Published online before print January 19, 2006, 10.1148/radiol.2383050636
(Radiology 2006;238:988-996.)
© RSNA, 2006
Three-dimensional US of the Fetus: Volume Imaging1
Beryl R. Benacerraf, MD,
Thomas D. Shipp, MD and
Bryann Bromley, MD
1 From the Department of Obstetrics and Gynecology, Division of Maternal-Fetal Medicine, Brigham and Women's Hospital, Boston, Mass (B.R.B., T.D.S., B.B.); Department of Obstetrics and Gynecology, Massachusetts General Hospital, Boston, Mass (B.R.B., T.D.S., B.B.); and Department of Radiology, Brigham and Women's Hospital, Harvard Medical School, Boston, Mass (B.R.B., T.D.S., B.B.). Received April 18, 2005; revision requested June 15; revision received June 29; accepted July 20; final version accepted August 23.
Address correspondence to B.R.B., Diagnostic Ultrasound Associates, 333 Longwood Ave, Suite 400, Boston, MA 02115. (e-mail: bbsono{at}aol.com).
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ABSTRACT
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Purpose: To retrospectively compare the rapidity, efficiency, and accuracy of three-dimensional (3D) and two-dimensional (2D) ultrasonography (US) for complete anatomic survey in fetuses at 17–21 weeks of gestation.
Materials and Methods: Institutional review board approval was obtained, informed consent was waived, and the study was HIPAA compliant. Fifty consecutive women undergoing fetal anatomic survey at 17–21 weeks of gestation formed the study cohort. After standard 2D US was performed by one of eight sonographers, the same sonographer also obtained five 3D volumes to encompass the entire fetal anatomy. Three physicians interpreting the scans independently evaluated the completeness of the examination and time needed to read the scans, comparing the standard 2D method with the 3D volume reconstruction technique. The paired t test was used to compare biparietal diameter (BPD), femur length, and performance times between the 3D measurements and the 2D measurement. The t test was used to compare fetal anatomy according to volume angle. Differences were significant when P < .05.
Results: Mean time to perform 2D US was 19.6 minutes per examination, whereas mean time to perform complete 3D volume acquisition was 1.8 minutes. Mean times needed to interpret 3D images and measure the BPD and femur were 5.53, 4.79, and 5.34 minutes for the three interpreting physicians. Compared with complete fetal surveys performed with 2D US, individual fetal anatomic landmarks (except for fetal arms and cavum septum pellucidum) were identified more than 94% of the time by using 3D US. Grouping anatomic views by region, the heart, head, extremities, and abdominal views were completely seen in 88%, 90%, 90%, and 95% of patients, respectively. No significant difference was seen between the three physicians regarding completeness of the 3D examinations (P = .7). One fetus had multiple anomalies, with 3D volumes identified as abnormal by all three physicians. Overall, 74% of 3D BPD measurements were within 1 mm of the 2D measurements, and 64% of 3D femur measurements were within 1 mm of the 2D measurements.
Conclusion: The standard fetal anatomic survey can be performed in less than 2 minutes with 3D volume US, and the volumes can be interpreted in 6–7 minutes, compared with a mean of 19.6 minutes to perform standard 2D US.
© RSNA, 2006
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INTRODUCTION
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Authors of numerous case reports and small studies purport the benefits of adding three-dimensional (3D) ultrasonography (US) to the already well-established two-dimensional (2D) US techniques to improve the accuracy of prenatal diagnosis (1–3). The major advantage of 3D, or "volume," US, however, is its potential to change the practice of US (4,5). This change could render US far less operator-dependent, markedly decrease scanning times, and standardize the entire process of performing an examination.
A standard 2D US examination today still requires a one-on-one encounter between a skilled practitioner and the patient, lasting at least 20 minutes, and the set of images produced is dependent on the skill and expertise of the operator. Meanwhile, other forms of cross-sectional imaging, such as computed tomography (CT) and magnetic resonance (MR) imaging, are able to produce 3D cross-sectional volumes that result in rapid displays of multiple sections of the anatomy viewable in any reconstructed plane. Because the volumes are stored, the patient need not spend large amounts of time awaiting completion of the examination and evaluation of the volumes.
The advent of 3D US enables US to compete with CT and MR imaging for efficiency and rapidity (5). Three-dimensional US permits the practitioner to obtain a series of volumes that can be displayed and reconstructed in any plane after the patient examination has been completed, akin to CT or MR imaging. This capability should allow the US specialist to perform a US examination in a fraction of the time that it takes to perform the same evaluation by using conventional 2D US (5). In addition, the examination would be far more comprehensive in that any anatomic structure could be reconstructed and evaluated. The practitioner would no longer need to rely on the areas of interest documented by the operator who performed the initial US evaluation. If an area of concern is identified after the patient has left, the volume can be reinterrogated to address the issue. Thus, the purpose of our study was to retrospectively compare the use of 3D and 2D US for performing a complete anatomic survey in fetuses at 17–21 weeks of gestation.
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MATERIALS AND METHODS
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Fetuses and Imaging
Institutional review board approval was obtained for the study, which included retrospective review of images and volumes for each patient. This study did not change our routine scanning protocol, which normally includes both 2D and 3D US imaging, and therefore this study was considered a review of medical records. Patient informed consent was waived by the institutional review board, and the study was compliant with the Health Insurance Portability and Accountability Act.
Fifty consecutive women undergoing US fetal anatomic survey between 17 and 21 weeks of gestation were included in the study. The fetuses were scanned for standard indications and were included in the study regardless of whether the anatomic survey results were normal or abnormal. All fetuses were scanned by using standard 2D US, which was performed initially by a sonographer and then by a staff sonologist. Eight sonographers and three sonologists (the three authors) participated in the scanning. The eight sonographers had 5–25 years of 2D US experience. The three sonologists had 10–28 years of 2D US experience. Each fetus was initially scanned by one of the sonographers and then was rescanned briefly by one of the three sonologists. Protocols for second-trimester anatomy scanning in our practice conform to all of the guidelines of the American Institute of Ultrasound in Medicine (6); evaluation of the fetal face was also performed. All anatomic landmarks were imaged according to our standard scanning protocol for 2D US. All second-trimester fetuses in our center also undergo the acquisition of several 3D volumes as part of their routine fetal examinations.
At the end of each 2D examination, the sonographer also obtained five consecutive volumes designed to include as much fetal anatomy as possible. The first volume was a head volume (volume 1), with the middle of the acquisition sweep fixed at the base of the skull (Fig 1). A chest volume (volume 2) was obtained by setting the midpoint at the level of the heart but not making an attempt to obtain any precise cardiac view (Fig 2). The abdominal volume (volume 3) was obtained with the middle of the sweep fixed at the level of the cord insertion, just above the fetal bladder. These three volumes were obtained with the fetus in a transverse orientation, preferably lying on its left or right side. Volume 4 was the face acquisition, which was obtained coronally, with the midpoint of the acquisition in front of the fetus, at the level of the fetal nose. The 5th volume was obtained to include the lower extremities in cross section and was obtained coronally with the midpoint just ventral to the fetal bladder. If the fetus was moving during the acquisition of a volume, acquisition was canceled and restarted.
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Figure 1: Multiplanar display of the first 3D US volume shows the fetal head in three orientations at right angles to each other. The planes are interactive and permit the display of any plane within the volume.
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Figure 2: Multiplanar display of the second 3D US volume shows the fetal chest in three orientations at right angles to each other. The planes are interactive and permit the display of any plane within the volume, including all views of the heart.
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These volumes were saved on the hard drive of the US unit and later downloaded onto compact disks. All 2D and 3D US scanning (Voluson 730; GE Medical Systems, Milwaukee, Wis) was performed with a 4–7-MHz 3D volume transducer. Some of our US machines default at an 85° angle of volume acquisition and others at a 65° angle; therefore, our data were composed of a mixture of volumes obtained by using two different angles of volume acquisition.
Data Acquisition and Comparisons
The actual scanning time, from the beginning to the end of obtaining the 3D volumes, was documented on the clock on the US scanner. The time required to complete the anatomic survey examination by using standard 2D US was similarly documented. The time included both the sonographers' time and the sonologist's time but not the intervening wait between the two practitioners.
The three sonologists independently reviewed the compact disks that contained the five US volumes for each patient. Each of these three physicians (physicians A, B, and C) timed him- or herself in reconstructing the five volumes and performing a complete anatomic survey off line that included measuring the BPD and femur length. The physicians were blinded to the original 2D US findings. The three physicians each had approximately 5 years of 3D US experience, although for the first 3 years that experience was only limited. Over the previous 1 years, 3D scanning had become part of our US scanning protocol, and 3D scanning was available on all of our equipment. One physician (B.R.B.) had more experience than did the other two physicians in regard to volume manipulation on the off-line review station. The other two physicians underwent a 10-minute tutorial on how to use the off-line 3D program to evaluate the volumes and then reviewed the data from the 50 patients in this study without additional instruction.
The time data and original reports from the 2D US examination were extracted from our picture archiving and communication system after all the 3D data had been analyzed. The 3D volume scanning was compared with the 2D examination (reference standard) for each fetus to determine whether 3D off-line review of the volumes allowed identification of all the specific anatomic landmarks in the American Institute of Ultrasound in Medicine guidelines. Comparisons were made among the three physicians regarding the completeness of the survey of these anatomic landmarks and regarding the 3D US and standard 2D US scan depiction of abnormalities. The 3D reconstruction times needed by the three physicians were also compared.
Statistical Analysis
All analyses were performed by using SAS software (version 9.3, 2004; SAS Institute, Cary, NC). We analyzed the following categorical statistical elements by using the 
2 test: (a) the comparison of anatomy seen by the three physicians and (b) the comparison of the number of 3D measurements for BPD and femur length that were within 1 mm of the 2D measurement. The paired t test was used in the comparison of the BPD, femur length, and performance times between the 3D measurements and the 2D measurement. The t test was used to compare the fetal anatomy by volume angle. Differences were considered to be significant when the P value was less than .05. We also performed pairwise 
tests for agreement between the physicians in all three physician combinations to compare their results on femur length and BPD measurements, as well as on the number of items missed on the 3D volumes.
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RESULTS
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Time
The mean time to perform the 2D scanning was 19.6 minutes, whereas the mean time to perform acquisition of the five 3D volumes was 1.8 minutes. With the 3D volumes, the mean times needed to perform the off-line survey and interpretation and measure the BPD and femur were as follows: 5.53 minutes for physician A, 4.79 minutes for physician B, and 5.34 minutes for physician C (Table 1). Adding the mean time for the acquisition of the five volumes to each of these times resulted in a mean of 7.33, 6.59, and 7.14 minutes for physicians A, B, and C, respectively, for the entire 3D evaluation. The entire 3D volume acquisition (which took under 2 minutes) and off-line interpretation took only slightly more than one-third of the time to perform than did the entire examination with traditional 2D US. The total time saved for performing the surveys on the entire set of 50 fetuses was 10.3 hours for physician A, 10.8 hours for physician B, and 10.4 hours for physician C.
Anatomy
Since three sonologist physicians were each evaluating the presence or absence of anatomic landmarks in 50 fetuses, the total number of findings for each landmark was 150 (Table 2, Figs 3–13). The 2D surveys had been reported as complete. The frequency with which each of the anatomic landmarks was identified was at least 94%, with the exception of the fetal arms and cavum septum pellucidum. For further analysis, these anatomic landmarks were assembled into four major groups—head, heart, extremities, and abdomen. The heart views were completely seen 88% of the time, the head views and extremities were completely seen 90% of the time, and the abdominal views were completely seen 95% of the time.
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Figure 10: Multiplanar display of the third 3D US volume shows the abdomen in three orientations at right angles to each other. The planes are interactive and permit the display of any plane within the volume.
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There was no statistically significant difference between physicians A, B, and C regarding the completeness of the survey by using the 3D construction of volumes: All anatomic landmarks were seen in 68% of fetuses by physician A, in 70% by physician B, and in 66% by physician C. Two or more anatomic landmarks were missing in 18%, 16%, and 12% of the surveys performed by physicians A, B, and C, respectively (Table 3). There were abnormal findings in five of the 50 fetuses at standard 2D US (Table 4). One fetus had multiple anomalies, which included a heart defect, two-vessel cord, and unilateral renal agenesis. Images in this fetus were identified as abnormal by all three physicians. All three noted the cardiac defect and two-vessel cord but not the unilateral renal agenesis. Another fetus had choroid plexus cysts, which were identified by all three physicians. Three fetuses were reported to have echogenic intracardiac foci at 2D US; the foci were seen on the 3D scans in all three fetuses by physicians B and C and in two of the three fetuses by physician A.
Measurements
The percentages of 3D BPD measurements that were within 1 mm of the 2D BPD measurements were 80% (40 cases), 68% (34 cases), and 72% (36 cases) for physicians A, B, and C, respectively (Table 5). Overall, 74% of the 3D BPD measurements were within 1 mm of the 2D measurements (P = .5). Similarly, the percentages of 3D femur measurements that were within 1 mm of the 2D femur measurements were 74% (37 cases), 60% (30 cases), and 58% (29 cases) for physicians A, B, and C, respectively. Overall, 64% of the 3D femur measurements were within 1 mm of the 2D measurements (P = .2). Curves (Figs 14, 15) of the BPD differences and femur length differences between 3D and 2D US scans for each of the physicians were not believed to be clinically meaningful.
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Figure 14: Graph of BPD measurement by the three physicians (MD-A, MD-B, MD-C) illustrates the difference between 2D and 3D measurements for each physician. The y-axis is the number (N) of fetuses, and the x-axis is the difference between 2D and 3D measurements.
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Figure 15: Graph of femur length measurement by the three physicians (MD-A, MD-B, MD-C) illustrates the difference between 2D and 3D measurements for each physician. The y-axis is the number (N) of fetuses, and the x-axis is the difference between 2D and 3D measurements.
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The results of the pairwise tests for agreement were determined between the physicians in all three physician combinations to compare their results on femur length and BPD (Table 5) and number of items missed on 3D US volumes (Table 2); the results showed statistically significant agreement between all combinations for all of these comparisons, with the exception of one comparison that was borderline (P = .06) between two of the physicians regarding the number of items missed.
Volume Angle
As previously noted, some of our US machines default to 85° while others default to 65° to obtain the volumes (Table 6). Therefore, some of the fetuses were imaged with an 85° volume setting and others were imaged with a 65° setting. In fact, 32 of 50 fetuses were imaged by using an 85° setting, whereas the other 18 fetuses were imaged by using a 65° setting. This gave us the opportunity to compare the ability to see the anatomy by using 85° versus 65° volume angles. Volumes acquired at an 85° angle always showed more anatomic landmarks per volume than did those acquired by using a 65° angle. The face volume was the only one of the five volumes for which this difference was significant (P = .02). The survey was incomplete for one of the three physicians in 25% of the studies obtained with an 85° angle compared with 33% of the studies obtained with a 65° angle (P = .5). A comparison of the numbers of volumes that were unnecessary in the completion of the survey (Table 6) indicated that in 78% (25 of 32) of the studies obtained by using the 85° angle compared with 50% (nine of 18) of the studies obtained by using the 65° angle, not all five volumes were needed.
There is an extensive overlap between the anatomy visible with the five volumes (Fig 16). This is particularly apparent on the chest and abdominal volumes. The degree of overlap was seen more often by using the 85° volume than the 65° volume acquisition. In fact, the 85° volume acquisitions afforded more redundancy in all of the anatomy visible. We could not determine which volume might be consistently eliminated, as there was variation from case to case.
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Figure 16: Graph shows distribution of anatomic parts seen with each of the five volume sets for the 50 fetuses. Note the redundancy between the volumes—an anatomic part such as the stomach bubble can be seen on both the chest volume and the abdominal volume.
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DISCUSSION
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The recent introduction of 3D US imaging into mainstream clinical practice has been focused on surface rendering with minimal focus on the structural evaluation of the fetus. With current 2D technology, the quality of the examination is largely based on the skill and experience of the person obtaining the images rather than on the physician interpreting the scans, unless the physician performs his or her own additional imaging (double scanning). If an image acquisition is omitted in a 2D US examination, the patient must return for a repeat US examination, as there is no permanent record of the entire survey. Three-dimensional volume US as described herein depends far less on the operator and introduces new flexibility to reconstruct volumes in any plane, regardless of the acquisition plane. This approach allows the physician interpreting the scan to review the entire volume, as though he or she was scanning the patient directly, and to assess areas that the sonographer might not have specifically recognized and recorded as an area of interest. Similarly, if a physician or patient desires a second opinion, the volume can be evaluated by a second practitioner without rescanning the patient. Volume US, therefore, permits US to achieve the efficiency and flexibility inaccessible by 2D US methods of acquisition and also allows for multiplanar reconstruction.
We have demonstrated the ability to perform a complete anatomic survey by using 3D volume US in less than 2 minutes. If screening US was performed by using the 3D technique in our study, the time set aside to perform US and interpret scans would be decreased by almost two-thirds, and the turnover of US examination rooms would be able to increase proportionately. All three physicians, who interpreted all 50 fetuses independently from each other, demonstrated that their times to reconstruct the images were within 1 minute of each other.
The repetitive motion injuries that have plagued obstetrics and gynecology sonographers for several decades could be alleviated with 3D volume US, as the sonographers would no longer need to spend hours a day holding and pressing the probe on the patients' abdomens to produce one image at a time. Those sonographers who are knowledgeable in fetal anatomy could also become responsible for the off-line reconstruction of the images. This would allow sonographers to perform various tasks during the day and limit musculoskeletal motion injuries (7).
Because the angles of the acquisitions varied between 85° and 65° in our study, we had the opportunity to evaluate the differences in our ability to see the anatomy by using the two different protocols. It is clear that the wider angle allowed a greater amount of anatomy to be viewed. Moreover, incomplete surveys were slightly more common among the fetuses imaged at 65° compared with those imaged at 85°. Among the fetuses imaged at 85°, there was a particular redundancy between the chest and abdominal volumes, which indicated that a future study may demonstrate that these can be compressed into one volume.
Other studies described in the literature have been focused on demonstrating the benefit of 3D US as an adjunct to the basic 2D US examination (1–3,8,9). Our study explored the concept that 3D US (sonographic tomography) can be used in lieu of 2D US and can be performed in a manner similar to contemporary CT and MR cross-sectional imaging. A small pilot study was initially performed by our group to explore the feasibility of performing structural surveys by using only 3D US volume imaging (5). We showed a dramatic reduction in the time needed to perform imaging and interpret a scan with 3D US in comparison with standard 2D US. Our current study expands the concept of using 3D US exclusively in a large US practice performing fetal structural surveys. Our data demonstrate that a group of eight sonographers and three physicians can perform structural fetal surveys by using 3D volume imaging in consecutive patients in one-third of the time it takes to obtain and interpret a traditional 2D US scan. The current study further affirms our ability to perform the examinations in less than 2 minutes of actual scanning time and validates the concept that fetal US screening could be far more automated, standardized, and efficient than it is with current traditional 2D US. Nelson et al (10) described the feasibility of obtaining 3D volumes and sending these volumes to a remote location to perform a virtual examination of a patient. While results of the study by Nelson et al did show that 3D US in general can provide volumes that can be evaluated at a different location, Nelson et al did not furnish information regarding the actual time involved in obtaining the scans that way.
The limitations of our study include the inability to evaluate fetal activity and behavior without real-time scanning. The goal of our approach is to produce US images that can allow us to perform the anatomic survey. In addition to the time required to acquire several 3D volumes, it might be necessary to perform a short, real-time scan to evaluate fetal activity, as well as to provide the patient some satisfaction of actually seeing the fetus move. The imaging of the heart also may require obtaining an additional real-time acquisition (a few seconds of acquisition time) to evaluate the rhythm. This was not done in our study. Another limitation is that the same sonographer who obtained the 2D study also obtained the 3D volumes to be reviewed by the physicians. Viewing the fetus before acquiring the 3D volumes may have made it slightly easier to obtain the volumes.
Another limitation is the reduced resolution of the reconstructed planes by using 3D volume scanning in comparison with the 2D acquisition planes. Three-dimensional technology is in its infancy. Matrix array techniques may become available soon, so as to improve the resolution available in any reconstructed planes. In a few years, the resolution of the reconstruction plane may no longer depend on the plane of acquisition, and the imaging display may become independent from the 2D scanning plane we currently use. As the technology and resolution improve so will our ability to utilize it effectively.
While 3D reconstruction from the structural survey was not as reliable as was standard 2D scanning in obtaining all of the necessary anatomic landmarks, the survey was complete in more than 90% of the patients by using 3D reconstruction. The 3D volume technique described here, therefore, is suggested as a method of screening rather than as a way to evaluate the high-risk patients at this time. One or two of the anatomic landmarks may be incompletely seen in 5%–10% of fetuses by using this technique. Nevertheless, among the 50 fetuses in this study, all three physicians correctly identified the one fetus with major anomalies, although one of the anomalies (unilateral renal agenesis) was missed on 3D reconstruction images. The BPD and femur were accurately measured off-line and, in 60%–80% of the patients, were measured within 1 mm of the original 2D measurement. These differences in measurements are not considered to be clinically meaningful.
Our study demonstrates that, in a sample of 50 consecutive patients between 17 and 21 weeks of gestation presenting for a standard fetal anatomic survey evaluation, the amount of time on the US examination table could be reduced to less than 2 minutes. The entire scanning and image interpretation time could be reduced to 6–7 minutes, from a mean of 19 minutes for standard 2D US. This would indicate a time savings of more than 10 hours in obtaining and interpreting 50 fetal sonograms. Adoption of this approach should bring US into the era of volume imaging, with all of the consequent additional benefits. Such a 3D US approach should enable more flexibility, less user dependence, and greater efficiency. A larger scale study will be needed to further evaluate the possibility that 3D volume US could eventually replace 2D fetal US for routine anatomic surveys.
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ADVANCE IN KNOWLEDGE
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- Three-dimensional volume US is faster, more automated, and less operator dependent than 2D US for anatomic surveys at 17–21 weeks of gestation.
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ACKNOWLEDGMENTS
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We are grateful to Amy Cohen, BS, for her valuable help with the statistics in this study.
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FOOTNOTES
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Abbreviations: BPD = biparietal diameter • 3D = three-dimensional • 2D = two-dimensional
Authors stated no financial relationship to disclose.
Author contributions: Guarantors of integrity of entire study, B.R.B., T.D.S., B.B.; study concepts/study design or data acquisition or data analysis/interpretation, B.R.B., T.D.S., B.B.; manuscript drafting or manuscript revision for important intellectual content, B.R.B., T.D.S., B.B.; approval of final version of submitted manuscript, B.R.B., T.D.S., B.B.; literature research, B.R.B.; clinical studies, B.R.B., T.D.S., B.B.; statistical analysis, T.D.S.; and manuscript editing, B.R.B., T.D.S., B.B.
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References
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- American Institute of Ultrasound in Medicine. AIUM practice guide for the performance of antepartum obstetrical ultrasound examination. Laurel, Md: American Institute of Ultrasound in Medicine, 2003.
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TOP
ABSTRACT
INTRODUCTION
