Duckelmann 3D Ultrasound in Evaluating the Fetus Prenat Diagn 2010

PRENATAL DIAGNOSISPrenat Diagn 2010; 30: 631–638.Published online in Wiley InterScience(www.interscience.wiley.com) DOI: 10.1002/pd.2561

30th Anniversary Issue of Prenatal Diagnosis

REVIEW OF CURRENT PRACTICE

Three-dimensional ultrasound in evaluating the fetus

Anna M. Duckelmann and Karim D. Kalache*Department of Obstetrics, Campus Charite Mitte, Charite University Hospital, Berlin, Germany

In recent years three-dimensional (3D) ultrasound has made a place in clinical practice and has become amajor field of research in obstetrics. In this article we will review the diagnostic performance of the mostwidely used 3D ultrasound applications in the assessment of fetal anomalies, explain the technique to gaincorrect 3D images and offer some practical advice for their efficient use. Examples are given to demonstratethe applicability and vividness of 3D in daily routine. Copyright 2010 John Wiley & Sons, Ltd.

KEY WORDS: three-dimensional ultrasound; fetal imaging; ultrasonography; prenatal diagnosis

INTRODUCTION

In recent years, the field of prenatal diagnosis hasbeen inundated with three-dimensional (3D) ultrasoundimaging tools for diagnosis in obstetrics. The currentliterature is extensive and filled with articles addressingthe application of 3D ultrasound to virtually everyaspect of fetal imaging (Goncalves et al., 2005). Theadvantages of 3D outlined here include the enhancedidentification of the nature, size and location of certainfetal defects (Merz et al., 1995a,b; Platt et al., 1998;Baba et al., 1999; Dyson et al., 2000; Xu et al., 2002);the precise measurement of the volumes of organswith irregular shapes (Kalache et al., 2003b; Ruanoet al., 2005); visualizing structures in reconstructedplanes (Kalache et al., 2006a,b); imaging of the fetalskeleton (Benoit, 2003); spatial presentation of bloodflow arborization and vessels (Chaoui and Kalache,2001; Kalache et al., 2003a; Lee et al., 2003b); theability to reconstruct a 3D rendered image of thefetal heart that contains depth and volume which mayprovide additional information that is not availablefrom two-dimensional (2D) ultrasound images (DeVoreet al., 2003); the storage and retrospective analysis (Leeet al., 2003a; Bergann et al., 2006) and exchange ofdata that can be used for second opinions (Nelsonet al., 2001; Vinals et al., 2005); and the facilitationof maternal–fetal bonding (Ji et al., 2005). Moreover,a study on the perception of non-pregnant sonographers,sonologists and undergraduate students on the use of3D ultrasound technology in fetal medicine showedthat both caregiver and laypersons believe that 3Dultrasound will play a role in the future, for medicalindications and in reassuring patients who are carrying

*Correspondence to: Karim D. Kalache, Department of Obstet-rics, Campus Charite Mitte, Charite University Hospital,Chariteplatz 1, 10117 Berlin, Germany.E-mail: [email protected]

normal fetuses (Lee et al., 2007). According to a recentstudy, 3D ultrasound is a time-saving method allowingcost-effective use of equipment and sonographer timeyielding an equally accurate anatomic examination ofthe second-trimester fetus in half the time required fora 2D survey (Benacerraf et al., 2005).

It remains difficult to understand, however, whetherthe additional diagnostic information gained from 3Dultrasound is clinically relevant and has a positiveimpact on improved patient care. Despite the fact thatlarge prospective studies on its clinical importance andaccuracy are lacking, 3D ultrasound has made a placein clinical practice and has become a major field ofresearch in obstetrics. The main reason is that thetechnology is now cheap, user-friendly and widelyavailable. This is partly related to rapid technologicalimprovements implemented at the end of the 1990s. Inthis article we will review the diagnostic performance ofthe most widely used 3D ultrasound applications in theassessment of fetal anomalies and offer some practicaladvice for their efficient use.

3D ULTRASOUND METHODS

For 3D ultrasound, a set of consecutive 2D ultrasoundslices at a preset angle are acquired using dedicatedmechanical volume probes. Upon activating the 3Dmodus, a render box appears on the screen that allowsselection of the scanned volume. The render box maybe modified regarding position and size (height, widthand depth). The speed of the acquisition of a 3Dimage depends on the position, height and width of therender box. There are generally three or four options forvolume resolution. We suggest choosing, on principle,the highest resolution.

To minimize artifacts that occur with movement,we ask our patients to hold their breath during theacquisition of volumes. It may happen of course that

Copyright 2010 John Wiley & Sons, Ltd. Received: 22 February 2010Revised: 27 April 2010

Accepted: 27 April 2010

632 A. M. DUCKELMANN AND K. D. KALACHE

the acquisition of a high-quality image is impossibledue to a very active fetus. The acquired volume canbe displayed either in three perpendicular planes thatare displayed simultaneously on the screen (multiplanarmode) or as a rendered image through the application ofvarious algorithms.

The multiplanar mode allows exact orientation by syn-chronous viewing of the longitudinal, transverse andcoronal planes. Each of these three planes can be rotatedaround the x , y and z axes. It is also possible to betterunderstand the spatial relationship of complex anatomi-cal structures by moving a cursor representing the com-mon intersection point referencing the three multiplanarimages to each other in each of these planes. Basically,any ultrasound section can be obtained from the 3Dblock, and clinical applications as an adjunct to 2D ultra-sound are innumerable. However, it is important to knowthat every deviation from the initial acquisition planeis associated with a loss of image quality. The experi-enced examiner will try to start from an optimal initialplane requiring minimal adjustments once the volume isacquired. Another very important issue is that the sameartifacts related to acoustic shadow may occur with 3Dultrasound as with 2D scanning. Yet, 3D ultrasound isoperator dependent, and factors such as fetal position andoverlaying bone can limit the examination. Thus, spe-cific acquisition techniques should be used for differentregions of interest avoiding the disadvantages inherent inthe two techniques. Most commercially available ultra-sound systems offer two rendering modes: the surface(skin) and the maximum (skeletal) rendering modes. Inthe surface mode, the limits between the surface of thefetal body and the amniotic fluid are scanned, and asculpture-like representation of the fetus is obtained.The viewing direction in the 3D scan is shown by arender line. After that, the region of interest is fixed.Thus, the render line disappears and the volume can beworked on with any desired method (by zoom, rotationor electronic scalpel). The image can then be rotatedin any direction, offering a perspective from differentangles. In the surface mode it is necessary to havea depot of amniotic fluid around the examined struc-ture. Structures that occlude the region of interest canbe removed using the electronic scalpel function whilerotating the volume around its three axes. Optimal resultsare achieved when these structures do not lie directly onthe region of interest, and they do not throw shadowsonto it.

The maximum rendering mode, which highlightsbony structures, has also great potential for imagingcranial sutures. Again, it is important to know thatevery deviation of the render line from its initialposition causes a loss of image quality. The well-trained sonographer is able to obtain an optimal initialsetup without further need to move the render line.Disturbances, like particles in the amniotic fluid, canbe removed with the use of a threshold.

In addition to static 3D ultrasound, it is possible toperform updates at a frame rate of up to 25 volumes persecond to obtain the impression of a live 3D ultrasound(also known as 4D ultrasound). This results in a moviethat allows the real-time observation of fetal movements

and other dynamic processes. The advantage of real-time3D scanning is the ability to get a quick idea of expectedresults while scanning. It is also possible to set up andadjust the gain while acquiring the volumes. This allowsthe sonographer to react immediately and optimally tochanges in fetal position. However, there is a trade-offin imaging quality in real time compared to static modesof 3D ultrasound. In our experience, it is advisable tostart with real-time 3D ultrasound and then continue withstatic 3D ultrasound under good conditions (visibility,position).

EVIDENCE-BASED ROLE OF 3D ULTRASOUNDIN EVALUATING THE FETUS

The authors of a recent study from Germany concludedthat 3D ultrasound is not only a useful tool in appreci-ating the severity of a fetal defect, but has also a betterspecificity in regard to the confirmation of normalitythan conventional 2D ultrasound in cases with increasedrisk of a recurrent surface malformation (Merz and Wel-ter, 2005). However, in this study on the accuracy of3D ultrasound in prenatal diagnosis, like in many others,the 3D examiner was not blinded to the 2D ultrasoundexamination. Another study from the NIH PerinatologyResearch Branch in Detroit, USA compared the abil-ity of 2D and 3D ultrasound to diagnose congenitalmalformations (Goncalves et al., 2006b). In this study,the examiner began with 3D ultrasound and added 2Dultrasound only later. In 91% of the cases, there wasagreement between the two techniques. The authors con-cluded that both the techniques are interchangeable forscreening for fetal anomalies in the second trimester.However, according to another study, 3D ultrasound asa primary examination was insufficient to study fetusesat high risk for anomalies (Benacerraf, 2006). Even for2D ultrasound there is a wide range of reported detec-tion rates, which is dependent on the type of anomaly,gestational age at time of the study, the skill of thesonographer and whether the population is at high orlow risk for congenital anomalies (Li et al., 1988; Leviet al., 1989; Lys et al., 1989; Saari-Kemppainen et al.,1990; Chitty et al., 1991; Shirley et al., 1992; Ewigmanet al., 1993; LeFevre et al., 1993; Crane et al., 1994;VanDorsten et al., 1998; Vintzileos et al., 2000)

SPECIFIC APPLICATIONS OF 3D ULTRASOUND

First trimester

The small size of the fetus in the first trimester allowsit to be encompassed in a single 3D ultrasound sweep.Furthermore, amniotic fluid is invariably present in thefirst trimester, allowing the obtention of a surface-rendered 3D ultrasound mode reconstruction without thedifficulties inherent to the second and third trimesters.Additionally, the visualization of structure within thevolume is good, with minimal acoustic shadows fromthe bones. It has been shown that by employing a single

Copyright 2010 John Wiley & Sons, Ltd. Prenat Diagn 2010; 30: 631–638.DOI: 10.1002/pd

3D ULTRASOUND IN EVALUATING THE FETUS 633

A B C D

Figure 1—Sirenomelia in an 11-week-old fetus (D). A single lower limb is obvious on surface-rendered 3D images (B, C), whereas it wasunrecognizable on the 2D ultrasound image (A). Bilateral radial aplasia in this case was suspected on real-time 3D ultrasound and confirmed inthe postmortem examination

A B C D

Figure 2—Megavesica from an urethral atresia in a 10-week-old fetus (D, ultrasound 2D image: A). On surface-rendered 3D images the fetuswas found to have bilateral lower limb amputation (B, C)

transabdominal sweep beginning from a mid-sagittalplane of the fetus with 3D ultrasound during a regularnuchal translucency (NT) screening examination at 11to 13 weeks 6 days of gestation, a volume dataset couldbe acquired that allows appropriate views of the fetusfor evaluation of both anatomy and NT in the vastmajority of cases (Fauchon et al., 2008). Another recentstudy showed that the first-trimester 3D ultrasound wasefficient for assessment of the head, abdominal wall,stomach, limbs and vertebral alignment (Bhaduri et al.,2010). However, it was less effective in evaluatingthe heart and excluding spinal defects. Figures 1 and 2show two examples of anomalies identified in the firsttrimester by 3D ultrasound.

Imaging of the fetal face

Congenital facial dysmorphic feature can be detectedin prenatal 2D scans. Although usually easily suspectedwith conventional 2D ultrasound, 3D ultrasound hasthe potential to visualize several structures in the sameimage, thus improving the comprehension of spatial rela-tionship and recognition of abnormal features. Abnor-malities that can be most reliably diagnosed by 3Dultrasound include distinctive facies such as microg-nathia as part of the spectrum of genetic disorders

(Figure 3), tumors such as cervical teratomas extend-ing to the face (Figure 4), facial clefts and markers oftrisomy 21 (Lee et al., 2003a; Bergann et al., 2006).Diagnosis of abnormalities of the hard and soft sec-ondary palate is amenable to prenatal diagnosis bymeans of 3D ultrasound (Benacerraf et al., 2006; Faureet al., 2007a). Several techniques have been developedto explore these structures including the ‘reverse-face’view (Campbell et al., 2005), the ‘flipped-face’ view(Platt et al., 2006) as well as other methods derived fromthese techniques (Faure et al., 2007b, Pilu and Segata,2007; Ten et al., 2009). Accurate visualization of thepalate, however, requires volumes in which the head isslightly deflected during acquisition. Furthermore, betterresults are obtained when those volumes are obtainedduring fetal swallowing with a rim of fluid between thefetal tongue and palate.

Fetal skeleton

The use of 3D ultrasound has proved to be useful in theassessment of limb extremities malformation especiallyin case of position anomalies and flexion deformity ofthe fingers (Figure 5). 2D ultrasound plays a major rolein prenatal diagnosis of major anomalies of the fetalskeletal system. However, small neural tube defects are



Figure 3—3D ultrasound images of a fetal face at 21 weeks’ gestation suggestive of a micrognathia

A B C

Figure 4—2D ultrasound and surface-rendered 3D ultrasound images of a large neck teratoma in a 26-week fetus (A). 2D ultrasound axial imagesdemonstrate the facial mass (arrow). It is, however, easier to appreciate the degree of facial involvement from surface-rendered 3D ultrasoundimages (B, C)

A B

Figure 5—2D ultrasound images suggesting that the 19-week-old fetus is affected with hand flexion deformities (A). The surface-rendered 3Dultrasound images assisted in the prenatal diagnosis of camptodactyly (B)

sometimes difficult to visualize (Figure 6). 3D ultra-sound localizes fetal neural tube defects with more accu-racy and helps in demonstrating the extent of neural tubedefects (Lee et al., 2002). Furthermore, 3D ultrasoundhas been applied to diagnose rib anomalies (Esser et al.,2006) and abnormal cranial sutures (Esser et al., 2005).Cranial bones may also be displayed, allowing the con-firmation of a small encephalocele (Figure 7). In someinstances, 3D ultrasound will provide a clearer image of

the fetus allowing the examiner to understand an abnor-mal spine curvature (Figure 8).

Neurosonography

3D ultrasound technology has been intensely appliedto study the fetal central nervous system (Monteagudoet al., 2000; Pilu et al., 2007; Monteagudo and Timor-Tritsch, 2009). The mid-sagittal view is the most



A B C

Figure 6—2D ultrasound (A) of a pathologic spine at 19 weeks (C). Abnormally splayed posterior elements (arrow) are easily appreciated on3D maximum-rendered image at the level of the defect (first lumbar vertebra) (B). Note the localization of last thoracic body on the renderedimage as indicated by the 12th rib

A B C

Figure 7—2D ultrasound image of the fetal skull in a 21-week fetus suggesting a small occipital encephalocele (A). The 3D maximum-renderedimage clearly displays the bony defect (arrow) below the posterior fontanel (B). Occipital bone with sagittal and lambdoidal sutures in a normalfetus (C)

A B

Figure 8—Conventional 2D ultrasound view of a fetus at 18 weeks’ gestation suggesting hyperextension of the fetal head (A). The 3Dmaximum-rendered image shows that there is an extreme extension of the cervical spine (B)



Figure 9—Multiplanar display of a 3D sonographic dataset of a normal fetal brain at 26 weeks with the three mutually related orthogonal planesat 90◦ to one another: (A) the sagittal plane; (B) the coronal plane and (C) the axial plane. Thick slice rendering (green box) may be used forenhanced soft tissue display. The corpus callosum (open arrow) as well as the vermis cerebelli (closed arrow) is better visualized in the resultantlower right image (D)

important complement to the three standard axial viewsthat are required during a routine 2D examination ofthe central nervous system. However, obtaining the cor-rect plane using conventional 2D ultrasound may bechallenging. Fetal brain imaging takes maximum advan-tages of 3D ultrasound capabilities to look at midlinebrain structures by allowing the physician to orient thefetal brain in any direction. The main advantage of 3Dultrasound is the easy obtention of a true sagittal view,allowing detailed investigation of the corpus callosumand the posterior fossa. However, the best results areobtained when the volume is acquired either through thefrontal suture or the anterior fontanelle. Thick slice 3Dultrasound rendering is able to demonstrate more detailsthan conventional 2D ultrasound through the superim-position of several layers of tissue (Figure 9).

Spatio-temporal image correlation

Another 3D/4D technique that is taking long stepsinto the future of routine use is 4D fetal echocardio-graphy. This new technique relies on spatio-temporalimage correlation (STIC), which is an indirect, motion-gated, offline scanning mode. Once a volume is acquiredthe information can be used to display multiplanarimages that allow the visualization of any given planewithin the heart. The information in the volume canalso be used to reconstruct a rendered image of anexaminer-defined region of interest. Some of the ren-dering modes that are useful for visualizing the heartinclude surface mode, minimum mode, inversion modeand glass body mode in combination with color or powerDoppler. 3D fetal echocardiography with STIC allows anaccurate prenatal characterization of aortic arch abnor-malities to a degree that was typically only attain-able previously with postpartum imaging (Goncalveset al., 2006a). However, the technique when used by

general obstetricians was found to be marginally clin-ically effective when compared to 2D fetal echocar-diography scanning by experts (Wanitpongpan et al.,2008). STIC offers the opportunity to reconstruct diverseplanes, but cannot be used as a tool to expand afetal cardiac screening program (Wanitpongpan et al.,2008).

CONCLUSION

In the last years, the use of 3D ultrasound has extendedgreatly and provides additional information in selectedindications. The main advantage is the possibility ofobtaining an infinite number of different scanning planesstarting from a single volume acquisition. Although 3Dultrasound allows several alternative viewing modalities,the extent to which a given structure can be demon-strated in a given reconstructed section is entirely depen-dent on the quality of the initial 2D image as well ason fetal position. Thus, expertise is not only mandatoryduring the manipulation and interpretation processes butalso while acquiring the volumes. At the moment thetechnique is always used as a complementary tool to the2D ultrasound examination that still remains the goldstandard to detect congenital anomalies.

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Duckelmann 3D Ultrasound in Evaluating the Fetus Prenat Diagn 2010

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