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Assessment of Right Ventricular Function in Recipient Twin of Twin to Twin Transfusion Syndrome with Speckle Tracking Echocardiography
Ultrasound in Med. & Biol., Vol. 38, No. 9, pp. 1502–1507, 2012 Copyright Ó 2012 World Federation for Ultrasound in Medicine & Biology Printed in the USA. All rights reserved 0301-5629/$ - see front matter
doi:10.1016/j.ultrasmedbio.2012.05.009
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Original Contribution ASSESSMENT OF RIGHT VENTRICULAR FUNCTION IN RECIPIENT TWIN OF TWIN TO TWIN TRANSFUSION SYNDROME WITH SPECKLE TRACKING ECHOCARDIOGRAPHY SHENG ZHAO,* YOU-BIN DENG,* XIN-LIN CHEN,y and RONG LIUy * Department of Medical Ultrasound, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China; and y Department of Medical Ultrasound, Hubei Maternal & Children’s Hospital, Wuhan, China (Received 19 December 2011; revised 2 May 2012; in final form 11 May 2012)
Abstract—This study was undertaken to evaluate the right ventricular myocardial systolic function and its relation to the fetal volume and pressure overload in recipient twin of twin to twin transfusion syndrome with speckle tracking echocardiography. Longitudinal peak systolic strains of the right ventricle were measured by speckle tracking echocardiography in 17 patients with twin-to-twin transfusion syndrome (TTTS) and 19 normal monochorionic diamniotic pregnancies. The right ventricular free wall thickness in recipient twin (0.43 ± 0.14 cm) was significantly larger than that in the donor (0.21 ± 0.04 cm, p , 0.05) and the control group (0.18 ± 0.03 cm, p , 0.05 for larger twin and 0.17 ± 0.02 cm, p , 0.05 for smaller twin). Although there were no significant differences in the right ventricular fractional shortening and cavity area percent change among control and the TTTS groups, the absolute value of peak systolic strains of ventricular septum, right ventricular free wall and global right ventricle in recipients were all significantly lower than those of the donors and the control group. Besides, the global right ventricular peak systolic strain correlated well with gestational age adjusted right ventricular free wall thickness (r 5 0.65, p 5 0.04) but not with gestational age adjusted right ventricular end-diastolic dimension (r 5 0.38, p 5 0.28) and cavity area percent change (r 5 0.33, p 5 0.35). Right ventricular systolic dysfunction measured with decreased right ventricular peak systolic longitudinal strain exists despite the absence of diminished fractional shortening and cavity area percent change and this reduced systolic function correlates with the right ventricular pressure overload as shown by increased right ventricular free wall thickness. (E-mail: ybdeng2007@hotmail. com) Ó 2012 World Federation for Ultrasound in Medicine & Biology. Key Words: Cardiac function, Speckle tracking echocardiography, Two-dimensional strain, Monochorionic twins, Twin to twin transfusion syndrome.
subsequent pressure overload as a consequence of elevated concentration of endothelin in the recipient and upregulation of the rennin-angiotension system in the donor twin (Bajoria et al. 1995; Bajoria et al. 1999; Mahieu-Caputo et al. 2000). Although the myocardial diastolic function has been demonstrated to be impaired by measuring the isovolume relaxation time and myocardial performance index with pulsed Doppler flow recording in recipient twin, the systolic function evaluated with fractional shortening is preserved in all or diminished only in a small number of recipient twin (Barrea et al. 2005; Raboisson et al. 2004). In addition, it is not known whether fetal cardiac function in TTTS is related to the volume or pressure overload. Speckle tracking echocardiography is a novel technique for analyzing myocardial motion (Amundsen et al. 2006). The method uses B-mode images for speckle tracking analysis and allows calculation of myocardial
INTRODUCTION Twin-to-twin transfusion syndrome (TTTS) is a gestational condition restricted to monochorionic twin pregnancies (Cincotta and Fisk 1997). Many studies have shown that the cardiac function decreased and right ventricular function seemed to be affected much more commonly than left ventricular function in recipient twin (Barrea et al. 2005; Michelfelder et al. 2007; Raboisson et al. 2004; Rychik et al. 2007). It was indicated that in TTTS, the fetal cardiac function decreased because of chronic volume overload as a consequence of the net transfer of blood from the donor twin to the recipient through placental vascular anastomoses and/or Address correspondence to: You-Bin Deng, M.D., Ph.D., Department of Medical Ultrasound, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, 1095 Jiefang Road, Wuhan 430030, China. E-mail: [email protected] 1502
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displacement and strain (Deng et al. 2010). Regional myocardial strain measured by speckle tracking echocardiography has been demonstrated to be a sensitive parameter for the evaluation of regional myocardial systolic function in patients with preserved global left ventricular systolic function, including those with diastolic heart failure, hypertension and coronary heart disease without visual regional wall motion abnormality (Deng et al. 2010; Liang et al. 2006; Yip et al. 2002; Wang et al. 2008). Recent studies have shown that speckle tracking echocardiography is feasible in assessing fetal cardiac function in fetuses with and without heart disease (Mieghem et al. 2010; Younoszai et al. 2008). Therefore, the present study was undertaken to evaluate the right ventricular myocardial systolic function and its relation to the fetal volume and pressure overload in recipient twin of twin to twin transfusion syndrome with speckle tracking echocardiography. MATERIALS AND METHODS Study population Study population consisted of 17 patients with TTTS. TTTS was diagnosed as the presence of oligohydramnios in the donor twin with a deepest vertical amniotic fluid pocket ,2 cm and polyhydramnios in the recipient twin with a deepest amniotic fluid .8 cm prior to 20 weeks and .10 cm after 20 weeks in a monochorionic twin pregnancy (Senat et al. 2004). Patients were staged based on Quintero’s staging system (Quintero et al. 1999). Nineteen subjects with normal monochorionic diamniotic pregnancies were recruited as the control group at a gestational age between 16.5 and 26.6 weeks. Monochorionicity was identified by the presence of ‘‘T’’ sign between 10 and 14 weeks, or twins of the same sex with a single placenta. Pathologic examination of the placenta after birth confirmed chorionicity in all cases. Those fetuses with pathologies that could lead to abnormal cardiac function (intrauterine growth restriction, gestational diabetes, fetal arrhythmia, fetal malformations and chromosomal defects) were excluded from this study. The study was approved by the local ethics committee and informed consent was obtained from all of the mothers. Fetal echocardiographic and speckle tracking recording and analysis Fetal echocardiography was performed according to the recommendations of the International Society of Ultrasound in Obstetrics & Gynecology (ISUOG 2006) with a 6C2 probe on Siemens Acuson Sequoia 512 (Siemens Medical Solutions, Mountain View, CA, USA). The following parameters were measured in all fetuses according to methods described previously: cardiothoracic ratio (Paladini et al. 1990), peak systolic velocity of middle
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cerebral artery (Mari and Deter 1992), pulsatility indexes of umbilical artery (Sonesson et al. 1993), middle cerebral artery and ductus venousus, end-diastolic and end-systolic dimensions of right ventricle and end-diastolic thickness of right ventricular free wall (Schiller et al. 1989). Enddiastolic and end-systolic right ventricular cavity areas were measured on four-chamber view by tracing the endocardium manually. The right ventricular fractional shortening was calculated by dividing the difference of the right ventricular end-diastolic and end-systolic dimensions with the end-diastolic dimension. Similarly, right ventricular cavity area percent change was calculated by dividing the difference of the right ventricular end-diastolic and end-systolic cavity areas with the enddiastolic cavity area. Right ventricular myocardial performance index was also measured on pulsed Doppler velocity waveforms as described before (Raboisson et al. 2004). The right ventricular dimension and cavity area and thickness of right ventricular free wall at enddiastole were adjusted with the gestational age. Fetal weight and gestational age were determined by the earliest second-trimester ultrasound measurements of head and abdominal circumferences and femur length (Hadlock et al. 1984). The fetal weight discordance was calculated by dividing the difference of the weight between larger and smaller twin with fetal weight of larger twin. Syngo VVI software (Siemens Medical Solutions) was used for speckle tracking analysis. First, a digital clip of zoomed fetal four-chamber view was recorded and then transferred to the offline workstation. Second, the beginning and end of a cardiac cycle was defined with M-mode tracing of ventricular wall or atrioventricular valve motion. Third, the endocardium of the right ventricle was traced manually from a single end-systolic frame with clear endocardial border. After the tracking quality was verified for each segment (with subsequent manual adjustment of the region-of-interest if necessary), myocardial motion was analyzed by speckle-tracking within the region-of-interest bound by endocardial and epicardial borders. Myocardial longitudinal strain profile was obtained and peak systolic strain value was measured (Fig. 1). Peak systolic longitudinal strain of the ventricular septum and right ventricular free wall were calculated by averaging the segmental strain values (Fig. 1). Interobserver and intraobserver reproducibility To assess the reproducibility of the strain measurements, peak systolic longitudinal strain in five recipient twins and five control twins were measured by two independent observers on the same day and by one observer twice, 1 week apart. The interobserver and intraobserver variability is calculated as a percentage of the absolute difference between the two measurements divided by the mean value of the measurements.
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Fig. 1. (a) Zoomed diastolic fetal four-chamber view from a fetus in the control group with demonstration of the endocardial tracing of the right ventricle. (b) Longitudinal strain curves from six segments of the right ventricular wall. Curves 1 to 3 are the longitudinal strain curve of the basal, middle and apical segments of the right ventricular free wall and the peak systolic longitudinal strain of the right ventricular free wall was calculated by averaging the 3 peak systolic longitudinal strains measured from these three curves. Curves 4 to 6 are the longitudinal strain curve of the apical, middle and basal segments of the ventricular septum and peak systolic longitudinal strain of the ventricular septum was calculated by averaging the three peak systolic longitudinal strains measured from these three curves. Curve 7 is the global longitudinal strain curve and global peak systolic longitudinal strain of the right ventricle is measured from the curve. LA 5 left atrium; LV 5 left ventricle; RA 5 right atrium; RV 5 right ventricle.
Statistical analysis Data are presented as mean 6SD. An unpaired t-test was used to compare parameters between control fetuses and fetuses with TTTS. Parameters among recipient and donor twins in TTTS and larger and smaller twins in controls were compared by analysis of variance. Significant differences between groups were assessed using the Scheffe F test for multiple comparisons. Differences in proportions were tested by c2 analysis. Relationship between parameters was assessed by simple linear regression analysis. All statistical analyses were performed using the SPSS 13.0 software (SPSS Inc, Chicago, IL, USA). A p value of less than 0.05 was considered significant. RESULTS Patient characteristics The majority of TTTS cases in this study were in Quintero stages III, with 1 at stage I, 2 at stage II, 11 at stage III and 3 at stage IV. Mean maternal age was 26.2 6 4.5 years. The gestational age at diagnosis was 22.7 6 2.8 weeks. Right ventricular outflow tract obstructions were detected in two recipient twins (stage III and stage IV, respectively), which manifested pulmonary valve atresia with detectable retrograde flow in pulmonary artery. Intracranial hemorrhage was detected in one recipient twin with stage IV. The clinical characteristics of each group are shown in Table 1. No differences were seen in maternal age,
gestational age, fetal weight of smaller twin between the TTTS and control group. However, fetal weight of larger twin and fetal weight discordance in TTTS group were significantly higher than those in the control group (p , 0.05). Doppler and echocardiographic findings Echocardiographic findings and Doppler parameters of TTTS and the control groups are shown in Table 2. No differences were seen in pulsatility index of umbilical artery, peak systolic velocity of middle cerebral artery, heart rate, right ventricular end-diastolic dimension and cavity area, gestational age adjusted right ventricular end-diastolic dimension and cavity area, and right ventricular fractional shortening and cavity area percent change between the TTTS and control group. However, cardiothoracic ratio, right ventricular free wall thickness, gestational age adjusted right ventricular free wall thickness and right ventricular myocardial performance index in the recipients were all significantly higher than those of donors and the control group (larger and smaller twins), whereas pulsatility index of middle cerebral artery in the recipients were significantly lower than that of other fetus. Speckle tracking echocardiographic findings Adequate speckle tracking analyses were available in 11 recipients and eight donors in TTTS group with
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Table 1. Clinical characteristics of study population Variable
Control group (pregnancy n 5 19) (fetus n 5 38)
TTTS group (pregnancy n 5 17) (fetus n 5 34)
p value
Maternal age (years) Gestational age (weeks) Larger twin FW (g) Smaller twin FW (g) FW discordance (%)
28.2 6 4.7 21.0 6 2.4 427 6 176 397 6 171 7.2 6 7.0
26.2 6 4.5 22.7 6 2.8 710 6 490 477 6 270 26.8 6 16.8
0.197 0.068 0.025 0.293 ,0.001
TTTS 5 twin-to-twin transfusion syndrome; FW 5 fetal weight. Data are expressed as mean 6SD.
a success rate of 64.7% (11/17) and 47.1% (8/17), respectively. In the control group, adequate speckle analyses were available in 30 twins with a success rate of 78.9% (30/38). The interobserver variability for peak systolic longitudinal strain was 8.3 6 6.7%, and the intraobserver variability for that index was 7.6 6 6.8%. Peak systolic longitudinal strains of right ventricle in TTTS and the control group are shown in Table 3. No statistically significant differences were seen in the peak systolic strains of ventricular septum, right ventricular free wall and global right ventricle among the donor twin and control group. However, the absolute value of peak systolic strains of ventricular septum, right ventricular free wall and global right ventricle in recipients were all significantly lower than those of donors and the control group. The global right ventricular peak systolic strain in recipients correlated with the gestational age adjusted right ventricular free wall thickness (r 5 0.65, p 5 0.04) but not with gestational age adjusted right ventric-
ular end-diastolic dimension (r 5 0.38, p 5 0.28) and cavity area (0.33, p 5 0.35). DISCUSSION In the present study, we found that although no right ventricular systolic dysfunction could be detected in recipient twin of TTTS with conventional measurement of right ventricular fractional shortening and cavity area percent change, peak systolic longitudinal strains of ventricular septum, right ventricular free wall and global right ventricle in recipient twins reduced significantly compared with those in the donor twin and control groups. Furthermore, we demonstrated that global right ventricular peak systolic strain in the recipient twin correlated with the right ventricular free wall thickness but not with the right ventricular end-diastolic dimension and cavity area. Previous studies indicated that ventricular dysfunction can occur and right ventricular function is affected
Table 2. Doppler and echocardiographic parameters of study population Control group (pregnancy n 5 19)
TTTS group (pregnancy n 5 17)
Variable
Larger twin (f n 5 19)
Smaller twin (f n 5 19)
Recipients (f n 5 17)
Donors (f n 5 17)
p value
UA-PI MCA-PSV (cm/s) MCA-PI DV-PI HR (beat/min) CTR RVEDD (cm) RVCA (cm2) RVEDD/GA (cm/w) RVCA/GA (cm2/w) RVFWT (cm) RVFWT/GA (cm/w) RVMPI RVFS (%) RVCAPC (%)
1.28 6 0.15 24.1 6 6.0 1.65 6 0.29 0.72 6 0.21 151 6 6 0.26 6 0.04 0.80 6 0.27 0.56 6 0.20 0.38 6 0.10 0.26 6 0.06 0.18 6 0.03 0.09 6 0.01 0.33 6 0.16 22 6 3 43 6 11
1.31 6 0.15 23.3 6 3.5 1.64 6 0.19 0.74 6 0.17 148 6 8 0.26 6 0.03 0.68 6 0.26 0.49 6 0.18 0.32 6 0.10 0.23 6 0.06 0.17 6 0.02 0.08 6 0.01 0.33 6 0.10 22 6 3 41 6 9
1.44 6 0.38 32.6 6 18.5 1.37 6 0.38* 0.89 6 0.39 146 6 9 0.36 6 0.06* 0.93 6 0.38 0.69 6 0.33 0.38 6 0.10 0.28 6 0.09 0.43 6 0.14* 0.18 6 0.06* 0.68 6 0.30* 22 6 10 38 6 6
1.49 6 0.27 29.1 6 10.7 1.66 6 0.46 0.96 6 0.40 150 6 11 0.29 6 0.08 0.84 6 0.22 0.63 6 0.47 0.35 6 0.05 0.29 6 0.13 0.21 6 0.04 0.09 6 0.02 0.31 6 0.22 24 6 6 40 6 10
0.074 0.073 0.039 0.062 0.396 ,0.001 0.072 0.131 0.157 0.286 ,0.001 ,0.001 ,0.001 0.592 0.671
TTTS 5 twin-to-twin transfusion syndrome; f 5 fetus; UA-PI 5 pulsatility index of umbilical artery; MCA-PSV 5 peak systolic velocity of middle cerebral artery; MCA-PI 5 pulsatility index of middle cerebral artery; DV-PI 5 pulsatility index of ductus venosus; HR 5 heart rate; CTR 5 cardiothoracic ratio; RVEDD 5 right ventricular end-diastolic dimension; RVCA 5 right ventricular end-diastolic cavity area; RVFWT 5 right ventricular free wall thickness; RVMPI 5 right ventricular myocardial performance index; RVFS 5 right ventricular fractional shortening; RVCAPC 5 right ventricular cavity area percent change; GA 5 gestational age; w 5 week. Data are expressed as mean 6SD. * p , 0.05 vs. other three groups.
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Table 3. Comparison of peak systolic longitudinal strain of right ventricle in TTTS and control groups Control group (pregnancy n 5 16)
TTTS group (pregnancy n 5 11)
Variable
Larger twin (f n 5 16)
Smaller twin (f n 5 14)
Recipients (f n 5 11)
Donors (f n 5 8)
p value
VS Free wall Global
218.6 6 6.3 213.4 6 5.6 216.2 6 4.8
216.5 6 8.5 216.0 6 5.2 216.3 6 5.8
28.7 6 4.6* 25.8 6 2.9* 27.2 6 3.4*
219.7 6 8.9 217.1 6 5.7 218.4 6 5.7
0.005 ,0.001 ,0.001
TTTS 5 twin-to-twin transfusion syndrome; f 5 fetus; VS 5 ventricular septum. Data are expressed as mean 6SD. * p , 0.05 vs. other three groups.
much more commonly than left ventricular function in the recipient twin of TTTS (Barrea et al. 2005; Michelfelder et al. 2007; Raboisson et al. 2004; Rychik et al. 2007). Ventricular dysfunction usually manifested as diastolic dysfunction in the early stage of TTTS and diastolic dysfunction can occur before the systolic dysfunction (Barrea et al. 2005; Raboisson et al. 2004). It was demonstrated that right ventricular systolic function evaluated with fractional shortening or isovolumic contraction time is preserved although diastolic function is impaired in most recipient twins of TTTS (Barrea et al. 2005; Raboisson et al. 2004). Barrea et al. reported that ventricular systolic dysfunction occurs in only one third of the recipients and ventricular diastolic dysfunction is present in approximately two thirds of the recipient twins (Barrea et al. 2005). Another study by Raboisson et al. showed normal ventricular fractional shortening and isovolumic contraction time and significant prolongation of the isovolumic relaxation time, indicating preserved right ventricular systolic function and diminished right ventricular diastolic function in recipient twin (Raboisson et al. 2004). All those studies mentioned above demonstrate that diastolic dysfunction can occur even in the absence of systolic dysfunction. We measured the right ventricular free wall thickness by using the two-dimensional (2-D) echocardiographic technique, which provides us information about the cardiac structure. We also measured the myocardial strain by using the speckle tracking echocardiographic technique, which provides us information about the cardiac function. Speckle tracking echocardiography is a new technique for analyzing myocardial motion (Amundsen et al. 2006), which uses B-mode images for speckle tracking analysis and allows calculation of myocardial displacement and strain (Deng et al. 2010). Regional myocardial strain obtained from speckle tracking echocardiography has been demonstrated to be a sensitive parameter for the evaluation of regional myocardial systolic function (Deng et al. 2010; Liang et al. 2006; Yip et al. 2002; Wang et al. 2008). In the present study, we found that although there was no statistically significant difference in right ventricular fractional shortening and cavity area percent change among the recipient, donor twins and control group, the peak systolic
strains of ventricular septum and right ventricular free wall, and global peak systolic right ventricular strain decreased compared with those in the donor twin and control group, suggesting that right ventricular systolic function declined even in the absence of decreased ventricular fractional shortening and cavity area percent change. Indeed, a recent study conducted by Mieghem et al. also showed reduced peak systolic right ventricular strain in TTTS compared with controls (Mieghem et al. 2010). Our findings go along with the concept that regional myocardial strain is a sensitive parameter for evaluation of regional myocardial systolic function in patients with preserved global left ventricular systolic function in adult patients, including those with diastolic heart failure, hypertension and coronary heart disease without visual regional wall motion abnormality (Deng et al. 2010; Liang et al. 2006; Yip et al. 2002; Wang et al. 2008). Our previous study conducted in patients with coronary artery disease and normal ejection fraction revealed a reduction in longitudinal peak systolic strain in myocardial segments subtended by larger than 75% coronary stenosis compared with those subtended by less than 75% coronary stenosis (Deng et al. 2010). Similarly, a decreased longitudinal systolic strain as measured by tissue spackle tracking, was reported in patients with diastolic heart failure and normal left ventricular ejection fraction (Yip et al. 2002; Wang et al. 2008). Traditionally, ventricular dysfunction in recipient twin of TTTS was thought to be a result of chronic volume overload as a consequence of the net transfer of blood from the donor twin to the recipient through placental vascular anastomoses and/or subsequent pressure overload as a consequence of elevated concentration of endothelin in the recipient and upregulation of the rennin-angiotensin system in the donor twin (Bajoria et al. 1995, 1999; Mahieu-Caputo et al. 2000). Recently, many studies found that there is a significantly increased ventricular wall thickness and ventricular dysfunction occurring in the absence of cardiac chamber dilation in recipient twin (Barrea et al. 2005; Raboisson et al. 2004). These findings support the hypothesis that ventricular dysfunction in the recipient results from the myocardial hypertrophy rather than ventricular dilation. Our
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study further expanded these observations by demonstrating that right ventricular dysfunction manifested as reduced global right ventricular peak systolic strain, which correlated well with gestational age-adjusted thickness of the right ventricular free wall, but not with right ventricular dimension, indicating that right ventricular systolic dysfunction in recipient twin is related with the right ventricular pressure overload, but not with right ventricular volume overload. Successful speckle tracking analysis depends on the accurate tracking of the subendocardium and this needs good 2-D image quality of the fetal heart (Mieghem et al. 2010). The success rate of adequate speckle tracking analysis reported before and in the present study was relatively low with a range of 79%–93% (Mieghem et al. 2010). The main reason for failing to obtain good quality image for speckle tracking analysis was maternal obesity, suboptimal fetal position and excessive fetal movement. In the recipient twin of TTTS, image acquisition was even more challenging than in uncomplicated pregnancies because of the presence of polyhydramnios. However, as experience with this new technique increases, success rate may improve. In summary, the present study demonstrated that right ventricular systolic dysfunction, as measured with decreased right ventricular peak systolic longitudinal strain, exists despite the absence of diminished fractional shortening and cavity area percent change, and correlates with the right ventricular pressure overload but not with the right ventricular volume overload. REFERENCES Amundsen BH, Helle-Valle T, Edvardsen T, Torp H, Crosby J, Lyseggen E, Stoylen A, Ihlen H, Lima JAC, Smiseth OA, Slordahl SA. Noninvasive myocardial strain measurement by speckle tracking echocardiography. Validation against sonomicrometry and tagged magnetic resonance imaging. J Am Coll Cardiol 2006;47:789–798. Bajoria R, Wigglesworth J, Fisk NM. Angioarchitecture of monochorionic placentas in relation to the twin–twin transfusion syndrome. Am J Obstet Gynecol 1995;172:856–863. Bajoria R, Sullivan M, Fisk NM. Endothelin in association with cardiac dysfunction in the recipient fetus to twin–twin transfusion syndrome. Hum Reprod 1999;14:1614–1618. Barrea C, Alkazaleh F, Ryan G, McCrindle BW, Roberts A, Bigras JL, Barrett J, Seaward GP, Smallhorn JF, Hornberger LK. Prenatal cardiovascular manifestations in the twin-to-twin transfusion syndrome recipients and the impact of therapeutic amnioreduction. Am J Obstet Gynecol 2005;192:892–902. Cincotta RB, Fisk NM. Current thoughts on twin–twin transfusion syndrome. Clin Obstet Gynecol 1997;40:290–302. Deng YB, Liu R, Wu YH, Xiong L, Liu YN. Evaluation of short-axis and long-axis myocardial function with two-dimensional strain echocardiography in patients with different degrees of coronary artery stenosis. Ultrasound Med Biol 2010;36:227–233.
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Hadlock FP, Harrist RB, Carpenter RJ, Deter RL, Park SK. Sonographic estimation of fetal weight: the value of femur length in addition to head and abdomen measurements. Radiology 1984;150:535–540. International Society of Ultrasound in Obstetrics & Gynecology. Cardiac screening examination of the fetus: guidelines for performing the ‘basic’ and ‘extended basic’ cardiac scan. Ultrasound Obstet Gynecol 2006;27:107–113. Liang HY, Cauduro S, Pellikka P, Wang J, Urheim S, Yang EH, Rihal C, Belohlavek M, Khandheria B, Miller FA, Abraham TP. Usefulness of two-dimensional speckle strain for evaluation of left ventricular diastolic deformation in patients with coronary artery disease. Am J Cardiol 2006;98:1581–1586. Mahieu-Caputo D, Muller F, Joly D. Pathogenesis of twin–twin transfusion syndrome: the renin-angiotensin system hypothesis. Fetal Diagn Ther 2000;16:241–244. Mari G, Deter RL. Middle cerebral artery flow velocity waveforms in normal and small for gestational age fetuses. Am J Obstet Gynecol 1992;166:1262–1270. Michelfelder E, Gottliebson W, Border W, Kinsel M, Polzin W, Livingston J, Khoury P, Crombleholme T. Early manifestations and spectrum of recipient twin cardiomyopathy in twin–twin transfusion syndrome: relation to Quintero stage. Ultrasound Obstet Gynecol 2007;30:965–971. Mieghem TM, Giusca S, DeKoninck P, Gucciardo L, Done E, Hindryckx A, D’Hooge J, Deprest J. Prospective assessment of fetal cardiac function with speckle tracking in healthy fetuses and recipient fetuses of twin-to-twin transfusion syndrome. J Am Soc Echocardiogr 2010;23:301–308. Paladini D, Chita SK, Allan LD. Prenatal measurement of cardiothoracic ratio in evaluation of heart disease. Arch Dis Child 1990;65:20–23. Quintero RA, Morales WJ, Allen MH, Bornick PW, Johnson PK, Kruger M. Staging of twin–twin transfusion syndrome. J Perinatol 1999;19:550–555. Raboisson MJ, Fouron JC, Lamoureux J, Leduc L, Grignon A, Proulx F, Gamache S. Early intertwin differences in myocardial performance during the twin-to-twin transfusion syndrome. Circulation 2004; 110:3043–3048. Rychik J, Tian ZY, Bebbington M, Xu F, McCann M, Mann S, Wilson RD, Johnson MP. The twin–twin transfusion syndrome: Spectrum of cardiovascular abnormality and development of a cardiovascular score to assess severity of disease. Am J Obstet Gynecol 2007;197:392.e1–392.e8. Schiller NB, Shah PM, Crawford M, DeMaria A, Devereux R, Feigenbaum H, Gutgesell H, Reichek N, Sahn D, Schnittger I. Recommendations for quantitation of the left ventricle by twodimensional echocardiography: American Society of Echocardiography Committee on Standards, Subcommittee on Quantitation of Two-Dimensional Echocardiograms. J Am Soc Echocardiogr 1989;2:358–367. Senat MV, Deprest J, Boulvain M, Paupe A, Winer N, Ville Y. Endoscopic laser surgery versus serial amnioreduction for severe twinto-twin transfusion syndrome. N Engl J Med 2004;351:136–144. Sonesson SE, Fouron JC, Drblik SP. Reference values for Doppler velocimetric indices from the fetal and placental ends of the umbilical artery during normal pregnancy. J Clin Ultrasound 1993;21: 317–324. Wang J, Khoury DS, Yue Y, Torre-Amione G, Nagueh SF. Preserved left ventricular twist and circumferential deformation, but depressed longitudinal and radial deformation in patients with diastolic heart failure. Eur Heart J 2008;29:1283–1289. Yip G, Wang M, Zhang Y, Fung JW, Ho PY, Sanderson JE. Left ventricular long axis function in diastolic heart failure is reduced in both diastole and systole: Time for a redefinition? Heart 2002;87:121–125. Younoszai AK, Saudek DE, Emery SP, Thomas JD. Evaluation of myocardial mechanics in the fetus by velocity vector imaging. J Am Soc Echocardiogr 2008;21:470–474.
doi:10.1016/j.ultrasmedbio.2012.05.009
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Original Contribution ASSESSMENT OF RIGHT VENTRICULAR FUNCTION IN RECIPIENT TWIN OF TWIN TO TWIN TRANSFUSION SYNDROME WITH SPECKLE TRACKING ECHOCARDIOGRAPHY SHENG ZHAO,* YOU-BIN DENG,* XIN-LIN CHEN,y and RONG LIUy * Department of Medical Ultrasound, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China; and y Department of Medical Ultrasound, Hubei Maternal & Children’s Hospital, Wuhan, China (Received 19 December 2011; revised 2 May 2012; in final form 11 May 2012)
Abstract—This study was undertaken to evaluate the right ventricular myocardial systolic function and its relation to the fetal volume and pressure overload in recipient twin of twin to twin transfusion syndrome with speckle tracking echocardiography. Longitudinal peak systolic strains of the right ventricle were measured by speckle tracking echocardiography in 17 patients with twin-to-twin transfusion syndrome (TTTS) and 19 normal monochorionic diamniotic pregnancies. The right ventricular free wall thickness in recipient twin (0.43 ± 0.14 cm) was significantly larger than that in the donor (0.21 ± 0.04 cm, p , 0.05) and the control group (0.18 ± 0.03 cm, p , 0.05 for larger twin and 0.17 ± 0.02 cm, p , 0.05 for smaller twin). Although there were no significant differences in the right ventricular fractional shortening and cavity area percent change among control and the TTTS groups, the absolute value of peak systolic strains of ventricular septum, right ventricular free wall and global right ventricle in recipients were all significantly lower than those of the donors and the control group. Besides, the global right ventricular peak systolic strain correlated well with gestational age adjusted right ventricular free wall thickness (r 5 0.65, p 5 0.04) but not with gestational age adjusted right ventricular end-diastolic dimension (r 5 0.38, p 5 0.28) and cavity area percent change (r 5 0.33, p 5 0.35). Right ventricular systolic dysfunction measured with decreased right ventricular peak systolic longitudinal strain exists despite the absence of diminished fractional shortening and cavity area percent change and this reduced systolic function correlates with the right ventricular pressure overload as shown by increased right ventricular free wall thickness. (E-mail: ybdeng2007@hotmail. com) Ó 2012 World Federation for Ultrasound in Medicine & Biology. Key Words: Cardiac function, Speckle tracking echocardiography, Two-dimensional strain, Monochorionic twins, Twin to twin transfusion syndrome.
subsequent pressure overload as a consequence of elevated concentration of endothelin in the recipient and upregulation of the rennin-angiotension system in the donor twin (Bajoria et al. 1995; Bajoria et al. 1999; Mahieu-Caputo et al. 2000). Although the myocardial diastolic function has been demonstrated to be impaired by measuring the isovolume relaxation time and myocardial performance index with pulsed Doppler flow recording in recipient twin, the systolic function evaluated with fractional shortening is preserved in all or diminished only in a small number of recipient twin (Barrea et al. 2005; Raboisson et al. 2004). In addition, it is not known whether fetal cardiac function in TTTS is related to the volume or pressure overload. Speckle tracking echocardiography is a novel technique for analyzing myocardial motion (Amundsen et al. 2006). The method uses B-mode images for speckle tracking analysis and allows calculation of myocardial
INTRODUCTION Twin-to-twin transfusion syndrome (TTTS) is a gestational condition restricted to monochorionic twin pregnancies (Cincotta and Fisk 1997). Many studies have shown that the cardiac function decreased and right ventricular function seemed to be affected much more commonly than left ventricular function in recipient twin (Barrea et al. 2005; Michelfelder et al. 2007; Raboisson et al. 2004; Rychik et al. 2007). It was indicated that in TTTS, the fetal cardiac function decreased because of chronic volume overload as a consequence of the net transfer of blood from the donor twin to the recipient through placental vascular anastomoses and/or Address correspondence to: You-Bin Deng, M.D., Ph.D., Department of Medical Ultrasound, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, 1095 Jiefang Road, Wuhan 430030, China. E-mail: [email protected] 1502
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displacement and strain (Deng et al. 2010). Regional myocardial strain measured by speckle tracking echocardiography has been demonstrated to be a sensitive parameter for the evaluation of regional myocardial systolic function in patients with preserved global left ventricular systolic function, including those with diastolic heart failure, hypertension and coronary heart disease without visual regional wall motion abnormality (Deng et al. 2010; Liang et al. 2006; Yip et al. 2002; Wang et al. 2008). Recent studies have shown that speckle tracking echocardiography is feasible in assessing fetal cardiac function in fetuses with and without heart disease (Mieghem et al. 2010; Younoszai et al. 2008). Therefore, the present study was undertaken to evaluate the right ventricular myocardial systolic function and its relation to the fetal volume and pressure overload in recipient twin of twin to twin transfusion syndrome with speckle tracking echocardiography. MATERIALS AND METHODS Study population Study population consisted of 17 patients with TTTS. TTTS was diagnosed as the presence of oligohydramnios in the donor twin with a deepest vertical amniotic fluid pocket ,2 cm and polyhydramnios in the recipient twin with a deepest amniotic fluid .8 cm prior to 20 weeks and .10 cm after 20 weeks in a monochorionic twin pregnancy (Senat et al. 2004). Patients were staged based on Quintero’s staging system (Quintero et al. 1999). Nineteen subjects with normal monochorionic diamniotic pregnancies were recruited as the control group at a gestational age between 16.5 and 26.6 weeks. Monochorionicity was identified by the presence of ‘‘T’’ sign between 10 and 14 weeks, or twins of the same sex with a single placenta. Pathologic examination of the placenta after birth confirmed chorionicity in all cases. Those fetuses with pathologies that could lead to abnormal cardiac function (intrauterine growth restriction, gestational diabetes, fetal arrhythmia, fetal malformations and chromosomal defects) were excluded from this study. The study was approved by the local ethics committee and informed consent was obtained from all of the mothers. Fetal echocardiographic and speckle tracking recording and analysis Fetal echocardiography was performed according to the recommendations of the International Society of Ultrasound in Obstetrics & Gynecology (ISUOG 2006) with a 6C2 probe on Siemens Acuson Sequoia 512 (Siemens Medical Solutions, Mountain View, CA, USA). The following parameters were measured in all fetuses according to methods described previously: cardiothoracic ratio (Paladini et al. 1990), peak systolic velocity of middle
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cerebral artery (Mari and Deter 1992), pulsatility indexes of umbilical artery (Sonesson et al. 1993), middle cerebral artery and ductus venousus, end-diastolic and end-systolic dimensions of right ventricle and end-diastolic thickness of right ventricular free wall (Schiller et al. 1989). Enddiastolic and end-systolic right ventricular cavity areas were measured on four-chamber view by tracing the endocardium manually. The right ventricular fractional shortening was calculated by dividing the difference of the right ventricular end-diastolic and end-systolic dimensions with the end-diastolic dimension. Similarly, right ventricular cavity area percent change was calculated by dividing the difference of the right ventricular end-diastolic and end-systolic cavity areas with the enddiastolic cavity area. Right ventricular myocardial performance index was also measured on pulsed Doppler velocity waveforms as described before (Raboisson et al. 2004). The right ventricular dimension and cavity area and thickness of right ventricular free wall at enddiastole were adjusted with the gestational age. Fetal weight and gestational age were determined by the earliest second-trimester ultrasound measurements of head and abdominal circumferences and femur length (Hadlock et al. 1984). The fetal weight discordance was calculated by dividing the difference of the weight between larger and smaller twin with fetal weight of larger twin. Syngo VVI software (Siemens Medical Solutions) was used for speckle tracking analysis. First, a digital clip of zoomed fetal four-chamber view was recorded and then transferred to the offline workstation. Second, the beginning and end of a cardiac cycle was defined with M-mode tracing of ventricular wall or atrioventricular valve motion. Third, the endocardium of the right ventricle was traced manually from a single end-systolic frame with clear endocardial border. After the tracking quality was verified for each segment (with subsequent manual adjustment of the region-of-interest if necessary), myocardial motion was analyzed by speckle-tracking within the region-of-interest bound by endocardial and epicardial borders. Myocardial longitudinal strain profile was obtained and peak systolic strain value was measured (Fig. 1). Peak systolic longitudinal strain of the ventricular septum and right ventricular free wall were calculated by averaging the segmental strain values (Fig. 1). Interobserver and intraobserver reproducibility To assess the reproducibility of the strain measurements, peak systolic longitudinal strain in five recipient twins and five control twins were measured by two independent observers on the same day and by one observer twice, 1 week apart. The interobserver and intraobserver variability is calculated as a percentage of the absolute difference between the two measurements divided by the mean value of the measurements.
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Fig. 1. (a) Zoomed diastolic fetal four-chamber view from a fetus in the control group with demonstration of the endocardial tracing of the right ventricle. (b) Longitudinal strain curves from six segments of the right ventricular wall. Curves 1 to 3 are the longitudinal strain curve of the basal, middle and apical segments of the right ventricular free wall and the peak systolic longitudinal strain of the right ventricular free wall was calculated by averaging the 3 peak systolic longitudinal strains measured from these three curves. Curves 4 to 6 are the longitudinal strain curve of the apical, middle and basal segments of the ventricular septum and peak systolic longitudinal strain of the ventricular septum was calculated by averaging the three peak systolic longitudinal strains measured from these three curves. Curve 7 is the global longitudinal strain curve and global peak systolic longitudinal strain of the right ventricle is measured from the curve. LA 5 left atrium; LV 5 left ventricle; RA 5 right atrium; RV 5 right ventricle.
Statistical analysis Data are presented as mean 6SD. An unpaired t-test was used to compare parameters between control fetuses and fetuses with TTTS. Parameters among recipient and donor twins in TTTS and larger and smaller twins in controls were compared by analysis of variance. Significant differences between groups were assessed using the Scheffe F test for multiple comparisons. Differences in proportions were tested by c2 analysis. Relationship between parameters was assessed by simple linear regression analysis. All statistical analyses were performed using the SPSS 13.0 software (SPSS Inc, Chicago, IL, USA). A p value of less than 0.05 was considered significant. RESULTS Patient characteristics The majority of TTTS cases in this study were in Quintero stages III, with 1 at stage I, 2 at stage II, 11 at stage III and 3 at stage IV. Mean maternal age was 26.2 6 4.5 years. The gestational age at diagnosis was 22.7 6 2.8 weeks. Right ventricular outflow tract obstructions were detected in two recipient twins (stage III and stage IV, respectively), which manifested pulmonary valve atresia with detectable retrograde flow in pulmonary artery. Intracranial hemorrhage was detected in one recipient twin with stage IV. The clinical characteristics of each group are shown in Table 1. No differences were seen in maternal age,
gestational age, fetal weight of smaller twin between the TTTS and control group. However, fetal weight of larger twin and fetal weight discordance in TTTS group were significantly higher than those in the control group (p , 0.05). Doppler and echocardiographic findings Echocardiographic findings and Doppler parameters of TTTS and the control groups are shown in Table 2. No differences were seen in pulsatility index of umbilical artery, peak systolic velocity of middle cerebral artery, heart rate, right ventricular end-diastolic dimension and cavity area, gestational age adjusted right ventricular end-diastolic dimension and cavity area, and right ventricular fractional shortening and cavity area percent change between the TTTS and control group. However, cardiothoracic ratio, right ventricular free wall thickness, gestational age adjusted right ventricular free wall thickness and right ventricular myocardial performance index in the recipients were all significantly higher than those of donors and the control group (larger and smaller twins), whereas pulsatility index of middle cerebral artery in the recipients were significantly lower than that of other fetus. Speckle tracking echocardiographic findings Adequate speckle tracking analyses were available in 11 recipients and eight donors in TTTS group with
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Table 1. Clinical characteristics of study population Variable
Control group (pregnancy n 5 19) (fetus n 5 38)
TTTS group (pregnancy n 5 17) (fetus n 5 34)
p value
Maternal age (years) Gestational age (weeks) Larger twin FW (g) Smaller twin FW (g) FW discordance (%)
28.2 6 4.7 21.0 6 2.4 427 6 176 397 6 171 7.2 6 7.0
26.2 6 4.5 22.7 6 2.8 710 6 490 477 6 270 26.8 6 16.8
0.197 0.068 0.025 0.293 ,0.001
TTTS 5 twin-to-twin transfusion syndrome; FW 5 fetal weight. Data are expressed as mean 6SD.
a success rate of 64.7% (11/17) and 47.1% (8/17), respectively. In the control group, adequate speckle analyses were available in 30 twins with a success rate of 78.9% (30/38). The interobserver variability for peak systolic longitudinal strain was 8.3 6 6.7%, and the intraobserver variability for that index was 7.6 6 6.8%. Peak systolic longitudinal strains of right ventricle in TTTS and the control group are shown in Table 3. No statistically significant differences were seen in the peak systolic strains of ventricular septum, right ventricular free wall and global right ventricle among the donor twin and control group. However, the absolute value of peak systolic strains of ventricular septum, right ventricular free wall and global right ventricle in recipients were all significantly lower than those of donors and the control group. The global right ventricular peak systolic strain in recipients correlated with the gestational age adjusted right ventricular free wall thickness (r 5 0.65, p 5 0.04) but not with gestational age adjusted right ventric-
ular end-diastolic dimension (r 5 0.38, p 5 0.28) and cavity area (0.33, p 5 0.35). DISCUSSION In the present study, we found that although no right ventricular systolic dysfunction could be detected in recipient twin of TTTS with conventional measurement of right ventricular fractional shortening and cavity area percent change, peak systolic longitudinal strains of ventricular septum, right ventricular free wall and global right ventricle in recipient twins reduced significantly compared with those in the donor twin and control groups. Furthermore, we demonstrated that global right ventricular peak systolic strain in the recipient twin correlated with the right ventricular free wall thickness but not with the right ventricular end-diastolic dimension and cavity area. Previous studies indicated that ventricular dysfunction can occur and right ventricular function is affected
Table 2. Doppler and echocardiographic parameters of study population Control group (pregnancy n 5 19)
TTTS group (pregnancy n 5 17)
Variable
Larger twin (f n 5 19)
Smaller twin (f n 5 19)
Recipients (f n 5 17)
Donors (f n 5 17)
p value
UA-PI MCA-PSV (cm/s) MCA-PI DV-PI HR (beat/min) CTR RVEDD (cm) RVCA (cm2) RVEDD/GA (cm/w) RVCA/GA (cm2/w) RVFWT (cm) RVFWT/GA (cm/w) RVMPI RVFS (%) RVCAPC (%)
1.28 6 0.15 24.1 6 6.0 1.65 6 0.29 0.72 6 0.21 151 6 6 0.26 6 0.04 0.80 6 0.27 0.56 6 0.20 0.38 6 0.10 0.26 6 0.06 0.18 6 0.03 0.09 6 0.01 0.33 6 0.16 22 6 3 43 6 11
1.31 6 0.15 23.3 6 3.5 1.64 6 0.19 0.74 6 0.17 148 6 8 0.26 6 0.03 0.68 6 0.26 0.49 6 0.18 0.32 6 0.10 0.23 6 0.06 0.17 6 0.02 0.08 6 0.01 0.33 6 0.10 22 6 3 41 6 9
1.44 6 0.38 32.6 6 18.5 1.37 6 0.38* 0.89 6 0.39 146 6 9 0.36 6 0.06* 0.93 6 0.38 0.69 6 0.33 0.38 6 0.10 0.28 6 0.09 0.43 6 0.14* 0.18 6 0.06* 0.68 6 0.30* 22 6 10 38 6 6
1.49 6 0.27 29.1 6 10.7 1.66 6 0.46 0.96 6 0.40 150 6 11 0.29 6 0.08 0.84 6 0.22 0.63 6 0.47 0.35 6 0.05 0.29 6 0.13 0.21 6 0.04 0.09 6 0.02 0.31 6 0.22 24 6 6 40 6 10
0.074 0.073 0.039 0.062 0.396 ,0.001 0.072 0.131 0.157 0.286 ,0.001 ,0.001 ,0.001 0.592 0.671
TTTS 5 twin-to-twin transfusion syndrome; f 5 fetus; UA-PI 5 pulsatility index of umbilical artery; MCA-PSV 5 peak systolic velocity of middle cerebral artery; MCA-PI 5 pulsatility index of middle cerebral artery; DV-PI 5 pulsatility index of ductus venosus; HR 5 heart rate; CTR 5 cardiothoracic ratio; RVEDD 5 right ventricular end-diastolic dimension; RVCA 5 right ventricular end-diastolic cavity area; RVFWT 5 right ventricular free wall thickness; RVMPI 5 right ventricular myocardial performance index; RVFS 5 right ventricular fractional shortening; RVCAPC 5 right ventricular cavity area percent change; GA 5 gestational age; w 5 week. Data are expressed as mean 6SD. * p , 0.05 vs. other three groups.
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Table 3. Comparison of peak systolic longitudinal strain of right ventricle in TTTS and control groups Control group (pregnancy n 5 16)
TTTS group (pregnancy n 5 11)
Variable
Larger twin (f n 5 16)
Smaller twin (f n 5 14)
Recipients (f n 5 11)
Donors (f n 5 8)
p value
VS Free wall Global
218.6 6 6.3 213.4 6 5.6 216.2 6 4.8
216.5 6 8.5 216.0 6 5.2 216.3 6 5.8
28.7 6 4.6* 25.8 6 2.9* 27.2 6 3.4*
219.7 6 8.9 217.1 6 5.7 218.4 6 5.7
0.005 ,0.001 ,0.001
TTTS 5 twin-to-twin transfusion syndrome; f 5 fetus; VS 5 ventricular septum. Data are expressed as mean 6SD. * p , 0.05 vs. other three groups.
much more commonly than left ventricular function in the recipient twin of TTTS (Barrea et al. 2005; Michelfelder et al. 2007; Raboisson et al. 2004; Rychik et al. 2007). Ventricular dysfunction usually manifested as diastolic dysfunction in the early stage of TTTS and diastolic dysfunction can occur before the systolic dysfunction (Barrea et al. 2005; Raboisson et al. 2004). It was demonstrated that right ventricular systolic function evaluated with fractional shortening or isovolumic contraction time is preserved although diastolic function is impaired in most recipient twins of TTTS (Barrea et al. 2005; Raboisson et al. 2004). Barrea et al. reported that ventricular systolic dysfunction occurs in only one third of the recipients and ventricular diastolic dysfunction is present in approximately two thirds of the recipient twins (Barrea et al. 2005). Another study by Raboisson et al. showed normal ventricular fractional shortening and isovolumic contraction time and significant prolongation of the isovolumic relaxation time, indicating preserved right ventricular systolic function and diminished right ventricular diastolic function in recipient twin (Raboisson et al. 2004). All those studies mentioned above demonstrate that diastolic dysfunction can occur even in the absence of systolic dysfunction. We measured the right ventricular free wall thickness by using the two-dimensional (2-D) echocardiographic technique, which provides us information about the cardiac structure. We also measured the myocardial strain by using the speckle tracking echocardiographic technique, which provides us information about the cardiac function. Speckle tracking echocardiography is a new technique for analyzing myocardial motion (Amundsen et al. 2006), which uses B-mode images for speckle tracking analysis and allows calculation of myocardial displacement and strain (Deng et al. 2010). Regional myocardial strain obtained from speckle tracking echocardiography has been demonstrated to be a sensitive parameter for the evaluation of regional myocardial systolic function (Deng et al. 2010; Liang et al. 2006; Yip et al. 2002; Wang et al. 2008). In the present study, we found that although there was no statistically significant difference in right ventricular fractional shortening and cavity area percent change among the recipient, donor twins and control group, the peak systolic
strains of ventricular septum and right ventricular free wall, and global peak systolic right ventricular strain decreased compared with those in the donor twin and control group, suggesting that right ventricular systolic function declined even in the absence of decreased ventricular fractional shortening and cavity area percent change. Indeed, a recent study conducted by Mieghem et al. also showed reduced peak systolic right ventricular strain in TTTS compared with controls (Mieghem et al. 2010). Our findings go along with the concept that regional myocardial strain is a sensitive parameter for evaluation of regional myocardial systolic function in patients with preserved global left ventricular systolic function in adult patients, including those with diastolic heart failure, hypertension and coronary heart disease without visual regional wall motion abnormality (Deng et al. 2010; Liang et al. 2006; Yip et al. 2002; Wang et al. 2008). Our previous study conducted in patients with coronary artery disease and normal ejection fraction revealed a reduction in longitudinal peak systolic strain in myocardial segments subtended by larger than 75% coronary stenosis compared with those subtended by less than 75% coronary stenosis (Deng et al. 2010). Similarly, a decreased longitudinal systolic strain as measured by tissue spackle tracking, was reported in patients with diastolic heart failure and normal left ventricular ejection fraction (Yip et al. 2002; Wang et al. 2008). Traditionally, ventricular dysfunction in recipient twin of TTTS was thought to be a result of chronic volume overload as a consequence of the net transfer of blood from the donor twin to the recipient through placental vascular anastomoses and/or subsequent pressure overload as a consequence of elevated concentration of endothelin in the recipient and upregulation of the rennin-angiotensin system in the donor twin (Bajoria et al. 1995, 1999; Mahieu-Caputo et al. 2000). Recently, many studies found that there is a significantly increased ventricular wall thickness and ventricular dysfunction occurring in the absence of cardiac chamber dilation in recipient twin (Barrea et al. 2005; Raboisson et al. 2004). These findings support the hypothesis that ventricular dysfunction in the recipient results from the myocardial hypertrophy rather than ventricular dilation. Our
Twin to twin transfusion syndrome d S. ZHAO et al.
study further expanded these observations by demonstrating that right ventricular dysfunction manifested as reduced global right ventricular peak systolic strain, which correlated well with gestational age-adjusted thickness of the right ventricular free wall, but not with right ventricular dimension, indicating that right ventricular systolic dysfunction in recipient twin is related with the right ventricular pressure overload, but not with right ventricular volume overload. Successful speckle tracking analysis depends on the accurate tracking of the subendocardium and this needs good 2-D image quality of the fetal heart (Mieghem et al. 2010). The success rate of adequate speckle tracking analysis reported before and in the present study was relatively low with a range of 79%–93% (Mieghem et al. 2010). The main reason for failing to obtain good quality image for speckle tracking analysis was maternal obesity, suboptimal fetal position and excessive fetal movement. In the recipient twin of TTTS, image acquisition was even more challenging than in uncomplicated pregnancies because of the presence of polyhydramnios. However, as experience with this new technique increases, success rate may improve. In summary, the present study demonstrated that right ventricular systolic dysfunction, as measured with decreased right ventricular peak systolic longitudinal strain, exists despite the absence of diminished fractional shortening and cavity area percent change, and correlates with the right ventricular pressure overload but not with the right ventricular volume overload. REFERENCES Amundsen BH, Helle-Valle T, Edvardsen T, Torp H, Crosby J, Lyseggen E, Stoylen A, Ihlen H, Lima JAC, Smiseth OA, Slordahl SA. Noninvasive myocardial strain measurement by speckle tracking echocardiography. Validation against sonomicrometry and tagged magnetic resonance imaging. J Am Coll Cardiol 2006;47:789–798. Bajoria R, Wigglesworth J, Fisk NM. Angioarchitecture of monochorionic placentas in relation to the twin–twin transfusion syndrome. Am J Obstet Gynecol 1995;172:856–863. Bajoria R, Sullivan M, Fisk NM. Endothelin in association with cardiac dysfunction in the recipient fetus to twin–twin transfusion syndrome. Hum Reprod 1999;14:1614–1618. Barrea C, Alkazaleh F, Ryan G, McCrindle BW, Roberts A, Bigras JL, Barrett J, Seaward GP, Smallhorn JF, Hornberger LK. Prenatal cardiovascular manifestations in the twin-to-twin transfusion syndrome recipients and the impact of therapeutic amnioreduction. Am J Obstet Gynecol 2005;192:892–902. Cincotta RB, Fisk NM. Current thoughts on twin–twin transfusion syndrome. Clin Obstet Gynecol 1997;40:290–302. Deng YB, Liu R, Wu YH, Xiong L, Liu YN. Evaluation of short-axis and long-axis myocardial function with two-dimensional strain echocardiography in patients with different degrees of coronary artery stenosis. Ultrasound Med Biol 2010;36:227–233.
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