- Email: [email protected]
Sonography of the fetal central nervous system
Neuroimag Clin N Am 14 (2004) 255 – 271
Sonography of the fetal central nervous system Carol E. Barnewolt, MDa,b,*, Judy A. Estroff, MDa,b a
Department of Radiology, Advanced Fetal Care Center, Children’s Hospital Boston, 300 Longwood Avenue, Boston, MA 02115, USA b Harvard Medical School, 25 Shattuck Street, Boston, MA 02115, USA
This article presents a general overview of fetal sonography and an approach to the sonographic evaluation of the fetal central nervous system. Annotated images of anomalies of the fetal head, brain, spine, face, and neck are shown. Sonographic technique, including the choice of transducers and imaging windows is presented. The complementary relationship of fetal neurosonography and fetal MR imaging is covered, and the strengths and weaknesses of each modality are discussed. Fetal sonography, in clinical use for more than 30 years, has become an integral part of prenatal care in developed countries around the world. Although mandated in several European countries, the utility of routine fetal sonography has not yet been accepted in the United States. Even so, approximately 70% of American women have at least one sonogram during their pregnancy [1]. Fetal sonography can be used (1) to establish gestational age, (2) to document fetal number and lie, (3) to evaluate the uterine environment (amniotic fluid, cervical length, and placental integrity and position), and (4) to assess fetal structure and well-being [2]. Normal development of the central nervous system, which begins with closure of the neural tube between the third and fourth week of fetal development (fifth and sixth week menstrual age), continues
* Corresponding author. Department of Radiology, Advanced Fetal Care Center, Children’s Hospital Boston, 300 Longwood Avenue, Boston, MA 02115. E-mail address: [email protected] (C.E. Barnewolt).
throughout gestation and well into postnatal life [3,4]. Most routine fetal surveys are performed between 15 and 22 weeks’ gestation, before much of fetal development and maturation is complete. Maternal infection, fetal intracranial hemorrhage, stroke, or tumor may tragically devastate a previously normally developed fetal brain [5 – 15]. Some clinical syndromes, chromosomal anomalies, genetic disorders, and endocrinopathies have subtle or no detectable sonographic markers. It is, therefore, impossible to guarantee that a structural survey showing a normal fetus, performed at any time in gestation, will result in a normal newborn child [15 – 18]. Many complex brain anomalies are associated with chromosomal anomalies or syndromes. Although built into the embryonic blueprint and therefore present from conception, many of these anomalies are detected because of abnormal intracranial findings, such as ventriculomegaly, intracranial cysts, or unusual head shape or size appreciated on a routine second-trimester fetal structural survey [19 – 40]. With increased experience and use of high-resolution endovaginal sonography, some central nervous system malformations, such as holoprosencephaly, anencephaly, neural tube defects, and Dandy-Walker syndrome, are detectable in the first trimester. Many subtle findings detected on sonography, such as choroid plexus cysts (Fig. 1), echogenic intracardiac foci, and mild renal pyelectasis, are clinically insignificant but may cause the pregnant woman great anxiety. In an attempt to deal with the possibility of undetected or undetectable anomalies, as well as the angst resulting from detected but inconsequential findings, some well-known sonologists require that all obstetric patients sign an informed consent docu-
1052-5149/04/$ – see front matter D 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.nic.2004.03.010
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Fig. 1. Choroid plexus cysts (arrow) may be markers for chromosomal abnormalities. If the fetal karyotype is normal, however, they generally involute as pregnancy progresses and are thought to be of no real clinical importance.
tional windows and planes, more of the fetal brain can be visualized, including a direct coronal and midline sagittal view of the corpus callosum, cavum septum pellucidum, and vergae; coronal and parasagittal views of the frontal horns of the lateral ventricles; and axial, coronal, and midline sagittal views of the third ventricle, fourth ventricle, individual cerebellar hemispheres, and the cerebellar vermis. Additionally, the contour of the cerebral surface and assessment of the extra-axial spaces is routinely evaluated using high-frequency linear array transducers. If a central nervous system anomaly is suspected, and the fetal part of interest (cranium, face, spine) is near the cervix, transvaginal sonography may be performed. The ossified fetal spine, cartilaginous sacrum, and the spinal cord are imaged whenever possible, the position of the conus medullaris is documented, and the integrity of the overlying skin is noted. In the setting of a neural tube defect, the level and extent of spinal dysraphism is estimated in the sagittal, coronal, and axial planes of section.
Technique
ment stating their understanding of the risks and benefits of fetal sonography. Guidelines for antepartum obstetric sonographic examination [41] developed by the American Institute of Ultrasound in Medicine in collaboration with the American College of Radiology and the American College of Obstetrics and Gynecology includes evaluation of the head and neck, cerebellum, choroid plexus, cisterna magna, lateral cerebral ventricles, midline falx, and cavum septum pellucidi. These guidelines include documentation of only the most basic anatomic structures and should not be considered sufficient effort to exclude many of the common and devastating anomalies of the fetal nervous system, which affect approximately 1 in 100 live births. At Children’s’ Hospital Boston, in addition to the usual sonographic views obtained in the axial plane through the fetal temporal bone, routine additional views are obtained following guidelines for the standardized newborn neurosonogram. In each fetus, whenever possible, images are obtained in the sagittal, parasagittal, axial, and angled coronal planes through the fetal anterior fontanelle, posterior fontanelle, mastoid, and metopic sutures. With these addi-
Sonography is rapidly evolving, with frequent and spectacular advances in image resolution, acquisition, processing, storage, and presentation. State-of-the-art sonography equipment has the capacity for image presentation in two dimensions, three dimensions and four dimensions (three dimensions in motion). Sensitive color, power and spectral Doppler capability is standard. Real-time fetal sonography is performed using the highest-frequency transducer possible to visualize a given structure adequately (Fig. 2). For most fetal imaging, a 5- to 15-MHz abdominal or transvaginal probe is used with awareness of the constant trade-off of decreased spatial resolution with increased tissue penetration. For imaging heavy patients, fetuses of advanced gestational age, assessment of twins or higher multiples, and for evaluating pregnancies with increased amniotic fluid, lower-frequency transducers (2 – 3.5 MHz) may be necessary. Although the energy output for diagnostic ultrasonic imaging equipment is considered safe for both mother and fetus, a sonographic examination should be performed for clinical purposes only and should be of the minimal duration necessary. Adequate documentation followed by timely written and verbal reporting of findings is a critical part of all obstetric imaging studies.
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Fig. 2. Detailed views of the fetal brain can be obtained with ultrasound if one takes advantage of windows created by normal fontanelles. Traditional views include (A) the axial plane at the level of the midbrain to obtain the biparietal diameter and (B) an axial view of the posterior fossa to evaluate the cerebellum and cisterna magna. One can follow the lead of traditional neonatal cranial sonography and obtain (C) direct coronal and (D) sagittal views of the corpus callosum. The ventricles can be evaluated in the (E) axial, (C) coronal, and ( F) sagittal planes. ( G) A coronal view of the posterior fossa is also often useful. Endovaginal ultrasound can provide even further detail if the fetus is in an optimal position (H), as is apparent in this sagittal view of the corpus callosum.
Fig. 3. Early in gestation, this fetus had a normal cranial contour. By 37 weeks’ gestation, extreme distortion of cranial shape, in a so-called ‘‘clover leaf pattern,’’ is evidence for coronal and lambdoid craniosynostosis.
Fig. 4. Whenever an intracranial cyst is identified by fetal ultrasound, color Doppler should be used to assess for the presence of blood flow within the presumed cyst. This coronal view of the brain in a 37-week fetus reveals a midline cyst that could be elongated in the sagittal plane and contained swirling flow on color Doppler confirming the diagnosis of a Galenic malformation.
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Accurate assessment of fetal gestational age is central to the evaluation of normal fetal structural development. Gestational age assignment is most accurate when established by (1) accurate conceptual dates, as in vitro fertilization or (2) adequate sonographic imaging in the early first trimester. Once gestational age has been established based on early imaging, it should not be reassigned. Determination of gestational age is based on the embryonic crown-torump length until approximately 13 weeks, or 60 mm,
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after which time other biometric measures, such as the biparietal diameter, head circumference, femur length, and abdominal circumference, are more accurate. Biparietal diameter is measured in the axial plane at the level of the frontal horns of the lateral ventricles, cavum septum pellucidum, thalami, and third ventricle. Head size, as reflected by biparietal diameter and head circumference, is an indirect measure of brain growth. With accurate knowledge of the gestational age, fetal brain development can be assessed.
Fig. 5. The finding of ventriculomegaly is relatively common and occurs in a spectrum of severity from mild (A, 30 weeks; B, 22 weeks) to severe (C, 20 weeks). Associated findings should always be sought. (D) Ventriculomegaly with associated porencephaly (arrow) at 35 weeks’ gestation.
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Fig. 6. This 21-week fetus was found to have a moderatesized occipital encephalocele (arrow).
Although some differences in size and shape of the fetal cranium may be normal in the third trimester because of intrinsic biologic variability, differences noted in the first and second trimesters are more likely to be pathologic (Fig. 3). Accurate sonographic evaluation of the fetal central nervous system depends on the imager’s knowledge of the sonographic appearance of the normal fetal central nervous system and familiarity with the many anomalies of neurodevelopment. Although this article discusses a general approach to fetal neurosonography and presents illustrations of normal and abnormal fetal central nervous system development, detailed descriptions of individual anomalies have not been included because many entities are discussed in other articles in this issue. The reader is referred to several excellent embryology, obstetric, pediatric, and fetal imaging texts for further study [42 – 49].
a MCA Doppler waveform showing vascular redistribution, with an increase in arterial blood flow to the brain during diastole. This redistribution may reflect so-called ‘‘brain-sparing’’ in the setting of fetal hypoxia [50]. The normal umbilical artery waveform demonstrates low-resistance arterial flow. In the compromised fetus, end-diastolic arterial flow may be diminished or reversed, the opposite pattern of flow in the MCA [51]. Color flow imaging is useful in evaluation of the fetal brain in the diagnosis of fetal vascular anomalies such as Galenic malformations (Fig. 4) and dural fistulas [52 – 55]. Sonographic evaluation of fetal behavior has been codified in the form of the biophysical profile in an effort to confirm fetal well-being. Insofar as fetal behavior reflects a normally functioning neuro-axis, a reassuring biophysical profile suggests but does not guarantee a normal fetal brain and brainstem. The components of the standard biophysical profile include fetal breathing movements, fetal body movements, fetal tone, amniotic fluid volume, and fetal reactivity [56,57]. Sonographic windows for evaluation of the fetal brain include the normal, relatively thin temporal bone, and various unfused sutures and open fontanelles, which are used in the neonate. Small footprint high frequency, probes allow the imager to use axial,
Sonography in the assessment of fetal well being Fetal cranial pulse-wave and color Doppler The normal waveform of the middle cerebral artery (MCA) demonstrates a high-resistance pattern with little flow in diastole. Fetuses at risk for intrauterine growth restriction or fetal compromise may have abnormal intracranial Doppler findings, reflected by
Fig. 7. Only amorphous tissue is seen superior to the level of the orbits (arrow) in this coronal view of the head in a 19-week fetus with anencephaly.
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Fig. 8. In absence of the corpus callosum, the classic configuration of (A) parallel lateral ventricles in the axial plane and (B) a socalled ‘‘steer-horn contour’’ of the frontal horns in the coronal plane (arrow) has been described. (C) It is also common to see an interhemispheric cyst above the third ventricle (38 weeks). (D) The potential associated finding of a callosal-region lipoma is seen as an ill-defined echogenic structure (arrow) on ultrasound (31weeks) but can be nearly invisible (E) using conventional fetal MR imaging techniques (31 weeks).
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Fig. 8 (continued).
sagittal, and coronal views to evaluate the fetal brain fully. When possible, sonographic views similar to those in newborn neurosonography are obtained. Recent advances in three-dimensional sonography have automated the process of multiplanar fetal brain imaging and may improve the accuracy of detection of fetal brain anomalies. Advances in technology, however, cannot substitute for the imager’s knowledge of normal and abnormal central nervous system development and anatomy (Figs. 5 – 7). Many studies have shown fetal MR imaging to be invaluable in the characterization of many fetal central nervous system anomalies, which are usually detected at fetal sonography performed for various clinical reasons [58,59]. Because of limited access and increased expense, fetal MR imaging is currently and will probably remain impractical for routine fetal assessment [60 – 62]. In certain situations fetal neurosonography provides more information than fetal MR neuroimaging, and vice versa. Sonography is better able to document and evaluate fetal viability, well-being, and early normal development of the central nervous system [63], to detect the corpus callosum in the early second trimester (Fig. 8), to detect develop-
ment and closure of the cerebellar vermis (Fig. 9) [64], to detect intracranial calcifications (Fig. 10) and cysts [36,65,66], and to detect the location of the spinal cord conus medullaris and the vertebral body level of an open neural tube defect (Figs. 11 – 16) [60,67 – 73]. Because of tradeoffs in signal-tonoise in MR imaging, thicker planes of sections are necessary in MR imaging, a requirement that limits spatial resolution. Sonography is often better able to determine differences in tissue characteristics such as the complex cystic and solid components of oropharyngeal or sacral teratomas (Figs. 17,18) [70,74,75]. Ultrasound has been the traditional method by which cleft lip and palate have been evaluated (Figs. 19,20), but MR imaging may have a future role. MR imaging is superior to ultrasound in demonstrating blood products (Fig. 21), cerebral cortical surface ultrastructure such as polymicrogyria or lissencephaly (Fig. 22), ventricle shape, and extra-axial fluid collections. In late gestation, when the fetal cranium is well ossified, MR imaging is not hindered by reverberation artifact from bone, as is sonography [58,76 – 78]. When possible, given their complementary nature, fetal sonography and fetal MR imaging should be performed by imagers who understand what each modality has previously shown, or has the promise to show, and the significance of the information. When maternal screening or imaging has identified a fetal anomaly, consultation with an experienced clinical geneticist is valuable and is routine at Children’s Hospital Boston. Geneticists specializing in dysmorphology are often able to guide the patient’s caregivers toward a unifying diagnosis and to determine whether the observed anomaly is chromosomal, syndromic, or results from environmental factors, such as teratogen exposure. Once a presumptive diagnosis has been made, the patient can be counseled regarding possible outcomes for the pregnancy and the risk for recurrence in future pregnancies. With deciphering of the human genome, preimplantation genetic counseling, screening, and diagnosis have become increasingly important. Future directions in fetal sonography will probably involve continued rapid and dramatic improvements in three-dimensional and four-dimensional imaging, in color Doppler imaging, in image resolution with ultra – high-frequency transducers, and in the speed of imaging data transfer and manipulation. These advances in technology may lead to opportunities for significant improvements in the accuracy of fetal diagnosis and treatment, resulting in improved parental counseling and neonatal outcomes.
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Fig. 9. The Dandy-Walker malformation consists of an enlarged posterior fossa, absence or deficiency of the cerebellar vermis, and direct continuity between the fourth ventricle and the cisterna madre as is revealed in these (A) axial and (B) sagittal views of the posterior fossa in this 24-week fetus. This presentation is to be distinguished from (C) the Dandy-Walker variant in which the inferior most vermis is deficient, but the posterior fossa is not enlarged (20 weeks).
Fig. 10. Thalamic vessel mineralization (arrow) is seen in this coronal view of a 38-week fetus. The finding is often subtle.
Fig. 11. The so-called ‘‘lemon and banana’’ signs are shown in this 18-week fetus with an open neural tube defect. The lemon sign indicates the narrowed interfrontal distance (arrow), and the banana sign indicates the flattened and inferiorly displaced cerebellar hemispheres (arrowhead) that are contained within the abnormally small posterior fossa, the Chiari II malformation.
Fig. 12. (A) The axial plane reveals the open lumbar posterior elements in a 19-week fetus with a lumbosacral myelomeningocele. (B) In another fetus, the sagittal plane shows the protuberant membranes and neural elements of a similar lesion (arrow). (C) The coronal plane reveals the low neural placode (arrow).
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Fig. 13. This 30-week fetus has a skin-covered thoracic meningocele (arrowhead) and a normal posterior fossa. The underlying thoracic cord (arrow) appears intact.
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Fig. 14. The presence of clubbed feet (arrow), although a common isolated finding, can be evidence for abnormal innervation of the lower extremities, as is frequent in the setting of an open neural tube defect. This 22-week fetus had a large myelomeningocele.
Fig. 15. The spine of this twin at 20 weeks’ gestation is abnormally truncated (arrow), and the lower vertebrae have a jumbled appearance. The diagnosis of caudal regression was made. The mother had poorly controlled gestational diabetes.
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Fig. 16. Fetal ultrasound is generally superior to MR imaging when evaluating the nature of vertebral anomalies. (A) This 20-week fetus has a complex kyphoscoliosis. Individual vertebrae are visible by ultrasound but can be difficult to resolve with current MR imaging techniques. The precise position of the tip of the conus medullaris, likewise, is often difficult to see with MR imaging but can be seen, with ideal scanning conditions, by ultrasound. (B) This spinal cord is tethered, with its tip at the upper sacral level (arrow). (C) In the normal fetal spine, seen at 33 weeks, the tip of the conus medullaris is normally positioned at the L1 – L2 level (arrow).
Fig. 17. This complex neck mass, containing cystic and solid regions, is typical of a cervical teratoma (arrow). At 34 weeks’ gestation, polyhydramnios had developed, and the mass could be seen to compress the airway. An ex utero intrapartum treatment was performed, and the infant did well.
Fig. 18. Sacrococcygeal teratomas can be primarily cystic or solid. This coronal view of a 26-week fetus reveals a large, exophytic, primarily cystic mass protruding from the coccygeal region, with little internal extension. These lesions are fragile and can bleed profusely at delivery with minor injuries.
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Fig. 19. (A) The normal fetal lip in this 24-week fetus is viewed in an oblique coronal plane so that the nose (arrowhead), vermillion border of the upper lip (arrow), lower lip, and chin are generally seen together. (B) Cleft lip is seen as a defect in the upper lip as in this 32-week fetus with unilateral complete cleft lip.
Fig. 20. (A) The normal fetal palate in this 22-week fetus can be seen as an arch of echogenic bone without any breaks in continuity. (B) In optimal settings, ultrasound can reveal the presence of a cleft palate (arrow) by a gap and often a misregistration in alignment of the alveolar ridge. This 19-week fetus had unilateral complete cleft lip and palate. It is difficult to view the secondary palate with ultrasound.
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Fig. 21. This 25-week fetus developed intracranial hemorrhage because of extreme thrombocytopenia related to maternal antiplatelet antibodies. This finding can be seen (A) as echogenic hemorrhage within the down-side lateral ventricle on ultrasound (arrow) and (B) as low signal intensity on single-shot fast spin echo T2 MR imaging sequences within both lateral ventricles.
Fig. 22. Fetal ultrasound is less reliable than MR imaging for evaluation of the extracerebral spaces and cerebral cortex. (A) This 29-week fetus was found to have abnormally large extracerebral spaces and a cortical contour suggestive of polymicrogyria by MR imaging. (B) Neither finding was appreciated prospectively by ultrasound.
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with three-dimensional color power angiography. Ultrasound Obstet Gynecol 2000;15:337 – 40. Manning FA, Platt LD, Sipos L. Antepartum fetal evaluation: development of a fetal biophysical profile. Am J Obstet Gynecol 1980;136:787 – 95. Vintzileos AM, Campbell WA, Ingardia CJ, et al. The fetal biophysical profile and its predictive value. Obstet Gynecol 1983;62:271 – 8. Malinger G, Lev D, Lerman-Sagie T. Is fetal magnetic resonance imaging superior to neurosonography for detection of brain anomalies? Ultrasound Obstet Gynecol 2002;20:317 – 21. Raybaud C, Levrier O, Brunel H, et al. MR imaging of fetal brain malformations. Childs Nerv Syst 2003;19: 455 – 70. Blaicher W, Prayer D, Bernaschek G. Magnetic resonance imaging and ultrasound in the assessment of the fetal central nervous system. J Perinat Med 2003;31: 459 – 68. Breysem L, Bosmans H, Dymarkowski S, et al. The value of fast MR imaging as an adjunct to ultrasound in prenatal diagnosis. Eur Radiol 2003;13:1538 – 48. Reichel TF, Ramus RM, Caire JT, et al. Fetal central nervous system biometry on MR imaging. AJR Am J Roentgenol 2003;180:1155 – 8. Aubry MC, Aubry JP, Dommergues M. Sonographic prenatal diagnosis of central nervous system abnormalities. Childs Nerv Syst 2003;19:391 – 402. Pilu G, Visentin A, Valeri B. The Dandy-Walker complex and fetal sonography. Ultrasound Obstet Gynecol 2000;16:115 – 7. Bernard JP, Moscoso G, Renier D, et al. Cystic malformations of the posterior fossa. Prenat Diagn 2001; 21:1064 – 9. Pierre-Kahn A, Sonigo P. Malformative intracranial cysts: diagnosis and outcome. Childs Nerv Syst 2003; 19:477 – 83. Aaronson OS, Hernanz-Schulman M, Bruner JP, et al. Myelomeningocele: prenatal evaluation—comparison between transabdominal US and MR imaging. Radiology 2003;227:839 – 43. Guo WY, Wong TT. Screening of fetal CNS anomalies by MR imaging. Childs Nerv Syst 2003;19:410 – 4. Hubbard AM. Ultrafast fetal MRI and prenatal diagnosis. Semin Pediatr Surg 2003;12:143 – 53. Hubbard AM, Simon EM. Fetal imaging. Magn Reson Imaging Clin N Am 2002;10:389 – 408. Levine D. MR imaging of fetal central nervous system abnormalities. Brain Cogn 2002;50:432 – 48. Levine D, Barnes PD, Madsen JR, et al. Fetal central nervous system anomalies: MR imaging augments sonographic diagnosis. Radiology 1997;204:635 – 42. Levine D, Smith AS, McKenzie C. Tips and tricks of fetal MR imaging. Radiol Clin North Am 2003;41: 729 – 45. Graf JL, Albanese CT. Fetal sacrococcygeal teratoma. World J Surg 2003;27:84 – 6. Chen CP, Shih JC, Huang JK, et al. Second-trimester evaluation of fetal sacrococcygeal teratoma using three-
C.E. Barnewolt, J.A. Estroff / Neuroimag Clin N Am 14 (2004) 255–271 dimensional color Doppler ultrasound and magnetic resonance imaging. Prenat Diagn 2003;23:602 – 3. [76] Abe S, Takagi K, Yamamoto T, et al. Assessment of cortical gyrus and sulcus formation using MR images in normal fetuses. Prenat Diagn 2003;23:225 – 31. [77] Twickler DM, Magee KP, Caire J, et al. Second-opinion magnetic resonance imaging for suspected fetal
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Sonography of the fetal central nervous system Carol E. Barnewolt, MDa,b,*, Judy A. Estroff, MDa,b a
Department of Radiology, Advanced Fetal Care Center, Children’s Hospital Boston, 300 Longwood Avenue, Boston, MA 02115, USA b Harvard Medical School, 25 Shattuck Street, Boston, MA 02115, USA
This article presents a general overview of fetal sonography and an approach to the sonographic evaluation of the fetal central nervous system. Annotated images of anomalies of the fetal head, brain, spine, face, and neck are shown. Sonographic technique, including the choice of transducers and imaging windows is presented. The complementary relationship of fetal neurosonography and fetal MR imaging is covered, and the strengths and weaknesses of each modality are discussed. Fetal sonography, in clinical use for more than 30 years, has become an integral part of prenatal care in developed countries around the world. Although mandated in several European countries, the utility of routine fetal sonography has not yet been accepted in the United States. Even so, approximately 70% of American women have at least one sonogram during their pregnancy [1]. Fetal sonography can be used (1) to establish gestational age, (2) to document fetal number and lie, (3) to evaluate the uterine environment (amniotic fluid, cervical length, and placental integrity and position), and (4) to assess fetal structure and well-being [2]. Normal development of the central nervous system, which begins with closure of the neural tube between the third and fourth week of fetal development (fifth and sixth week menstrual age), continues
* Corresponding author. Department of Radiology, Advanced Fetal Care Center, Children’s Hospital Boston, 300 Longwood Avenue, Boston, MA 02115. E-mail address: [email protected] (C.E. Barnewolt).
throughout gestation and well into postnatal life [3,4]. Most routine fetal surveys are performed between 15 and 22 weeks’ gestation, before much of fetal development and maturation is complete. Maternal infection, fetal intracranial hemorrhage, stroke, or tumor may tragically devastate a previously normally developed fetal brain [5 – 15]. Some clinical syndromes, chromosomal anomalies, genetic disorders, and endocrinopathies have subtle or no detectable sonographic markers. It is, therefore, impossible to guarantee that a structural survey showing a normal fetus, performed at any time in gestation, will result in a normal newborn child [15 – 18]. Many complex brain anomalies are associated with chromosomal anomalies or syndromes. Although built into the embryonic blueprint and therefore present from conception, many of these anomalies are detected because of abnormal intracranial findings, such as ventriculomegaly, intracranial cysts, or unusual head shape or size appreciated on a routine second-trimester fetal structural survey [19 – 40]. With increased experience and use of high-resolution endovaginal sonography, some central nervous system malformations, such as holoprosencephaly, anencephaly, neural tube defects, and Dandy-Walker syndrome, are detectable in the first trimester. Many subtle findings detected on sonography, such as choroid plexus cysts (Fig. 1), echogenic intracardiac foci, and mild renal pyelectasis, are clinically insignificant but may cause the pregnant woman great anxiety. In an attempt to deal with the possibility of undetected or undetectable anomalies, as well as the angst resulting from detected but inconsequential findings, some well-known sonologists require that all obstetric patients sign an informed consent docu-
1052-5149/04/$ – see front matter D 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.nic.2004.03.010
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Fig. 1. Choroid plexus cysts (arrow) may be markers for chromosomal abnormalities. If the fetal karyotype is normal, however, they generally involute as pregnancy progresses and are thought to be of no real clinical importance.
tional windows and planes, more of the fetal brain can be visualized, including a direct coronal and midline sagittal view of the corpus callosum, cavum septum pellucidum, and vergae; coronal and parasagittal views of the frontal horns of the lateral ventricles; and axial, coronal, and midline sagittal views of the third ventricle, fourth ventricle, individual cerebellar hemispheres, and the cerebellar vermis. Additionally, the contour of the cerebral surface and assessment of the extra-axial spaces is routinely evaluated using high-frequency linear array transducers. If a central nervous system anomaly is suspected, and the fetal part of interest (cranium, face, spine) is near the cervix, transvaginal sonography may be performed. The ossified fetal spine, cartilaginous sacrum, and the spinal cord are imaged whenever possible, the position of the conus medullaris is documented, and the integrity of the overlying skin is noted. In the setting of a neural tube defect, the level and extent of spinal dysraphism is estimated in the sagittal, coronal, and axial planes of section.
Technique
ment stating their understanding of the risks and benefits of fetal sonography. Guidelines for antepartum obstetric sonographic examination [41] developed by the American Institute of Ultrasound in Medicine in collaboration with the American College of Radiology and the American College of Obstetrics and Gynecology includes evaluation of the head and neck, cerebellum, choroid plexus, cisterna magna, lateral cerebral ventricles, midline falx, and cavum septum pellucidi. These guidelines include documentation of only the most basic anatomic structures and should not be considered sufficient effort to exclude many of the common and devastating anomalies of the fetal nervous system, which affect approximately 1 in 100 live births. At Children’s’ Hospital Boston, in addition to the usual sonographic views obtained in the axial plane through the fetal temporal bone, routine additional views are obtained following guidelines for the standardized newborn neurosonogram. In each fetus, whenever possible, images are obtained in the sagittal, parasagittal, axial, and angled coronal planes through the fetal anterior fontanelle, posterior fontanelle, mastoid, and metopic sutures. With these addi-
Sonography is rapidly evolving, with frequent and spectacular advances in image resolution, acquisition, processing, storage, and presentation. State-of-the-art sonography equipment has the capacity for image presentation in two dimensions, three dimensions and four dimensions (three dimensions in motion). Sensitive color, power and spectral Doppler capability is standard. Real-time fetal sonography is performed using the highest-frequency transducer possible to visualize a given structure adequately (Fig. 2). For most fetal imaging, a 5- to 15-MHz abdominal or transvaginal probe is used with awareness of the constant trade-off of decreased spatial resolution with increased tissue penetration. For imaging heavy patients, fetuses of advanced gestational age, assessment of twins or higher multiples, and for evaluating pregnancies with increased amniotic fluid, lower-frequency transducers (2 – 3.5 MHz) may be necessary. Although the energy output for diagnostic ultrasonic imaging equipment is considered safe for both mother and fetus, a sonographic examination should be performed for clinical purposes only and should be of the minimal duration necessary. Adequate documentation followed by timely written and verbal reporting of findings is a critical part of all obstetric imaging studies.
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Fig. 2. Detailed views of the fetal brain can be obtained with ultrasound if one takes advantage of windows created by normal fontanelles. Traditional views include (A) the axial plane at the level of the midbrain to obtain the biparietal diameter and (B) an axial view of the posterior fossa to evaluate the cerebellum and cisterna magna. One can follow the lead of traditional neonatal cranial sonography and obtain (C) direct coronal and (D) sagittal views of the corpus callosum. The ventricles can be evaluated in the (E) axial, (C) coronal, and ( F) sagittal planes. ( G) A coronal view of the posterior fossa is also often useful. Endovaginal ultrasound can provide even further detail if the fetus is in an optimal position (H), as is apparent in this sagittal view of the corpus callosum.
Fig. 3. Early in gestation, this fetus had a normal cranial contour. By 37 weeks’ gestation, extreme distortion of cranial shape, in a so-called ‘‘clover leaf pattern,’’ is evidence for coronal and lambdoid craniosynostosis.
Fig. 4. Whenever an intracranial cyst is identified by fetal ultrasound, color Doppler should be used to assess for the presence of blood flow within the presumed cyst. This coronal view of the brain in a 37-week fetus reveals a midline cyst that could be elongated in the sagittal plane and contained swirling flow on color Doppler confirming the diagnosis of a Galenic malformation.
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Accurate assessment of fetal gestational age is central to the evaluation of normal fetal structural development. Gestational age assignment is most accurate when established by (1) accurate conceptual dates, as in vitro fertilization or (2) adequate sonographic imaging in the early first trimester. Once gestational age has been established based on early imaging, it should not be reassigned. Determination of gestational age is based on the embryonic crown-torump length until approximately 13 weeks, or 60 mm,
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after which time other biometric measures, such as the biparietal diameter, head circumference, femur length, and abdominal circumference, are more accurate. Biparietal diameter is measured in the axial plane at the level of the frontal horns of the lateral ventricles, cavum septum pellucidum, thalami, and third ventricle. Head size, as reflected by biparietal diameter and head circumference, is an indirect measure of brain growth. With accurate knowledge of the gestational age, fetal brain development can be assessed.
Fig. 5. The finding of ventriculomegaly is relatively common and occurs in a spectrum of severity from mild (A, 30 weeks; B, 22 weeks) to severe (C, 20 weeks). Associated findings should always be sought. (D) Ventriculomegaly with associated porencephaly (arrow) at 35 weeks’ gestation.
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Fig. 6. This 21-week fetus was found to have a moderatesized occipital encephalocele (arrow).
Although some differences in size and shape of the fetal cranium may be normal in the third trimester because of intrinsic biologic variability, differences noted in the first and second trimesters are more likely to be pathologic (Fig. 3). Accurate sonographic evaluation of the fetal central nervous system depends on the imager’s knowledge of the sonographic appearance of the normal fetal central nervous system and familiarity with the many anomalies of neurodevelopment. Although this article discusses a general approach to fetal neurosonography and presents illustrations of normal and abnormal fetal central nervous system development, detailed descriptions of individual anomalies have not been included because many entities are discussed in other articles in this issue. The reader is referred to several excellent embryology, obstetric, pediatric, and fetal imaging texts for further study [42 – 49].
a MCA Doppler waveform showing vascular redistribution, with an increase in arterial blood flow to the brain during diastole. This redistribution may reflect so-called ‘‘brain-sparing’’ in the setting of fetal hypoxia [50]. The normal umbilical artery waveform demonstrates low-resistance arterial flow. In the compromised fetus, end-diastolic arterial flow may be diminished or reversed, the opposite pattern of flow in the MCA [51]. Color flow imaging is useful in evaluation of the fetal brain in the diagnosis of fetal vascular anomalies such as Galenic malformations (Fig. 4) and dural fistulas [52 – 55]. Sonographic evaluation of fetal behavior has been codified in the form of the biophysical profile in an effort to confirm fetal well-being. Insofar as fetal behavior reflects a normally functioning neuro-axis, a reassuring biophysical profile suggests but does not guarantee a normal fetal brain and brainstem. The components of the standard biophysical profile include fetal breathing movements, fetal body movements, fetal tone, amniotic fluid volume, and fetal reactivity [56,57]. Sonographic windows for evaluation of the fetal brain include the normal, relatively thin temporal bone, and various unfused sutures and open fontanelles, which are used in the neonate. Small footprint high frequency, probes allow the imager to use axial,
Sonography in the assessment of fetal well being Fetal cranial pulse-wave and color Doppler The normal waveform of the middle cerebral artery (MCA) demonstrates a high-resistance pattern with little flow in diastole. Fetuses at risk for intrauterine growth restriction or fetal compromise may have abnormal intracranial Doppler findings, reflected by
Fig. 7. Only amorphous tissue is seen superior to the level of the orbits (arrow) in this coronal view of the head in a 19-week fetus with anencephaly.
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Fig. 8. In absence of the corpus callosum, the classic configuration of (A) parallel lateral ventricles in the axial plane and (B) a socalled ‘‘steer-horn contour’’ of the frontal horns in the coronal plane (arrow) has been described. (C) It is also common to see an interhemispheric cyst above the third ventricle (38 weeks). (D) The potential associated finding of a callosal-region lipoma is seen as an ill-defined echogenic structure (arrow) on ultrasound (31weeks) but can be nearly invisible (E) using conventional fetal MR imaging techniques (31 weeks).
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Fig. 8 (continued).
sagittal, and coronal views to evaluate the fetal brain fully. When possible, sonographic views similar to those in newborn neurosonography are obtained. Recent advances in three-dimensional sonography have automated the process of multiplanar fetal brain imaging and may improve the accuracy of detection of fetal brain anomalies. Advances in technology, however, cannot substitute for the imager’s knowledge of normal and abnormal central nervous system development and anatomy (Figs. 5 – 7). Many studies have shown fetal MR imaging to be invaluable in the characterization of many fetal central nervous system anomalies, which are usually detected at fetal sonography performed for various clinical reasons [58,59]. Because of limited access and increased expense, fetal MR imaging is currently and will probably remain impractical for routine fetal assessment [60 – 62]. In certain situations fetal neurosonography provides more information than fetal MR neuroimaging, and vice versa. Sonography is better able to document and evaluate fetal viability, well-being, and early normal development of the central nervous system [63], to detect the corpus callosum in the early second trimester (Fig. 8), to detect develop-
ment and closure of the cerebellar vermis (Fig. 9) [64], to detect intracranial calcifications (Fig. 10) and cysts [36,65,66], and to detect the location of the spinal cord conus medullaris and the vertebral body level of an open neural tube defect (Figs. 11 – 16) [60,67 – 73]. Because of tradeoffs in signal-tonoise in MR imaging, thicker planes of sections are necessary in MR imaging, a requirement that limits spatial resolution. Sonography is often better able to determine differences in tissue characteristics such as the complex cystic and solid components of oropharyngeal or sacral teratomas (Figs. 17,18) [70,74,75]. Ultrasound has been the traditional method by which cleft lip and palate have been evaluated (Figs. 19,20), but MR imaging may have a future role. MR imaging is superior to ultrasound in demonstrating blood products (Fig. 21), cerebral cortical surface ultrastructure such as polymicrogyria or lissencephaly (Fig. 22), ventricle shape, and extra-axial fluid collections. In late gestation, when the fetal cranium is well ossified, MR imaging is not hindered by reverberation artifact from bone, as is sonography [58,76 – 78]. When possible, given their complementary nature, fetal sonography and fetal MR imaging should be performed by imagers who understand what each modality has previously shown, or has the promise to show, and the significance of the information. When maternal screening or imaging has identified a fetal anomaly, consultation with an experienced clinical geneticist is valuable and is routine at Children’s Hospital Boston. Geneticists specializing in dysmorphology are often able to guide the patient’s caregivers toward a unifying diagnosis and to determine whether the observed anomaly is chromosomal, syndromic, or results from environmental factors, such as teratogen exposure. Once a presumptive diagnosis has been made, the patient can be counseled regarding possible outcomes for the pregnancy and the risk for recurrence in future pregnancies. With deciphering of the human genome, preimplantation genetic counseling, screening, and diagnosis have become increasingly important. Future directions in fetal sonography will probably involve continued rapid and dramatic improvements in three-dimensional and four-dimensional imaging, in color Doppler imaging, in image resolution with ultra – high-frequency transducers, and in the speed of imaging data transfer and manipulation. These advances in technology may lead to opportunities for significant improvements in the accuracy of fetal diagnosis and treatment, resulting in improved parental counseling and neonatal outcomes.
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Fig. 9. The Dandy-Walker malformation consists of an enlarged posterior fossa, absence or deficiency of the cerebellar vermis, and direct continuity between the fourth ventricle and the cisterna madre as is revealed in these (A) axial and (B) sagittal views of the posterior fossa in this 24-week fetus. This presentation is to be distinguished from (C) the Dandy-Walker variant in which the inferior most vermis is deficient, but the posterior fossa is not enlarged (20 weeks).
Fig. 10. Thalamic vessel mineralization (arrow) is seen in this coronal view of a 38-week fetus. The finding is often subtle.
Fig. 11. The so-called ‘‘lemon and banana’’ signs are shown in this 18-week fetus with an open neural tube defect. The lemon sign indicates the narrowed interfrontal distance (arrow), and the banana sign indicates the flattened and inferiorly displaced cerebellar hemispheres (arrowhead) that are contained within the abnormally small posterior fossa, the Chiari II malformation.
Fig. 12. (A) The axial plane reveals the open lumbar posterior elements in a 19-week fetus with a lumbosacral myelomeningocele. (B) In another fetus, the sagittal plane shows the protuberant membranes and neural elements of a similar lesion (arrow). (C) The coronal plane reveals the low neural placode (arrow).
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Fig. 13. This 30-week fetus has a skin-covered thoracic meningocele (arrowhead) and a normal posterior fossa. The underlying thoracic cord (arrow) appears intact.
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Fig. 14. The presence of clubbed feet (arrow), although a common isolated finding, can be evidence for abnormal innervation of the lower extremities, as is frequent in the setting of an open neural tube defect. This 22-week fetus had a large myelomeningocele.
Fig. 15. The spine of this twin at 20 weeks’ gestation is abnormally truncated (arrow), and the lower vertebrae have a jumbled appearance. The diagnosis of caudal regression was made. The mother had poorly controlled gestational diabetes.
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Fig. 16. Fetal ultrasound is generally superior to MR imaging when evaluating the nature of vertebral anomalies. (A) This 20-week fetus has a complex kyphoscoliosis. Individual vertebrae are visible by ultrasound but can be difficult to resolve with current MR imaging techniques. The precise position of the tip of the conus medullaris, likewise, is often difficult to see with MR imaging but can be seen, with ideal scanning conditions, by ultrasound. (B) This spinal cord is tethered, with its tip at the upper sacral level (arrow). (C) In the normal fetal spine, seen at 33 weeks, the tip of the conus medullaris is normally positioned at the L1 – L2 level (arrow).
Fig. 17. This complex neck mass, containing cystic and solid regions, is typical of a cervical teratoma (arrow). At 34 weeks’ gestation, polyhydramnios had developed, and the mass could be seen to compress the airway. An ex utero intrapartum treatment was performed, and the infant did well.
Fig. 18. Sacrococcygeal teratomas can be primarily cystic or solid. This coronal view of a 26-week fetus reveals a large, exophytic, primarily cystic mass protruding from the coccygeal region, with little internal extension. These lesions are fragile and can bleed profusely at delivery with minor injuries.
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Fig. 19. (A) The normal fetal lip in this 24-week fetus is viewed in an oblique coronal plane so that the nose (arrowhead), vermillion border of the upper lip (arrow), lower lip, and chin are generally seen together. (B) Cleft lip is seen as a defect in the upper lip as in this 32-week fetus with unilateral complete cleft lip.
Fig. 20. (A) The normal fetal palate in this 22-week fetus can be seen as an arch of echogenic bone without any breaks in continuity. (B) In optimal settings, ultrasound can reveal the presence of a cleft palate (arrow) by a gap and often a misregistration in alignment of the alveolar ridge. This 19-week fetus had unilateral complete cleft lip and palate. It is difficult to view the secondary palate with ultrasound.
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Fig. 21. This 25-week fetus developed intracranial hemorrhage because of extreme thrombocytopenia related to maternal antiplatelet antibodies. This finding can be seen (A) as echogenic hemorrhage within the down-side lateral ventricle on ultrasound (arrow) and (B) as low signal intensity on single-shot fast spin echo T2 MR imaging sequences within both lateral ventricles.
Fig. 22. Fetal ultrasound is less reliable than MR imaging for evaluation of the extracerebral spaces and cerebral cortex. (A) This 29-week fetus was found to have abnormally large extracerebral spaces and a cortical contour suggestive of polymicrogyria by MR imaging. (B) Neither finding was appreciated prospectively by ultrasound.
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