ORIGINAL RESEARCH CME ARTICLE

Diagnostic Evaluation of the Fetal Face Using 3-Dimensional Ultrasound Gladys A. Ramos, MD,* Marissa V. Ylagan, MD,* Lorene E. Romine, MD,Þ Deborah A. D’Agostini, RDMS,* and Dolores H. Pretorius, MD, FACRÞ Abstract: Evaluation of the fetal face with 3-dimensional ultrasound allows for evaluation of the fetal face using surface rendering, multiplanar and multislice displays. Three-dimensional ultrasound offers many benefits in evaluating the fetal face because it can be rotated into a standard symmetrical orientation and reviewed millimeters by millimeters by scrolling through the volumes. New rendering tools now allow imaging of the hard palate. Clinical applications where 3-dimensional ultrasound adds value as an adjunct to 2-dimensional ultrasound imaging that are reviewed in this paper include cleft lip and palate, micrognathia and other profile abnormalities, metopic suture abnormalities, presence and absence of the nasal bones, orbit abnormalities, and ear abnormalities. In addition, the literature regarding parental bonding to the fetus after viewing 3-dimensional images of their fetuses is reviewed. Key Words: fetal face, 3-dimensional ultrasound, fetus, cleft lip, face (Ultrasound Quarterly 2008;24:215Y223)

LEARNING OBJECTIVES 1. Demonstrate how to display a fetal face with 3-dimensional ultrasound. 2. Describe clinical applications where 3-dimensional imaging is a useful adjunct to 2-dimensional ultrasound. 3. Identify the literature regarding parental bonding and 3-dimensional images of the fetus. Received for publication May 21, 2008; accepted September 7, 2008. *Clinical Fellow (Ramos and Ylagan), Ultrasound Technician (D’Agostini), Department of Reproductive Medicine, and †Associate Clinical Professor of Radiology (Romine), Professor of Radiology (Pretorius), Department of Radiology, University of CaliforniaYSan Diego, San Diego, CA. Dr Pretorius has disclosed that he received grant/research from General Electric Healthcare and Philips Medical Systems and is a consultant/ advisor for Philips Medical Systems. The remaining authors have disclosed that they have no interests in or significant relationships with any commercial companies pertaining to this educational activity. All staff members in a position to control the content of this CME activity have disclosed that they have no financial relationships with, or financial interests in, any commercial companies pertaining to this educational activity. Lippincott CME Institute, Inc, has identified and resolved all faculty and staff conflicts of interest regarding this educational activity. Reprints: Dolores H. Pretorius, MD, FACR, Department of Radiology, University of CaliforniaYSan Diego, 9300 Campus Point Drive, San Diego, CA 7756 (e-mail: [email protected]). Copyright * 2008 by Lippincott Williams & Wilkins

Ultrasound Quarterly

E

valuation of the fetal face with 3-dimensional (3D) ultrasound allows the patient and physician to see the forehead, eyes, nose, lips, and chin in a single frontal rendered image (Fig. 1) that is easy to recognize. Pretty faces are the basis of identification of facial anomalies, both with rendered and multiplanar imaging. Sonographers, physicians, and other health care providers that perform ultrasound examinations should understand the techniques available to examine the fetal face with 3D ultrasound (3DUS) as well as 2-dimensional (2D) ultrasound. Rendered images allow the face to be displayed as a curved structure, whereas multiplanar image displays show 3 perpendicular planar images of the face that are similar to conventional 2D imaging.

CLEFTING OF THE LIP AND PALATE Fetal cleft lip and palate occur in approximately 1 per 1000 infants born in the United States.1 The accurate prenatal diagnosis of this condition can aid with the prognosis and management of this condition. Characterization of the extent of clefting allows for counseling of parents and preparation for a significant anomaly. Conventional (2D ultrasound [2DUS]) has been used to make initial diagnosis of cleft lips and primary palate. The detection rate has been reported to range from 20% to 30%.2 However, clefts of the hard or secondary palate and of the soft palate are difficult to visualize with this modality. Three-dimensional ultrasound has recently been used to improve detection of cleft palate. Different rendering techniques have been proposed to aid in the detection of clefting particularly of the secondary palate.

PRIMARY PALATE Imaging of the lips and primary palate are now commonly included in the evaluation of fetal anatomy performed in the midtrimester; the 2007 American Institute of Ultrasound Medicine Guidelines now recommend that the lip be evaluated on all fetuses. Conventional 2DUS can detect clefting involving the lips; however, shadowing and artifact can make detection of associated clefts involving the primary palate difficult. This is important in regard to management because approximately 80% of clefts of the lip involve the primary palate.3 Three-dimensional ultrasound has allowed for improvements in the visualization of the primary palate. Multiplanar reconstruction has allowed for the visualization of the face in the sagittal, axial, and coronal planes. The rendering mode has allowed for the visualization of the soft tissues of the face and the bony alveolar ridge. Multislice reconstructions of 3D volumes display data in parallel slices similar to magnetic resonance imaging. This modality allows

& Volume 24, Number 4, December 2008

Copyright @ 2008 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

215

Ultrasound Quarterly

Ramos et al

FIGURE 1. Normal fetal face at 31 weeks. Notice the normal eyes, nose, and lips. The right forehead is obscured by overlying placenta.

clear visualization of the primary palate and distinction from the mandible (Fig. 2).4

SECONDARY PALATE Complete evaluation of the palate including both the primary (alveolar ridge) and the secondary palate (hard and soft palate) is difficult. The secondary palate has 2 anatomical components: the hard palate runs posterior and horizontal from the alveolar ridge, whereas the soft palate continues

& Volume 24, Number 4, December 2008

posteriorly and backward in a curved manner ending in the uvula.5 Isolated clefting of the secondary palate have been reported in 25% to 80% of cases.5 Isolated clefting of either of the 2 components can occur. Clefting of the soft palate is easily missed prenatally and even on postnatal evaluation. Several different techniques to improve the visualization of these structures have been introduced including the flipped face6 and reverse face view.7 The flipped face technique allows for evaluation of the hard palate by obtaining a volume in the sagittal plane, visualizing a profile, and then flipping that profile on its head.6 The cursor dot is then placed in the palate region, and the palate is rendered with a thin box. The image displayed is a rendered axial image of the primary and secondary palate. This allows for systematic visualization of all components of the primary and secondary palate. In our center, we have used a modification of this technique in which the face is kept upright, and a curved thin render box is used to view the hard palate from the inferior aspect of the maxilla (Figs. 3, 4). The initial volume is acquired slightly obliquely from the inferior aspect of the maxilla, pointing upward. We have successfully imaged the hard palate using this modification that we find more intuitive because of the upright orientation of the face. The reverse face view technique developed by Campbell et al7 to evaluate the hard palate entails obtaining a slow 3D sweep of a fetal profile. This is then rotated 180 degrees to a coronal view, and the volume is then scrolled from back to front. This allows the secondary palate to be viewed in coronal plane while avoiding shadowing from the maxilla. With this technique, 7 cases of clefts were correctly identified; however, 1 cleft of the soft palate was missed.7 This technique relies on obtaining optimal fetal profiles because oblique views did not allow for optimal visualization. Rotten and Levaillant2 took a systematic approach on 96 cases of cleft lip and palate, with the hopes of identifying

FIGURE 2. Multislice of the normal orbits, palate, and mandible at 30 weeks’ gestational age. The upper left image is a reference image of the face in profile. Middle image, upper row, is the mandible (arrows); middle image, middle row, is the primary palate (double arrows); right image, lower row, is the orbits (open arrows).

216

* 2008 Lippincott Williams & Wilkins

Copyright @ 2008 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

Ultrasound Quarterly

& Volume 24, Number 4, December 2008

Evaluation of Fetal Face Using 3DUS

FIGURE 3. Evaluation of the palate. A, Normal palate at 29 weeks. Rendered image using a mixture of surface rendering and radiograph light shows both the primary (alveolar ridge, PP) and secondary (hard, HP) palate to be intact. B, Acquisition of rendered image in A. Upright fetal face in sagittal (upper left image) and coronal (upper right) planes with narrow rendering box overlying palate. Notice that the green region of interest viewing line is curved upward slightly to follow the contour of the palate. Lower left image shows axial plane through the palate with alveolar ridge displayed. Lower right hand image is the rendered image shown in A.

the anatomical region involved. They noted that imaging the maxilla in the axial view and the lips (anteriorly) and secondary palate (posteriorly) in the coronal view provided the diagnosis in 84 cases of cleft lip and palate. In 8 cases (5 of them involving the secondary palate), the diagnosis was missed2; 4 false-positive cases were due to artifact, mainly from the maxilla. Axial imaging of the secondary palate has been further investigated by Faure et al8 and Pilu and Segata.9 Faure et al8 conducted a prospective study in which ultrasound scans in which the anterior axial view of the palate was obtained, and the 3D underside of the fetal palate was rendered. The palate, and its associated anatomical components, was visualized in all 100 cases at gestational ages ranging from 17, 22, 27, and 32 weeks,8 although some patients did have to return for a second examination. Using tomographic ultrasound imaging, Pilu and Segata9 found that acquiring a volume of the sec-

ondary palate with an angle of insonation of 45 degrees allowed for complete evaluation of the secondary palate. The 45-degree insonation was thought to aid in overcoming shadowing by the alveolar ridge when imaging the secondary palate. Fifteen normal and 1 abnormal fetuses were correctly diagnosed with this technique. This method, however, is dependent on optimal fetal positioning. Evaluation of the soft palate component of the secondary palate is still limited. Although reports using 3DUS to diagnose isolated soft palate clefts are described,10 there is still difficulty in consistently imaging this area because of artifact. In our experience, the false-positive rate is high mainly because of shadowing.

FACIAL PROFILE The normal facial profile can be displayed with multiplanar or rendered display (Fig. 5) by rotating the face into a

FIGURE 4. Cleft of the lip and primary and secondary palate at 19 weeks. A, Rendered image on lower right shows a cleft extending from the alveolar ridge posteriorly through the secondary (hard) palate (arrow). Upper images show upright fetal face in coronal (left) and sagittal (right) planes, both with narrow rendering box overlying palate and green region of interest viewing line slightly curved upward to follow the contour of the palate. Lower left image shows axial plane through the palate. B, Rendered image of the face clearly demonstrates accompanying cleft lip. * 2008 Lippincott Williams & Wilkins

Copyright @ 2008 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

217

Ultrasound Quarterly

Ramos et al

& Volume 24, Number 4, December 2008

FIGURE 5. Evaluation of the fetal profile. A, Rendered images showing a normal profile at 28 weeks. B, Rendered image of the profile at 30 weeks demonstrates midface hypoplasia with frontal bossing in a fetus with achondroplasia.

symmetrical standard orientation. Anomalies involving the mandible are associated with at least 100 genetic syndromes.11 Midface hypoplasia is often seen in the setting of skeletal dysplasias such as achondroplasia (Fig. 5) and thanatophoric dysplasia.

MICROGNATHIA AND RETROGNATHIA Micrognathia is defined as insufficient size of the mandible, whereas retrognathia is abnormal recession of the chin.11 Micrognathia is associated with Pierre Robin and Treacher Collins syndromes (Fig. 6) and with chromosomal anomalies such as trisomy 13, 18, triploidy, and translocations or gene deletions.12 These abnormalities can be associated with

airway obstruction due to abnormal positioning of the tongue. Identification of these abnormalities can allow for delivery planning including an ex utero intrapartum treatment procedure and for a neonatologist and other specialist to aid in the management of potentially difficult airways. The fetal profile has been shown to be adequately obtained in only 69% of cases using 2DUS alone.12 This limitation can lead to misdiagnosis of malformations, and 3DUS allows for a true profile to be reliably obtained in most fetuses. Mandibular disorders have traditionally been diagnosed by subjective evaluation of the chin on profile evaluation. Recently, in an attempt to use objective measures, Rotten et al11 described 2 indices to aid in the diagnosis. The first measurement involves the inferior facial angle for assessment

FIGURE 6. Micrognathia in Treacher Collins syndrome. A, Rendered image of the fetal profile at 34 weeks shows micrognathia and small malformed ear. B, Postnatal photograph in profile confirms prenatal findings.

218

* 2008 Lippincott Williams & Wilkins

Copyright @ 2008 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

Ultrasound Quarterly

& Volume 24, Number 4, December 2008

of posterior displacement (retrognathia). The second is the ratio of mandible width to maxilla width for assessment of restriction in size (micrognathia).11 His group found that an inferior facial angle of less than 49.2degrees (mean j 2 SDs) defined retrognathia,11 whereas a mandible width/maxilla width ratio of less than 0.785 was diagnostic of micrognathia.11 Paladini et al13 introduced the measurement of the anteroposterior and laterolateral diameter of the mandible to calculate the jaw index to diagnose micrognathia.

METOPIC SUTURES Cranial sutures and fontanelles are sites of bone expansion both prenatally and postnatally, allowing for progressive development of the brain and skull bones.14 Craniosynostosis, or abnormal development of the sutures and fontanelles, may be an isolated finding but can be associated with various chromosomal aberrations or syndromes.15 Historically, prenatal sonographic diagnosis of craniosynostosis has been difficult, with most cases diagnosed in the first year of life.14 Conventional 2DUS allows for only limited evaluation of sutures and fontanelles as cross-sectional slices.14,16 Most cases of craniosynostosis are identified because of an abnormal shape of the head on 2DUS imaging. Three-dimensional ultrasound has been shown to reliably identify most cranial sutures and fontanelles.14Y16 It is unclear, however, whether craniosynostosis will be identified without abnormal head shape by only imaging the sutures. Pretorius and Nelson16 suggested in 1994 that 3DUS could be used in evaluating the fetal cranial sutures and fontanelles. Dikkeboom et al15 demonstrated satisfactory visualization of the metopic, coronal, squamosal, and lambdoid sutures as well as anterior, sphenoid, and mastoid fontanelles in 82% to100% of 120 cases. However, they noted that the sagittal suture and posterior fontanelle were more difficult to identify. They also found that image quality decreased with advancing gestational age. Faro et al17 used 3DUS to describe the morphology and normal development of the fetal frontal bone and metopic suture between 9 and 34 weeks of gestation. In the first trimester, they observed that ossification of the frontal bones occurs in medial and lateral directions from a supraorbital ossification center. The frontal bones expand radically in the second trimester, delineating the metopic suture in the midline (Fig. 7). At approximately 32 weeks of gestation, onset of closure of the metopic suture was observed, starting in the supranasal region and extending superiorly toward the anterior fontanelle. Abnormal development of the fetal metopic suture can be associated with other fetal malformations and numerous genetic syndromes.17,18 Several studies have used 3DUS in evaluating abnormalities of the metopic suture.18,19 Faro et al19 evaluated the metopic sutures in fetuses with holoprosencephaly, trisomy 21, and Apert syndrome. Measurements of the height and gap between the frontal bones were compared between the abnormal and normal fetuses. Holoprosencephaly was associated with accelerated bone development and premature closure of the metopic suture in the first trimester.20 Fetuses with Apert syndrome were noted to have a wide gap in the metopic suture (15Y23 mm) at 22 to 27 weeks of ges-

Evaluation of Fetal Face Using 3DUS

tation.21 No differences in development of the frontal bones and metopic sutures were noted between trisomy 21 fetuses and healthy fetuses in the first trimester.19 In another study, Chaoui et al18 used 3DUS to describe 4 general patterns of abnormal development of the metopic suture: V- or Y-shape, U-shape, premature closure, and presence of an additional bone. They observed V-, Y-, and U-shaped metopic sutures in fetuses with facial defects and confirmed previous reports of an association of premature closure with holoprosencephaly.

NASAL BONE The fetal nasal bone develops from paired ossification centers in a membrane that covers the cartilaginous nasal capsule.22 Absence or hypoplasia of the nasal bone is associated with an increased risk of Down syndrome. Assessment of the fetal nasal bone has been performed primarily with 2DUS using the facial profile view. This technique, however, is technically difficult and requires proficiency to obtain a perfect midsagittal image.23 To overcome the limitations of 2DUS in evaluation of the fetal nasal bone, 3-dimensional multiplanar imaging was proposed as an alternate method. With this technique, Lee et al24 identified 40% to 45% of Down syndrome fetuses in the second and early third trimester using absence of the nasal bone as a sonographic marker (Fig. 8). Rembouskos et al25 examined the fetal nasal bone at 11 to 14 weeks’ gestation and found that 3D multiplanar imaging does allow a perfect midsagittal view of the fetal face to be obtained for assessment of the nasal bone. However, they noted that the extent to which the nasal bone can be demonstrated in the reconstructed image is dependent on obtaining a good initial 2D view.

FIGURE 7. Evaluation of the metopic suture at 21 weeks. Coronal skeletal-rendered image shows a normal metopic suture, which separates the 2 frontal bones in the forehead.

* 2008 Lippincott Williams & Wilkins

Copyright @ 2008 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

219

Ultrasound Quarterly

Ramos et al

& Volume 24, Number 4, December 2008

FIGURE 8. Evaluation of the nasal bones. A, Normal nasal bones at 19 weeks. Sagittal (upper left), axial (upper right), and coronal (bottom left) images with rendering box and focus of interest (small dot) on nasal bone. Rendered image (bottom right) shows the normal nasal bones (arrow). B, Absence of the nasal bones at 22 weeks. Images in the sagittal (upper left), axial (upper right), and coronal (bottom left) planes with rendering box and focus of interest in expected region of nasal bone. Rendered image (bottom right) confirms absence of nasal bones (compare with rendered image from A).

Recent studies have used a 3D volume rendering technique that displays the fetal bony facial structures and allows assessment of the nasal bones. Gon0alves et al26 and Benoit and Chaoui27 identified 3 nasal bone ossification patterns in second-trimester fetuses: (1) normal development with the paired nasal bones visualized as a single structure fused in the midline, (2) delayed ossification with unilateral or bilateral nasal bones not fused in the midline, and (3) absent nasal bones. They confirmed previous findings that absence of nasal bones is associated with the highest risk of Down syndrome. Importantly, they suggested that these ossification patterns may be indistinguishable on 2DUS or multiplanar 3DUS. Similarly, Benoit and Chaoui27 demonstrated more accurate evaluation of the paired nasal bones with 3D rendered images. They observed unilateral absence of the nasal bone in 3 of 20 fetuses with Down syndrome. Furthermore, a discrepancy between 2D and 3D findings was noted in 3 of 9 cases; unilateral absence of a nasal bone was identified on 3DUS when complete absence had been noted on 2DUS.

ORBITS Abnormalities of the fetal orbits include hypotelorism and hypertelorism, masses, anophthalmia, microphthalmia, and cataracts.28 A multitude of genetic syndromes and chromosomal abnormalities can be associated with any of these findings. Hypotelorism refers to abnormal closeness of the eyes, whereas hypertelorism refers to an abnormally increased distance between the eyes. Measurements of the biorbital and interorbital distances are made in the transverse view of the orbits on 2DUS. There are no published studies to date examining the role of 3DUS in assessing hypotelorism or hypertelorism. In a few case reports, however, 3DUS has been used to confirm these orbital abnormalities as well as other facial dysmorphic features (Fig. 9).29Y31 Orbital and periorbital masses include dacrocystocele, frontal encephalocele, glioma, hemangioma, and teratoma.32 Prenatal diagnosis by 2DUS is difficult, although location, Doppler findings, and associated structural abnormalities can

220

help to distinguish these masses. Congenital dacrocystocele is a dilatation of the lachrymal drainage system due to obstruction of the proximal and distal ducts, resulting in a collection of mucous or amniotic fluid.28 It is often detected on 2DUS as a periorbital mass located medial and inferior to the orbit. There have been few case reports using 3DUS in the diagnostic evaluation of a dacrocystocele. Petrikovsky and Kaplan33 found that the 3D image relieved parental concern over facial distortion by bilateral dacrocystoceles. Sepulveda et al34 reported that 3D sonography allowed for the precise localization and degree of intranasal extension of the lesion in their 3 cases. Chmait et al35 demonstrated excellent visualization of a suspected unilateral dacrocystocele on 3DUS, which ultimately was diagnosed as a nasal glioma postnatally.

EARS Fetal ear abnormalities can be associated with chromosomal aberrations such as trisomy 13, 18, and 21, as well as a variety of genetic syndromes.36,37 Microtia, large ears, or abnormal position are characteristic of many congenital anomalies.37 The Treacher Collins syndrome, Fraser syndrome, CHARGE association, and VACTERL association are all related to a malformed ear.36,37 Several authors have suggested the application of fetal ear length and width measurements for the prediction of aneuploidy, but the results have been controversial.38Y40 Prenatal identification of an anomalous ear has been quite difficult, however, because of the complexity of the fetal ear and the limitations of conventional 2DUS. Assessment of the fetal ear using 3DUS has now been evaluated in a few studies, with promising results (Fig. 10). Shih et al36 successfully reconstructed 3D images of 1 or both ears in more than 80% of fetuses in their study and demonstrated greater accuracy and clarity as compared with 2DUS. They found that 3DUS of the fetal ear allowed better recognition of ear shape, ridge pattern, and helix development and provided information on cranial location, axis, and orientation of the ear. Similarly, Chang et al37 found 3DUS to be superior to 2DUS in the qualitative evaluation of the fetal ear. They also proposed a nomogram of fetal ear length, width, and area for normal pregnancies and suggested that the * 2008 Lippincott Williams & Wilkins

Copyright @ 2008 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

Ultrasound Quarterly

& Volume 24, Number 4, December 2008

Evaluation of Fetal Face Using 3DUS

FIGURE 9. Hypotelorism in a 21-week fetus with holoprosencephaly. Multislice display of contiguous axial images through the head shows that the orbits are too close together in the middle 3 images. Notice also that there is a midline cleft lip and palate seen in the middle bottom image (arrow). Reference lines are shown across a profile of the face in the upper left image.

combination of these parameters may aid in enhancing the detection rate of aneuploidy. Two cases of Treacher Collins syndrome initially diagnosed by findings on 3DUS have been reported (Fig. 6).41,42 In both cases, the characteristic craniofacial features of micrognathia, downward slanting palpebral fissures, and low-set malformed ears were more clearly seen by 3DUS and proved to be helpful in refining the diagnosis prenatally.

BONDING Parents related to the images of the fetus and particularly, the fetal face. Many investigators have reported that 2DUS images increase bonding between parents and their fetuses.43Y45 Three-dimensional ultrasound images are very appealing to parents and probably also increase bonding.46Y50 Pretorius et al51 reported that 3DUS was very beneficial for the following patients: previous anomalies or fetal demise, surrogate parents, hospice patients carrying fatal anomalies, infertility, and family history of anomalies. Ji et al46 reported on 100 patients, 50 with 2DUS and 50 with 3DUS and found that the patients with 3DUS shared their photographic images with more people (median, 27.5) compared with those who had 2DUS (median, 11.0).47 Pretorius et al47 studied 189 parents using a validated questionnaire that had been modified for fetuses (that had initially been tested for maternal-attachment in neonates) and found that bonding was increased.48 Parental drawings have also been used to suggest that there is increased bonding after patients undergo 3DUS.52 Rustico et al49 found little difference in maternal emotional status between women who had 2DUS alone compared with women who had 2DUS and 4DUS. Much controversy exists as to whether parents should be allowed to have 3DUS studies for bonding alone, not as part of a diagnostic ultrasound study performed for medical

indications. The Federal Drug Administration and the American Institute of Ultrasound in Medicine have both developed statements that say ultrasound should only be performed on fetuses for medical indications. The medical community is concerned about nonmedical use of ultrasound for the following reasons: studies performed by commercial vendors may not have adequate training to understand the biohazards of ultrasound and may misinterpret the images, both missing abnormalities and identifying normal findings as abnormalities. Academic physicians have varying opinions.

FIGURE 10. Normal ear at 22 weeks. Rendered image in sagittal plane shows normally-developed ear.

* 2008 Lippincott Williams & Wilkins

Copyright @ 2008 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

221

Ultrasound Quarterly

Ramos et al

Doubilet50 wrote in an editorial that many instruments began as single-use devices and, only later, were used for many different reasons (eg, computer, microscope, and camera). He suggests that to ban or condemn use of ultrasound for entertainment is wholly inconsistent with our acceptance of many other goods and services that provide enjoyment, while carrying a small potential risk.50

TECHNICAL POINTS Currently in our laboratory, we perform 3-dimensional ultrasound (3DUS) evaluation of the fetal face when it aids in the diagnosis of a suspected anomaly on 2DUS or if it is requested by referring physicians for diagnostic purposes. The timing of the evaluation is typically optimal at 22 weeks; however, with the rising rates of first trimester screening, we now are able to perform 3DUS of the face as early as 12 weeks; in patients at risk for cleft lip and palate, we generally do our first examination at 18 weeks, although we have seen abnormal faces as early as 12 weeks. Minimum requirements to perform 3DUS, include multiplanar display, rendered display, 3DUS, and 4-dimensional ultrasound (4DUS). Presets for surface rendering and skeletal display are also used. Fourdimensional ultrasound aids in rendering and movement, whereas 3DUS allows for improved multiplanar and multislice rendering. Typically, our examinations are scheduled for 60 minutes. If upon examining the fetal face we note that fetal positioning is not optimal, we have the mother perform toe touches, walk around, or empty her bladder. If diagnostic evaluation is still not possible, we may need to reschedule her visit.

SUMMARY Three-dimensional ultrasound has become an important tool as an adjunct to 2DUS in the evaluation of the fetal face. It allows for better characterization of the normal anatomy of the fetal face and has increased the diagnostic accuracy of anomalies. Three-dimensional ultrasound can also enhance parents’ understanding of the anomalies and may allow for earlier bonding with their fetuses. It is important for sonologists and sonographers to have an understanding of how to evaluate the fetal face with 3DUS. ACKNOWLEDGMENTS The authors thank Philips Medical Systems and General Electric Healthcare for equipment loan. The authors also thank Vivian Cohen for manuscript assistance. REFERENCES 1. Lee W, Kirk J, Shaheen K, et al. Fetal cleft lip and palate detection by three-dimensional ultrasonography. Ultrasound Obstet Gynecol. 2000;16:314Y320. 2. Rotten D, Levaillant J. Two- and three-dimensional sonographic assessment of the fetal face. 2. Analysis of cleft lip, alveolus and palate. Ultrasound Obstet Gynecol. 2004;24:402Y411. 3. Johnson D, Pretorius D, Budorick N, et al. Fetal lip and primary palate: three-dimensional versus two-dimensional US. Radiology. 2000;217: 236Y239. 4. McGahan MC, Ramos GA, Landry C, et al. Multislice display of the fetal face using 3-dimensional ultrasonography. J Ultrasound Med. 2008; 27(11):1573Y1581.

222

& Volume 24, Number 4, December 2008

5. Campbell S. Prenatal ultrasound examination of the secondary palate. Ultrasound Obstet Gynecol. 2007;29(2):124Y127. 6. Platt L, Devore G, Pretorius D. Improving cleft palate/cleft lip antenatal diagnosis by 3-dimensional sonography: the Bflipped face[ view. J Ultrasound Med. 2006;25:1423Y1430. 7. Campbell S, Lees C, Moscoso G, et al. Ultrasound antenatal diagnosis of cleft palate by a new technique: the 3D Breverse face[ view. Ultrasound Obstet Gynecol. 2005;25:12Y18. 8. Faure J, Captier G, Baumeler M, et al. Sonographic assessment of normal fetal palate using three-dimensional imaging: a new technique. Ultrasound Obstet Gynecol. 2007;29:159Y165. 9. Pilu G, Segata M. A novel technique for visualization of the normal and cleft fetal secondary palate: angled insonation and three-dimensional ultrasound. Ultrasound Obstet Gynecol. 2007;29:166Y169. 10. Benacerraf B, Sadow P, Barnewolt C, et al. Cleft of the secondary palate without cleft lip diagnosed with three-dimensional ultrasound and magnetic resonance imaging in a fetus with Fryns’ syndrome. Ultrasound Obstet Gynecol. 2006;27:566Y570. 11. Rotten D, Levaillant J, Martinez H, et al. The fetal mandible: a 2D and 3D sonographic approach to the diagnosis of retrognathia and micrognathia. Ultrasound Obstet Gynecol. 2002;19(2):122Y130. 12. Kurjak A, Azumendi G, Andonotopo W, et al. Three- and four-dimensional ultrasonography for the structural and functional evaluation of the fetal face. Am J Obstet Gynecol. 2007;196(1): 16Y28. 13. Paladini D, Morra T, Teodoro A, et al. Objective diagnosis of micrognathia in the fetus: the jaw index. Obstet Gynecol. 1999;93(3):382Y386. 14. Ginath S, Debby A, Malinger G. Demonstration of cranial sutures and fontanelles at 15 to 16 weeks of gestation: a comparison between two-dimensional and three-dimensional ultrasonography. Prenat Diagn. 2004;24(10):812Y815. 15. Dikkeboom C, Roelfsema N, Van Adrichem L, et al. The role of three-dimensional ultrasound in visualizing the fetal cranial sutures and fontanels during the second half of pregnancy. Ultrasound Obstet Gynecol. 2004;24(4):412Y416. 16. Pretorius D, Nelson T. Prenatal visualization of cranial sutures and fontanelles with three-dimensional ultrasonography. J Ultrasound Med. 1994;13(11):871Y876. 17. Faro C, Benoit B, Wegrzyn P, et al. Three-dimensional sonographic description of the fetal frontal bones and metopic suture. Ultrasound Obstet Gynecol. 2005;26:618Y621. 18. Chaoui R, Levaillant J, Benoit B, et al. Three-dimensional sonographic description of abnormal metopic suture in second- and third-trimester fetuses. Ultrasound Obstet Gynecol. 2005;26:761Y764. 19. Faro C, Wegrzyn P, Benoit B, et al. Metopic suture in fetuses with holoprosencephaly at 11 + 0 to 13 + 6 weeks of gestation. Ultrasound Obstet Gynecol. 2006;27:162Y166. 20. Faro C, Wegrzyn P, Benoit B, et al. Metopic suture in fetuses with trisomy 21 at 11 + 0 to 13 + 6 weeks of gestation. Ultrasound Obstet Gynecol. 2006;27:286Y289. 21. Faro C, Chaoui R, Wegrzyn P, et al. Metopic suture in fetuses with Apert syndrome at 22-27 weeks of gestation. Ultrasound Obstet Gynecol. 2006;27:28Y33. 22. Sandikcioglu M, MLlsted K, Kjaer I. The prenatal development of the human nasal and vomeral bones. J Craniofac Genet Dev Biol. 1994;14:124Y234. 23. Cicero S, Dezerega V, Andrade E, et al. Learning curve for sonographic examination of the fetal nasal bone at 11Y14 weeks. Ultrasound Obstet Gynecol. 2003;22:135Y137. 24. Lee W, DeVore G, Comstock C, et al. Nasal bone evaluation in fetuses with Down syndrome during the second and third trimesters of pregnancy. J Ultrasound Med. 2003;22:55Y60. 25. Rembouskos G, Cicero S, Longo D, et al. Assessment of the fetal nasal bone at 11Y14 weeks of gestation by three-dimensional ultrasound. Ultrasound Obstet Gynecol. 2004;23:232Y236. 26. Gon0alves L, Espinoza J, Lee W, et al. Phenotypic characteristics of absent and hypoplastic nasal bones in fetuses with Down syndrome: description by 3-dimensional ultrasonography and clinical significance. J Ultrasound Med. 2004;23:1619Y1627. 27. Benoit B, Chaoui R. Three-dimensional ultrasound with maximal mode rendering: a novel technique for the diagnosis of bilateral or unilateral

* 2008 Lippincott Williams & Wilkins

Copyright @ 2008 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

Ultrasound Quarterly

28. 29.

30.

31. 32. 33. 34. 35. 36. 37. 38. 39. 40. 41.

& Volume 24, Number 4, December 2008

absence or hypoplasia of nasal bones in second-trimester screening for Down syndrome. Ultrasound Obstet Gynecol. 2005;25:19Y24. Benacerraf B, Nyberg D. The face and neck. In: Nyberg D, McGahan J, Pretorius D, Pilu G, eds. Diagnostic Imaging of Fetal Anomalies. Philadelphia, PA: Lippincott Williams & Wilkins; 2003:335Y379. Tonni G, Ventura A, Centini G, et al. First trimester three-dimensional transvaginal imaging of alobar holoprosencephaly associated with proboscis and hypotelorism (ethmocephaly) in a 46,XX fetus. Congenit Anom (Kyoto). 2008;48(1):51Y55. Sase M, Hasegawa K, Honda R, et al. Ultrasonographic findings of facial dysmorphism in Wolf-Hirschhorn syndrome. Am J Perinatal. 2005;22(2):99Y102. Lee G, Hur S, Shin J, et al. Prenatal diagnosis of holoprosencephaly with ethmocephaly via 3-dimensional sonography. J Clin Ultrasound. 2006;34(6):306Y308. Mernagh JR, Mohide PT, Lappalainen RE, et al. US assessment of the fetal head and neck: a state-of-the-art pictorial review. Radiographics. 1999;19:S229YS241. Petrikovsky B, Kaplan G. Fetal dacryocystocele: comparing 2D and 3D imaging. Pediatr Radiol. 2003;33:582Y583. Sepulveda W, Wojakowski A, Elias D, et al. Congenital dacryocystocele: prenatal 2- and 3-dimensional sonographic findings. J Ultrasound Med. 2005;24:225Y230. Chmait R, Pretorius D, Hull A. Nasal glioma. Ultrasound Obstet Gynecol. 2002;20:417Y418. Shih J, Shyu M, Lee C, et al. Antenatal depiction of the fetal ear with three-dimensional ultrasonography. Obstet Gynecol. 1998;91: 500Y505. Chang C, Chang F, Yu C, et al. Fetal ear assessment and prenatal detection of aneuploidy by the quantitative three-dimensional ultrasonography. Ultrasound Med Biol. 2000;26:743Y749. Awwad J, Azar G, Karam K, et al. Ear length: a potential sonographic marker for Down syndrome. Int J Gynecol Obstet. 1994;44: 233Y238. Birnholz J, Farrell E. Fetal ear length. Pediatrics. 1988;81:555Y558. Gill P, Vanhook J, Fitzsimmons J, et al. Fetal ear measurements in the prenatal detection of trisomy 21. Prenat Diagn. 1994;14(8):739Y743. Hsu TYHJ, Chang SY, Chang MS. Prenatal three-dimensional

Evaluation of Fetal Face Using 3DUS

42. 43. 44. 45. 46. 47. 48.

49.

50. 51. 52.

sonographic images associated with Treacher Collins syndrome. Ultrasound Obstet Gynecol. 2002;19(4):413Y422. Tanaka YKK, Tanaka H, Yanagihara T, et al. Antenatal three-dimensional sonographic features of Treacher Collins syndrome. Ultrasound Obstet Gynecol. 2002;19(4):414Y415. Whynes D. Receipt of information and women’s attitudes towards ultrasound scanning during pregnancy. Ultrasound Obstet Gynecol. 2002;19(1):7Y12. Zechmeister I. Foetal images: the power of visual technology in antenatal care and the implications for women’s reproductive freedom. Health Care Anal. 2001;9(4):387Y400. Campbell S, Reading A, Coxs D, et al. Ultrasound scanning in pregnancy: the short term psychological effects of early real time scanning. J Psychosom Obstet Gyn. 1982;1:57Y61. Ji E, Pretorius D, Newton R, et al. Effects of ultrasound on maternal-fetal bonding: a comparison of 2-dimensional vs. 3-dimensional imaging. Ultrasound Obstet Gynecol. 2005;25:473Y477. Pretorius D, Hearon H, Hollenbach K, et al. Parental artistic drawings of the fetus pre and post 3 / 4 dimensional ultrasound examination. J Ultrasound Med. 2007;26:301Y308. Pretorius D, Gattu S, Ji E, et al. Preexamination and postexamination assessment of parental-fetal bonding in patients undergoing 3-/4-dimensional obstetric ultrasonography. J Ultrasound Med. 2006;25(11):1411Y1421. Rustico MAMC, Grigio M, Maggioni C, et al. Two-dimensional vs. two- plus four-dimensional ultrasound in pregnancy and the effect on maternal emotional status: a randomized study. Ultrasound Obstet Gynecol. 2005;25(5):468Y472. Doubilet P. Entertainment ultrasound. J Ultrasound Med. 2005;24(2):251Y253. Pretorius D, Hull A, Newton R, et al. Impact of patient initiated 3-dimensional ultrasound examination. Ultrasound Obstet Gynecol. 2000;16(suppl 1):94. Maier B, Steiner H, Wienerroither H, et al. The psychological impact of three-dimensional fetal imaging on the fetomaternal relationship. In: Baba K, Jurkovic D, eds. Three-Dimensional Ultrasound in Obstetrics and Gynecology. New York, NY: Parthenon; 1997:67Y74.

* 2008 Lippincott Williams & Wilkins

Copyright @ 2008 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

223