Feasibility and accuracy of fetal echocardiography using four-dimensional spatiotemporal image correlation technology before 16 weeks gestation

Transcription

1 Ultrasound Obstet Gynecol 2009; 33: Published online in Wiley InterScience ( DOI: /uog.6374 Feasibility and accuracy of fetal echocardiography using four-dimensional spatiotemporal image correlation technology before 16 weeks gestation M. BENNASAR, J. M. MARTÍNEZ, A. OLIVELLA, M. DEL RÍO, O. GÓMEZ,F.FIGUERAS, B. PUERTO and E. GRATACÓS Maternal-Fetal Medicine Department, Institut Clínic de Ginecologia, Obstetrícia I Neonatologia (ICGON), Hospital Clínic, Institut d Investigacions Biomèdiques Augusto Pi i Sunyer (IDIBAPS), University of Barcelona, and Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER), Barcelona, Spain KEYWORDS: congenital heart defects; early fetal echocardiography; early prenatal diagnosis; four-dimensional echocardiography; STIC ABSTRACT Objectives To evaluate the potential value of early fetal echocardiography (EFE) by means of four-dimensional (4D) spatiotemporal image correlation (STIC) technology for either reassurance of normality or prenatal diagnosis of major congenital heart defects (CHDs). Methods Sixty-nine pregnant women from 11 to 15 weeks gestation underwent EFE. 4D-STIC volumes were acquired by the transvaginal approach for later review by two different examiners. STIC evaluation was considered complete when the four-chamber view, and the origin and double-crossing of the great arteries were identified correctly. Color Doppler imaging was used to detect either septal shunts or transvalvular regurgitation/aliasing suggesting abnormalities. STIC diagnoses were compared with those of conventional EFE. Reliability was assessed by postnatal examination, or autopsy in cases of termination of pregnancy or perinatal death. Results The median gestational age at volume acquisition was weeks. Eleven (15.9%) cases of CHD were diagnosed. A complete EFE was possible in 64 cases. We were able to provide reassurance of normality in 51 of the 53 confirmed normal hearts, with no false-positive results for major defects, although two minor defects (one ventricular septal defect (VSD) and one persistent left superior vena cava) were falsely suspected. The only false negative was a significant VSD at birth overlooked by both observers. Therefore, the total accuracy of STIC- EFE was 95.3% (61/64), with sensitivity, specificity, and positive and negative predictive values of 90.9%, 96.2%, 83.3% and 98.1%. The accuracy of conventional EFE (98.4%, 63/64) was slightly better than that of STIC, with no false-positive results recorded. Conclusions Offline evaluation of 4D-STIC acquired volumes of the fetal heart in the first and early second trimester of pregnancy is reliable not only for early reassurance of normal cardiac anatomy but also to diagnose most major structural heart defects. Copyright 2009 ISUOG. Published by John Wiley & Sons, Ltd. INTRODUCTION Congenital heart defects (CHDs) are the most common severe congenital malformations. They account for about eight in 1000 live births, and are still a major cause of mortality and disability in infancy 1,2. It is widely accepted that prenatal diagnosis may improve the postnatal outcome of affected newborns, particularly those with conditions requiring patency of the ductus arteriosus in early neonatal life 3,4. Nowadays, most major CHDs and some minor forms can be detected prenatally 5. However, the overall prenatal detection of major CHDs in the screening population remains disappointingly low in recent studies, with only about a third being diagnosed, usually after 22 weeks gestation 6. Such low detection rates are mainly attributed to examiner experience 7,8.One of the approaches suggested to improve prenatal detection of CHDs is to decrease the dependency on the examiner s skills by relying on four-dimensional (4D) ultrasound imaging with spatiotemporal image correlation (STIC) technology 9,10. STIC offers the possibility of storing information acquired from the fetal heart in an endless Correspondence to: Dr J. M. Martínez, Sabino de Arana 1, Barcelona, Spain ( jmmarti@clinic.ub.es) Accepted: 3 December 2008 Copyright 2009 ISUOG. Published by John Wiley & Sons, Ltd. ORIGINAL PAPER

2 646 Bennasar et al. 4D cineloop sequence, so that other observers can review it without the need for the patient being scanned. Several groups have reported encouraging results using STIC for exploring the fetal heart during the second and third trimesters of pregnancy The finding of an increased nuchal translucency thickness at weeks gestation in fetuses with a normal karyotype has been demonstrated to be the strongest predictor of CHDs at this early stage of gestation 12. This has prompted research to explore the feasibility of advancing cardiac screening to the first trimester in high-risk patients. Consequently an increasing number of studies on nuchal translucency and CHD have been published during the past decade A recent review of previous results concluded that, in experienced hands, early fetal echocardiography (EFE) before 14 weeks gestation is feasible and accurate in diagnosing most major CHDs, potentially achieving a sensitivity of around 85% and a specificity approaching 100% 17. Unfortunately EFE is still limited to a few specialized centers and is not available for most patients at risk. The aim of this study was to evaluate the feasibility and accuracy of EFE from 4D-STIC volumes acquired transvaginally before 16 weeks gestation, compared with conventional EFE, for an early reassurance of normality or a prenatal diagnosis of major congenital heart disease. METHODS We conducted a prospective study involving 69 women with singleton pregnancies attending our Fetal Medicine Unit from September 2006 to November The study population consisted of two groups: a consecutive sample of 45 fetuses with no risk factors for CHDs recruited from pregnant women undergoing routine firsttrimester ultrasound examination, and a consecutive sample of 24 fetuses referred to our unit for targeted EFE. The indications for EFE were: suspected cardiac or extracardiac anomalies at screening scan (n = 1), increased nuchal translucency (> 99 th centile) (n = 14), abnormal (reversed a-wave) ductus venosus blood flow (n = 3), fetus affected by a chromosomal abnormality (n = 4; two trisomy 21, one trisomy 18 and one 46,XX,inv(14)(p11.1q24)), and others (n = 2; family risk, pregestational diabetes). Gestational age ranged from to15+ 5 weeks on the day of the examination, as determined by first-trimester fetal crown rump length measurement. Informed consent was obtained from each patient and the study was approved by our ethics committee. Ultrasound examinations were performed using a Voluson 730 Expert scanner (GE Medical Systems, Zipf, Austria) and the 4D-STIC volumes were acquired with a transvaginal real-time probe (RIC 5 9 MHz) using gray-scale and color Doppler imaging. The acquisition was performed by non-expert operators trained in first-trimester ultrasound examination and fetal echocardiography. The standardized acquisition plane was the four-chamber view, preferably by an apical approach. The acquisition time and angle ranged between 7.5 and 10 s, and 15 and 25, respectively, depending on the gestational age and the distance of the fetus from the transducer. The color Doppler maximal velocity setting was adjusted so that the great arteries were homogeneous in color, did not demonstrate aliasing and color signal filled the lumen of the vessels. Mechanical and thermal indices in color Doppler imaging were kept as low as possible (ALARA principle) 18. Maternal and fetal movements were avoided when possible. When the fetal position was not favorable for STIC acquisition the patientwasaskedtocomebackin30min.afterstic volumes had been acquired, a conventional EFE was performed by an experienced observer. 4D-STIC volumes were stored for later offline analysis with the STIC software (4D View; GE Medical Systems). All 4D volumes were reviewed by two different observers experienced in EFE who were unaware of the specific diagnosis, and had no previous knowledge about the referral population (screening vs. indicated EFE). To evaluate the cardiac anatomy, the following items were identified Abdominal situs: heart and stomach relation, abdominal aorta and inferior cava vein location. 2. Four-chamber view: two equal sized ventricles and atria, the moderator band, the cardiac crux, and the normal insertion and movement of the atrioventricular valves. 3. Five-chamber view: continuity between the aortic root and the interventricular septum. 4. Pulmonary trunk in a short-axis view, pulmonary branching. 5. Crossing-over of the aorta and pulmonary trunk. 6. Three-vessel and trachea view. Finally, color Doppler imaging was used to detect either septal shunts or transvalvular regurgitation/aliasing suggesting abnormalities. Cardiac examination was considered complete when the four-chamber view, and the origin and crossing of the great arteries had been correctly identified. Each case was classified as normal or abnormal depending on whether the parameters studied met the criteria established previously 19.Thetime taken for the offline cardiac examination was recorded. Second-trimester echocardiography was performed in all continuing pregnancies in order to confirm the firsttrimester diagnosis. Reliability was assessed by postnatal examination or by autopsy in cases of termination of pregnancy or perinatal death. The diagnosis and accuracy of STIC were compared with those of conventional EFE. The visualization success rate of the parameters evaluated was expressed as a percentage and was stratified by complete gestational week. Standard statistical analysis was used to evaluate the sensitivity, specificity and predictive values for EFE by 4D-STIC in diagnosing CHDs.

3 STIC echocardiography before 16 weeks 647 RESULTS A total of 69 fetuses were studied, including 11 (15.9%) with CHD and 58 normal cases, as revealed by postnatal follow-up or autopsy evaluation. The median maternal age was 35 (range, 23 44) years and the median gestational age at sonographic evaluation was (range, to15+ 5) weeks. The case distribution of gestational age at examination was: four cases at 11 weeks, 14 cases at 12 weeks, 25 cases at 13 weeks, 21 cases at 14 weeks and five cases at 15 weeks. A satisfactory volume acquisition was always achieved; the median number of STIC volumes acquired from each patient was 3 (range, 2 6). A total of 65 (94.2%) cases were acquired at the first examination, whereas a second scan was necessary in four (5.8%) patients and no patient needed to be rescheduled for another day. STIC acquisition was aborted if significant fetal movements were detected. Although aborted attempts were frequent, they were not recorded. The median time needed for a satisfactory STIC acquisition was calculated instead, and was 7 (range, 4 13) min. The median time for offline analysis was 10.7 (range, 4 27) min. The visualization success rate for each of the previously described cardiac planes was excellent beyond 12 weeks gestation. This rate, for the whole group and stratified by gestational age, is shown in Table 1. Data on the performance of STIC and conventional EFE are shown in Table 2. Twelve cases of CHD were diagnosed after STIC evaluation. Of these, 10 were confirmed by autopsy or postnatal evaluation. There were two false-positive cases (3.4%) with minor defects (ventricular septal defect (VSD) and persistent left superior vena cava). After STIC evaluation five cases were classified as unsatisfactory and were excluded from the analysis. Among the 52 cases considered normal after STIC analysis, normality was confirmed in all cases but one. There was only one false-negative case: a significant perimembranous VSD, 8 mm at birth, needing surgery (Case 11), that was overlooked by both observers. Thus, the accuracy of EFE by 4D-STIC was 95.3% (61/64), with sensitivity, specificity, and positive and negative predictive values of 90.9%, 96.2%, 83.3% and 98.1%, respectively (Tables 3 and 4). A tomographic ultrasound image of Case 8 and a rendered image of the four-chamber view of Case 1 are shown in Figures 1 and 2, respectively. Table 1 Visualization success rate of the different cardiac views among the 57 cases with no suspicion of congenital heart disease on spatiotemporal image correlation analysis, by completed gestational weeks GA (weeks) n Four-chamber view Pulmonary trunk Aortic root Crossing arteries Three-vessel view Full examination Total GA, gestational age in completed weeks. Table 2 Characteristics of the cases Case GA (weeks) CHD risk STIC Conventional EFE Follow-up or autopsy Outcome Increased NT Tricuspid atresia Idem Confirmed Fetal death Increased NT PAAtr + VSD Idem Confirmed TOP Increased NT Perimembranous VSD Idem Confirmed TOP Trisomy 18 DORV + mitral atresia Idem Confirmed TOP None HLH Idem Confirmed TOP Increased NT AVSD Idem Confirmed TOP Increased NT HLH + PLSVC HLH Confirmed TOP Increased NT AVSD + situs ambiguous Idem Confirmed Fetal death Increased NT PAAtr + VSD Idem Confirmed TOP Increased NT HLH Idem Confirmed Fetal death 11* None Normal Normal VSD 8 mm Alive None VSD Normal Normal Normal None PLSVC Normal Normal Normal *False negative. False positive. AVSD, atrioventricular septal defect; CHD, congenital heart defect; DORV, double-outlet right ventricle; EFE, early fetal echocardiography; GA, gestational age; HLH, hypoplastic left heart; Idem, same findings as by STIC; NT, nuchal translucency; PAAtr, tetralogy of Fallot with pulmonary atresia; PLSVC, persistent left superior vena cava; STIC, spatiotemporal image correlation; TOP, termination of pregnancy; VSD, ventricular septal defect.

4 648 Bennasar et al. Figure 3 shows an en-face view of Cases 1 and 8, as well as an en-face view of a normal heart. Conventional two-dimensional (2D) EFE diagnosed 10 cases of CHD with no false-positive results (Table 2). Normality was confirmed in 53/54 fetuses considered as normal by 2D ultrasound imaging. Case 11 was also missed by real-time EFE examination. There was a very high level of agreement between STIC and conventional EFE. STIC completed the diagnosis in Case 7, adding a further finding of a persistent left superior vena cava not previously identified by conventional EFE. Although no conclusions about prognosis can be drawn owing to the small number of affected cases, the overall outcome of fetuses with major CHDs was very poor. In seven cases, a termination of pregnancy was performed at Table 3 Detection of congenital heart defects (CHDs) in our population by four-dimensional spatiotemporal image correlation (STIC) and conventional two-dimensional early fetal echocardiography (EFE) before 16 weeks Status of heart STIC Conventional EFE Normal Abnormal Normal Abnormal Normal heart (n = 53) Abnormal heart (n = 11) All hearts (n = 64) Incidence of CHDs, 15.9% (11/69). Table 4 Diagnostic indices of four-dimensional spatiotemporal image correlation (STIC) and conventional two-dimensional early fetal echocardiography (EFE) in detecting congenital heart defects before 16 weeks in our population Diagnostic index STIC (% (n)) Conventional EFE (% (n)) Sensitivity 90.9 (10/11) 90.9 (10/11) Specificity 96.2 (51/53) 100 (53/53) Positive predictive value 83.3 (10/12) 100 (10/10) Negative predictive value 98.1 (51/52) 98.1 (53/54) Total accuracy 95.3 (61/64) 98.4 (63/64) the parents request. Among the continuing pregnancies there were three fetal demises and only one newborn survived beyond the sixth month of postnatal life. DISCUSSION This case series provides two main findings. First, early evaluation of the fetal heart is feasible using 4D-STIC technology, particularly beyond 12 weeks, and, second, a highly accurate diagnosis of major CHDs can confidently be achieved by this means. Both findings may have clinical implications in the management of the early pregnancy at high risk for CHDs. Antenatal detection of CHDs remains one of the most challenging aspects of prenatal diagnosis. However, it can Figure 1 Tomographic fetal ultrasound imaging at weeks gestation. The image on the right shows a common atrioventricular valve (*). The azygos vein can be seen to the right and parallel to the aorta (arrow). The lower left image shows an inferior plane in which the stomach can be seen on the right (arrow).

5 STIC echocardiography before 16 weeks 649 Figure 2 Rendered image of the four-chamber view in Case 1 showing hypoplastic right ventricle (RV) associated with a ventricular septal defect (*) at weeks gestation. The atretic and echogenic tricuspid valve (TV) is shown (arrow). LA, left atrium; LV, left ventricle. be properly achieved as early as 11 weeks gestation by experienced groups 20 22, although it is widely accepted that the optimal gestational age for performing EFE is at least 13 weeks gestation 20,23. Therefore, in a clinical setting, EFE might be offered to families considered to be at risk of cardiac defects, particularly when fetal nuchal translucency is increased 12. It can be a powerful tool to reassure families regarding normality of major cardiac structures and connections. We believe this is of utmost importance as CHDs diagnosed early in pregnancy tend to be more complex than those detected later, with a higher incidence of associated structural malformations, chromosomal abnormalities and miscarriage 24. Unfortunately, EFE is still limited to a few specialized centers and is not available for most patients at risk for CHDs. Since it was first described in 2003, 4D-STIC technology has been incorporated by some groups into the management of fetuses at high risk of CHDs 9,10, The use of STIC in the first trimester has been reported Figure 3 Coronal atrioventricular (en-face view) plane evaluated with the three-dimensional rendering mode: (a) normal heart, (b) tricuspid atresia (Case 1) and (c) an atrioventricular septal defect (AVSD) with common valve (Case 8). MV, mitral valve; TV, tricuspid valve.

6 650 Bennasar et al. only in a very recent series 28. In their pioneer paper, Viñals et al. 28 demonstrated that volume datasets from a firsttrimester fetal heart can be acquired in a high proportion of cases by properly trained non-expert operators and sent to an expert in EFE for offline evaluation via telemedicine. Although non-experts in echocardiography could acquire correct volumes in all patients in our series, more studies are needed and we acknowledge that the capability of screening sonographers for early STIC acquisition is still to be proven. The effectiveness of STIC in diagnosing CHDs cannot be inferred from Viñals et al. s results, as they failed to obtain an adequate volume in almost 30% of the cases and just two CHDs were diagnosed 28. Moreover, as the authors acknowledge, no pathological confirmation was provided in any case, which is essential to assess the actual role of early STIC. In contrast, we provide data on STIC performance in the first and early second trimester that may be used to counsel parents at risk, as long as our results are reproduced by others. The overall time needed for STIC acquisition and analysis (17 min) was probably not much different from that for conventional EFE. Interestingly, offline analysis obtained a 90% rate of full cardiac visualization from 12 weeks onwards. This is in accordance with Viñals et al. 28, but differs from the majority of reports and our own experience with conventional EFE, which showed similar high rates of visualization only after the 13 th week 23,24. This is novel information and merits further evaluation by others. In our opinion, it is very likely that several features of 4D-STIC, such as zoom and sharpness settings, endless repetition sequence, the possibility of shortening the cardiac rate to 50% or even less and, particularly, the offline analysis, may explain the small but significant increase in the definition of cardiac structures at 12 weeks gestation. Moreover, further improvements in the quality, storage and processing of the acquired volumes will probably allow better resolution in the near future, thus increasing the potential usefulness of EFE by 4D-STIC. Our study also demonstrates that CHDs can be diagnosed from 4D-STIC volumes with high accuracy, similarly to that described in previous studies of standard EFE (85% sensitivity and 99% specificity) 17. Indeed, we were able to diagnose all major CHDs by offline analysis with no false-positive diagnosis for major defects. Finally, limitations to performing early 4D-STIC are the same as those reported for the second trimester, such as rhythm anomalies or maternal obesity 9,10, whereas avoiding fetal movements is particularly more challenging in the first than in the second trimester. Although the number of affected cases is too small to draw firm conclusions, we suggest that echocardiography before 16 weeks gestation can be reliably performed by means of 4D-STIC technology, if it involves expert operators. Because STIC offline analysis makes it feasible to send volumes to experts without displacement of the patient, it might be offered to a high-risk population if needed. The ultimate goal would be to improve the detection rates of congenital heart disease by decreasing the dependency on operator skills required by 2D ultrasound imaging. This is important as congenital heart disease is the leading cause of death among infants with congenital anomalies, and prenatal diagnosis is associated with decreased neonatal morbidity and mortality rates. REFERENCES 1. Sharland G. Routine fetal cardiac screening: what are we doing and what should we do? Prenat Diagn 2004; 24: Abu-Harb M, Hey E, Wren C. Death in infancy from unrecognised congenital heart disease. Arch Dis Child 1994; 71: Kumar RK, Newburger JW, Gauvreau K, Kamenir SA, Hornberger LK. Comparison of outcome when hypoplastic left heart syndrome and transposition of the great arteries are diagnosed prenatally versus when diagnosis of these two conditions is made only postnatally. Am J Cardiol 1999; 83: Copel JA, Tan AS, Kleinman CS. Does a prenatal diagnosis of congenital heart disease alter short-term outcome? Ultrasound Obstet Gynecol 1997; 10: Allan L. Prenatal diagnosis of structural cardiac defects. Am J Med Genet C Semin Med Genet 2007; 145C: Garne E, Stoll C, Clementi M. Evaluation of prenatal diagnosis of congenital heart diseases by ultrasound: experience from 20 European registries. Ultrasound Obstet Gynecol 2001; 17: Gembruch U. Prenatal diagnosis of congenital heart disease. Prenat Diagn 1997; 17: Tegnander E. The examiner s ultrasound experience has a significant impact on the detection rate of congenital heart defects at the second-trimester fetal examination. Ultrasound Obstet Gynecol 2006; 28: Viñals F, Poblete P, Giuliano A. Spatio-temporal image correlation (STIC): a new tool for the prenatal screening of congenital heart defects. Ultrasound Obstet Gynecol 2003; 22: DeVore GR, Falkensammer P, Sklansky MS, Platt LD. Spatiotemporal image correlation (STIC): new technology for evaluation of the fetal heart. Ultrasound Obstet Gynecol 2003; 22: Goncalves LF, Espinoza J, Romero R, Lee W, Treadwell MC, Huang R, Devore G, Chaiworapongsa T, Schoen ML, Beyer B. Four-dimensional fetal echocardiography with spatiotemporal image correlation (STIC): a systematic study of standard cardiac views assessed by different observers. J Matern Fetal Neonatal Med 2005; 17: Makrydimas G, Sotiriadis A, Ioannidis JP. Screening performance of first-trimester nuchal translucency for major cardiac defects: a meta-analysis. Am J Obstet Gynecol 2003; 189: Hyett J, Moscoso G, Papapanagiotou G, Perdu M, Nicolaides KH. Abnormalities of the heart and great arteries in chromosomally normal fetuses with increased nuchal translucency thickness at weeks of gestation. Ultrasound Obstet Gynecol 1996; 7: Galindo A, Comas C, Martinez JM, Gutierrez-Larraya F, Carrera JM, Puerto B, Borrell A, Mortera C, de la Fuente P. Cardiac defects in chromosomally normal fetuses with increased nuchal translucency at weeks of gestation. J Matern Fetal Neonatal Med 2003; 13: Lopes LM, Brizot ML, Lopes MA, Ayello VD, Schultz R, Zugaib M. Structural and functional cardiac abnormalities identified prior to 16 weeks gestation in fetuses with increased nuchal translucency. Ultrasound Obstet Gynecol 2003; 22: McAuliffe FM, Fong KW, Toi A, Chitayat D, Keating S, Johnson JA. Ultrasound detection of fetal anomalies in conjunction with first-trimester nuchal translucency screening: a feasibility study. Am J Obstet Gynecol 2005; 193:

7 STIC echocardiography before 16 weeks Rasiah SV, Publicover M, Ewer AK, Khan KS, Kilby MD, Zamora J. A systematic review of the accuracy of firsttrimester ultrasound examination for detecting major congenital heart disease. Ultrasound Obstet Gynecol 2006; 28: Campbell S, Platt L. The publishing of papers on first-trimester Doppler. Ultrasound Obstet Gynecol 1999; 14: Cardiac screening examination of the fetus: guidelines for performing the basic and extended basic cardiac scan. Ultrasound Obstet Gynecol 2006; 27: Comas C, Galindo A, Martínez JM, Carrera JM, Gutiérrez- Larraya F, de la Fuente P, Puerto B, Borrell A. Early prenatal diagnosis of major cardiac anomalies in a high-risk population. Prenat Diagn 2002; 22: Carvalho JS. Early prenatal diagnosis of major congenital heart defects. Curr Opin Obstet Gynecol 2001; 13: Huggon IC, Ghi T, Cook AC, Zosmer N, Allan LD, Nicolaides KH. Fetal cardiac abnormalities identified prior to 14 weeks gestation. Ultrasound Obstet Gynecol 2002; 20: Haak MC, Twisk JW, Van Vugt JM. How successful is fetal echocardiographic examination in the first trimester of pregnancy? Ultrasound Obstet Gynecol 2002; 20: Martínez JM, Gómez O, Del Río M, Puerto B, Borrell A, Cararach V, Fortuny A. Early fetal echocardiography: a new challenge in prenatal diagnosis. Ultrasound Rev Obstet Gynecol 2002; 4: Paladini D, Vassallo M, Sglavo G, Lapadula C, Martinelli P. The role of spatio-temporal image correlation (STIC) with tomographic ultrasound imaging (TUI) in the sequential analysis of fetal congenital heart disease. Ultrasound Obstet Gynecol 2006; 27: Goncalves LF, Espinoza J, Romero R, Kusanovic JP, Swope B, Nien JK, Erez O, Soto E, Treadwell MC. Four-dimensional ultrasonography of the fetal heart using a novel Tomographic Ultrasound Imaging display. JPerinatMed2006; 34: Chaoui R, Hoffmann J, Heling KS. Three-dimensional (3D) and 4D color Doppler fetal echocardiography using spatio-temporal image correlation (STIC). Ultrasound Obstet Gynecol 2004; 23: Viñals F, Ascenzo R, Naveas R, Huggon I, Giuliano A. Fetal echocardiography at to weeks using fourdimensional spatiotemporal image correlation telemedicine via an Internet link: a pilot study. Ultrasound Obstet Gynecol 2008; 31: