginal US images of the fetal head show an absent cranial vault and an amorphous mass of neural tissue (arrow). The facial structures and orbits are present.
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Figure 3b. Acrania and exencephaly at 12 weeks gestation. Coronal (a) and sagittal (b) transvaginal US images of the fetal head show an absent cranial vault and an amorphous mass of neural tissue (arrow). The facial structures and orbits are present.
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Encephalocele
The term encephalocele refers to herniation of intracranial structures through a cranial defect due to either incomplete closure of the neural tube or disruption by an amniotic band. Most cases are occipital in location (75%) (Fig 4), but some are frontal or parietal. An associated calvarial defect helps differentiate encephaloceles from cystic hygromas. Diagnosis may not be possible before the onset of cranial ossification. Encephaloceles may occur with genetic conditions such as Meckel-Gruber syndrome, an autosomal recessive disor-der characterized by renal cystic dysplasia, encephalocele, and polydactyly (Fig 5).
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Figure 4. Encephalocele at 14 weeks gestation. Axial transvaginal US image of the fetal head shows an occipital encephalocele (arrow), with brain tissue herniating through a defect in the occipital bone. The head is microcephalic.
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Figure 5a. Meckel-Gruber syndrome at 12 weeks gestation. (a) Sagittal transabdominal US image of the fetus shows an occipital encephalocele (arrow). (b) Coronal transvaginal US image of the fetal abdomen shows large, echogenic kidneys (cursors). The urinary bladder is not visible. (c) Transvaginal US image of the fetal hand shows postaxial polydactyly (arrow).
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Figure 5b. Meckel-Gruber syndrome at 12 weeks gestation. (a) Sagittal transabdominal US image of the fetus shows an occipital encephalocele (arrow). (b) Coronal transvaginal US image of the fetal abdomen shows large, echogenic kidneys (cursors). The urinary bladder is not visible. (c) Transvaginal US image of the fetal hand shows postaxial polydactyly (arrow).
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Figure 5c. Meckel-Gruber syndrome at 12 weeks gestation. (a) Sagittal transabdominal US image of the fetus shows an occipital encephalocele (arrow). (b) Coronal transvaginal US image of the fetal abdomen shows large, echogenic kidneys (cursors). The urinary bladder is not visible. (c) Transvaginal US image of the fetal hand shows postaxial polydactyly (arrow).
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Spina Bifida
Vertebral bodies start ossifying in the midthoracic region by 7 weeks, and ossification extends toward the head and sacrum. Neural arches in con-trast start ossifying in the neck and proceed cau-dally. Braithwaite et al (10) reported successful examination of the vertebrae and overlying skin by 12–13 weeks gestation. In some cases of spina bifida, the lemon sign can be present before 14 weeks gestation (11). The term lemon sign refers to scalloping or indentation of the frontal bones (Fig 6). We have also seen a case of Arnold-Chiari malformation with the banana sign and meningomyelocele at 14 weeks gestation (Fig 7). The term banana sign refers to anterior curvature of the cerebellum and associated obliteration of the cisterna magna. In the second trimester, the lemon sign and banana sign are useful US markers for identifying fetuses with open spina bifida (12). However, these signs have not been fully evaluated in early pregnancy. When ventriculomegaly occurs, the choroid plexuses (which have higher specific gravity than cerebrospinal fluid) gravitate to the dependent wall of the lateral ventricle. The choroid plexus in the more dependent ventricle appears to dangle from its point of fixation near the foramen of Monro (13) (Fig 6).
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Figure 6. Lemon sign and ventriculomegaly at 13 weeks gestation. Axial transabdominal US image of the fetal head shows bilateral frontal indentation (arrows) and ventriculomegaly, as evidenced by a dangling choroid plexus (C) and convexity of the lateral wall of the lateral ventricle (arrowheads).
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Figure 7a. Arnold-Chiari malformation with the banana sign and meningomyelocele at 14 weeks gestation. (a) Axial transabdominal US image of the fetal head shows a banana-shaped cerebellum (arrows) and effacement of the cisterna magna (CM). (b) Sagittal US image of the fetal lumbosacral region shows a meningomyelocele (arrow).
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Figure 7b. Arnold-Chiari malformation with the banana sign and meningomyelocele at 14 weeks gestation. (a) Axial transabdominal US image of the fetal head shows a banana-shaped cerebellum (arrows) and effacement of the cisterna magna (CM). (b) Sagittal US image of the fetal lumbosacral region shows a meningomyelocele (arrow).
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Holoprosencephaly
Holoprosencephaly results from incomplete cleavage of the primitive forebrain into two cerebral hemispheres. The most severe form, alobar holoprosencephaly, has a monoventricle and thalamic fusion (Fig 8). Associated facial abnormalities are common.
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Figure 8. Holoprosencephaly at 14 weeks gestation. Coronal transabdominal US image of the fetal head shows fused thalami (T), a monoventricle (M) with virtually no cerebral tissue, and absence of the interhemispheric fissure and falx. Small echogenic choroid plexuses (arrow) are seen on either side of the fused thalami.
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Dandy-Walker Complex
Dandy-Walker complex (Dandy-Walker malformation) consists of a posterior fossa cyst, partial or complete absence of the cerebellar vermis, and in some cases hydrocephalus (Fig 9). It may be associated with chromosomal abnormalities, single gene disorders, congenital infection, or exposure to teratogens. It can be isolated or associated with other abnormalities.
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Figure 9a. Dandy-Walker complex at 12 weeks gestation. (a) Axial transvaginal US image of the fetal head shows a cyst (arrow) in the posterior fossa. (b) Coronal transvaginal US image of the fetal mouth shows a bilateral cleft lip (arrows). The fetus had trisomy 13.
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Figure 9b. Dandy-Walker complex at 12 weeks gestation. (a) Axial transvaginal US image of the fetal head shows a cyst (arrow) in the posterior fossa. (b) Coronal transvaginal US image of the fetal mouth shows a bilateral cleft lip (arrows). The fetus had trisomy 13.
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Fetal Nasal Bone
Ossification of the nasal bones first appears at a crown-rump length of 42 mm, and nasal bone length increases linearly with gestation (Fig 10). A common characteristic of patients with Down syndrome is a flat face with a small nose. In a study that evaluated the association between nasal bone hypoplasia and Down syndrome at 11–14 weeks gestation, nasal ossification was absent in 73% of Down syndrome fetuses versus 0.5% of chromosomally normal fetuses (14), suggesting that nasal bone evaluation may be useful in screening for Down syndrome (Fig 11).
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Figure 11. Absent nasal bone ossification at 12 weeks gestation in a fetus with trisomy 21. Transabdominal US image of the fetal facial profile shows no ossification in the expected location of the nasal bone (NB).
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Fetal Neck and NT Screening
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Normally, a thin layer of fluid is seen in the posterior nuchal region in the first-trimester fetus. This layer is called the nuchal translucency, and its thickness can be measured with US (Fig 12).
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Figure 12. Normal NT thickness at 12 weeks gestation. Sagittal transabdominal US image of the fetus shows an NT thickness of 1.5 mm (cursors). The amnion is seen separately (arrow).
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Most fetuses with Down syndrome and some normal fetuses show an increased NT (>95th percentile) in the first trimester (Fig 13). Recently, NT measurement in conjunction with maternal age and maternal serum biochemistry has been used to assess the risk for having a baby with Down syndrome. It has been shown that measuring NT thickness between 11–14 weeks gestation and combining it with maternal age allows identification of 75% of fetuses with Down syndrome and approximately 70% of fetuses with other chromosome abnormalities (trisomy 13, trisomy 18, and Turner syndrome) with a false-positive rate of 5% (1). By using a combination of maternal age, fetal NT thickness, and maternal serum biochemistry (free ß–human chorionic gonadotropin and pregnancy-associated plasma protein-A), the detection rate for fetuses with Down syndrome is increased to 89%, with a false-positive rate of 5% (2).
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Figure 13a. Increased NT thickness at 12 weeks gestation associated with trisomy 21. (a) Sagittal transvaginal US image of a fetus with trisomy 21 shows an increased NT thickness of 8 mm (cursors). The skin is elevated along the back due to subcutaneous edema. (b) Photograph of another fetus with trisomy 21 shows a subcutaneous fluid collection at the back of the neck (arrow). (Fig 13b courtesy of Eva Pajkrt, MD, PhD, University College London Hospitals, England.)
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Figure 13b. Increased NT thickness at 12 weeks gestation associated with trisomy 21. (a) Sagittal transvaginal US image of a fetus with trisomy 21 shows an increased NT thickness of 8 mm (cursors). The skin is elevated along the back due to subcutaneous edema. (b) Photograph of another fetus with trisomy 21 shows a subcutaneous fluid collection at the back of the neck (arrow). (Fig 13b courtesy of Eva Pajkrt, MD, PhD, University College London Hospitals, England.)
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In addition, an increased NT in the presence of a normal karyotype is associated with an increased frequency of many structural abnormalities (including major cardiac defects, skeletal dysplasias, fetal akinesia, diaphragmatic hernia) as well as a variety of genetic syndromes (3,4). Therefore, an increased NT is an indication for detailed anatomic scanning of the fetus and fetal echocardiography.
During the second trimester, this fluid collection often resolves. However, in some cases it evolves into either nuchal fold thickening or cystic hygroma, with or without generalized hydrops (Fig 14).
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Figure 14a. Cystic hygroma and hydrops fetalis in a 13-week fetus with Turner syndrome. (a) Axial transabdominal US image of the fetal neck shows a hygroma with a typical midline septum (arrow). Note the normal cervical spine (S), which helps differentiate a hygroma from a meningocele. (b) Axial US image of the fetal thorax shows a right pleural effusion (arrow) and edema of the skin (arrowheads).
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Figure 14b. Cystic hygroma and hydrops fetalis in a 13-week fetus with Turner syndrome. (a) Axial transabdominal US image of the fetal neck shows a hygroma with a typical midline septum (arrow). Note the normal cervical spine (S), which helps differentiate a hygroma from a meningocele. (b) Axial US image of the fetal thorax shows a right pleural effusion (arrow) and edema of the skin (arrowheads).
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Fetal Heart
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Abnormalities of the heart and great arteries are the most common congenital defects, with a prevalence of 5–10 per 1,000 births. Fetal echocardiography can be performed in the first trimester. Using transvaginal US, Haak et al (15) found that a complete cardiac examination (four chambers, aorta, and pulmonary artery) was successfully performed in 92% of cases at 13 weeks gestation. They also reported the following findings:
1. The four-chamber view was the easiest image to obtain.
2. The frequency of successful acquisition of the four-chamber view increased with gestational age, from 85% in week 11 to 98% in week 13.
3. It was possible to visualize the pulmonary trunk earlier in gestation than the aortic root. However, this difference disappeared by 13 weeks, with a visualization rate of 95% for the aorta and 98% for the pulmonary artery.
4. The success rate for a complete cardiac examination increased from 20% in week 11 to 92% in week 13. The best time in the first trimester to perform echocardiography was at 13 weeks 0 days to 13 weeks 6 days gestation.
A wide spectrum of cardiac malformations have been diagnosed in the first trimester (16). Some of the abnormalities that we have detected include ventricular septal defect (Fig 15), ectopia cordis (Fig 16), and left atrial isomerism with complex heart disease (Fig 17). The sensitivity and accuracy of first-trimester echocardiography are limited by the small size of the fetal heart and also the later manifestation of certain structural and functional abnormalities, such as hypoplasia of one cardiac chamber and myocardial hypertrophy. Therefore, a subsequent assessment at 18–20 weeks is still warranted in pregnancies at risk for fetal cardiac disease.
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Figure 15. Ventricular septal defect at 12 weeks gestation. Transvaginal US image of the fetal thorax (four-chamber view) shows a small ventricular septal defect (arrowhead) and a small pericardial effusion (arrow). The fetus had trisomy 18, along with an increased NT thickness and an omphalocele.
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Figure 16. Ectopia cordis at 14 weeks gestation. Transvaginal US image of the fetal thorax and upper abdomen shows both ventricles and at least one of the atria protruding from the anterior chest wall. LA = left atrium, LV = left ventricle, RA = right atrium, RV = right ventricle, S = stomach.
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Figure 17a. Left atrial isomerism with complex heart disease at 14 weeks gestation. (a) Axial transabdominal US image of the fetal abdomen shows a left-sided stomach (S) and midline liver (L) with a right-sided descending aorta (Ao) and left-sided azygos vein (Az). (b) Transabdominal US image of the fetal thorax (four-chamber view) shows dextrocardia; the morphologic left ventricle (LV) is on the right side, and the morphologic right ventricle (RV) is on the left side. There is also an atrioventricular septal defect (arrow). Other views showed both great arteries arising from the morphologic right ventricle. M-mode imaging showed a 2:1 atrioventricular block. The fetus developed progressive obstruction of both outflow tracts, complete atrioventricular block, and hydrops fetalis and died in the neonatal period.
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Figure 17b. Left atrial isomerism with complex heart disease at 14 weeks gestation. (a) Axial transabdominal US image of the fetal abdomen shows a left-sided stomach (S) and midline liver (L) with a right-sided descending aorta (Ao) and left-sided azygos vein (Az). (b) Transabdominal US image of the fetal thorax (four-chamber view) shows dextrocardia; the morphologic left ventricle (LV) is on the right side, and the morphologic right ventricle (RV) is on the left side. There is also an atrioventricular septal defect (arrow). Other views showed both great arteries arising from the morphologic right ventricle. M-mode imaging showed a 2:1 atrioventricular block. The fetus developed progressive obstruction of both outflow tracts, complete atrioventricular block, and hydrops fetalis and died in the neonatal period.
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An increased NT allows identification of fetuses at high risk for cardiac defects (17,18). In a study of 45 first-trimester fetuses with an NT greater than the 95th percentile, transvaginal echocardiography had a sensitivity of 88% and specificity of 97% for detection of heart defects (19).
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Fetal Abdominal Wall
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At 8–10 weeks, there is physiologic herniation of the midgut, which is visible as an echogenic mass at the base of the umbilical cord (Fig 18). By 12 weeks, the intestine has returned to its normal position in the abdominal cavity. The diagnosis of omphalocele should not be made before 12 weeks gestation or a crown-rump length of 45 mm or less (7), unless the anterior abdominal mass is greater than 7 mm (20) or contains the liver or stomach (21). Fluid is normally visible in the stomach by 12–13 weeks (10).
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Figure 18. Physiologic herniation of the midgut at 10 weeks gestation. Transvaginal US image shows a small (4-mm-diameter) echogenic mass at the base of the umbilical cord (arrow) as it enters the fetal abdomen (A).
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Omphalocele
Prenatal US diagnosis of omphalocele is based on demonstration of a midline anterior abdominal wall defect, a herniated sac with visceral contents, and umbilical cord insertion at the apex of the sac (Fig 19). A defect in the formation of the cephalic embryonic fold results in pentalogy of Cantrell (supraumbilical defect, anterior diaphragmatic hernia, sternal cleft, ectopia cordis, and cardiac defects). A defect in the formation of the caudal fold results in omphalocele associated with exstrophy of the bladder, imperforate anus, and sacral vertebral defects (OEIS syndrome). Omphaloceles, especially those containing only intestine, are often associated with chromosomal abnormalities, most commonly trisomy 18 (21).
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Figure 19. Omphalocele at 12 weeks gestation. Axial transabdominal US image of the fetal abdomen shows a 1.7-cm-diameter mass (arrow), which has herniated through a defect in the anterior abdominal wall. It contains the liver (L) and stomach (S). The fetus had trisomy 18, as well as multiple anomalies.
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Gastroschisis
In gastroschisis, the bowel loops herniate through an abdominal wall defect located lateral and usually to the right of the umbilical cord insertion. Prenatal US diagnosis is based on demonstration of the normal position of the umbilicus and herniated bowel loops, which are freely floating in the amniotic fluid (Fig 20). Associated chromosomal abnormalities are rare.
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Figure 20a. Gastroschisis and skeletal dysplasia at 13 weeks gestation. (a) Sagittal transabdominal US image of the fetus shows free-floating bowel loops (arrow), which have herniated through a defect in the anterior abdominal wall. The NT thickness is 5 mm (cursors). (b) Axial transabdominal US image of the fetal abdomen shows the insertion of the umbilical cord (curved arrow), which is to the left of the bowel loops (straight arrow). S = stomach. (c) Transabdominal US image shows the femur, which is 7 mm long (cursors), below -4 standard deviations for gestation. All of the long bones were abnormally short. Bilateral clubfoot was also seen. These findings were confirmed at pathologic examination; the skeletal dysplasia was a form of chondrodysplasia punctata.
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Figure 20b. Gastroschisis and skeletal dysplasia at 13 weeks gestation. (a) Sagittal transabdominal US image of the fetus shows free-floating bowel loops (arrow), which have herniated through a defect in the anterior abdominal wall. The NT thickness is 5 mm (cursors). (b) Axial transabdominal US image of the fetal abdomen shows the insertion of the umbilical cord (curved arrow), which is to the left of the bowel loops (straight arrow). S = stomach. (c) Transabdominal US image shows the femur, which is 7 mm long (cursors), below -4 standard deviations for gestation. All of the long bones were abnormally short. Bilateral clubfoot was also seen. These findings were confirmed at pathologic examination; the skeletal dysplasia was a form of chondrodysplasia punctata.
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Figure 20c. Gastroschisis and skeletal dysplasia at 13 weeks gestation. (a) Sagittal transabdominal US image of the fetus shows free-floating bowel loops (arrow), which have herniated through a defect in the anterior abdominal wall. The NT thickness is 5 mm (cursors). (b) Axial transabdominal US image of the fetal abdomen shows the insertion of the umbilical cord (curved arrow), which is to the left of the bowel loops (straight arrow). S = stomach. (c) Transabdominal US image shows the femur, which is 7 mm long (cursors), below -4 standard deviations for gestation. All of the long bones were abnormally short. Bilateral clubfoot was also seen. These findings were confirmed at pathologic examination; the skeletal dysplasia was a form of chondrodysplasia punctata.
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Fetal Urinary Tract
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By 12–13 weeks gestation, when both transabdominal and transvaginal US are used, the bladder could be visualized in 98% of cases and the kidneys in 99% (10) (Fig 21). Abnormalities of the amniotic fluid volume do not usually occur before the second trimester because most of the fluid in the first trimester is formed by the yolk sac and from transmembranous exudation from the fetus and placenta. After 16 weeks, fetal urination is the major source of amniotic fluid. A normal US appearance of the kidneys in the first trimester does not exclude the diagnosis of polycystic kidney disease in a pregnancy at risk for this condition, since most cases appear only later in pregnancy. Detection of multicystic kidneys (Fig 22) and bilateral renal agenesis has been reported in the first trimester (22). Failure to visualize the fetal bladder can be due to renal abnormalities or bladder exstrophy (Fig 23).
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Figure 22a. Multicystic dysplastic kidney. (a) Sagittal transabdominal US image of a fetus at 14 weeks gestation shows several cysts (arrow) in a slightly enlarged kidney (cursors). (b) Follow-up transabdominal US image obtained at 18 weeks gestation shows multiple cysts (arrows) in the enlarged kidney (cursors).
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Figure 22b. Multicystic dysplastic kidney. (a) Sagittal transabdominal US image of a fetus at 14 weeks gestation shows several cysts (arrow) in a slightly enlarged kidney (cursors). (b) Follow-up transabdominal US image obtained at 18 weeks gestation shows multiple cysts (arrows) in the enlarged kidney (cursors).
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Figure 23a. Cloacal exstrophy at 14 weeks gestation. (a) Sagittal transabdominal US image of the fetal lower abdomen shows an irregular mass (arrows) arising from the anterior abdominal wall. The bladder is not seen. There is mild hydronephrosis (H). (b) Postmortem photograph of the fetus at 15 weeks gestation shows a defect in the anterior abdominal wall below the umbilicus (U) and an irregular mass of exposed intestine and exstrophied bladder (arrows). No intact bladder, external genitalia, or anus can be identified.
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Figure 23b. Cloacal exstrophy at 14 weeks gestation. (a) Sagittal transabdominal US image of the fetal lower abdomen shows an irregular mass (arrows) arising from the anterior abdominal wall. The bladder is not seen. There is mild hydronephrosis (H). (b) Postmortem photograph of the fetus at 15 weeks gestation shows a defect in the anterior abdominal wall below the umbilicus (U) and an irregular mass of exposed intestine and exstrophied bladder (arrows). No intact bladder, external genitalia, or anus can be identified.
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Megacystis: In a study of 300 normal fetuses at 10–14 weeks gestation, the longitudinal bladder diameter was less than or equal to 6 mm and the ratio of bladder diameter to crown-rump length was less than 10% (23). Among 145 fetuses with megacystis (longitudinal bladder diameter 
7 mm), chromosomal abnormalities were detected in 21% (24). In the chromosomally normal group, if the bladder length was greater than 15 mm, the condition was invariably associated with progressive obstructive uropathy (24). However, if the bladder length was 7–15 mm, there was spontaneous resolution of the megacystis by 20 weeks in 90% of the cases. In 10%, there was enlargement of the megacystis and/or the development of echogenic kidneys. Follow-up US is necessary to correctly interpret the significance of megacystis detected in the first trimester (Fig 24).
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Figure 24. Megacystis at 12 weeks gestation. Sagittal transabdominal US image of a male fetus shows a distended thick-walled bladder (arrow), which is 13 mm long. It did not empty during a 30-minute examination. There was no hydronephrosis. At subsequent US examinations, the bladder remained large, but it was seen to empty partially on several occasions when the observation was prolonged (up to 1 hour). Postnatal US showed a large bladder (no thickening or trabeculation) and normal kidneys. Voiding cystourethrography performed at 3 months of age showed a large bladder (which accepted 100 mL of contrast material), a diverticulum in the proximal urethra, and bilateral vesicoureteric reflux. Further follow-up is not yet available.
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Fetal Skeleton
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At transvaginal US, limb buds are first identified at 8–9 weeks gestation (25). The ossification centers of the humerus, ulna, radius, femur, tibia, and fibula can be seen at 10 weeks; the terminal phalanges of the hands can be seen at 11 weeks (25). Limb movements are readily seen by 11 weeks. From 11 weeks onward, the long bones can be measured with satisfactory accuracy (25), and reference ranges in early pregnancy have been published (26). The ratios between corresponding segments of the upper and lower limbs are close to 1, and the mean femur-to-foot ratio is 0.85 (26).
Skeletal dysplasias are a heterogeneous group of bone abnormalities resulting in abnormal growth and shape of the fetal skeleton. In lethal dysplasias, bone shortening may be obvious as early as 11 weeks (Fig 20). In addition, the disproportion between body and limbs, the lack of limb movements, and the lack of mineralization are helpful features. Many of the reported cases of skeletal defects in the first trimester were associated with an increased NT (4). Isolated limb abnormalities such as localized shortening or absence may be detected, as well as clubfoot (Fig 25) and polydactyly (Figs 5, 25).
Jarcho-Levin syndrome is a genetically heterogeneous disorder characterized by vertebral and rib abnormalities. US findings include misalignment of the spine due to hemivertebrae or fused vertebrae and misaligned ribs (Fig 26).
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Figure 26. Jarcho-Levin syndrome at 13 weeks gestation. Sagittal transabdominal US image of the fetus shows major ossification and segmentation errors of the thoracolumbar spine (arrows).
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Multiple Gestations
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In twins and higher-order gestations, accurate assignment of chorionicity and amnionicity is important during US of early pregnancy. Chorionicity is the main factor determining pregnancy outcome. In monochorionic twins, the rates of miscarriage and perinatal morbidity and mortality are much higher than in dichorionic twins. In twin pregnancies with a single placental mass at US, the presence of a triangular projection of placental tissue beyond the chorionic surface, extending between the layers of the intertwin membrane—the twin peak or lambda sign—is virtually 100% predictive of dichorionicity (27) (Fig 27). This sign is best visualized between 10 and 14 weeks and becomes progressively more difficult to identify with advancing gestation (28). In monochorionic diamniotic twins, the intertwin membrane is very thin and inserts in a "T" junction (Fig 28).
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Figure 27. Dichorionic diamniotic twins at 13 weeks gestation. Axial transabdominal US image of the uterus shows the twin peak sign (arrow). P = single placental mass due to contiguous or fused placentas.
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NT measurement is useful in multiple gestations to screen for chromosomal abnormalities because conventional screening methods (eg, maternal serum screening) are not as useful as with singletons (29). In dichorionic twins, the NT is measured in each fetus and this is combined with maternal age to calculate the risk for trisomies in each fetus. In monochorionic twins (always monozygotic), current data are insufficient to conclude whether the calculation of risk for trisomies should be based on the NT of the fetus with the larger or the smaller measurement. If both NT measurements are within the normal range or both are increased, it does not matter much in practical terms which measurement is used to calculate risk. However, an increased NT in one of the fetuses is more likely due to an increased risk of twin-twin transfusion syndrome rather than discordant risk for a chromosomal abnormality, and close monitoring should be initiated.
Conjoined Twins
Conjoined twins result from incomplete division of the embryonic disk when it attempts to split after day 12 of fertilization. Conjoined twins are classified according to the dominant site of the interfetal body part connection. There are five major types: thoracopagus (thorax), omphalopagus (abdomen), pygopagus (sacrum), ischiopagus (pelvis), and craniopagus (head). Thoracopagus, omphalopagus, and thoraco-omphalopagus (Fig 29) account for 70% of conjoined twins (30).
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Figure 29. Conjoined twins at 12 weeks gestation. Transvaginal US image shows two fetuses joined at the chest (C) and abdomen (A). A thick NT with septa (arrow) is seen in both fetuses.
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Hydatidiform Mole
Hydatidiform mole is classified as complete or partial molar pregnancy on the basis of cytogenetic, morphologic, and clinical features. Complete molar pregnancy is thought to arise as a result of abnormal fertilization (of an empty ovum). In this condition, the normal placenta is replaced by hydropic villi, which are seen at US as multiple tiny cystic spaces, giving a "snowstorm" appearance (Fig 30). In complete moles, a fetus is absent except in the rare event of a coexistent twin pregnancy. This is most likely to occur when there is fertilization of multiple ova, one of which was empty. At US, if a hydatidiform mole is seen in association with a fetus, it can be difficult to distinguish a twin complete mole–normal fetus combination from a singleton partial mole with a triploid fetus (resulting from fertilization of a normal ovum by two haploid sperm). However, identification of a separate normal placenta would help exclude a partial mole with a triploid fetus (Fig 30).
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Figure 30a. Complete hydatidiform mole with a coexistent fetus at 13 weeks gestation. (a) Axial transabdominal US image of the uterus shows a large posterior hydatidiform mole (M), a separate anterior placenta (P), and a live fetus (F). (b) Photograph of the curettage specimen shows multiple grapelike vesicles (hydropic villi) up to 9 mm in diameter (arrows). Immunostaining for p56 kiP2 indicated a dual genetic population of chorionic villi, thus confirming the diagnosis of a twin gestation: a complete hydatidiform mole and a normal fetus.
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Figure 30b. Complete hydatidiform mole with a coexistent fetus at 13 weeks gestation. (a) Axial transabdominal US image of the uterus shows a large posterior hydatidiform mole (M), a separate anterior placenta (P), and a live fetus (F). (b) Photograph of the curettage specimen shows multiple grapelike vesicles (hydropic villi) up to 9 mm in diameter (arrows). Immunostaining for p56 kiP2 indicated a dual genetic population of chorionic villi, thus confirming the diagnosis of a twin gestation: a complete hydatidiform mole and a normal fetus.
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Discussion
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Braithwaite et al (10) have shown that a complete anatomic survey is possible in 95% of fetuses at 12–13 weeks gestation, using transabdominal US in all cases and transvaginal US in 20% of cases. They used a standardized protocol similar to that shown in Table 1, which we propose for the 11–14-week fetal anatomic US examination. This protocol is the subject of an ongoing prospective study to assess its usefulness in the early diagnosis of fetal anomalies. We perform transvaginal US when visibility is poor at transabdominal US owing to maternal body habitus or persistent unfavorable fetal position. In addition, we proceed to transvaginal US when transabdominal US raises the possibility of a fetal anomaly or there is a history of an abnormality that might be detectable with early scanning.
There have been several studies of US during early pregnancy for detection of fetal anomalies in unselected populations (31–35). The reported detection rates range from 22% to 61%. US was performed at 11–14 weeks gestation in three studies (31,33,34), at 14 weeks gestation in one study (32), and at 11–15 weeks gestation in another study (35). In three studies, transvaginal US was used in all cases (31,32,35); in two studies, transvaginal US was performed only when deemed necessary (33,34). An important factor that contributed to the wide range of reported detection rates was the definition of structural abnormalities: Some studies included isolated nuchal abnormalities as structural abnormalities. The study that had the highest detection rate (61%) considered all nuchal abnormalities (nuchal edema and cystic hygroma) in the total number of structural abnormalities identified (32). The study that had the lowest detection rate (22%) did not include an isolated nuchal abnormality or an abnormal karyotype (with no associated structural abnormality) as abnormal (34).
The prevalence of congenital abnormalities varied from 1.2% to 4.6% among the studies, likely reflecting the referral population and the extent of follow-up and ascertainment of anomalies. The study with the lowest detection rate reported the highest prevalence of congenital abnormalities (4.6%) and included minor abnormalities (such as small atrial septal defect, clinodactyly, pyelectasis) in the calculation of fetal malformations that were not diagnosed at 11–14-week US (34). In the other studies, which had lower prevalences of anomalous fetuses (1.2%–2.1%), minor abnormalities were either not reported or not included (31–33,35).
By combining the results of the five studies (31–35) and excluding isolated nuchal abnormality (increased NT or cystic hygroma) as an abnormality, the detection rates for the different organ systems can be summarized as in Table 2. The overall detection rate for major fetal anomalies with early pregnancy scanning was 23%.
Additional fetal anomalies were detected at second-trimester scanning, which formed part of the protocol in four studies (31–34), and at third-trimester scanning when it was performed (31,34). Second-trimester scanning allowed detection of an additional 33.7% (93 of 276) of the fetal anomalies reported in four studies (31–34). Therefore, the 18–20-week anatomic US examination still has a major role in prenatal detection of fetal anomalies and should not be abandoned.
Early detection of fetal anomalies has advantages compared with detection at 18 weeks gestation. It allows time for the instigation of therapy, where appropriate. The couple can protect their privacy, since at this stage the pregnancy is not obvious; if they choose to terminate the pregnancy, the procedure can be performed on an outpatient basis. This is also associated with a more favorable cost-benefit ratio. The reassurance of normality in early pregnancy may be of particular advantage to those women who are at high risk of having an affected fetus.
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Conclusions
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US performed at 11–14 weeks gestation, along with NT measurement and a detailed anatomic survey, can play an important role in early diagnosis of fetal anomalies. A thorough knowledge of the US features of embryologic development is necessary to avoid potential diagnostic pitfalls. The anatomic US examination at 18–20 weeks gestation should also be performed, since a number of anomalies may not be evident at scanning during early pregnancy.
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Footnotes
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Abbreviation: NT = nuchal translucency
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References
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Abstract
LEARNING OBJECTIVES
