Ir J Med Sci DOI 10.1007/s11845-014-1184-2

ORIGINAL ARTICLE

The place of four-dimensional ultrasound in evaluating fetal anomalies ¨ cal • T. Nas • I˙. Gu¨ler D. F. O

Received: 28 October 2013 / Accepted: 6 August 2014 Ó Royal Academy of Medicine in Ireland 2014

Abstract Objective To analyze the capability of four-dimensional surface rendering mode ultrasound (4D SRM USG) in the detection of fetal abnormalities, and also compare it with 2D USG. Materials and methods A total of 1,379 pregnant women were enrolled in the study, and they all underwent 2D USG screening. In the same session, they were all subsequently screened using 4D USG. The findings of both methods were compared. Results A total of 194 fetal anomalies were detected in 176 of 1,379 pregnant women by 2D USG. When all cases, including superficial and non-superficial anomalies, were evaluated together, we found that 2D USG was significantly better than 4D SRM USG in detecting anomalies (p \ 0.001). However, 4D SRM USG was superior to 2D USG in terms of image quality, clarity, the distinction between the surrounding structures, and intelligibility among the cases with a superficial anomaly (p \ 0.005). Conclusion 4D USG is superior to 2D USG in detecting malformations related to fetus face, spine, extremities, abdominal wall, and the body surface. However, 4D SRM USG detected only approximately half of the cases with anomalies, and showed a better quality of image in only 15 % of all cases. Therefore, 4D SRM USG may only be suitable for use as a complementary tool in the evaluation

¨ cal (&) D. F. O Dr. Sami Ulus Women Health and Research Hospital, Ankara, Turkey e-mail: [email protected] T. Nas  I˙. Gu¨ler Department of Obstetrics and Gynecology, Faculty of Medicine, Gazi University, Ankara, Turkey

of fetal anomalies, especially those of the face, spine, extremity, and abdominal wall. Keywords

4D ultrasound  Fetus  Anomaly  Prenatal

Introduction Ultrasonography (USG) has been used to detect fetal anomalies for medical diagnosis and treatment for over 40 years. It was initially introduced by Donald in 1961 at the time he determined fetal hydrocephalus [1]. After the 1970s, USG has been the main method used for detecting fetal malformations, and traditional two-dimensional (2D) ultrasound has been used for this purpose for many years [2]. However, there remains a need to evolve the capability to detect fetal malformations. On the basis of this demand, three dimensional (3D) and four-dimensional (4D) USG have been developed, and these possess advanced imaging and storage capabilities. Therefore, could this modern imaging technology help in clearly and correctly diagnosing major malformations from the beginning of pregnancy through until birth? The currently available literature lacks confirmatory studies, and consists of a small series of articles and case reports. In this study, we aimed to analyze the capability of 4D surface rendering mode (SRM) USG in the detection of fetal abnormalities, and to compare 4D SRM with 2D USG.

Materials and methods A total of 1,379 pregnant women who attended the Faculty of Medicine Department of Obstetrics and Gynecology, Gazi University, Turkey, between December 2007 and

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2009, enrolled in the study, and underwent a routine anomaly scan, regardless of obstetric history. Of these 1,379 women, the majorities were of between 16 and 28 gestational weeks; however, 35 of these women were known to have fetal anomalies, and were outside of the gestational timeframe. The ultrasonographer was blind to the previous history of the study participants, so he was unaware of who did and did not have a fetal anomaly at the time of screening. The study was approved by the ethics committee of the Gazi University Faculty of Medicine, and we obtained the written informed consent from all participants before the procedure. All USG images were obtained using a Philips HD 11 XE ultrasound device, and a C5-2 Curved Linear Array 2.0–5.0 MHz probe was used for 2D imaging. A V6-2 broadband volume curved ultrasound transducer of 2–6 MHz was used for 4D imaging. One perinatologist with 4 years’ experience of using 3D/4D ultrasound performed all of the examinations. The mean duration of each examination was 22 min (20–35 min). In addition, no time limit was predetermined for performing the anomaly scan. First, all pregnant women underwent 2D USG screening, via the use of a C5-2 Curved Linear Array Probe. All the fetal parts were screened, beginning with the fetal cranium, and the findings were recorded. Following 2D USG examination with a V6-2 broadband volume curved probe, 4D USG was performed in the same way during the same session. First, 2D image was obtained with V6-2 broad band volume curved probe. After creating a field box that was fitted to the area of interest, the volume images were obtained by 4D sonography. 2D and 4D images were initially put side-by-side on the screen, and then a 4D image was obtained on the full screen. The volume data sets of the fetal parts were acquired with the 4D real time option, and acquisition times were under 20 s per cine volume, with scan angles ranging from 30° to 60°. Detected fetal anomalies were stored digitally on a disk, and also in a written document. Of the imaging modalities of 4D-USG, only SRM was used. Detected anomalies were classified into two groups: superficial and non-superficial malformations. Fetal body surface, fetal extremities, and fetal spine anomalies were classified as superficial anomalies. USG visualization quality and the distinction between surrounding structures was evaluated as being ‘‘imaged better’’, ‘‘imaged worse’’, or ‘‘imaged in a similar way’’ for both USG modalities. Detection rates of anomalies found with 2D and 4D SRM USG were compared, and detected anomalies were confirmed during post-mortem or post-natal follow-ups. Furthermore, detection of some of these malformations was endorsed by other diagnostic methods, such as antenatal fetal MRI and echocardiography. Data were analyzed with SPSS for Windows 11.5, and differences of significance between 2D and 4D SRM USG were identified and

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evaluated using the Marginal Homogeneity test. Pearson’s Chi-square was used to assess whether the detection of superficial anomalies showed a significant variation, depending on whether 2D or 4D SRM USG was used. p \ 0.05 was considered statistically significant.

Results Of the 1,379 pregnancies, 1,329 women had single births, 46 had twins, and four had triplets. The mean age of the participants was 29 years (range 17–45), and the mean gestational age was 22 weeks (range 16–28) in women who had an anomaly scan, and 21 weeks (range 12–36.4) in both women who had a known fetal anomaly and women who had an anomaly scan on the basis of their last menstrual period. A total of 194 anomalies in 176 of 1,433 fetuses were detected with 2D USG. These 194 anomalies consisted of 61 (31.4 %) superficial anomalies, and 133 (68.6 %) non-superficial anomalies, and they were all clearly identified with 2D USG; each was confirmed by post-natal or post-mortem findings, or by using the other imaging modalities during the antenatal period. 4D SRM USG detected 84 of the 194 anomalies (43.3 %, p \ 0.01, see Table 1), but did not identify the remaining 110 anomalies. Of the 84 anomalies diagnosed with 4D USG, 54 (88.5 %) were superficial anomalies. When all anomalies were considered, 138 (71.6 %) were better visualized with 2D compared to 4D SRM USG, 31 (15.5 %) were better visualized with 4D SRM USG compared to 2D USG, and 25 (12.9 %) were similarly visualized with both methods (Tables 2, 3). In the 61 cases of superficial anomalies, 31 (49 %) were better visualized with 4D SRM USG, 11 (19.7 %) were better visualized with 2D USG, and 19 (31.1 %) were similarly visualized with both methods. The 2D USG method was superior in detecting both superficial and non-superficial anomalies (p \ 0.001). In the participants with a superficial anomaly, 4D USG was

Table 1 Detection rates of anomalies by 2D USG and 4D USG Nonsuperficial anomalies (%) Anomalies only detected by 2D USG

103 (77.4)

Anomalies only detected by 4D USG Anomalies detected by both 2D and 4D USG

0 (0)

Total 2

v = 74.128; p \ 0.001

Superficial anomalies (%)

All cases (%)

7 (11.5)

110 (56.7)

0 (0)

0 (0)

30 (22.6)

54 (88.5)

84 (43.3)

133 (100.0)

61 (100.0)

194 (100.0)

Ir J Med Sci Table 2 Comparison of 4D USG and 2D USG for assessing of all anomalies Anomaly

2D is better

4D is better

Similar

Table 2 continued Anomaly

2D is better

Total

Similar

1

Total

Diaphragmatic hernia

2

0

0

2

Abnormal flexion deformity foot

Cleft palate

0

1

0

1

Encephalocele

0

0

1

1

Cleft lip Hemivertebra ˙Intracardiac hyperechogenic focus

0 0

2 0

0 1

2 1

Renal agenesis

1

0

0

1

15

0

0

15

Duodenal atresia

2

0

0

2

13

0

0

13

Posterior urethral valve

1

0

0

1

VSD

1

0

0

1

Osteogenesis imperfect

1

0

0

1

Tetralogy of Fallot

1

0

0

1

Total

138

31

25

194

Pleural effusion

0

0

2

2

AVSD

1

0

0

1

Ventriculomegaly

9

0

0

9

Choroid plexus cysts

7

0

0

7

Polyhydramnios

1

0

0

1

Table 3 Comparison the results of 2D USG and 4D USG for assessing of superficial, non-superficial and all anomalies

Cardiomegaly Hypoplastic left heart syndrome

2 2

0 0

0 0

2 2

Non-superficial anomalies

Omphalocele

0

5

0

5

Amniotic sheet

1

0

10

11

Kyphosis

0

4

0

4

Scoliosis

0

4

0

4

Pericardial effusion

0

4D is better

0

1

Polydactyly hand

0

0

2

2

Esophageal atresia

3

0

0

3

Superficial anomalies

All cases

N

133

61

194

2D USG better than 4D USG (%)

127 (95.5)

11 (19.7)

138 (71.6)

2D USG is similar to 4D USG (%)

6 (4.5)

19 (31.1)

25 (12.9)



31 (49.2)

31 (15.5)

CCAM type 1

0

0

2

2

Mesenteric cyst

0

0

1

1

4D USG better than 2D USG (%)

Gastroschisis

0

2

0

2

MH test statistics

-11.269

2.777

-8.385

p

\0.001

0.005

\0.001

Fetal ascites

0

0

1

1

10

0

0

10

Meconium peritonitis Agenesis of corpus callosum

1 2

0 0

0 0

1 2

Low-set ears

0

1

0

1

Hydrocephaly

Hydrops fetalis

1

0

0

1

Galen vein aneurysm

1

0

0

1

Dandy-Walker malformation

2

0

0

1

Large cavum septum pellucidum

1

0

0

1

Cystic hygroma

0

1

0

1

Spina bifida

0

4

3

7

Chorion-amnion separation

5

0

0

5

Hypospadias

0

1

0

1

Anorectal atresia

2

0

0

2

Hyperechogenic bowel Liver calcification

7 4

0 0

0 0

7 4

Pes equinovarus ˙Iniencephaly

2

7

0

9

0

0

1

1

Polycystic kidney Pelvicaliceal dilatation Umbilical cord insertion abnormalities

3

0

0

3

29

0

0

29

3

0

0

3

MH Marginal Homogeneity Test

superior to 2D USG in terms of image quality, clarity, the distinction between surrounding structures, and intelligibility (p \ 0.005).

Discussion In the literature, most of the studies that have evaluated 4D SRM USG have assessed only fetal behavior [3–6]. To our knowledge, no previous study has compared 4D SRM USG and 2D USG with respect to detection of fetal anomalies. Although the technique we used in the present study provided limited waves, and it was not possible to obtain sliced sections, we demonstrated that using 4D SRM USG the detection rate of fetal anomalies was similar to that of 2D USG in accordance with previous studies. Xu et al. [7] reported that 3D USG improved diagnostic capability compared to 2D USG by offering a greater amount of information in the evaluation of fetal malformations particularly in the display of malformations of the cranium and

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face, spine, extremities and body surfaces in a study of 41 fetuses with a total of 62 malformations. In a similar manner to our study in a review of 11 studies comparing 2D and 3D USG to evaluate facial anomalies, Goncalves et al. [8] reported that 3D USG provided additional diagnostic information particularly for the diagnosis of facial clefts in seven studies. The remaining four studies provided similar information across both modalities. The present study revealed that when all anomalies were considered 2D USG was superior to 4D USG in diagnosis, however, the structures that were difficult to evaluate with 2D USG such as fetal face, ears (see Fig. 1), and fingers were the easiest parts of the body to evaluate with 4D USG. With regard to the detection of limb deformities for seven of nine pes equinovarus and one flexion deformity of the legs 4D SRM USG was superior to 2D USG in the present study. It is important to differentiate the genuine anomalies such as severe flexion and overlapping fingers from transient situations that recover during repeated evaluations of the fetus. Abnormal severe flexion (see Fig. 2), anatomic axis distortion (such as clubfoot), and abnormal curvature of extremities can be identified more easily and accurately with 4D USG compared to 2D USG [9]. Kos et al. [10] reported 41 suspected cases of limb abnormality using 2D USG and the diagnosis of abnormalities in 28 cases such as clubfoot, hand polydactyly, upper- lower limb contractures and micromelia were determined after 3D USG examination. Conversely, although the diagnostic advantage of 3D USG was shown in 51–64 % of cases of intra-thoracic malformations 4D SRM USG failed to image the intrathoracic malformations with insufficient fluid accumulation around the midriff such as diaphragmatic hernia. In the detection of abdominal abnormalities, the role of 4D SRM USG could be limited to superficial abdominal wall defects such as omphalocele and gastroschisis (see Fig. 3): this modality has not been used in the evaluation of intra-

Fig. 1 Low-set ear

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Fig. 2 Hyperflexion deformities, legs

Fig. 3 Gastroschisis

abdominal abnormalities with the exception of cystic anomalies. In a similar manner to the present study Merz et al. [11] found that 3D USG made a small contribution to the identification of fetal and abdominal malformations (Fig. 3). 4D SRM USG was superior to 2D USG in the evaluation of one case of hypospadias but it made no contribution to the detection of anomalies of the intra-abdomina genitourinary tract. In addition 4D SRM USG did little to identify intracranial anomalies, unless they did not cause a deformity in the calvarium such as encephalocele. Hydrocephalus was detected with 4D SRM USG in six of 10 cases however, these were better visualized with 2D USG and 4D SRM USG did not detect hydrocephalus in the remaining four cases. With regard to the assessment of spine

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Fig. 4 Scoliosis

Fig. 5 Hemivertebrae

anomalies several previous studies have reported the efficacy of 3D USG in the visualization of columna vertebralis [12–15]. In a similar manner, we found that 4D SRM USG was superior to 2D USG especially in cases of superficial deformities such as spina bifida and inclination anomalies such as iniencephaly, hemivertebrae, kyphosis, and scoliosis (see Figs. 4 and 5). The contribution made by 4D SRM USG to the evaluation of cardiac anomalies has been scarce, due to limitations resulting from the abnormal accumulation of fluid, and we detected no cardiac anomalies using this modality. In the present study, 4D SRM USG could detect 11 % of cases with superficial anomalies. One of the major reasons for this was the lack of contrast between tissues such as oligohydramnios, thin fetal skin, and subcutaneous tissue. Since there were too many parts of fetuses in front of the screened area, multiple pregnancies, particularly at later gestation, is another

limitation in performing 4D SRM USG. It is difficult, or sometimes even impossible, to visualize non-superficial fetal structures with the superficial mode of 4D USG. Of the 84 fetal anomalies detected with 4D SRM USG, only 23 were non-superficial. We demonstrated that 4D SRM USG was superior to 2D USG in the identification of anomalies related to the face, spine/extremities, abdominal wall, and body surface. These differences depend on imaging principles and the preconditions of current 4D USG: there must be sufficient fluid around the screened area to obtain an optimal 4D image. Furthermore, no other structure (limb, placenta, fetal cord, etc.) should be in front of the screened area. The position of the fetus and the gestational week should be suitable. The structures of the face, spine/extremities, abdominal wall, and body surface are distinguished from adjacent amniotic fluid through an evidently different contrast. Therefore, these structures are appropriate for assessment via 4D USG. In addition, there are relatively large differences in contrast between the fetal bone structure of the extremities and spine and adjacent structures. Since face, spine, and extremity malformations occur with specific curvature deformity, they are impossible to display exactly on a single section image. Therefore, it is difficult to describe the malformations and their relationship with adjacent structures using traditional 2D USG. The small difference in contrast between non-superficial structures and adjacent tissues, and the lack of sufficient fluid accumulation around intra-fetal structures, makes it impossible to visualize these structures with 4D SRM USG. The internal structures can be assessed with multiplan mode. 4D SRM USG may be a fine method to use in helping parents to understand fetal anomalies, and may also be effective in helping to develop maternal-fetal affinity. This modality is 2D dependent, due to the necessity of performing 2D USG prior to 4D USG, and the latter had its limitations, because the device we used provided limited waves and we lacked obtained sliced sections, as we only used the SRM. Higher success rates may be achieved with devices that provide sliced sections and versatile waves and use different modalities of 4D USG if it is possible to perform a measurement with such a device. A potential bias of our study is that the examiner was aware of the indications for and the results of the 2D USG examination at the time that the 4D datasets were assessed. Therefore, we could only evaluate the complementary role of 4D SRM USG with 2D USG because both methods were applied by the same individual and 4D USG was performed on fetuses in which anomalies had been previously determined by 2D USG. Goncalves et al. [16] examined 99 fetuses by 3D/4D volume USG in a study that began with 3D volume imaging and in which 2D imaging was added only after an attempted diagnosis had been made via arevies of the 3D volume sets. The volume data sets were

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evaluated by a blinded independent examiner who after forming an initial diagnostic impression via 3D/4D USG then performed a 2D USG examination. There was agreement between 3D/4D USG and 2D USG with regard to 90.4 % of the findings. This approach enables the evaluation of 3D/4D volume imaging as a primary tool for detecting fetal anomalies without the potential bias of having first performed a standard 2D examination. Similarly, Benacerraf et al. [17] studied 26 fetuses. 20 of which had malformations on 2D USG and six of which had no abnormalities. The acquired volumes of each fetus designed to include the entire fetal anatomy were downloaded and reviewed several weeks later by a physician who had no clinical information or knowledge of the original 2D findings. A total of 57 anomalies were diagnosed by standard 2D USG, 49 (86 %) of which were observed on 3D sonography. Nevertheless, it is necessary to perform 2D USG to detect the correct area for 4D imaging as expected. Another limitation of the present study which may have affected the obtained results may be the inclusion of anomalies that do not appear to change fetal prognosis such as intra-cardiac hyperechogenic focus chorionamnion seperation pelvicaliceal dilatation and hyperechogenic bowel. Exclusion of these anomalies may also increase the rates of non superficial anomalies detected by both 2D and 4D USG. In conclusion, 4D SRM is superior to 2D USG in visualizing the malformaitons related to fetal face, spine, extremities, abdominal wall, and the body surface. However, 4D SRM USG may only be of use as a complementary tool in the evaluation of fetal anomalies particularly those of the face, spine, extremities, and abdominal wall. Conflict of interest

None.

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The place of four-dimensional ultrasound in evaluating fetal anomalies.

To analyze the capability of four-dimensional surface rendering mode ultrasound (4D SRM USG) in the detection of fetal abnormalities, and also compare...
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