Objective
To evaluate cardiac function by tissue Doppler imaging vs conventional echocardiography in intrauterine growth restriction.
Study Design
A prospective study in 25 intrauterine growth restriction, and in 50 normally grown fetuses between 24 and 34 weeks. Conventional echocardiography (E/A ratios, outflow tract velocities and myocardial performance index), and tissue Doppler (myocardial peak velocities, E’/A’ ratios and myocardial performance index’) measurements were performed.
Results
With conventional echocardiography, intrauterine growth restriction fetuses showed an increase in left myocardial performance index but similar values of E/A ratios, outflow tract velocities and right myocardial performance index as compared with controls. Tissue Doppler imaging demonstrated that intrauterine growth restriction fetuses had significantly lower systolic and diastolic myocardial velocities in mitral and tricuspid annulus, higher mitral E’/A’ ratio and higher mitral, tricuspid and septal myocardial performance index’ values.
Conclusion
Tissue Doppler imaging demonstrated the presence of both systolic and diastolic cardiac dysfunction in intrauterine growth restriction. Tissue Doppler imaging may constitute a more sensitive tool than conventional echocardiography to evaluate cardiac dysfunction in intrauterine growth restriction.
Intrauterine growth restriction (IUGR) caused by placental insufficiency affects 1-3% of pregnancies and is associated with an increased risk of perinatal mortality and morbidity. Cardiac dysfunction with maintained cardiac output has consistently been reported to be present in IUGR. Although earlier studies suggested that cardiac parameters became abnormal only in severely affected fetuses, more recent research strongly suggests that subclinical cardiac dysfunction could be present from early stages of fetal deterioration. The identification and monitoring of cardiac dysfunction may be relevant for clinical purposes and to advance in the understanding of the relation between IUGR and long-term cardiovascular outcome.
New developments in echocardiography enable a much fuller assessment of cardiac function, including measurement of myocardial motion by tissue Doppler imaging (TDI). TDI is a robust and reproducible echocardiographic tool that permits a quantitative assessment of motion and timing of myocardial events. Myocardial velocities are a sensitive marker of mildly impaired systolic or diastolic function and therefore useful in the early identification of subtle cardiac dysfunction in preclinical stages. In adults and children, TDI has demonstrated its use in the prediction of future cardiovascular diseases. Recently, TDI has been shown to be feasible in fetuses. The results of preliminary studies in IUGR fetuses suggest that there is a reduction in myocardial velocities. We postulated that TDI could constitute a more sensitive tool than conventional echocardiography to detect the presence of cardiac dysfunction in fetuses with IUGR.
We performed a prospective study to evaluate cardiac function parameters with TDI and with conventional echocardiography in a group of fetuses with early onset IUGR.
Materials and Methods
Study populations
The study population included 25 IUGR fetuses and 50 controls. Patients were selected from women who attended the Maternal-Fetal Medicine Department at Hospital Clinic in Barcelona, Spain. The study protocol was approved by the local Ethics Committee and patients provided their written informed consent. In all pregnancies, gestational age was calculated based on the crown-rump length at first-trimester ultrasound. IUGR was defined as an estimated fetal weight below the 10th percentile according to local reference curves, together with umbilical artery (UA) pulsatility index (PI) above the 95th percentile. For the purpose of this study, only patients who were delivered between 26 and 34 weeks of gestation were included. The control group consisted of 50 normally grown fetuses matched 2 to 1 with cases by gestational age at ultrasound (± 1 week). Exclusion criteria were structural/chromosomal anomalies or evidence of fetal infection.
All patients underwent ultrasonographic examination using a Siemens Sonoline Antares (Siemens Medical Systems, Malvern, PA). Basic Doppler examination included UA, middle cerebral artery, and ductus venosus. At delivery, gestational age, mode of delivery, birthweight, birthweight percentile, Apgar score, umbilical pH, and perinatal mortality and morbidity were recorded. Perinatal mortality was defined as either intrauterine death or neonatal death within the first 28 days of life. Adverse perinatal outcome was defined by the presence of perinatal death, bronchopulmonary dysplasia, hyaline membrane disease, neonatal intraventricular hemorrhage grade 3 or 4, necrotizing enterocolitis, sepsis, or retinopathy grade 3 or 4.
Cardiac function was assessed in all cases and controls by conventional echocardiography and TDI.
Conventional echocardiography
Conventional echocardiography included peak early (E) and late (A) transvalvular filling and outflow tracts velocities and myocardial performance index (MPI). Atrioventricular flows were obtained from a basal or apical 4-chamber view, placing the pulsed Doppler sample volume just below valve leaflets, and left and right E/A ratios were calculated. Aortic and pulmonary artery peak velocities were obtained from a long- or short-axis view of the left and right ventricle respectively. Left MPI was obtained using the clicks of mitral and aorta valves as landmarks, as previously described. The following periods were calculated: isovolumetric contraction time (ICT), ejection time (ET), and isovolumetric relaxation time (IRT). Finally, the MPI was calculated as (ICT + IRT)/ET. Right MPI was calculated by obtaining right ventricle inflow and outflow obtained in series from separate cardiac cycles.
TDI
TDI was obtained in real time using a 2-10 MHz phased-array transducer. First, a clear 4-chamber view was obtained in an apical or basal view. The TDI program was set to the pulsed-wave mode with a sample volume size between 2 and 4 mm. Sample volumes were placed in the basal part of the left ventricular wall (mitral annulus), interventricular septum and right ventricular wall (tricuspid annulus) ( Figure 1 ). The insonation ultrasound beam was kept at an angle of <30° to the orientation of the ventricular wall or the interventricular septum and no angle correction was applied. Peak annular velocities were measured in early diastole (PVE’), atrial contraction (PVA’), and systole (PVS’). The ratio of E’ to A’ was calculated in each location. Left, right, and septal MPI’ were also measured by TDI. To calculate MPI by TDI (MPI’), the following periods were calculated: ICT’, ET’, and IRT’. Finally, left, right, and septal MPI’ were calculated as (ICT’ + IRT’)/ET’. Measurement of all MPI’ components were made from the same cardiac cycle.
To determine TDI reliability, 50 fetuses were evaluated by the same operator and 30 fetuses by 2 independent operators.
Statistical analysis
Data were analyzed with the SPSS 15.0 statistical package (SPSS Inc, Chicago, IL). Results are expressed as mean ± standard deviation or proportions. Comparisons between groups were performed by t test, and echocardiographic parameters were also compared by logistic regression adjusted by estimated fetal weight. Reliability analyses were performed by means of the intraclass correlation coefficient for agreement.
Results
Characteristics of the study populations
The characteristics of the study populations are reported in Table 1 . Preeclampsia was present in 54% of the IUGR pregnancies. As expected, UA, middle cerebral artery, cerebroplacental ratio, and ductus venosus PI were significantly different in IUGR fetuses compared with controls. Among the IUGR fetuses, 10 had UA absent-end diastolic flow, 1 had UA reverse diastolic flow, and 2 had absent or reverse flow in the ductus venosus. Compared with controls, pregnancies with IUGR presented lower gestational age at delivery, birthweight, Apgar score, and umbilical artery pH, and higher rates of cesarean section, perinatal mortality, and adverse outcome.
| Characteristics | Controls | IUGR |
|---|---|---|
| n | 50 | 25 |
| Clinical characteristics | ||
| Maternal age, y | 31 (5) | 32 (5) |
| White, % | 70 | 65 |
| Nulliparous, % | 70 | 52 |
| Maternal body mass index, g/m 2 | 23 (5) | 24 (6) |
| Smoker, % | 9 | 19 |
| Preeclampsia, % | 0 | 54 a |
| Basic Doppler data | ||
| Gestational age at ultrasound, wk | 30 (3) | 30 (3) |
| Umbilical artery PI | 1.06 (0.24) | 1.89 (0.34) a |
| Middle cerebral artery PI | 2.08 (0.38) | 1.37 (0.30) a |
| Cerebroplacental ratio | 2.05 (0.55) | 0.77 (0.24) a |
| Ductus venosus PI | 0.56 (0.16) | 0.79 (0.35) a |
| Perinatal outcome | ||
| Gestational age at delivery, wk | 39 (1) | 31 (2) a |
| Cesarean section, % | 18 | 91 a |
| Birthweight, g | 3347 (453) | 993 (330) a |
| Birthweight percentile | 53 (29) | 5 (4) a |
| 5-min Apgar | 10 (1) | 8 (2) a |
| Umbilical artery pH | 7.25 (0.07) | 7.21 (0.09) a |
| Perinatal death, % | 0 | 15 a |
| Adverse perinatal outcome, % | 2 | 30 a |
Conventional echocardiography
Values of conventional echocardiographic parameters are shown in Table 2 . E and A velocities were significantly reduced in IUGR. However, E/A ratios were not significantly different in IUGR as compared with controls. Aortic and pulmonary artery peak velocity were reduced with respect to controls, but the difference was not statistically different when adjusting by fetal weight. Although IUGR fetuses showed increased left MPI values, right MPI values were similar among cases and controls.
| Parameters | Controls | IUGR | P value a | Adjusted P value b |
|---|---|---|---|---|
| Diastolic parameters | ||||
| Left E velocity, cm/s | 37 (5.4) | 31 (7.4) | < .001 | .002 |
| Left A velocity, cm/s | 50 (8.5) | 41 (10.1) | < .001 | < .001 |
| Left E/A | 0.74 (0.1) | 0.78 (0.2) | .34 | .07 |
| Right E velocity, cm/s | 43 (7.9) | 32 (7.5) | < .001 | < .001 |
| Right A velocity, cm/s | 57 (9.2) | 39 (7.2) | < .001 | < .001 |
| Right E/A | 0.76 (0.1) | 0.81 (0.1) | .13 | .2 |
| Systolic parameters | ||||
| Aortic peak velocity, cm/s | 94 (20.2) | 81 (16.5) | .02 | .245 |
| Pulmonary artery peak velocity, cm/s | 91 (20.9) | 84 (24.5) | .4 | .122 |
| MPI | ||||
| Left MPI | 0.45 (0.06) | 0.52 (0.09) | .02 | .006 |
| Right MPI | 0.47 (0.19) | 0.45 (0.13) | .34 | .38 |
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