Methods

A retrospective review of pregnancies with TTTS evaluated at the Fetal Care Center of Cincinnati between 2004 and 2010 was conducted. The study was approved by the institutional review board of Cincinnati Children’s Hospital Medical Center. Fetal echocardiographic reports and maternal clinical records were reviewed for all subjects. Patients were included when initial evaluation identified Quintero stage I or II TTTS without evidence of RT cardiomyopathy on fetal echocardiography. The diagnosis of TTTS was based on a monochorionic-diamniotic twin pregnancy with a single placenta, a thin dividing membrane, and same-gender twins, with polyhydramnios in the recipient (>8 cm depth of amniotic fluid) and oligohydramnios in the donor (<2 cm depth of amniotic fluid). Quintero score was assigned at the initial evaluation on the basis of established criteria. Outcomes analyses for a portion of this cohort have previously been reported. Pregnancies with Doppler abnormalities or hydrops that would meet classification for Quintero stage III or IV were excluded. Cardiomyopathy was defined as presence of ventricular wall hypertrophy (on qualitative assessment), atrioventricular valve regurgitation, and ventricular dysfunction with elevated myocardial performance index (MPI) values above 2 standard deviations of the mean. Patients with Quintero stage I and II TTTS without cardiomyopathy are offered observation, amnioreduction, or SFLP at our center. Patients electing observation or amnioreduction are followed with serial ultrasound and fetal echocardiography. Progression to cardiomyopathy was defined as the development of abnormal recipient echocardiographic parameters, including ventricular wall hypertrophy, atrioventricular valve regurgitation, and/or ventricular dysfunction with elevated MPI. Additional exclusion criteria included patients who underwent initial treatment with SFLP, patients who subsequently underwent SFLP without cardiomyopathy, patients who elected pregnancy termination, in utero demise before echocardiogram, and pregnancies with fetal chromosomal or structural anomalies.

The initial fetal echocardiographic examination performed at the Fetal Heart Program at Cincinnati Children’s Hospital at the time of TTTS staging for each RT and DT was reviewed. Fetal echocardiography is performed on all patients undergoing evaluation for TTTS at our center. Complete fetal echocardiograms were obtained according to published standards using either Acuson Sequoia C512 or S2000 (Siemens Medical Solutions, Inc, Malvern, PA) or Vivid 7 (GE Medical Systems, Milwaukee, WI) ultrasound systems. For all pulsed-wave Doppler interrogation, the angle of insonation was kept parallel to or <20° from the direction of flow. Information on ventricular hypertrophy, atrioventricular valve regurgitation, and right and left ventricular MPI and are reported for all TTTS echocardiograms at our center, and data for these values were taken from the echocardiographic reports. MPIs for the right and left ventricles were calculated as described previously ( Figure 1 ) and were averaged from three beats. Right ventricular MPI was calculated from tricuspid and pulmonic Doppler tracings with a heart rate difference of ≤5 beats/min. Additionally, a single blinded observer (J.K.V.-S.) reviewed the studies retrospectively to obtain the following measurements: Doppler inflow durations, cardiac cycle length, and digitized analysis of DV, MCA, and umbilical artery (UA) flow patterns, as described below, all of which were measured from a single cardiac cycle taken during fetal apnea. Doppler inflow duration for the mitral and tricuspid valves was measured as E-wave duration + A-wave duration, and corresponding cycle length duration for each filling time was measured as time from beginning of the E wave of one beat to the beginning of the E wave of the subsequent beat. Diastolic filling time corrected for heart rate (DFTc) was calculated as Doppler inflow duration divided by cycle length for each ventricle ( Figure 1 ). MCA and UA measurements included peak systolic velocity, end-diastolic velocity, and time-averaged maximum velocity (TAMX). PI of the MCA and UA were calculated as (peak systolic velocity − end-diastolic velocity)/TAMX ( Figure 2 ). DV measurements included peak systolic velocity (S), velocity during atrial contraction (A), and TAMX. DV pulsatility index (PI) for veins was calculated as (S − A)/TAMX ( Figure 2 ). Because normal values are known to vary over the course of gestation, gestational age–based Z scores of PI of the DV, MCA, and UA were calculated using published normal values, and MCA peak systolic velocity was assessed by calculating multiple of the median for gestational age. Cerebroplacental resistance ratio (CPR) was calculated as MCA PI/UA PI. A normal CPR value is >1.08 throughout gestation, as the placental vascular bed should have lower resistance than the cerebral vascular bed.

Pulsed Doppler tracing of left ventricular inflow and outflow demonstrating the intervals used to calculate the ventricular MPI and DFTc. The difference between time (A) and the ventricular ejection time (B) represents the combined time spent in isovolumic contraction and relaxation; MPI = (A − B)/B. The MPI increases with ventricular systolic and diastolic dysfunction, as time spent in isovolumic contraction and relaxation increases and the ejection time shortens. The DFT shortens as diastolic dysfunction causes impaired ventricular filling. The DFT is corrected for heart rate by dividing it by the total cardiac CL using the equation DFTc = DFT/CL. CL , Cycle length; DFT , diastolic filling time; DFTc , diastolic filling time corrected for heart rate; MPI , myocardial performance index.

Examples of arterial and venous pulsed Doppler measurements. ( Top ) MCA pulsed Doppler, with measurements of PSV, EDV, and TAMX. PI of the MCA as well as the UA is calculated as MCA PI = (PSV − EDV)/TAMX. ( Bottom ) DV pulsed Doppler with measurements of PSV (S), velocity during atrial contraction (A), and TAMX. DV PI = (S − A)/TAMX. DV , Ductus venosus; EDV , end-diastolic velocity; MCA , middle cerebral artery; PI , pulsatility index; PSV , peak systolic velocity; TAMX , time-averaged maximum velocity; UA , umbilical artery.

Pregnancies were categorized into two groups on the basis of whether the RT eventually developed cardiomyopathy. Unpaired t tests were used to compare continuous variables between RTs and DTs of the two groups. Statistical analysis was performed using SAS version 9.3 (SAS Institute, Inc, Cary, NC). Categorical data were compared using χ ² or Fisher exact tests as appropriate. Statistical significance was assigned to P values < .05. No adjustment was made to P values to account for the number of tests.

Results

Among 174 pregnancies with Quintero stage I and II TTTS evaluated during the study period, 122 (70%) had RT cardiomyopathy and were excluded from subsequent analysis. Of those without initial cardiomyopathy, seven met additional exclusion criteria, including two initially treated with SFLP (both of whom were randomized to SFLP as part of a separate study), two with subsequent SFLP without cardiac progression, one pregnancy termination, one in utero demise, and one fetal anomaly. Thus, 45 TTTS pregnancies met the inclusion criteria and constituted the study group. Among these cases, 20 (44%) had development of RT cardiomyopathy on subsequent echocardiography, an average of 2.1 ± 1.9 weeks from the initial study, while the other 25 (56%) RTs had stable, normal results on echocardiography. The development of cardiomyopathy included elevated MPIs in 19 of 20 cases. No cardiac abnormalities were noted in any DT. Baseline characteristics of the study population are given in Table 1 . RTs with subsequent progression to cardiomyopathy had lower gestational ages on initial evaluation, were less frequently in Quintero stage I (and more frequently in Quintero stage II) on initial evaluation, and were more likely to undergo amnioreduction instead of observation as the initial treatment.

Echocardiographic and Doppler parameters are given in Table 2 . There was no significant difference in right or left ventricular MPI between groups; however, RTs with subsequent development of cardiomyopathy had significantly shorter DFTc for both ventricles ( Table 2 , Figure 3 ). There was no significant difference in heart rate between the groups. DV PI Z scores were significantly higher in RTs who went on to develop cardiomyopathy ( Table 2 , Figure 4 ). Monophasic Doppler inflow patterns were rare in both groups.

Comparison of DFTc for the left (A) and right (B) ventricles from first echocardiogram between RTs who did and did not go on to develop cardiomyopathy. An “X” marks the mean value for each group. DFTc , Diastolic filling time corrected for heart rate; RT , recipient twin.

Comparison of DV PI Z -score data points from first echocardiogram between RTs who did and did not go on to develop cardiomyopathy. An “X” marks the mean value for each group. DV , Ductus venosus; PI , pulsatility index; RT , recipient twin.

CPR was significantly lower in the RTs who later developed cardiomyopathy, and the mean CPR value of 0.93 in the RTs who later developed cardiomyopathy was abnormally low (<1.08), whereas it was a normal range for the RTs who did not develop cardiomyopathy ( Table 2 , Figure 5 a). Seventy-seven percent of the RTs who went on to develop cardiomyopathy had CPR < 1.08, whereas this was seen in 28% of the RTs without progression to cardiomyopathy ( P = .007). Additionally, MCA PI Z scores were significantly lower in the RTs who later developed cardiomyopathy ( Table 2 , Figure 5 b), though only one RT in that group had an MCA PI Z score < −2. UA PI Z scores did not display significant differences between groups, indicating that lower cerebral vascular resistance was responsible for the observed difference in CPR between the groups, rather than elevated umbilical vascular resistance. MCA peak systolic velocities, expressed as multiples of the median for gestational age, did not vary between groups.

Comparison of CPR (A) and MCA PI Z -score (B) data points from first echocardiogram for RTs who did and did not go on to develop cardiomyopathy. An “X” marks the mean value for each group. RT with points falling below the dashed line in (A) demonstrate abnormally low CPR (<1). CPR , Cerebroplacental resistance ratio; MCA , middle cerebral artery; PI , pulsatility index; RT , recipient twin.

When the DTs, grouped by whether their RTs later developed cardiomyopathy, were compared, no significant differences were found for any of the parameters evaluated ( Table 3 ). However, of note, the mean CPR for the DTs whose RTs went on to develop cardiomyopathy was abnormally low at 1.05. Overall, 16 of 35 DTs (44%) with cerebral and umbilical measurements available had low CPR (<1.08), including 53% of those whose RTs developed cardiomyopathy and 39% of those whose RTs did not develop cardiomyopathy ( P = NS).

Table 3

Echocardiographic parameters of DTs on initial cardiac evaluation

Parameter	DTs with RT progression to cardiomyopathy ( n = 20)	DTs with no RT cardiomyopathy ( n = 25)	P
RV MPI	0.31 ± 0.06	0.34 ± 0.10	.35
LV MPI	0.32 ± 0.07	0.34 ± 0.06	.20
RV DFTc	0.44 ± 0.04	0.43 ± 0.03	.28
LV DFTc	0.45 ± 0.04	0.44 ± 0.04	.32
DV PI Z score	0.46 ± 1.37	0.88 ± 1.39	.33
UA PI Z score	1.14 ± 1.59	1.02 ± 1.59	.81
MCA PI Z score	−0.55 ± 0.94	−0.65 ± 0.99	.76
CPR	1.05 ± 0.24	1.10 ± 0.22	.54
MCA PSV MOM	0.89 ± 0.27	0.88 ± 0.29	.94

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