A systematic technique using 3-dimensional ultrasound provides a simple and reproducible mode to evaluate the corpus callosum
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A systematic technique using 3-dimensional ultrasound provides a simple and reproducible mode to evaluate the corpus callosum Eran Bornstein, MD; Ana Monteagudo, MD; Rosalba Santos, RDMS; Sean M. Keeler, MD; Ilan E. Timor-Tritsch, MD OBJECTIVE: The aim of this study was to evaluate a rapid 3-dimen-
RESULTS: The median plane was easily obtained in all cases. Diagnos-
sional ultrasound-assisted technique for evaluation of the corpus callosum as an integral part of the anatomic survey.
tic-quality images of the corpus callosum were recorded in 93.1% and 99.0% and of the pericallosal arteries in 94.4% and 95.5% of the cases, by the 2 examiners, respectively.
STUDY DESIGN: Transabdominal 3-dimensioal gray scale and power
Doppler volumes of the fetal brain were acquired in 102 consecutive healthy fetuses at 20 –23 postmenstrual weeks. Offline analysis was performed by 2 of the authors using a systematic approach of “volume manipulation.” Diagnostic-quality visualization of the corpus callosum and the pericallosal arteries on the median plane was recorded by the 2 examiners independently.
CONCLUSION: Three-dimensional ultrasound enables a rapid and easy
evaluation of the corpus callosum that may facilitate its inclusion as an integral part of the routine anatomic survey. Key words: agenesis of corpus callosum, anatomic survey, corpus callosum, fetal neurosonogram, pericallosal artery, 3D ultrasound
Cite this article as: Bornstein E, Monteagudo A, Santos R, et al. A systematic technique using 3-dimensional ultrasound provides a simple and reproducible mode to evaluate the corpus callosum. Am J Obstet Gynecol 2010;202:201.e1-5.
he corpus callosum, a thick plate of dense myelinated fibers, is the main connection between the 2 cerebral hemispheres. Its formation (anterior to posterior) is initiated in the embryonic period and is completed by 18 –20 postmenstrual weeks.1-3 This structure is thought to play a sentinel role in integrating mo-
From the Divisions of Maternal-Fetal Medicine (Drs Bornstein, Monteagudo, and Keeler) and Ultrasound in Obstetrics and Gynecology (Drs Monteagudo and TimorTritsch and Ms Santos), Department of Obstetrics and Gynecology, New York University School of Medicine, New York, NY. Presented at the 29th Annual Meeting of the Society for Maternal-Fetal Medicine, San Diego, CA, Jan. 26-31, 2009. Received May 19, 2009; revised July 30, 2009; accepted Oct. 7, 2009. Reprints not available from the authors. 0002-9378/$36.00 © 2010 Mosby, Inc. All rights reserved. doi: 10.1016/j.ajog.2009.10.705
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tor, sensory, and cognitive functions in the human brain. Partial and complete agenesis of the corpus callosum (AGCC) are relatively common brain anomalies thought to occur in 0.1– 0.7% of the general population.4,5 Higher prevalence was documented in selected populations, such as developmentally delayed children (2– 3%), and among fetuses with dilatation of the lateral ventricles (3–10%).6-10 The poor outcome associated with both complete and partial AGCC depends mainly on the presence of associated fetal anomalies and the fetal karyotype. Nevertheless, even fetuses with isolated AGCC, which account for only onethird of all cases, have been associated with a significant risk of developmental delay.11 Acceptable guidelines for the routine fetal brain examination during the second-trimester anatomic survey have been provided by the American College of Obstetricians and Gynecologists, the American Institution of Ultrasound in Medicine, and the International Society of Ultrasound in Obstetrics and Gynecology.12-14 These guidelines are based on transabdominal axial brain planes on which the falx, thalami, cavum septi pel-
lucidi, lateral ventricles with the choroids, cerebellum, and cisterna magna should be demonstrated. These axial planes, however, are not sufficient to evaluate the corpus callosum. Therefore, the diagnosis of AGCC on these axial planes is based on indirect clues, such as colpocephaly, absence of the cavum septi pellucidi, and the widely separated parallel frontal horns. However, these indirect signs are not always present at the time of the anatomic survey and may progress to be apparent only later in the mid or third trimester. To date, direct evaluation of the corpus callosum is not officially recommended as an integral part of the basic routine anatomic survey.12-14 To directly visualize the corpus callosum, a meticulous scanning technique, in which the fetal brain is scrutinized in the coronal and midsagittal (median) planes, has to be implemented. Figure 1 demonstrates a simplified anatomic diagram of the median plane providing evaluation of the entire corpus callosum and pericallosal artery. Malinger and Zakut15 have shown that dedicated transvaginal fetal neurosonography, performed by an expert examiner, provides excellent visualization of the corpus cal-
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A simplified diagram of the fetal brain median plane
larly aimed for a transabdominal, rapid, and simple application, which might facilitate the demonstration of the corpus callosum as an integral part of the routine second-trimester anatomic survey.
M ATERIALS AND M ETHODS
A simplified diagram of the median plane of the fetal brain demonstrating the entire corpus callosum (arrow, CC), the anterior cerebral artery (arrow, ACA) and its branch, and the pericallosal artery (arrow, PA). Bornstein. Evaluation of the CC with 3D ultrasound. Am J Obstet Gynecol 2010.
losum. Similar findings were found by other investigators, who, in cases of vertex presentation, successfully used the transvaginal approach in the evaluation of the corpus callosum.1,16-19 Unfortunately, this practical technique did not gain popularity in the United States and is perceived by many as cumbersome and time consuming. This attitude might be attributed mainly to the lack of expertise or training of most diagnostic fetal ultrasound providers in obtaining the median plane using transvaginal sonography, as well as in interpreting the “nontraditional” brain planes (coronal and sagittal). In addition, some clini201.e2
cians are reluctant to use the transvaginal approach even when the fetus is in vertex presentation. Three-dimensional (3D) ultrasound has emerged in recent years, facilitating the examination of an entire volume of ultrasound information, which can be scrutinized using an infinite number of planes to obtain the desired view. The technique allows the simultaneous presentation of the image in the 3 ortogonal planes. In this study, we sought to investigate a systematic approach using the 3D multiplanar mode to obtain a diagnostic-quality imaging of the corpus callosum on the median plane. We particu-
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This prospective, observational study was conducted in our ultrasound unit between January 2008 –September 2008. The study population included 102 consecutively scanned sonographically normal fetuses presenting for a routine second-trimester anatomic survey at 20 –23 postmenstrual weeks. Exclusion criteria included multiple gestations and known congenital or chromosomal anomalies. Transabdominal 3D volume acquisition of the fetal brain was performed by 1 of 3 sonographers, who are experienced in 3D techniques. All scans were performed using a single General Electric Voluson E8 (Milwaukee, WI), equipped with a 5– 8 MHz transabdominal 3D transducer, which was designated for that purpose. There was no selection as to which patients were assigned to this examination room. Initially, a gray scale volume of the fetal brain was acquired. Depending on the fetal position, the volume acquisition was obtained in the sagittal or coronal planes, using the anterior fontanelle, the sagittal, or metopic sutures as acoustic windows. If fetal position did not enable easy and rapid access to these structures and acquisition in these planes, we acquired the volume in the axial plane at the biparietal diameter level. Additional volume was acquired using the power Doppler mode (with the pulse repetition frequency set at 0.6 kHz) to image the brain vasculature in 90 patients. We used an acquisition sweep angle of 45° to include the entire fetal brain within the volume. In most cases, several volumes were acquired, accounting for possible motion artifacts that would have precluded our evaluation. The sonographers were instructed to acquire the volumes during the routine anatomic brain survey and not to extend the scan beyond the routine American Institution of Ultrasound in Medicine guidelines to scrutinize the brain or optimize the visualization of the corpus callosum
www.AJOG.org before the acquisition. Visualization of the corpus callosum by 2-dimensionl (2D) ultrasound was not performed before the acquisition of the volume. Subsequently, all volumes were deidentified and stored on a serially numbered computer disk. Offline analysis was conducted using dedicated software (4D View; General Electric) on 1 of 2 personal laptop computers. Each volume was examined separately and independently by 2 of the authors, versed in fetal neurosonography. A systematic approach of “volume manipulation” on the multiplanar display mode was performed in which the volumes were positioned into a standard, symmetric orientation of the orthogonal planes. This resulted in display of the coronal plane in box A, the median plane in box B, and the axial plane in box C. In this manner the entire corpus callosum could be depicted on the median plane (Video 1). Moreover, the axial and coronal planes were simultaneously displayed and were evaluated as well. The volume containing the power Doppler was positioned in a similar fashion to trace the anterior cerebral artery and its branch, the pericallosal artery, on the median plane (Video 2). Diagnostic-quality visualization of the entire corpus callosum (on the gray scale volume) and the pericallosal artery (on the power Doppler volume) on the median plane was then recorded by the 2 examiners, who were blinded to each other’s evaluations and results. The agreement rate between the 2 examiners was also calculated. This was derived from the number of cases in which both examiners reached a similar conclusion, either both adequately visualized the structure or both did not adequately visualize it. All images were reviewed for quality assurance by the first author (E.B), who is a Fellow in maternal-fetal medicine. Furthermore, this author also performed an independent offline evaluation of all of the acquired volumes. The study was approved by the institutional review board committee.
Gray scale volume displayed in the multiplanar mode
Gray scale volume displayed in the multiplanar mode demonstrating the fetal brain in the A, coronal plane, B, median plane, and C, axial plane. The entire corpus callosum can be seen on the median plane (arrows). Bornstein. Evaluation of the CC with 3D ultrasound. Am J Obstet Gynecol 2010.
nal planes, using this technique (as demonstrated in Videos 1 and 2), the median plane was successfully obtained within 1 minute in all cases. This allowed for simultaneous evaluation of the axial, coronal, and median planes of the fetal brain. Diagnostic-quality images of the entire corpus callosum on the median plane were recorded by the 2 examiners, in 93.1% (95/102) and 99.0% (101/102) of the cases, respectively (Figure 2). Diagnostic-quality images of the pericallosal artery on the median plane were recorded by the 2 examiners in 94.4% (85/90) and 95.5% (86/90) of the cases, respectively (Figure 3). Excellent agreement rates for diagnostic visualization of the corpus callosum and the pericallosal artery by the 2 examiners were detected, 94% and 95%, respectively.
C OMMENT R ESULTS By rotating the volume into the symmetric, standard orientation of the orthogo-
Our results indicate that this novel application, using the 3D multiplanar display mode, provides a simple
method to rapidly obtain the median plane, which enables diagnostic-quality evaluation of the entire corpus callosum. It also enables imaging of the pericallosal artery, a useful, marker of callosal integrity, on the volumes acquired with power Doppler. This application is specifically useful, as it facilitates adequate visualization of the corpus callosum through the transabdominal route without significant prolongation of the time dedicated for the scan. Moreover, this is an appealing method to most providers who do not feel comfortable using the transvaginal scanning route. Therefore, it may accommodate the implementation of a routine visualization of the corpus callosum during the second-trimester fetal anatomic survey by complementing the traditional 2D ultrasound in cases in which the median plane is difficult or impossible to obtain because of unfavorable fetal position. In addition, the simultaneous presentation of the 3
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Power Doppler volume displayed in the multiplanar mode
Power Doppler volume displayed in the multiplanar mode demonstrating the fetal brain in the A, coronal plane, B,median plane, and C, axial. The brain vasculature, as well as the entire pericallosal artery (arrows), is seen branching off of the anterior cerebral artery (single arrow) on the median plane as well as on the D, rendered image. Bornstein. Evaluation of the CC with 3D ultrasound. Am J Obstet Gynecol 2010.
orthogonal planes provides detailed information that is valuable in both normal as well as anomalous cases. As previously mentioned, proper evaluation of the corpus callosum is based on successive coronal planes or on a perfectly aligned median plane in which the entire corpus callosum is depicted (Figure 1). Recently, the International Society of Ultrasound in Obstetrics and Gynecology published practice guidelines for dedicated neurosonography that are intended to be used by experienced providers in cases at increased risk of a brain malformation.14 These guidelines are based on a transvaginal evaluation of both successive coronal and a midsagittal plane and include the visualization of the corpus callosum.14 Furthermore, it has been demonstrated that dedicated neurosonography can be as efficient as fetal brain magnetic resonance imaging in diagnosing fetal brain anomalies by experienced providers.20 Clearly, exper201.e4
tise in aligning the ultrasound transducer with the anterior fontanelle is required to maximize the quality of the image.2,15,16 Unfortunately, even 15 years after the introduction of the neurosonographic transvaginal approach, this modality remains underused, and its use is limited to a small group of examiners who are highly interested in fetal neurosonography. Our group considers transvaginal neurosonography, if enabled by fetal presentation, the gold standard imaging modality to evaluate the fetal brain during the second trimester. However, we recognize the importance of alternative imaging techniques for the demonstration of the corpus callosum on the median plane, so that this important view may also be obtained by providers who do not use the transvaginal approach. The transfrontal view, which uses the metopic suture as an acoustic window, was described as a transabdominal tech-
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nique allowing the visualization of the corpus callosum.21 However, obtaining the perfect midline through the metopic suture also requires expertise and, depending on the fetal position, may be time consuming. Moreover, obtaining the correct midline is not always an easy task. For example, the section selected by sonologists as a midline profile was shown to significantly deviate from the true median plane in one-third of the cases.22 Similar deviations from the true midline were noted in the evaluation of nuchal translucency measurments.23 These findings emphasize the complexity of both obtaining as well as recognizing the true median plane. Our ability to manipulate an acquired volume into the standard symmetric orientation of the 3 orthogonal planes using this 3D application eliminates such deviations from the midline. The simultaneously displayed coronal and axial planes act as controls, allowing “fine tuning,” and thus enabling consistent visualization of the true median plane in all cases. Our findings are consistent with prior successful experience in using 3D applications to depict the corpus callosum.24-26 Moreover, in a previous comparison between 2D and 3D sonography, Wang et al27 were able to visualize the corpus callosum in 78% (25/32) of fetuses using 3D ultrasound, compared with only 3% (1 fetus) using 2D ultrasound. Although we do not agree with their findings, as they suggest that 3D ultrasound is superior to 2D ultrasound in the visualization of the corpus callosum, we find it valuable in emphasizing 2 important issues. First, providers have difficulty in depicting the corpus callosum using transabdominal traditional 2D methods, and, second, 3D applications to depict the corpus callosum are fairly simple to obtain even by examiners who are unsuccessful performing 2D scanning. Additional advantages of 3D sonography make its routine use in scanning the fetal brain attractive both in normal as well as in pathologic cases. The sonographic information is stored as a volume data, enabling offline analysis with the potential to revise and obtain additional images in multiple display modes.
www.AJOG.org In addition, electronic transmittal of the saved volume can be easily performed to obtain an offsite expert consultation. In addition, reviewing the saved volume is a valuable training tool, which can simulate real-time examination of complex cases. Our data also point to the excellent reproducibility of this technique, demonstrated by the high interobserver agreement rates for the identification of both the corpus callosum and the pericallosal artery. To note, comparable diagnostic visualization rates were obtained by the first author (E.B.), who is a Fellow in maternal-fetal medicine, suggesting that the scope of this technique is not limited only to expert neurosonologists. Therefore, we suggest the use of this 3D ultrasound-assisted application as an alternative modality to the transvaginal approach to rapidly evaluate the presence and integrity of the corpus callosum. This technique can be used as an adjunct to 2D ultrasound and be easily adopted either by providers who are not versed in transvaginal neurosonography or in cases in which the fetal presentation precludes the former. Our routine practice includes evaluation of the corpus callosum during every second-trimester anatomic survey, and we believe that this could or even should become the standard of care. This novel technique can be used for this purpose and facilitate the inclusion of the corpus callosum as an integral structure to be examined at the second-trimester anatomic survey. Given the increased availability of 3D capability in most modern ultrasound machines, with a relatively short training and understanding of the brain anatomy in the median plane, this technique can be performed successfully by most providers. As we demonstrated, this can be achieved in the vast majority of cases without a significant prolongation of the examination time. f
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