Evaluation of Ventricular Dyssynchrony Measured by Tissue Doppler Indices in Fetuses of Diabetic Mothers: A Case-Control Study
Abstract
Background: This study aimed to evaluate the effects of overt maternal diabetes on fetal cardiac function.
Methods: In this case-control study, 26 pregnant women with overt diabetes (the case group) and 26 women with uncomplicated pregnancies (the control group) were examined using tissue Doppler echocardiography. Cardiac function was assessed twice in the fetal period (18–22 weeks and 28 weeks of gestation) and once in the neonatal period (1 week postnatal). Fetal cardiac function was assessed using early-diastolic maximum velocity index (Em), end-diastolic maximum velocity index (Am), Em/Am, left ventricular myocardial function index (LVMPI), and interventricular mechanical delay index (IVMDI).
Results: The case and control groups were not significantly different in maternal and gestational age in fetal Doppler evaluation. Em (P=0.007), Am (P<0.001), LVMPI (P=0.003), and IVMDI (P=0.026) were significantly higher in the case group than in the control group, while there was no significant difference in Em/Am (P=0.264). Eight fetuses (30.8%) of diabetic mothers had dyssynchrony, while no cases of dyssynchrony were seen in fetuses of non-diabetic mothers (P=0.004). Infants of diabetic mothers were 8.8 times more likely to develop adverse neonatal outcomes than infants of healthy mothers (RR: 8.8, 95% CI: 1.71 to 45.31, P=0.009).
Conclusion: The findings of the current study revealed significant cardiac dysfunction and dyssynchrony in fetuses of diabetic pregnant women. Additionally, IVMDI and LVMPI can be used to predict adverse neonatal outcomes in pregnancies complicated with overt diabetes.
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11. Malaza N, Masete M, Adam S, Dias S, Nyawo T, Pheiffer C. A Systematic Review to Compare Adverse Pregnancy Outcomes in Women with Pregestational Diabetes and Gestational Diabetes. Int J Environ Res Public Health 2022;19:10846.
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13. Zoroufian A, Razmi T, Taghavi-Shavazi M, Lotfi-Tokaldany M, Jalali A. Evaluation of subclinical left ventricular dysfunction in diabetic patients: longitudinal strain velocities and left ventricular dyssynchrony by two-dimensional speckle tracking echocardiography study. Echocardiography 2014;31:456-463.
14. Willruth AM, Geipel AK, Berg CT, Fimmers R, Gembruch UG. Comparison of global and regional right and left ventricular longitudinal peak systolic strain, strain rate and velocity in healthy fetuses using a novel feature tracking technique. J Perinat Med 2011;39:549-556.
15. Buckberg G, Hoffman JI, Mahajan A, Saleh S, Coghlan C. Cardiac mechanics revisited: the relationship of cardiac architecture to ventricular function. Circulation 2008;118:2571-2587.
16. Crispi F, Sepulveda-Swatson E, Cruz-Lemini M, Rojas-Benavente J, Garcia-Posada R, Dominguez JM, Sitges M, Bijnens B, Gratacós E. Feasibility and reproducibility of a standard protocol for 2D speckle tracking and tissue Doppler-based strain and strain rate analysis of the fetal heart. Fetal Diagn Ther 2012;32:96-108.
17. Fujiwara S, Komamura K, Nakabo A, Masaki M, Fukui M, Sugahara M, Itohara K, Soyama Y, Goda A, Hirotani S, Mano T, Masuyama T. The association between left ventricular twisting motion and mechanical dyssynchrony: a three-dimensional speckle tracking study. Heart Vessels 2016;31:158-164.
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19. Rolf N, Kerschke L, Braun J, Falkenberg MK, Hammer K, Köster HA, Möllers M, Oelmeier de Murcia K, Klockenbusch W, Schmitz R. Quantification of fetal myocardial function in pregnant women with diabetic diseases and in normal controls using speckle tracking echocardiography (STE). J Perinat Med 2018;47:68-76.
20. Hatém MA, Zielinsky P, Hatém DM, Nicoloso LH, Manica JL, Piccoli AL, Zanettini J, Oliveira V, Scarpa F, Petracco R. Assessment of diastolic ventricular function in fetuses of diabetic mothers using tissue Doppler. Cardiol Young 2008;18:297-302.
21. Hornberger LK. Maternal diabetes and the fetal heart. Heart 2006;92:1019-1021.
22. Bogo MA, Pabis JS, Bonchoski AB, Santos DCD, Pinto TJF, Simões MA, Silva JC, Pabis FC. Cardiomyopathy and cardiac function in fetuses and newborns of diabetic mothers. J Pediatr (Rio J) 2021;97:520-524.
23. Oncel Alanyali M, Alkan F, Artunc Ulkumen B, Coskun S. Use of the modified myocardial performance index for evaluating fetal cardiac functions in pregestational diabetic pregnancy babies. J Obstet Gynaecol 2021;41:187-192.
24. Sanhal CY, Daglar HK, Kara O, Uygur D, Yucel A. Assessment of fetal myocardial performance index in women with pregestational and gestational diabetes mellitus. J Obstet Gynaecol Res 2017;43:65-72.
25. Zielinsky P, Piccoli AL Jr. Myocardial hypertrophy and dysfunction in maternal diabetes. Early Hum Dev 2012;88:273-278.
26. Figueroa H, Silva MC, Kottmann C, Viguera S, Valenzuela I, Hernandez-Andrade E, Gratacos E, Arraztoa JA, Illanes SE. Fetal evaluation of the modified-myocardial performance index in pregnancies complicated by diabetes. Prenat Diagn 2012;32:943-948.
27. Bui YK, Kipps AK, Brook MM, Moon-Grady AJ. Tissue Doppler is more sensitive and reproducible than spectral pulsed-wave Doppler for fetal right ventricle myocardial performance index determination in normal and diabetic pregnancies. J Am Soc Echocardiogr 2013;26:507-514.
28. Fujiwara S, Komamura K, Nakabo A, Masaki M, Fukui M, Sugahara M, Itohara K, Soyama Y, Goda A, Hirotani S, Mano T, Masuyama T. The association between left ventricular twisting motion and mechanical dyssynchrony: a three-dimensional speckle tracking study. Heart Vessels 2016;31:158-64.
29. Friedberg MK, Silverman NH, Dubin AM, Rosenthal DN. Mechanical dyssynchrony in children with systolic dysfunction secondary to cardiomyopathy: a Doppler tissue and vector velocity imaging study. J Am Soc Echocardiogr 2007;20:756-763.
30. Dandel M, Lehmkuhl H, Knosalla C, Suramelashvili N, Hetzer R. Strain and strain rate imaging by echocardiography - basic concepts and clinical applicability. Curr Cardiol Rev 2009;5:133-148.
31. Chan YH, Wang CL, Kuo CT, Yeh YH, Wu CT, Wu LS. Clinical Assessment and Implication of Left Ventricular Mechanical Dyssynchrony in Patients with Heart Failure. Acta Cardiol Sin 2013;29:505-514.
2. McCance DR. Diabetes in pregnancy. Best Pract Res Clin Obstet Gynaecol 2015;29:685-699.
3. Tabib A, Shirzad N, Sheikhbahaei S, Mohammadi S, Qorbani M, Haghpanah V, Abbasi F, Hasani-Ranjbar S, Baghaei-Tehrani R. Cardiac malformations in fetuses of gestational and pre-gestational diabetic mothers. Iran J Pediatr 2013;23:664-668.
4. Kallem VR, Pandita A, Pillai A. Infant of diabetic mother: what one needs to know? J Matern Fetal Neonatal Med 2020;33:482-492.
5. Liu F, Liu S, Ma Z, Zhan X, Tao G, Cheng L, Song X. Assessment of left ventricular systolic function in fetuses without myocardial hypertrophy of gestational diabetes mellitus mothers using velocity vector imaging. J Obstet Gynaecol 2012;32:252-256.
6. Simpson J. Speckle tracking for the assessment of fetal cardiac function. Ultrasound Obstet Gynecol 2011;37:133-134.
7. Corrigan N, Brazil DP, McAuliffe F. Fetal cardiac effects of maternal hyperglycemia during pregnancy. Birth Defects Res A Clin Mol Teratol 2009;85:523-530.
8. Köster HA, Hammer K, Braun J, Oelmeier de Murcia K, Möllers M, Klockenbusch W, Schmitz R. Comparison of strain and dyssynchrony measurements in fetal two-dimensional speckle tracking echocardiography using Philips and TomTec. J Perinat Med 2020;48:266-273.
9. Gardiner HM, Pasquini L, Wolfenden J, Kulinskaya E, Li W, Henein M. Increased periconceptual maternal glycated haemoglobin in diabetic mothers reduces fetal long axis cardiac function. Heart 2006;92:1125-1130.
10. Vogel M, Cheung MM, Li J, Kristiansen SB, Schmidt MR, White PA, Sorensen K, Redington AN. Noninvasive assessment of left ventricular force-frequency relationships using tissue Doppler-derived isovolumic acceleration: validation in an animal model. Circulation 2003;107:1647-1652.
11. Malaza N, Masete M, Adam S, Dias S, Nyawo T, Pheiffer C. A Systematic Review to Compare Adverse Pregnancy Outcomes in Women with Pregestational Diabetes and Gestational Diabetes. Int J Environ Res Public Health 2022;19:10846.
12. Moses RG. New consensus criteria for GDM: problem solved or a pandora's box? Diabetes Care 2010;33:690-691.
13. Zoroufian A, Razmi T, Taghavi-Shavazi M, Lotfi-Tokaldany M, Jalali A. Evaluation of subclinical left ventricular dysfunction in diabetic patients: longitudinal strain velocities and left ventricular dyssynchrony by two-dimensional speckle tracking echocardiography study. Echocardiography 2014;31:456-463.
14. Willruth AM, Geipel AK, Berg CT, Fimmers R, Gembruch UG. Comparison of global and regional right and left ventricular longitudinal peak systolic strain, strain rate and velocity in healthy fetuses using a novel feature tracking technique. J Perinat Med 2011;39:549-556.
15. Buckberg G, Hoffman JI, Mahajan A, Saleh S, Coghlan C. Cardiac mechanics revisited: the relationship of cardiac architecture to ventricular function. Circulation 2008;118:2571-2587.
16. Crispi F, Sepulveda-Swatson E, Cruz-Lemini M, Rojas-Benavente J, Garcia-Posada R, Dominguez JM, Sitges M, Bijnens B, Gratacós E. Feasibility and reproducibility of a standard protocol for 2D speckle tracking and tissue Doppler-based strain and strain rate analysis of the fetal heart. Fetal Diagn Ther 2012;32:96-108.
17. Fujiwara S, Komamura K, Nakabo A, Masaki M, Fukui M, Sugahara M, Itohara K, Soyama Y, Goda A, Hirotani S, Mano T, Masuyama T. The association between left ventricular twisting motion and mechanical dyssynchrony: a three-dimensional speckle tracking study. Heart Vessels 2016;31:158-164.
18. Enzensberger C, Achterberg F, Degenhardt J, Wolter A, Graupner O, Herrmann J, Axt-Fliedner R. Feasibility and Reproducibility of Two-Dimensional Wall Motion Tracking (WMT) in Fetal Echocardiography. Ultrasound Int Open 2017;3:E26-E33.
19. Rolf N, Kerschke L, Braun J, Falkenberg MK, Hammer K, Köster HA, Möllers M, Oelmeier de Murcia K, Klockenbusch W, Schmitz R. Quantification of fetal myocardial function in pregnant women with diabetic diseases and in normal controls using speckle tracking echocardiography (STE). J Perinat Med 2018;47:68-76.
20. Hatém MA, Zielinsky P, Hatém DM, Nicoloso LH, Manica JL, Piccoli AL, Zanettini J, Oliveira V, Scarpa F, Petracco R. Assessment of diastolic ventricular function in fetuses of diabetic mothers using tissue Doppler. Cardiol Young 2008;18:297-302.
21. Hornberger LK. Maternal diabetes and the fetal heart. Heart 2006;92:1019-1021.
22. Bogo MA, Pabis JS, Bonchoski AB, Santos DCD, Pinto TJF, Simões MA, Silva JC, Pabis FC. Cardiomyopathy and cardiac function in fetuses and newborns of diabetic mothers. J Pediatr (Rio J) 2021;97:520-524.
23. Oncel Alanyali M, Alkan F, Artunc Ulkumen B, Coskun S. Use of the modified myocardial performance index for evaluating fetal cardiac functions in pregestational diabetic pregnancy babies. J Obstet Gynaecol 2021;41:187-192.
24. Sanhal CY, Daglar HK, Kara O, Uygur D, Yucel A. Assessment of fetal myocardial performance index in women with pregestational and gestational diabetes mellitus. J Obstet Gynaecol Res 2017;43:65-72.
25. Zielinsky P, Piccoli AL Jr. Myocardial hypertrophy and dysfunction in maternal diabetes. Early Hum Dev 2012;88:273-278.
26. Figueroa H, Silva MC, Kottmann C, Viguera S, Valenzuela I, Hernandez-Andrade E, Gratacos E, Arraztoa JA, Illanes SE. Fetal evaluation of the modified-myocardial performance index in pregnancies complicated by diabetes. Prenat Diagn 2012;32:943-948.
27. Bui YK, Kipps AK, Brook MM, Moon-Grady AJ. Tissue Doppler is more sensitive and reproducible than spectral pulsed-wave Doppler for fetal right ventricle myocardial performance index determination in normal and diabetic pregnancies. J Am Soc Echocardiogr 2013;26:507-514.
28. Fujiwara S, Komamura K, Nakabo A, Masaki M, Fukui M, Sugahara M, Itohara K, Soyama Y, Goda A, Hirotani S, Mano T, Masuyama T. The association between left ventricular twisting motion and mechanical dyssynchrony: a three-dimensional speckle tracking study. Heart Vessels 2016;31:158-64.
29. Friedberg MK, Silverman NH, Dubin AM, Rosenthal DN. Mechanical dyssynchrony in children with systolic dysfunction secondary to cardiomyopathy: a Doppler tissue and vector velocity imaging study. J Am Soc Echocardiogr 2007;20:756-763.
30. Dandel M, Lehmkuhl H, Knosalla C, Suramelashvili N, Hetzer R. Strain and strain rate imaging by echocardiography - basic concepts and clinical applicability. Curr Cardiol Rev 2009;5:133-148.
31. Chan YH, Wang CL, Kuo CT, Yeh YH, Wu CT, Wu LS. Clinical Assessment and Implication of Left Ventricular Mechanical Dyssynchrony in Patients with Heart Failure. Acta Cardiol Sin 2013;29:505-514.
| Files | ||
| Issue | Vol 19 No 4 (2024): J Teh Univ Heart Ctr | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/jthc.v19i4.17614 | |
| Keywords | ||
| Pregnancy Diabetes mellitus Fetus | ||
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How to Cite
1.
Kalai Moghadam M, Hemmatian MN, Mirmohammadkhani M, Rahmanian M. Evaluation of Ventricular Dyssynchrony Measured by Tissue Doppler Indices in Fetuses of Diabetic Mothers: A Case-Control Study. J Tehran Heart Cent. 2024;19(4):276-282.
