Evaluating Spatiotemporal Image Correlation Technology as a Tool for Training Nonexpert Sonographers to Perform Examinations of the Fetal Heart

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1 ORIGINAL RESEARCH Evaluating Spatiotemporal Image Correlation Technology as a Tool for Training Nonexpert Sonographers to Perform Examinations of the Fetal Heart Hagai Avnet, MD, Eyal Mazaaki, MD, Ori Shen, MD, Sarah Cohen, MPH, Simcha Yagel, MD Received January 23, 2015, from the School of Women s and Children's Health, University of New South Wales Medicine, and Department of Maternal-Fetal Medicine, Royal Hospital for Women, Randwick, New South Wales, Australia (H.A.); Department of Obstetrics and Gynecology, Shaare Zedek Medical Center, Jerusalem, Israel (E.M., O.S.); and Ultrasound Center, Department of Obstetrics and Gynecology, Hadassah-Hebrew University Medical Centers, Mt Scopus, Jerusalem, Israel (S.C., S.Y.). Revision requested March 2, Revised manuscript accepted for publication May 5, Address correspondence to Simcha Yagel, MD, Ultrasound Center, Department of Obstetrics and Gynecology, Hadassah-Hebrew University Medical Centers, Mt Scopus, PO Box 24035, Mt Scopus, Jerusalem, Israel. simcha.yagel@gmail.com Abbreviations BMI, body mass index; 4D, 4-dimensional; ROI, region of interest; STIC, spatiotemporal image correlation; 3D, 3-dimensional; 2D, 2-dimensional doi: /ultra Objectives We aimed to evaluate the use of spatiotemporal image correlation (STIC) as a tool for training nonexpert examiners to perform screening examinations of the fetal heart by acquiring and examining STIC volumes according to a standardized questionnaire based on the 5 transverse planes of the fetal heart. Methods We conducted a prospective study at 2 tertiary care centers. Two sonographers without formal training in fetal echocardiography received theoretical instruction on the 5 fetal echocardiographic transverse planes, as well as STIC technology. Only women with conditions allowing 4-dimensional STIC volume acquisitions (grayscale and Doppler) were included in the study. Acquired volumes were evaluated offline according to a standardized protocol that required the trainee to mark 30 specified structures on 5 required axial planes. Volumes were then reviewed by an expert examiner for quality of acquisition and correct identification of specified structures. Results Ninety-six of 112 pregnant women examined entered the study. Patients had singleton pregnancies between 20 and 32 weeks gestation. After an initial learning curve of 20 examinations, trainees succeeded in identifying 97% to 98% of structures, with a highly significant degree of agreement with the expert s analysis (P <.001). A median of 2 STIC volumes for each examination was necessary for maximal structure identification. Acquisition quality scores were high ( of a maximal score of 10) and were found to correlate with identification rates (P =.017). Conclusions After an initial learning curve and under expert guidance, STIC is an excellent tool for trainees to master extended screening examinations of the fetal heart. Key Words echocardiography; fetal heart; 4-dimensional sonography; prenatal diagnosis; screening examination; spatiotemporal image correlation; 3-dimensional sonography; training Congenital heart defects are the most common severe congenital malformations. 1,2 It is widely accepted that prenatal diagnosis may improve the outcomes of affected neonates. 3 5 However, screening performed during the second trimester has shown highly variable detection rates. 6 8 Disappointing results were mainly attributed to examiner experience. 9,10 It was suggested that implementation of 4-dimensional (4D) sonography with spatiotemporal image correlation (STIC) technology might improve prenatal detection of congenital heart defects by decreasing dependence on the examiner s skills. 11, by the American Institute of Ultrasound in Medicine J Ultrasound Med 2016; 35:

2 Spatiotemporal image correlation is an automatic volume acquisition providing offline information on the entire fetal heart, including surrounding structures, with the heart in motion. 13 It offers the possibility of storing information, allowing other observers to review acquired volumes. It also improves patient counseling and interdisciplinary management team consultation. 14 Several groups have reported encouraging results using STIC for exploring the fetal heart during the second and third trimesters of pregnancy It is feasible to incorporate STIC into tertiary routine prenatal sonographic examinations performed by experienced sonographers High intercenter agreement and accurate interpretation of STIC volumes were found in a study comprising 7 different centers with expertise in 4D fetal echocardiography. 23 One group evaluated STIC as a tool for training inexperienced sonographers to identify outflow tract abnormalities by reviewing the A-planes of STIC cardiac volume data sets. 24 Spatiotemporal image correlation volumes acquired during the first 25 or second 26 trimester can be obtained by a properly trained nonexpert operator and then transmitted for specialist analysis, enabling heart assessment. The single 30 craniocaudal sweep performed automatically by STIC acquisition is similar to that performed by the operator when sliding the transducer to obtain the 5 short-axis cardiac planes, which were proposed by Yagel et al 27 for optimal heart screening (Figure 1). This method allows a shorter examination time and greater ease for the examiner to scan the fetal heart, simplifying and streamlining the fetal cardiac examination without compromising diagnostic effectiveness. We aimed to evaluate the use of STIC for training nonexpert examiners to perform an extended screening of the fetal heart by acquiring and examining STIC volumes according to a standardized questionnaire based on the 5 transverse planes of the fetal heart, which are compatible with International Society of Ultrasound in Obstetrics and Gynecology guidelines for sonographic screening of the fetal heart. 28 Materials and Methods We conducted a prospective study at 2 tertiary care centers. Two sonographers (H.A. and E.M.), both obstetricians with fewer than 3 years of experience in obstetric sonography and without formal training in fetal echocardiography, received 4 hours of theoretical instruction on the 5 transverse fetal echocardiographic planes, as well as STIC technology, acquisition technique, and its associated applications, as summarized by Yagel et al. 29 In addition, they received 2 hours of practical instruction regarding the optimal conditions for STIC volume acquisition, as described by Gonçalves et al, 30,31 concerning fetal position, region of interest (ROI), acquisition angle, and acquisition time. The study population consisted of a mixed population of pregnant women older than 18 years undergoing routine sonographic examinations. Gestational ages ranged from 20 to 32 weeks on the day of the examination. Pregnancies earlier than 20 weeks and later than 32 weeks and multifetal pregnancies were not included. Pregnancies with diagnosed congenital heart defects were excluded. Informed consent was obtained from each patient, and our Ethics Committee approved the study. Sonographic examinations were performed with a Voluson E8 Expert or Voluson 730 Expert scanner (GE Healthcare, Zipf, Austria) and a motorized 4 8-MHz curved array transducer. The first 20 cases were dedicated to the primary learning curve and were not included in the study analysis. Afterward, only cases in which the trainee succeeded in completing the acquisition as instructed were included in the study group. Maternal and fetal movements were avoided when possible. If the fetal position was not favorable for STIC acquisition, the patient was asked to repeat the examination 30 minutes later. Patients with heart volumes of low quality, resulting from such issues as excessive fetal movements, an insufficient ROI setting, an apex position, or shadowing, that prevented proper heart structure identification were excluded from the study. Trainees first acquired a 30 2-dimensional (2D) sonographic sweep of the fetal abdomen to upper mediastinum. This cine loop was saved to the archive. Next, 3 grayscale and 2 high-definition power flow Doppler STIC volumes were acquired with acquisition times and angles ranging from 10 seconds and 25 to 12.5 seconds and 40, as appropriate, depending on the gestational age and the distance of the fetus from the transducer. Four-dimensional STIC volumes were stored for later offline analysis with the STIC software (4D View; GE Healthcare). Possible factors that could influence image quality were documented for correlation evaluation: body mass index (BMI), parity, gestational age, history of abdominal surgery; interfering fetal activity was defined as absent, seldom, or frequent; and position was defined as favorable, intermediate, or poor. Examination performance difficulty was classified as easy, intermediate, or difficult. Saved materials were evaluated offline without the patient present, according to a standardized protocol that required the trainee to mark 30 specified structures iden- 112 J Ultrasound Med 2016; 35:

3 Figure 1. The 5 axial views for optimal fetal heart screening. The color image shows the trachea (T), heart and great vessels, liver, and stomach, with the 5 planes of insonation indicated by polygons corresponding to the grayscale images, as indicated. I, Most caudal plane, showing the fetal stomach (St), cross-section of the descending aorta (Ao), spine, and liver (Li). II, Four-chamber view of the fetal heart, showing the right and left ventricles (RV and LV) and atria (RA and LA), foramen ovale (FO), and pulmonary veins (PV) to the right and left of the descending aorta. III, Left ventricular outflow tract view, showing the aortic root (Ao), left and right ventricles, left and right atria, and a cross-section of the descending aorta. IV, Slightly more cephalad view (right ventricular outflow tract view), showing the main pulmonary artery (MPA), the bifurcation into the right and left pulmonary arteries (RPA and LPA), and cross-sections of the ascending aorta (Ao) and descending aorta (dao). V, Three-vessel and trachea view, showing the superior vena cava (SVC), pulmonary artery (PA), ductus arteriosus (DA), transverse aortic arch (from proximal aorta to descending aorta), and trachea (Tr). IVC indicates inferior vena cava; LAA, left atrial appendage; Lt, left; RAA, right atrial appendage; and Rt, right. Reproduced with permission from Carvalho et al. 28 J Ultrasound Med 2016; 35:

4 tified on the following 5 required planes, according to the checklist shown in Table 1: 1. Transverse view of the fetal upper abdomen, showing the spine, stomach, and inferior vena cava. This view establishes fetal orientation and is important for evaluating normal situs. Table 1. Checklist of Fetal Heart Structures Visualized in Each Cardiac View Retrieved From the Volume Data Sets Acquired by Grayscale and High-Definition Power Flow Doppler STIC View Upper abdomen 4-Chamber view 5-Chamber view Pulmonary artery view 3-Vessel and trachea view Doppler Structure Stomach on the left side Aorta on the left side of the spine Inferior vena cava anterior and to the right of the spine 4 cardiac chambers present Majority of heart located in the left chest Heart occupies about ⅓ of the thoracic area Normal cardiac situs, axis, and position Pericardial effusion not seen Atria appear approximately equal in size Foramen ovale flap lies in the left atrium Lower rim of the atrial septum (septum primum) is present Ventricles approximately equal in size Ventricular septum appears intact from apex to crux Both atrioventricular valves open and move freely Tricuspid valve septal insertion more apical than mitral valve At least 1 pulmonary vein enters the left atrium Aortic root emerges from the left ventricle Interventricular septum in contiguity with the anterior wall of the ascending aorta Pulmonary artery visualized exiting the right ventricle At least 1 of the branches of PA bifurcating at its distal end Pulmonary artery communicates directly with the ductus arteriosus Transverse aortic arch between the pulmonary artery and superior vena cava Superior vena cava visualized on the right side of the chest Trachea visualized posterior to the superior vena cava Absence of interventricular flow Proper left atrioventricular flow without retrograde flow Proper right atrioventricular flow without retrograde flow Proper flow through the aortic valve without retrograde flow Proper flow through the pulmonary valve without retrograde flow 3-vessel and trachea view 2. Four-chamber view. 3. Five-chamber view. Here the aortic root is visualized. 4. Bifurcation of the pulmonary arteries. 5. Three-vessel and trachea view. This view is the most cephalic transverse view, visualized on a plane crossing the fetal upper mediastinum, and is easily visualized by showing a plane cephalad and slightly oblique from the 4-chamber view. The 3-vessel and trachea view shows the main pulmonary artery in direct communication with the ductus arteriosus. A transverse section of the aortic arch is seen to the right of the main pulmonary artery and ductus arteriosus. Cross sections of the superior vena cava, and the trachea posterior to it, are visualized. 32 High-definition power Doppler flow STIC volumes were evaluated for Doppler flow parameters: presence or absence of interventricular flow, proper atrioventricular flow, and proper flow through the semilunar valves without retrograde flow. After file interpretation was completed by the trainees, an expert examiner (S.Y.) reviewed the files for quality of acquisition and correct identification of required structures. Spatiotemporal image correlation volumes were assessed for movement artifacts, the ROI setting, the acquisition angle, the fetal position, and shadowing artifacts, using the scoring system proposed by Uittenbogaard et al 17 and shown in Table 2. Summation of the scores determined the acquisition condition score, which had a maximum of 10. All STIC volumes were assessed with respect to the fetal heart structures identified or missed by the operators. Operator and expert identification success rates for each structure were compared. Structure identification was also correlated with regard to the acquisition condition score, maternal biometric parameters, and examination performance difficulty, as defined by the trainee. Results were compared to neonatal examinations. For statistical analysis, the Cohen κ test was used to determine the degree of agreement between nonexpert and expert examiner item visualization. The Wilcoxon signed ranks test was used for comparing nonexpert and expert total average visualization success rates. To assess the correlation between visualization success rates and various parameters, the following were used as appropriate: Spearman correlation for gestational age and BMI and Kruskal-Wallis test for examination performance difficulty, history of abdominal surgery, finding of oligohydramnios, and interfering fetal activity. Correlation between acquisition conditions and the average visualization rate were assessed with the Spearman correlation. P <.05 was considered statistically significant. 114 J Ultrasound Med 2016; 35:

5 Table 2. Acquisition Condition Scoring System Proposed by Uittenbogaard et al 17 Score Movements ROI Setting Acquisition Angle Apex Position Shadowing 0 Frequent Too small Too narrow 4 8-o clock Extensive 1 Rare Too large Too wide or 2 4-o clock Moderate 2 Absent Sufficient Sufficient 11 2-o clock Absent Results At first, the trainees scanned 20 women whose volumes formed a learning curve group to practice the technique they had learned. After this process, recruitment of patients for the study began. Only patients whose examination conditions, including fetal movements, position, and shadowing, allowed sufficient volume acquisition quality entered the study. Thus, 96 women from 112 examined (86%) were included. Patients ranged in age from 18 to 43 years (mean, 29.6 years), were in their first to ninth pregnancies, and were between 20 and 31 weeks gestation (mean, 23.7 weeks). Women s weights ranged from 50 to 87 kg (mean, 65.6 kg); height ranged from 1.50 to 1.78 m (mean, 1.66 m); and BMI ranged from of 17.9 to 35.3 kg/m 2 (mean, 23.9 kg/m 2 ). Twenty-two women reported a history of 1 abdominal surgery (23%), whereas the rest had none. Examination conditions were defined by the trainees: fetal movement median score, 1.7 (1, none; 2, seldom; and 3, frequent); fetal position median score, 1.5 (1, good; 2, intermediate; and 3, poor); and examination difficulty median score, 1.4 (1, easy; 2, intermediate; and 3, difficult). Trainees eventually used a variable number of volumes (1 4) from among the 5 STIC volumes acquired from each fetus to achieve maximal structure identification. The median was 2 volumes for both trainees (Figure 2). During the study, we found that to ensure high-quality volumes, one must limit the acquisition time to 10 seconds and acquisition angle to 30. A longer acquisition time or wider acquisition angle usually impaired volume quality. While examining women with a relatively younger gestational age, it was possible to obtain a single STIC volume that imaged all 5 axial planes required for evaluation. However, while examining women of more advanced gestational age, with a larger fetal heart or when the distance between the heart and the transducer was short, 2 volumes were most often required to achieve satisfactory imaging of the whole heart. The first, relatively caudal, volume included the first axial plane (upper abdomen), and the other, more cephalic, included the fifth plane (3-vessel and trachea). Acquisition Quality Acquisition quality was assessed by the acquisition score (detailed in Table 2), which was given by the expert while evaluating the volumes acquired by the trainees. Average scores for trainees 1 and 2 were high: 8.7 (SD, 1.20) and 8.6 (SD, 1.22), respectively (of a maximal score of 10). Structure Identification Rates The trainees identification rates for each structure are detailed in Table 3. Trainee 1 s identification rates for different structures ranged from 91.7% to 100%. The average rate was 98.3%. The expert s identification rates, compared to trainee 1 while evaluating the same volumes, ranged 91.7% and 100% (average, 98.1%; Figure 3). Trainee 2 s identification rate ranged from 83.3% to 100% for different fetal heart structures (Table 3) and averaged 97.2%. By comparison, the expert identified 85.4% to 100% (average, 97.2%) of the structures while evaluating the same volumes (Figure 3). The trainees evaluation was assessed in relation to the expert s evaluation, which was considered the reference standard. Correct identification excluded misidentification (ie, seeing something that was not there or missing something that was there, compared to the expert). The correct identification rate was calculated for each structure, as displayed in Table 3. The mean of all of these correct structure identification rates gave us the overall correct identification rate. The overall correct identification rates for trainees 1 and 2 were 99.3% and 99%, respectively (Figure 3). Figure 2. Distribution of the number of volumes (among the 5 STIC volumes acquired from each fetus) required for a trainee to achieve maximal structure identification in a single screening examination of the fetal heart. The median was 2 volumes per fetus for both trainees. J Ultrasound Med 2016; 35:

6 Comparing total structure identification rates, there was no difference between trainee 1 and the expert (P=.232) or between trainee 2 and the expert (P =.528). A highly significant degree of agreement between both trainees and the expert s analysis was found. Agreement on identification or nonidentification of all specific heart structures was evaluated by the Cohen κ test, and the degree of agreement for each of the structures was found to be significant (P <.001). One ventricular septal defect, identified by trainee 1 and the expert (which was confirmed after delivery) and 2 cases (1 for each trainee) of intracardiac echogenic foci were diagnosed and confirmed during the expert s evaluation. Postnatal examinations did not reveal additional findings that were undetected prenatally. Several parameters were evaluated for their impact on the structure identification rate: the acquisition score, as assessed by the expert, was found to have a positive correlation with the identification rate. This correlation was significant for trainee 2 (Spearman ρ = 0.34; P =.017), and whereas a trend was observed for trainee 1, the correlation did not reach statistical significance (Spearman ρ = 0.21; P =.15). Another parameter evaluated was gestational age. We found that as weeks gestation advanced, the identification rate dropped. This correlation was significant for trainee 1 (Spearman ρ = 0.4; P =.004) but not for trainee 2 (Spearman ρ = 0.172; P =.243). Data from trainee 1 showed a negative correlation between maternal BMI and the identification rate (Spearman ρ= 0.182; P=.216, not significant). This correlation was not seen for trainee 2. While evaluating the influence of the following parameters on both trainees structure identification rates, no correlation was found: maternal age, parity, examination per- Table 3. Trainees Heart Structure Identification Rates and Correct Identification Rates Compared to the Expert While Evaluating the Same Volumes Trainee Expert, Identification, Trainee Expert, Identification, View Structure 1, % % % 2, % % % UA view Stomach on the left side Aorta on the left side of the spine Inferior vena cava anterior and to the right of the spine C view 4 cardiac chambers present Majority of heart located in the left chest Heart occupies about ⅓ of the thoracic area Normal cardiac situs, axis, and position Pericardial effusion not seen Atria appear approximately equal in size Foramen ovale flap lies in the left atrium Lower rim of the atrial septum (septum primum) is present Ventricles approximately equal in size Ventricular septum appears intact from apex to crux Both atrioventricular valves open and move freely Tricuspid valve septal insertion more apical than mitral valve At least 1 pulmonary vein enters the left atrium C view Aortic root emerges from the left ventricle Interventricular septum in contiguity with the anterior wall of the ascending aorta PA view Pulmonary artery visualized exiting the right ventricle At least 1 of the branches of PA bifurcating at its distal end VT view Pulmonary artery communicates directly with the ductus arteriosus Transverse aortic arch between the pulmonary artery and superior vena cava Superior vena cava visualized on the right side of the chest Trachea visualized posterior to the superior vena cava Doppler Absence of interventricular flow Proper left atrioventricular flow without retrograde flow Proper right atrioventricular flow without retrograde flow Proper flow through the aortic valve without retrograde flow Proper flow through the pulmonary valve without retrograde flow vessel and trachea view C indicates 5-chamber; 4C, 4-chamber; PA, pulmonary artery; 3VT, 3-vessel and trachea; and UA, upper abdomen. 116 J Ultrasound Med 2016; 35:

7 formance difficulty (as defined by trainees), history of abdominal surgery, and interfering fetal activity. Discussion Fetal echocardiography is one of the more complex examinations among the obstetric sonographic repertoire. It demands theoretical knowledge, spatial reasoning, and technical skill. However, the fetal heart is the organ most often affected by major congenital malformations, and congenital heart defects are associated with substantial neonatal morbidity and mortality. Therefore, effective professional training in this system is essential. Until now, fetal sonographers were trained to examine the fetal heart by using 2D sonography. It may be difficult to create a 3- dimensional (3D) mental image that faithfully reproduces the spatial relationships among the various heart structures. Several authors have evaluated the use of STIC technology for fetal heart assessment Bennasar et al 18 found that the advantages of STIC, such as slow-motion imaging and the capability of analyzing the fetal heart without fetal movements, allowed better assessment of anomalies. They concluded that STIC can confidently be used for assessment of fetuses affected by any congenital heart defect with a high degree of accuracy. 18 Spatiotemporal image correlation has been shown to be an effective imaging tool in fetal echocardiography. 23,29,31,33 In light of its demonstrated advantages, our objective was to evaluate, for the first time to our knowledge, whether it could also serve as a tool for training operators to perform extended fetal heart screening examinations. Figure 3. Trainees and expert s mean structure identification rates and overall correct identification rate for each trainee relative to the expert s identification. After receiving theoretical instruction on fetal heart structures, STIC technology, and the 5 axial plane assessment method 27 compatible with International Society of Ultrasound in Obstetrics and Gynecology guidelines for comprehensive fetal echocardiography, 28 the trainees began practicing. After a relatively short learning curve of 20 cases, the trainees acquisition quality, as evaluated by an expert fetal echocardiographer, was high, averaging 8.6 to 8.7 (on a scale of 1 10). Trainees succeeded in identifying most of the target structures. Thus, whereas systematically adhering to a set checklist, they identified structures in each of the 5 required planes and in the Doppler volume. Trainees correct identification rates reached 97% to 98%. Notably, several targeted structures proved more difficult to identify, including entry of the pulmonary vein into the atrium (identified in 84% 89% of cases), the inferior vena cava (83% 96%), the trachea (87% 93%), and the main pulmonary artery bifurcation (93% 95%). A highly significant degree of agreement was found between the trainees and expert s analyses. A positive correlation between the volume acquisition quality and identification rate and a negative correlation between gestational age and the identification rate were found as expected. These correlations were observed for both trainees but were statistically significant only for one. The difficulty in reaching significant correlation can be explained by the relatively small distribution of identification rates and by the number of participants in the research group. We acknowledge that having only 2 sonographers trained in this study may limit its applicability, and in the future, a study in which a larger number of sonographers are trained would be able to further validate this technique. The 2 main results of this program, achieving volume acquisition skills and the ability to identify target anatomy correctly, can be gained by incorporating STIC in a course of theoretical and technical instruction. Spatiotemporal image correlation can be used as a tool for training nonexpert sonographers to perform extended screening examinations of the fetal heart, as shown by the high performance level achieved by the trainees after a relatively short learning curve. Spatiotemporal image correlation technology has several advantages that make it an excellent learning tool. A volume containing all information required for identifying cardiac anatomy and blood flow, once acquired and saved, is available for offline processing after the patient has been dismissed, which allows the trainee to observe atrial and ventricle contractions in slow motion and appreciate heart structure and function on 3D and 4D sonography. J Ultrasound Med 2016; 35:

8 The operator can manipulate and rotate the volume to display predefined standard planes, thereby systematically identifying the heart structures they contain Shen and Yagel 36 found that 3D and 4D modalities enhanced depth perception through rendered images. They reconstruct information and display a more complete and therefore more comprehensible picture, so those examiners least experienced in mental reconstruction stand to gain most from the technology. Spatiotemporal image correlation has several inherent disadvantages. To obtain a volume that is suitable for interpretation, fetal movements should be avoided, and the fetus must be in an optimal lie. Uittenbogaard et al 17 found that sonographers who were given 30-minute time slots to acquire an STIC volume made successful acquisitions in only 75% of the cases, and only 65% of the analyzed volumes were of high or sufficient quality. Good scanning conditions are difficult to meet in all cases. In this study, the examinations were not bound to strict time limits, and additional time was allowed if the fetal position was not favorable for STIC acquisition. Nevertheless, satisfactory STIC volume acquisition was not achieved in all patients (86% of cases were suitable for evaluation). Another drawback is the accessibility of the technology. However, in centers where it is available, it is an effective tool for training sonographers to perform extended screening examinations of the fetal heart, particularly by internalizing 3D heart structures. However, it seems that it will not replace routine 2D sonography. This study focused on acquiring basic skills for performing screening sonographic examinations of the fetal heart in the general pregnant population, and its aim was to explore the possibility of teaching normal heart structure identification by using STIC technology. 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