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Fetal cardiac Doppler indices in fetuses with hemoglobin Bart's disease at 12–14 weeks of gestation
International Journal of Cardiology 184 (2015) 614–616
Contents lists available at ScienceDirect
International Journal of Cardiology journal homepage: www.elsevier.com/locate/ijcard
Letter to the Editor
Fetal cardiac Doppler indices in fetuses with hemoglobin Bart's disease at 12–14 weeks of gestation Suchaya Luewan, Fuanglada Tongprasert, Kasemsri Srisupundit, Theera Tongsong ⁎ Department of Obstetrics and Gynecology, Faculty of Medicine Chiang Mai University, Thailand
a r t i c l e
i n f o
Article history: Received 5 January 2015 Accepted 21 February 2015 Available online 24 February 2015 Keywords: Cardiac function Fetus Myocardial performance (Tei) index Doppler velocity Hydrops fetalis Hemoglobin Bart's disease
Hemodynamic changes caused by Hb Bart's disease can appear as early as 12–13 weeks of gestation [1–3] and myocardial workload secondary to anemia and hypervolemia may possibly occur in early gestation. Abnormal cardiac function may probably be an early subtle sign of fetal anemia occurring prior to development of hydrops fetalis. Myocardial performance index or Tei index has been reported to be increased in fetuses with anemia in the second or third trimester [4–6]. Nevertheless, to date, fetal myocardial performance in response to anemia in early gestation has never been explored. Therefore, this study was aimed to assess cardiac function in fetuses with Hb Bart's disease at 12–14 weeks of gestation compared with that in unaffected fetuses. The prospective diagnostic study was conducted between January 2011 and March 2014, with ethical approval of the Institute Review Boards. The inclusion criteria consisted of: 1) singleton pregnancies, 2) at risk of fetal Hb Bart's disease, both of the couple were a carrier which was confirmed by PCR for Southeast Asian type, and 3) gestational age of 12–14 weeks. Fetuses with sonographic signs of hydrops fetalis or chromosomal/structural abnormalities were excluded. All pregnancies underwent ultrasound examination for fetal biometry and anomaly screening including cardiac Doppler indices. All examinations were performed by the authors using a real-time scanner GE Voluson E8 (GE ⁎ Corresponding author at: Department of Obstetrics and Gynecology, Faculty of Medicine, Chiang Mai University, Chiang Mai 50200, Thailand. E-mail address: [email protected] (T. Tongsong).
http://dx.doi.org/10.1016/j.ijcard.2015.02.053 0167-5273/© 2015 Published by Elsevier Ireland Ltd.
Healthcare, Wisconsin, USA). In the assessment of fetal cardiac function, Tei index of the left ventricle was measured, using the techniques as described elsewhere [7]. Tei index was the value derived by dividing the sum of the isovolumetric contraction time (ICT) and the isovolumetric relaxation time (IRT) by the ventricular ejection time (ET), (ICT + IRT) / ET as presented in Fig. 1. Other cardiac Doppler indices were also measured and recorded, including E/A ratio at the mitral valves and tricuspid valves, peak systolic velocity (PSV) of the aortic valve and pulmonary valve, time to peak velocity (TPV) at the aortic valve and pulmonary valve, and velocity time integral (VTI) at the aortic valve and pulmonary valve. Definitive diagnosis of Hb Bart's disease was made by either DNA analysis of chorionic villous samples or cord blood typing. During the study period, a total of 58 fetuses were recruited and 20 fetuses were finally confirmed to be affected by Hb Bart's disease whereas the remaining 38 were unaffected. Mean gestational age (± SD) at the time of fetal echocardiography was 12.47 ± 0.56 and 12.75 ± 0.85 weeks, in the unaffected and affected group, respectively (Student's T test, p = 0.142). In comparison of various cardiac Doppler indices between the two groups, the median (interquartile range; IQR) of ICT and Tei index was significantly higher in fetuses with Hb Bart's disease than those in the unaffected group, 5.78(3.90) vs 4.84(3.60), p = 0.006 and 0.52(0.05) vs 0.43(0.06), Mann–Whitney-U test: p b 0.001, respectively, as presented in Table 1 and Fig. 2. Other cardiac Doppler indices were not significantly different between the two groups, as presented in Table 1. The insight gained from this study is that abnormal Tei index and ICT in response to fetal hypervolemia and increased cardiac output caused by anemia could be expressed as early as in late first trimester prior to development of hydropic changes, implying that myocardial function is very sensitive to fetal anemia and shows functional change long before morphological change is visualized by 2D ultrasound. Since it is impossible to study the cardiac change secondary to anemia caused by other non-lethal diseases in early gestation, Hb Bart's disease could be a live model to understand the adaptation of the fetal heart to maintain tissue oxygenation. Theoretically, Tei index may be used to assess fetal ventricular myocardial performance in fetal anemia or hypervolemia due to various causes other than Hb Bart's disease or any condition associated with an increase in cardiac afterload. In most fetuses with Hb Bart's disease, anemia has occurred as early as in the first trimester leading to an increased cardiac output and hypervolemia to maintain tissue oxygenation and some degree of cardiomegaly can be visualized as early as 11–14 weeks of gestation [3,8]. Notably, ICT was the only one
S. Luewan et al. / International Journal of Cardiology 184 (2015) 614–616
615
Fig. 1. Image and diagram of cardiac Doppler waveform depict calculation of the left ventricular Tei index; interval a extends from the cessation to the onset of mitral inflow and includes the isovolumetric contraction time (ICT), b or the ejection time (ET, the duration of left ventricular outflow) and the isovolumetric relaxation time (IRT), Note: arrow represents valve clicks. Example of cardiac Doppler waveform of fetuses with Hb Bart's disease at 13 weeks of gestation, depicts components of left ventricular Tei index; interval a extends from the cessation to the onset of mitral inflow and includes the isovolumetric contraction time (ICT), b or the ejection time (ET, the duration of left ventricular outflow) and the isovolumetric relaxation time (IRT), Note: arrow represents valve clicks.
component of Tei index that was significantly increased, signifying that cardiac workload in the early phase of anemia is firstly involved in systolic dysfunction rather than diastolic function. This is based on the fact that the ICT is an important index reflexive of systolic function [9], while IRT is reflexive of diastolic function [10]. Interestingly, ICT may be mainly responsible for an increase in Tei index in early stage and this may be an independent indicator for fetal anemia whereas all of the other isolated Doppler indices were not significantly different from those in unaffected fetuses. According to our previous studies, fetal anemia secondary to Hb Bart's disease in the early phase is not associated with increased preload and deterioration of myocardial contractility [11,12], in spite of hypervolemia but increased cardiac output. Nevertheless, this study indicated that in early fetal anemia, myocardium shows some degree of increased workload by increasing ICT and Tei index. Therefore, we speculate that this may be fetal physiologic adaptation to cope with anemic state rather than pathologic ventricular dysfunction. An increase in the ICT and Tei index in the early stage may not be a sign of cardiac dysfunction, just a good response to hemodynamic overload. Since fetal anemia in this study was lethal, cardiac Doppler studies in these fetuses are of no clinical value. However, it could be a study model for anemia secondary to non-lethal causes such as pavovirus B19 or Rh
isoimmunization. Thus cardiac Doppler assessment may be helpful in predicting the prognosis and, therefore, in making a choice of management. In conclusion, ICT and Tei index of the fetuses with Hb Bart's disease were significantly increased as early as in late first trimester, suggesting that they may be helpful in predicting affected fetuses among those at risk. Additionally, this study helps us more in understand the pathophysiology regarding fetal cardiac adaptation to anemia early in fetal life and also indicates that assessment of cardiac Doppler velocity may theoretically be useful in identifying fetal anemia from any causes in early stage.
Disclosure statement No conflict of interest.
Acknowledgment The authors wish to thank the National Research University Project under Thailand's Office of the Higher Education Commission (NRUCMU19-01-2554) for financial support.
Table 1 Comparison of various cardiac Doppler indices between the group of Hb Bart's fetuses and unaffected fetuses. Diagnosis
ICT IRT ET Tei index E/A ratio at mitral valve E/A ratio at tricuspid valve PSV of the aorta TPV of the aorta VTI of the aorta PSV of the pulmonary artery TPV of the pulmonary artery VTI of the pulmonary artery
Unaffected fetuses
Hb Bart's fetuses
Mean
SD
Mean
SD
5.65 7.80 30.57 0.44 0.53 0.60 43.86 12.02 1428.15 58.60 7.76 1533.29
3.03 3.52 13.36 0.06 0.06 0.08 37.99 15.93 1077.40 24.33 5.66 840.69
7.16 6.95 27.56 0.51 0.50 0.59 56.33 6.80 1418.21 57.29 5.98 1367.69
2.49 2.43 7.67 0.06 0.08 0.05 28.61 3.21 1249.24 27.08 2.60 1044.34
p-Valuea
0.061 0.337 0.357 0.000 0.151 0.541 0.228 0.157 0.977 0.864 0.209 0.551
Unaffected fetuses
Hb Bart's fetuses
Median
IQR
Median
IQR
4.84 7.37 26.69 0.43 0.52 0.61 52.55 7.25 1166.78 62.96 5.64 1661.42
3.60 2.87 16.72 0.06 0.10 0.11 36.81 5.05 1536.55 28.12 3.52 959.67
5.78 6.79 27.01 0.52 0.50 0.61 45.12 6.15 1157.20 46.40 5.08 996.40
3.90 4.02 11.77 0.05 0.05 0.07 36.31 5.06 1144.02 20.75 1.57 927.61
p-Valueb
0.006 0.395 0.600 0.000 0.119 0.864 0.375 0.506 0.657 0.410 0.140 0.179
SD: standard deviation; IQR: interquartile range; ICT: isovolumetric contraction time; IRT: isovolumetric relaxation time; ET: ejection time; PSV: peak systolic velocity; TPV: time-to-peak; VTI: velocity time integral. a Student's T test. b Mann–Whitney U test.
616
S. Luewan et al. / International Journal of Cardiology 184 (2015) 614–616
Fig. 2. Boxplots of the components of myocardial performance (Tei) index of the fetuses with Hb Bart's disease and unaffected fetuses A: isovolumetric contraction time (ICT), B: isovolumetric relaxation time (IRT), C: ejection time (ET), and D: Tei index.
References [1] Y.H. Lam, M.H. Tang, C.P. Lee, H.Y. Tse, Nuchal translucency in fetuses affected by homozygous alpha-thalassemia-1 at 12–13 weeks of gestation, Ultrasound Obstet. Gynecol. 13 (4) (Apr 1999) 238–240. [2] K.Y. Leung, K.B. Cheong, C.P. Lee, V. Chan, Y.H. Lam, M. Tang, Ultrasonographic prediction of homozygous alpha(0)-thalassemia using placental thickness, fetal cardiothoracic ratio and middle cerebral artery Doppler: alone or in combination? Ultrasound. Obstet. Gynecol 35 (2) (Jan 2010) 149–154. [3] S. Sirichotiyakul, S. Luewan, K. Srisupundit, F. Tongprasert, T. Tongsong, Prenatal ultrasound evaluation of fetal Hb Bart's disease among pregnancies at risk at 11 to 14 weeks of gestation, Prenat. Diagn. 34 (3) (Mar 2014) 230–234. [4] G. Chao, C. Zheng, D. Meng, J. Su, X. Xie, W. Li, et al., Tei index: the earliest detectable cardiac structural and functional abnormality detectable in Hb Bart's foetal edema, Int. J. Cardiol. 134 (3) (May 29 2009) e150–e154. [5] S. Luewan, F. Tongprasert, K. Srisupundit, T. Tongsong, Fetal myocardial performance (Tei) index in fetal hemoglobin Bart's disease, Ultraschall Med. 34 (4) (Aug 2013) 355–358. [6] K. Ichizuka, R. Matsuoka, J. Hasegawa, N. Shirato, M. Jimbo, K. Otsuki, et al., The Tei index for evaluation of fetal myocardial performance in sick fetuses, Early Hum. Dev. 81 (3) (Mar 2005) 273–279.
[7] S. Luewan, F. Tongprasert, K. Srisupundit, K. Traisrisilp, T. Tongsong, Reference ranges of myocardial performance index from 12 to 40 weeks of gestation, Arch. Gynecol. Obstet. 290 (5) (Nov 2014) 859–865. [8] Y.H. Lam, M.H. Tang, C.P. Lee, H.Y. Tse, Prenatal ultrasonographic prediction of homozygous type 1 alpha-thalassemia at 12 to 13 weeks of gestation, Am. J. Obstet. Gynecol. 180 (1 Pt 1) (Jan 1999) 148–150. [9] M.J. Wolk, J.F. Keefe, O.H. Bing, L.J. Finkelstein, H.J. Levine, Estimation of Vmax in auxotonic systoles from the rate of relative increase of isovolumic pressure: (dP-dt)kP, J. Clin. Invest. 50 (6) (Jun 1971) 1276–1285. [10] W. Grossman, L.P. McLaurin, E.L. Rolett, Alterations in left ventricular relaxation and diastolic compliance in congestive cardiomyopathy, Cardiovasc. Res. 13 (9) (Sep 1979) 514–522. [11] T. Tongsong, F. Tongprasert, K. Srisupundit, S. Luewan, Venous Doppler studies in low-output and high-output hydrops fetalis, Am. J. Obstet. Gynecol. 203 (5) (Nov 2010) 488.e1–488.e6. [12] T. Tongsong, C. Wanapirak, W. Piyamongkol, S. Sirichotiyakul, F. Tongprasert, K. Srisupundit, et al., Fetal ventricular shortening fraction in hydrops fetalis, Obstet. Gynecol. 117 (1) (Jan 2011) 84–91.
Contents lists available at ScienceDirect
International Journal of Cardiology journal homepage: www.elsevier.com/locate/ijcard
Letter to the Editor
Fetal cardiac Doppler indices in fetuses with hemoglobin Bart's disease at 12–14 weeks of gestation Suchaya Luewan, Fuanglada Tongprasert, Kasemsri Srisupundit, Theera Tongsong ⁎ Department of Obstetrics and Gynecology, Faculty of Medicine Chiang Mai University, Thailand
a r t i c l e
i n f o
Article history: Received 5 January 2015 Accepted 21 February 2015 Available online 24 February 2015 Keywords: Cardiac function Fetus Myocardial performance (Tei) index Doppler velocity Hydrops fetalis Hemoglobin Bart's disease
Hemodynamic changes caused by Hb Bart's disease can appear as early as 12–13 weeks of gestation [1–3] and myocardial workload secondary to anemia and hypervolemia may possibly occur in early gestation. Abnormal cardiac function may probably be an early subtle sign of fetal anemia occurring prior to development of hydrops fetalis. Myocardial performance index or Tei index has been reported to be increased in fetuses with anemia in the second or third trimester [4–6]. Nevertheless, to date, fetal myocardial performance in response to anemia in early gestation has never been explored. Therefore, this study was aimed to assess cardiac function in fetuses with Hb Bart's disease at 12–14 weeks of gestation compared with that in unaffected fetuses. The prospective diagnostic study was conducted between January 2011 and March 2014, with ethical approval of the Institute Review Boards. The inclusion criteria consisted of: 1) singleton pregnancies, 2) at risk of fetal Hb Bart's disease, both of the couple were a carrier which was confirmed by PCR for Southeast Asian type, and 3) gestational age of 12–14 weeks. Fetuses with sonographic signs of hydrops fetalis or chromosomal/structural abnormalities were excluded. All pregnancies underwent ultrasound examination for fetal biometry and anomaly screening including cardiac Doppler indices. All examinations were performed by the authors using a real-time scanner GE Voluson E8 (GE ⁎ Corresponding author at: Department of Obstetrics and Gynecology, Faculty of Medicine, Chiang Mai University, Chiang Mai 50200, Thailand. E-mail address: [email protected] (T. Tongsong).
http://dx.doi.org/10.1016/j.ijcard.2015.02.053 0167-5273/© 2015 Published by Elsevier Ireland Ltd.
Healthcare, Wisconsin, USA). In the assessment of fetal cardiac function, Tei index of the left ventricle was measured, using the techniques as described elsewhere [7]. Tei index was the value derived by dividing the sum of the isovolumetric contraction time (ICT) and the isovolumetric relaxation time (IRT) by the ventricular ejection time (ET), (ICT + IRT) / ET as presented in Fig. 1. Other cardiac Doppler indices were also measured and recorded, including E/A ratio at the mitral valves and tricuspid valves, peak systolic velocity (PSV) of the aortic valve and pulmonary valve, time to peak velocity (TPV) at the aortic valve and pulmonary valve, and velocity time integral (VTI) at the aortic valve and pulmonary valve. Definitive diagnosis of Hb Bart's disease was made by either DNA analysis of chorionic villous samples or cord blood typing. During the study period, a total of 58 fetuses were recruited and 20 fetuses were finally confirmed to be affected by Hb Bart's disease whereas the remaining 38 were unaffected. Mean gestational age (± SD) at the time of fetal echocardiography was 12.47 ± 0.56 and 12.75 ± 0.85 weeks, in the unaffected and affected group, respectively (Student's T test, p = 0.142). In comparison of various cardiac Doppler indices between the two groups, the median (interquartile range; IQR) of ICT and Tei index was significantly higher in fetuses with Hb Bart's disease than those in the unaffected group, 5.78(3.90) vs 4.84(3.60), p = 0.006 and 0.52(0.05) vs 0.43(0.06), Mann–Whitney-U test: p b 0.001, respectively, as presented in Table 1 and Fig. 2. Other cardiac Doppler indices were not significantly different between the two groups, as presented in Table 1. The insight gained from this study is that abnormal Tei index and ICT in response to fetal hypervolemia and increased cardiac output caused by anemia could be expressed as early as in late first trimester prior to development of hydropic changes, implying that myocardial function is very sensitive to fetal anemia and shows functional change long before morphological change is visualized by 2D ultrasound. Since it is impossible to study the cardiac change secondary to anemia caused by other non-lethal diseases in early gestation, Hb Bart's disease could be a live model to understand the adaptation of the fetal heart to maintain tissue oxygenation. Theoretically, Tei index may be used to assess fetal ventricular myocardial performance in fetal anemia or hypervolemia due to various causes other than Hb Bart's disease or any condition associated with an increase in cardiac afterload. In most fetuses with Hb Bart's disease, anemia has occurred as early as in the first trimester leading to an increased cardiac output and hypervolemia to maintain tissue oxygenation and some degree of cardiomegaly can be visualized as early as 11–14 weeks of gestation [3,8]. Notably, ICT was the only one
S. Luewan et al. / International Journal of Cardiology 184 (2015) 614–616
615
Fig. 1. Image and diagram of cardiac Doppler waveform depict calculation of the left ventricular Tei index; interval a extends from the cessation to the onset of mitral inflow and includes the isovolumetric contraction time (ICT), b or the ejection time (ET, the duration of left ventricular outflow) and the isovolumetric relaxation time (IRT), Note: arrow represents valve clicks. Example of cardiac Doppler waveform of fetuses with Hb Bart's disease at 13 weeks of gestation, depicts components of left ventricular Tei index; interval a extends from the cessation to the onset of mitral inflow and includes the isovolumetric contraction time (ICT), b or the ejection time (ET, the duration of left ventricular outflow) and the isovolumetric relaxation time (IRT), Note: arrow represents valve clicks.
component of Tei index that was significantly increased, signifying that cardiac workload in the early phase of anemia is firstly involved in systolic dysfunction rather than diastolic function. This is based on the fact that the ICT is an important index reflexive of systolic function [9], while IRT is reflexive of diastolic function [10]. Interestingly, ICT may be mainly responsible for an increase in Tei index in early stage and this may be an independent indicator for fetal anemia whereas all of the other isolated Doppler indices were not significantly different from those in unaffected fetuses. According to our previous studies, fetal anemia secondary to Hb Bart's disease in the early phase is not associated with increased preload and deterioration of myocardial contractility [11,12], in spite of hypervolemia but increased cardiac output. Nevertheless, this study indicated that in early fetal anemia, myocardium shows some degree of increased workload by increasing ICT and Tei index. Therefore, we speculate that this may be fetal physiologic adaptation to cope with anemic state rather than pathologic ventricular dysfunction. An increase in the ICT and Tei index in the early stage may not be a sign of cardiac dysfunction, just a good response to hemodynamic overload. Since fetal anemia in this study was lethal, cardiac Doppler studies in these fetuses are of no clinical value. However, it could be a study model for anemia secondary to non-lethal causes such as pavovirus B19 or Rh
isoimmunization. Thus cardiac Doppler assessment may be helpful in predicting the prognosis and, therefore, in making a choice of management. In conclusion, ICT and Tei index of the fetuses with Hb Bart's disease were significantly increased as early as in late first trimester, suggesting that they may be helpful in predicting affected fetuses among those at risk. Additionally, this study helps us more in understand the pathophysiology regarding fetal cardiac adaptation to anemia early in fetal life and also indicates that assessment of cardiac Doppler velocity may theoretically be useful in identifying fetal anemia from any causes in early stage.
Disclosure statement No conflict of interest.
Acknowledgment The authors wish to thank the National Research University Project under Thailand's Office of the Higher Education Commission (NRUCMU19-01-2554) for financial support.
Table 1 Comparison of various cardiac Doppler indices between the group of Hb Bart's fetuses and unaffected fetuses. Diagnosis
ICT IRT ET Tei index E/A ratio at mitral valve E/A ratio at tricuspid valve PSV of the aorta TPV of the aorta VTI of the aorta PSV of the pulmonary artery TPV of the pulmonary artery VTI of the pulmonary artery
Unaffected fetuses
Hb Bart's fetuses
Mean
SD
Mean
SD
5.65 7.80 30.57 0.44 0.53 0.60 43.86 12.02 1428.15 58.60 7.76 1533.29
3.03 3.52 13.36 0.06 0.06 0.08 37.99 15.93 1077.40 24.33 5.66 840.69
7.16 6.95 27.56 0.51 0.50 0.59 56.33 6.80 1418.21 57.29 5.98 1367.69
2.49 2.43 7.67 0.06 0.08 0.05 28.61 3.21 1249.24 27.08 2.60 1044.34
p-Valuea
0.061 0.337 0.357 0.000 0.151 0.541 0.228 0.157 0.977 0.864 0.209 0.551
Unaffected fetuses
Hb Bart's fetuses
Median
IQR
Median
IQR
4.84 7.37 26.69 0.43 0.52 0.61 52.55 7.25 1166.78 62.96 5.64 1661.42
3.60 2.87 16.72 0.06 0.10 0.11 36.81 5.05 1536.55 28.12 3.52 959.67
5.78 6.79 27.01 0.52 0.50 0.61 45.12 6.15 1157.20 46.40 5.08 996.40
3.90 4.02 11.77 0.05 0.05 0.07 36.31 5.06 1144.02 20.75 1.57 927.61
p-Valueb
0.006 0.395 0.600 0.000 0.119 0.864 0.375 0.506 0.657 0.410 0.140 0.179
SD: standard deviation; IQR: interquartile range; ICT: isovolumetric contraction time; IRT: isovolumetric relaxation time; ET: ejection time; PSV: peak systolic velocity; TPV: time-to-peak; VTI: velocity time integral. a Student's T test. b Mann–Whitney U test.
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S. Luewan et al. / International Journal of Cardiology 184 (2015) 614–616
Fig. 2. Boxplots of the components of myocardial performance (Tei) index of the fetuses with Hb Bart's disease and unaffected fetuses A: isovolumetric contraction time (ICT), B: isovolumetric relaxation time (IRT), C: ejection time (ET), and D: Tei index.
References [1] Y.H. Lam, M.H. Tang, C.P. Lee, H.Y. Tse, Nuchal translucency in fetuses affected by homozygous alpha-thalassemia-1 at 12–13 weeks of gestation, Ultrasound Obstet. Gynecol. 13 (4) (Apr 1999) 238–240. [2] K.Y. Leung, K.B. Cheong, C.P. Lee, V. Chan, Y.H. Lam, M. Tang, Ultrasonographic prediction of homozygous alpha(0)-thalassemia using placental thickness, fetal cardiothoracic ratio and middle cerebral artery Doppler: alone or in combination? Ultrasound. Obstet. Gynecol 35 (2) (Jan 2010) 149–154. [3] S. Sirichotiyakul, S. Luewan, K. Srisupundit, F. Tongprasert, T. Tongsong, Prenatal ultrasound evaluation of fetal Hb Bart's disease among pregnancies at risk at 11 to 14 weeks of gestation, Prenat. Diagn. 34 (3) (Mar 2014) 230–234. [4] G. Chao, C. Zheng, D. Meng, J. Su, X. Xie, W. Li, et al., Tei index: the earliest detectable cardiac structural and functional abnormality detectable in Hb Bart's foetal edema, Int. J. Cardiol. 134 (3) (May 29 2009) e150–e154. [5] S. Luewan, F. Tongprasert, K. Srisupundit, T. Tongsong, Fetal myocardial performance (Tei) index in fetal hemoglobin Bart's disease, Ultraschall Med. 34 (4) (Aug 2013) 355–358. [6] K. Ichizuka, R. Matsuoka, J. Hasegawa, N. Shirato, M. Jimbo, K. Otsuki, et al., The Tei index for evaluation of fetal myocardial performance in sick fetuses, Early Hum. Dev. 81 (3) (Mar 2005) 273–279.
[7] S. Luewan, F. Tongprasert, K. Srisupundit, K. Traisrisilp, T. Tongsong, Reference ranges of myocardial performance index from 12 to 40 weeks of gestation, Arch. Gynecol. Obstet. 290 (5) (Nov 2014) 859–865. [8] Y.H. Lam, M.H. Tang, C.P. Lee, H.Y. Tse, Prenatal ultrasonographic prediction of homozygous type 1 alpha-thalassemia at 12 to 13 weeks of gestation, Am. J. Obstet. Gynecol. 180 (1 Pt 1) (Jan 1999) 148–150. [9] M.J. Wolk, J.F. Keefe, O.H. Bing, L.J. Finkelstein, H.J. Levine, Estimation of Vmax in auxotonic systoles from the rate of relative increase of isovolumic pressure: (dP-dt)kP, J. Clin. Invest. 50 (6) (Jun 1971) 1276–1285. [10] W. Grossman, L.P. McLaurin, E.L. Rolett, Alterations in left ventricular relaxation and diastolic compliance in congestive cardiomyopathy, Cardiovasc. Res. 13 (9) (Sep 1979) 514–522. [11] T. Tongsong, F. Tongprasert, K. Srisupundit, S. Luewan, Venous Doppler studies in low-output and high-output hydrops fetalis, Am. J. Obstet. Gynecol. 203 (5) (Nov 2010) 488.e1–488.e6. [12] T. Tongsong, C. Wanapirak, W. Piyamongkol, S. Sirichotiyakul, F. Tongprasert, K. Srisupundit, et al., Fetal ventricular shortening fraction in hydrops fetalis, Obstet. Gynecol. 117 (1) (Jan 2011) 84–91.