Decreased fetal cardiac performance in the first trimester correlates with hyperglycemia in pregestational maternal diabetes
Abstract
Objective: In‐vitro animal studies suggest that high glucose levels impair fetal cardiac function early in gestation. We aimed to study whether evidence of first‐trimester myocardial dysfunction can be detected in fetuses of women with pregestational diabetes mellitus. Methods: Women with diabetes mellitus underwent fetal echocardiography at 11–14 weeks' gestational age. In fetuses with normal anatomy, the cardiac preload, diastolic function, global myocardial performance and placental afterload were studied by Doppler of the ductus venosus (DV), mitral and tricuspid early/atrial (E/A) ratios, left and right ventricular myocardial performance index (MPI) and umbilical artery (UA) Doppler, respectively. Cases were matched for gestational age and UA and DV Doppler with controls that had no diabetes mellitus. Results: Sixty‐three singleton diabetic pregnancies were matched with 63 controls. Mean gestational age at enrollment was 12.6 (range, 11.1–13.6) weeks. Diabetic mothers had moderate to poor glycemic control (median (range) glycosylated hemoglobin A1 (HbA1c), 7.5 (5.1–12.7)%, and the HbA1c level was ≥ 7% in 37 (59%)). Fetuses of diabetic mothers exhibited worse measures of diastolic dysfunction: the isovolumetric relaxation time (IRT) was significantly prolonged (left ventricle: 36.9 ± 7.4 ms vs. 45.8 ± 6.8 ms; right ventricle: 35.6 ± 8 ms vs. 46.4 ± 7.3 ms,P< 0.0001 for both). The mitral E/A ratio was lower in diabetics (0.55 ± 0.06 vs. 0.51 ± 0.08,P= 0.03), and the global myocardial performance was lower in both ventricles (left ventricle MPI: 0.5 ± 0.08; right ventricle MPI: 0.52 ± 0.08,P= 0.03 and P< 0.0001, respectively). This lower global myocardial performance was caused by a prolonged myocardial relaxation time, which was most marked in diabetics with an HbA1c of ≥ 7% (P< 0.001 vs. controls for both ventricles). There were no significant correlations between cardiac Doppler parameters and DV, UA indices and fetal heart rate (P> 0.05 for all). Conclusions: Fetuses of poorly controlled diabetic mothers demonstrate significant differences in first‐trimester diastolic myocardial function compared with non‐diabetic controls. The decrease in myocardial performance is more marked with increasing HbA1c and appears to be independent of preload and afterload. The ability to document these cardiac functional changes this early in pregnancy opens potential new avenues to understand the consequences of maternal glycemic status. Copyright © 2011 ISUOG. Published by John Wiley & Sons, Ltd.
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Fetal hypertrophic cardiomyopathy is a well-recognized feature of gestational diabetes mellitus, though it was believed that this resolved within a few months of birth.
“Fetal hypertrophic cardiomyopathy is a well-recognized feature of GDM, though it was believed that this resolved within a few months of birth [78,79,80,81,82].”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [78]
Cites
STATISTICAL METHODS FOR ASSESSING AGREEMENT BETWEEN TWO METHODS OF CLINICAL MEASUREMENT
Martin Bland, J., & Altman, D. (1986) · The Lancet · doi:10.1016/s0140-6736(86)90837-8 · Cited by 47,965 · see citing works
Beckett, A. H., Rowland, M., & TURNER, P. (1965) · The Lancet · doi:10.1016/s0140-6736(65)91037-8 · Cited by 16,917 · see citing works
Fetal origins of adult disease: strength of effects and biological basis
Barker, D., Eriksson, J., Forsén, T., & Osmond, C. (2002) · International Journal of Epidemiology · doi:10.1093/ije/31.6.1235 · Cited by 2,024 · see citing works
Casson, I. F., Clarke, C. A., Howard, C. V., McKendrick, O., Pennycook, S., Pharoah, P. O. D., Platt, M. J., Stanisstreet, M., van Velszen, D., & Walkinshaw, S. A. (1997) · BMJ · doi:10.1136/bmj.315.7103.275 · Cited by 522 · see citing works
The role of secondary heart field in cardiac development
Dyer, L. A., & Kirby, M. L. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.10.009 · Cited by 262 · see citing works
Hernandez‐Andrade, E. A., Horacio Figueroa, D., Kottmann, C., Illanes, S. E., Arraztoa, J., Acosta‐Rojas, R., & Gratacós, E. (2007) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.3947 · Cited by 160 · see citing works
Pathologic ventricular hypertrophy in the offspring of diabetic mothers: a retrospective study
Ullmo, S., Vial, Y., Bernardo, S. D., Roth‐Kleiner, M., Mivelaz, Y., Sekarski, N., Ruiz, J. C., & Meijboom, E. J. (2006) · European Heart Journal · doi:10.1093/eurheartj/ehl416 · Cited by 142 · see citing works
Morgan, S. C., Relaix, F., Sandell, L. J., & Loeken, M. R. (2008) · Birth Defects Research Part A Clinical and Molecular Teratology · doi:10.1002/bdra.20457 · Cited by 140 · see citing works
Srinivasan, D. K., Dheen, S. T., & Tay, S. S. W. (2007) · Cardiovascular Diabetology · doi:10.1186/1475-2840-6-34 · Cited by 125 · see citing works
Effect of pregestational diabetes mellitus on fetal cardiac function and structure
Russell, N. E., Foley, M., Kinsley, B., Firth, R. G., Coffey, M., & McAuliffe, F. M. (2008) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2008.07.016 · Cited by 105 · see citing works
Fetal cardiac hypertrophy and cardiac function in diabetic pregnancies
Gandhi, J. A., Zhang, X. Y., & Maidman, J. E. (1995) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(95)91339-4 · Cited by 87 · see citing works
Neural Crest is Involved in Development of Abnormal Myocardial Function
Conway, S. J., Godt, R. E., Hatcher, C. J., Leatherbury, L., Zolotouchnikov, V. V., Brotto, M. A. P., Copp, A. J., Kirby, M. L., & Creazzo, T. L. (1997) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.1997.0499 · Cited by 82 · see citing works
Accelerated cardiac growth and abnormal cardiac flow in fetuses of type I diabetic mothers.
Rizzo, G., Arduini, D., & Romaninï, C. (1992) · PubMed · Cited by 81 · see citing works
Cardiac growth in fetuses of diabetic mothers with good metabolic control
WEBER, H., Copel, J. A., Reece, E. A., GREEN, J., & Kleinman, C. S. (1991) · The Journal of Pediatrics · doi:10.1016/s0022-3476(05)81858-x · Cited by 79 · see citing works
Self-citationFalcon, O., Auer, M., Gerovassili, A., Spencer, K., & Nicolaides, K. H. (2005) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.2699 · Cited by 75 · see citing works
Gurjarpadhye, A. A., Hewett, K. W., Justus, C. D., Wen, X., Stadt, H. A., Kirby, M. L., Sedmera, D., & Gourdie, R. G. (2006) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01017.2006 · Cited by 75 · see citing works
Assessment of diastolic ventricular function in fetuses of diabetic mothers using tissue Doppler
Hatem, M. A. B., Zielinsky, P., Hatem, D. M., Nicoloso, L. H. S., Mânica, J. L., Piccoli, A. L., Jr., Zanettini, J. S., Oliveira, V., Scarpa, F., & Petracco, R. G. (2008) · Cardiology in the Young · doi:10.1017/s1047951108002138 · Cited by 69 · see citing works
Farrell, M. J., Burch, J. L., Wallis, K. T., Rowley, L., Kumiski, D. H., Stadt, H. A., Godt, R. E., Creazzo, T. L., & Kirby, M. L. (2001) · Journal of Clinical Investigation · doi:10.1172/jci9317 · Cited by 63 · see citing works
Turan, S., Turan, O. M., Ty-Torredes, K., Harman, C. R., & Baschat, A. (2009) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.6372 · Cited by 62 · see citing works
Self-citationHuggon, I. C., Turan, O. M., & Allan, L. D. (2004) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.1720 · Cited by 60 · see citing works
Self-citationVenous Doppler in the assessment of fetal cardiovascular status
Baschat, A., & Harman, C. R. (2006) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/01.gco.0000192988.07471.f9 · Cited by 54 · see citing works
Self-citationRizzo, G., Arduini, D., Capponi, A., & Romaninï, C. (1995) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(95)90426-3 · Cited by 50 · see citing works
Macklon, N. S., Hop, W. C. J., & Wladimiroff, J. W. (1998) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1998.tb10182.x · Cited by 38 · see citing works
Examination of the fetal cardiovascular system
Baschat, A. (2010) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2010.09.002 · Cited by 37 · see citing works
Self-citationAltered fetal circulation in type‐1 diabetic pregnancies
Lisowski, L. A., Verheijen, P. M., de Smedt, M. M. C., Visser, G. H. A., & Meijboom, E. J. (2003) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.88 · Cited by 33 · see citing works
First-Trimester Fetal Cardiac Function
Russell, N. E., & McAuliffe, F. M. (2008) · Journal of Ultrasound in Medicine · doi:10.7863/jum.2008.27.3.379 · Cited by 26 · see citing works
Cell biology of cardiac development
Farrell, M. J., & Kirby, M. L. (2001) · International review of cytology · doi:10.1016/s0074-7696(01)02004-6 · Cited by 25 · see citing works
Leatherbury, L., Braden, D. S., Tomita, H., GAULDIN, H. E., & Jackson, W. F. (1990) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1990.tb13220.x · Cited by 24 · see citing works
Analysis of factors influencing ventricular filling patterns in fetuses of type I diabetic mothers
Rizzo, G., Pietropolli, A., Capponi, A., Cacciatore, C., Arduini, D., & Romaninï, C. (1994) · Journal of Perinatal Medicine · doi:10.1515/jpme.1994.22.2.149 · Cited by 22 · see citing works
Neural Crest, Great Arteries, and Outflow Septation
Kirby, M. L. (2007) · doi:10.1093/oso/9780195178197.003.0011 · Cited by 5 · see citing works
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Fetal Cardiac Function: Technical Considerations and Potential Research and Clinical Applications
Crispi, F., & Gratacós, E. (2012) · Fetal Diagnosis and Therapy · doi:10.1159/000338003 · Cited by 155 · see citing works
Depla, A. L., de Wit, L., Steenhuis, T. J., Slieker, M. G., Voormolen, D. N., Scheffer, P. G., de Heus, R., van Rijn, B. B., & Bekker, M. N. (2020) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.22163 · Cited by 120 · see citing works
Al‐Beltagi, M., Tolba, O., Rowisha, M. A., Mahfouz, A. E., & Elewa, M. A. (2014) · Pediatric Cardiology · doi:10.1007/s00246-014-1033-0 · Cited by 76 · see citing works
Ultrasound assessment of fetal cardiac function
Crispi, F., Valenzuela‐Alcaraz, B., Cruz‐Lemini, M., & Gratacós, E. (2013) · Australasian Journal of Ultrasound in Medicine · doi:10.1002/j.2205-0140.2013.tb00242.x · Cited by 70 · see citing works
Fetal myocardial deformation in maternal diabetes mellitus and obesity
Kulkarni, A., Li, L., Craft, M., Nanda, M., Lorenzo, J. M. M. D., Danford, D. A., & Kutty, S. (2016) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.15971 · Cited by 61 · see citing works
Maternal obesity affects fetal myocardial function as early as in the first trimester
Ingul, C. B., Loraas, L., Tegnander, E., Eik‐Nes, S. H., & Brantberg, A. (2015) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.14841 · Cited by 59 · see citing works
Sanhal, C. Y., Dağlar, H. K., Kara, Ö., Uygur, D., & Yücel, A. (2016) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.13174 · Cited by 58 · see citing works
Early Evaluation of the Fetal Heart
Hernandez‐Andrade, E. A., Patwardhan, M., Cruz-Lemini, M., & Luewan, S. (2017) · Fetal Diagnosis and Therapy · doi:10.1159/000477564 · Cited by 54 · see citing works
Mahajan, A., Henry, A., Meriki, N., Hernandez‐Andrade, E. A., Crispi, F., Wu, L., & Welsh, A. W. (2015) · Fetal Diagnosis and Therapy · doi:10.1159/000363181 · Cited by 50 · see citing works
The effect of pregestational diabetes on fetal heart function
Pauliks, L. B. (2014) · Expert Review of Cardiovascular Therapy · doi:10.1586/14779072.2015.988141 · Cited by 49 · see citing works
Ghawi, H., Gendi, S., Mallula, K. K., Zghouzi, M., Faza, N. N., & Awad, S. M. M. (2013) · Pediatric Cardiology · doi:10.1007/s00246-013-0709-1 · Cited by 44 · see citing works
Maternal hyperglycemia leads to fetal cardiac hyperplasia and dysfunction in a rat model
Lehtoranta, L., Vuolteenaho, O. J., Laine, V. J. O., Koskinen, A., Soukka, H., Kytö, V., Määttä, J. A., Haapsamo, M., Ekholm, E. M. K., & Rasanen, J. P. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00043.2013 · Cited by 39 · see citing works
Using speckle‐tracking echocardiography to assess fetal myocardial deformation: are we there yet?
Day, T. G., Charakida, M., & Simpson, J. M. (2019) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.20233 · Cited by 39 · see citing works
Rizzo, G., Capponi, A., Pietrolucci, M. E., Aiello, E., & Arduini, D. (2012) · Prenatal Diagnosis · doi:10.1002/pd.3848 · Cited by 37 · see citing works
Lin, X., Yang, P., Reece, E. A., & Yang, P. (2017) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2017.04.008 · Cited by 36 · see citing works
Self-citationKereliuk, S. M., & Dolinsky, V. W. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23084467 · Cited by 34 · see citing works
Bui, Y. K., Kipps, A. K., Brook, M. M., & Moon‐Grady, A. J. (2013) · Journal of the American Society of Echocardiography · doi:10.1016/j.echo.2013.02.006 · Cited by 33 · see citing works
Assessment of Fetal Cardiac Function in Mild Preeclampsia
Ballı, Ş., Kibar, A. E., Ece, İ., Oflaz, M. B., & Yilmaz, O. (2013) · Pediatric Cardiology · doi:10.1007/s00246-013-0702-8 · Cited by 29 · see citing works
Functional echocardiography in the fetus with non-cardiac disease
Mieghem, T. V., Hodges, R. J., JAEGGI, E. T., & Ryan, G. (2013) · Prenatal Diagnosis · doi:10.1002/pd.4254 · Cited by 28 · see citing works
Zidere, V., Vigneswaran, T. V., Syngelaki, A., Charakida, M., Allan, L. D., Nicolaides, K. H., Simpson, J. M., & Akolekar, R. (2021) · Journal of the American Society of Echocardiography · doi:10.1016/j.echo.2021.04.017 · Cited by 27 · see citing works
Fetal Cardiac Function: Myocardial Performance Index
Oliveira, M., Dias, J. P., & Guedes‐Martins, L. (2021) · Current Cardiology Reviews · doi:10.2174/1573403x18666211227145856 · Cited by 25 · see citing works
Pregestational diabetes and fetal heart rate in the first trimester of pregnancy
Sirico, A., Sarno, L., Zullo, F., Martinelli, P., & Maruotti, G. M. (2018) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2018.11.003 · Cited by 25 · see citing works
Pregestational Diabetes and Congenital Heart Defects
Maduro, C. S. C., de Castro, L. F., Moleiro, M. L., & Guedes‐Martins, L. (2022) · Revista Brasileira Ginecologia e Obstetrícia · doi:10.1055/s-0042-1755458 · Cited by 23 · see citing works
Valenzuela‐Alcaráz, B., Crispi, F., Cruz-Lemini, M., Bijnens, B. H., García‐Otero, L., Sitges, M., Balasch, J., & Gratacós, E. (2016) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.16217 · Cited by 23 · see citing works
Exposure of the developing heart to diabetic environment and early cardiac assessment: A review
Asoğlu, M. R., Gabbay‐Benziv, R., Turan, O. M., & Turan, Ş. (2018) · Echocardiography · doi:10.1111/echo.13811 · Cited by 22 · see citing works
Self-citationCorrelation analysis of ductus venosus velocity indices and fetal cardiac function
Sanapo, L., Turan, O. M., Turan, S., Ton, J., Atlas, M., & Baschat, A. (2013) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.13242 · Cited by 21 · see citing works
Self-citationImpact of maternal diabetes and obesity on fetal cardiac functions
Bayoumy, S., Habib, M., & Abdelmageed, R. (2020) · The Egyptian Heart Journal · doi:10.1186/s43044-020-00077-x · Cited by 19 · see citing works
Perkovic-Kepeci, S., Cirkovic, A. M., Milic, N. M., Dugalić, S., Stanisavljevic, D. M., Milinčić, M., Kostić, K., Milic, N., Todorović, J., Marković, K., et al. (2023) · Medicina · doi:10.3390/medicina59081502 · Cited by 16 · see citing works
Persistent Aortic Stiffness and Left Ventricular Hypertrophy in Children of Diabetic Mothers
Do, V., Eckersley, L., Lin, L., Davidge, S. T., Stickland, M. K., Ojala, T., Serrano-Lomelin, J., & Hornberger, L. K. (2021) · CJC Open · doi:10.1016/j.cjco.2020.10.020 · Cited by 15 · see citing works
Bravo‐Valenzuela, N. J., Peixoto, A. B., Mattar, R., Júnior, J. F. M., Pares, D. B. D. S., & Júnior, E. A. (2020) · Pediatric Cardiology · doi:10.1007/s00246-020-02362-7 · Cited by 16 · see citing works
Gudigar, A., Samanth, J., Raghavendra, U., Dharmik, C., Vasudeva, A., Ramachandran, P., Tan, R., Ciaccio, E. J., Molinari, F., & Acharya, U. R. (2020) · IEEE Access · doi:10.1109/access.2020.3042594 · Cited by 15 · see citing works
Aasa, K. L., Kwong, K. K., Adams, M. A., & Croy, B. A. (2013) · Biology of Reproduction · doi:10.1095/biolreprod.112.105759 · Cited by 14 · see citing works
Wahab, R. J., Jaddoe, V. W. V., Roest, A. A. W., Toemen, L., & Gaillard, R. (2020) · Diabetes Care · doi:10.2337/dc19-2580 · Cited by 13 · see citing works
Prospective longitudinal assessment of the fetal left modified Myocardial Performance Index
MacDonald, T. M., Robinson, A. J., Walker, S. P., & Hui, L. (2017) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767058.2017.1391777 · Cited by 11 · see citing works
Darwish, A., Abdel-Raouf, M., Kamel, R., Salah, E., Salah, M., & Okasha, A. (2022) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-022-04969-5 · Cited by 9 · see citing works
RetractedLee, M., Won, H., Shim, J., Lee, P., Kim, A., Kil, E., & Kim, M. (2017) · Journal of Ultrasound in Medicine · doi:10.7863/ultra.16.07079 · Cited by 9 · see citing works
Beşer, D. M., Oluklu, D., Hendem, D. U., Yıldırım, M., Turgut, E., & Şahın, D. (2023) · Echocardiography · doi:10.1111/echo.15649 · Cited by 8 · see citing works
de Wit, L. (2020) · doi:10.33540/195 · Cited by 9 · see citing works
The effect of maternal pregestational diabetes on fetal autonomic nervous system
Mercado, L., Escalona‐Vargas, D., Blossom, S. J., Siegel, E. R., Whittington, J. R., Preissl, H. T., Walden, K. N., & Eswaran, H. (2023) · Physiological Reports · doi:10.14814/phy2.15680 · Cited by 7 · see citing works
Akkaya, H., Büke, B., & Destegül, E. (2018) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767058.2018.1509310 · Cited by 7 · see citing works
Impaired myocardial deformation persists at 2 years in offspring of mothers with diabetes mellitus
Jacquemyn, X., Kutty, S., Dhanantwari, P., Ravekes, W. J., & Kulkarni, A. (2023) · Pediatric Research · doi:10.1038/s41390-023-02566-6 · Cited by 6 · see citing works
Şenol, G., Çetin, B. A., Esin, D., Selçuki, N. F. T., Tayyar, A., Turhan, U., Bütün, Z., & Yüksel, M. A. (2021) · Journal of Obstetrics and Gynaecology · doi:10.1080/01443615.2021.1882971 · Cited by 5 · see citing works
Comparison of Parameters of Fetal Doppler Echocardiography Between Mothers with and Without Diabetes
Pooransari, P., Mehrabi, S., Mirzamoradi, M., Salehgargari, S., & Afrakhteh, M. (2022) · Intern J Endocrinol Metab · doi:10.5812/ijem-117524 · Cited by 5 · see citing works
Bravo‐Valenzuela, N. J., Peixoto, A. B., Mattar, R., & Júnior, E. A. (2021) · Obstetrics & Gynecology Science · doi:10.5468/ogs.20274 · Cited by 4 · see citing works
Foetal cardiac function in third trimester pregnancies with reduced fetal movements
Sağlam, A., Derwig, I. E., Gül, M., Kasap, B., Yılmaz, N., Sezi̇k, M., Çelik, Ö., Tiryaki, S., Özçil, M. D., Sipahioğlu, H., et al. (2021) · Journal of Obstetrics and Gynaecology · doi:10.1080/01443615.2020.1869706 · Cited by 4 · see citing works
Maternal Complications of Pregnancy that Affect Fetal Development
Longo, L. D. (2018) · Springer eBooks · doi:10.1007/978-1-4939-7483-2_11 · Cited by 3 · see citing works
Impact of maternal diabetes mellitus on fetal atrial strain
Pathan, F. K., Lam, P., Sivapathan, S., Pathan, S., Gao, Z., Orde, S. R., Nirthanakumaran, D., Negishi, K., & Nanan, R. K. H. (2024) · The International Journal of Cardiovascular Imaging · doi:10.1007/s10554-024-03194-9 · Cited by 3 · see citing works
Arterial and Venous Doppler in Evaluation of the “At-risk” Fetus
Turan, Ş., Bucak, M., & Turan, O. M. (2024) · Clinical Obstetrics & Gynecology · doi:10.1097/grf.0000000000000890 · Cited by 3 · see citing works
Self-citationMeriki, N., & Welsh, A. W. (2017) · Australasian Journal of Ultrasound in Medicine · doi:10.1002/ajum.12035 · Cited by 3 · see citing works
Fetal circulation in maternal diabetes mellitus
Ermakova, L. B., Чечнева, М. А., Лысенко, С. Н., Petrukhin, V. A., & Фархадовна, Б. Ф. (2016) · Russian Bulletin of Obstetrician-Gynecologist · doi:10.17116/rosakush201616316-22 · Cited by 2 · see citing works
Kurt, D., İşgüder, Ç. K., Unlu, N., Ayvacı, H., Yilmaz, A., & Tuğ, N. (2025) · Journal of Clinical Ultrasound · doi:10.1002/jcu.70048 · Cited by 1 · see citing works
The Fetal Heart in Early Pregnancy
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Features of the development of the cardiovascular system in the fetus with diabetic fetopathy
Putilova, T. A., Dankova, I. V., & Tretyakova, T. B. (2022) · Russian Bulletin of Obstetrician-Gynecologist · doi:10.17116/rosakush20222206142 · Cited by 1 · see citing works
Maternal diabetes during pregnancy – obstetrical considerations and long term effects
Stuart, A. (2012) · Lund University Publications (Lund University)
Rego, M. A. F. (2012) · Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT)
Negm, S., & Kamel, R. (2012) · Evidence Based Women s Health Journal · doi:10.1097/01.ebx.0000415480.05259.f5
Fetal Imaging and Effects of Exposures on Growth and Function
Demicheva, E., & Crispi, F. (2016) · Molecular and integrative toxicology · doi:10.1007/978-3-319-27449-2_6
JAEGGI, E. T., & Donofrio, M. T. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-802393-8.00028-4
Akçöltekin, Z. (2018) · Haydarpasa Numune Training and Research Hospital Medical Journal · doi:10.14744/hnhj.2018.95530
Doppler Sonography in Pregnancies Complicated by Pre-gestational Diabetes Mellitus
Vilchez, G., & Maulik, D. (2023) · Springer eBooks · doi:10.1007/978-3-031-06189-9_22
The Fetal Heart in Early Pregnancy
Hernandez‐Andrade, E. A., & Huntley, E. S. (2023) · Springer eBooks · doi:10.1007/978-3-031-24133-8_12
Darwish, A., Abdel-Raouf, M., Kamel, R., Salah, E., Salah, M., & Okasha, A. (2022) · Figshare · doi:10.6084/m9.figshare.20517155
Goudar, S., JAEGGI, E. T., & Donofrio, M. T. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-13279-7.00053-5
Preconception Health and Future Cardiovascular Disease
Harville, E., & Gill, E. (2026) · Contemporary cardiology · doi:10.1007/978-3-032-14256-6_1
Drummond, R. F., Seif, K. E., & Reece, E. A. (2026) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2026.07.009
Self-citationFetal programming under hyperglycemic stress: the vascular system at risk
Xavier, F. E. (2026) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00390.2026
- Authors
- Turan, S., Turan, O. M., Miller, J., Harman, C., Reece, E. A., & Baschat, A. A.
- Affiliations
- University of Maryland, Baltimore (US)
- Corresponding author
- Turan, S.
- Venue
- Ultrasound in Obstetrics & Gynecology
- Publisher
- Wiley
- Published
- 2011-08-10
- Volume
- 38
- Issue
- 3
- Pages
- 325-331
- ISSN
- 0960-7692 (ISSN-L)
- 1469-0705
- OpenAlex
- W2153259159
- Cited by
- 66
- References
- 30
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 2 · 2023: 6 · 2022: 5 · 2021: 5 · 2020: 7 · 2019: 1 · 2018: 5 · 2017: 6 · 2016: 5 · 2015: 3 · 2014: 2 · 2013: 8 · 2012: 6
- FWCI
- 6.59
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Ultrasound in Obstetrics and Gynecology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Obstetrics and Gynecology › Gestational Diabetes Research and Management
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Function and Risk Factors
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Keywords
- pregestational diabetes, fetal cardiac function, first trimester, hyperglycemia, diastolic dysfunction, myocardial performance index, isovolumic relaxation time, umbilical artery Doppler, ductus venosus Doppler, maternal glycemic control, HbA1c, fetal echocardiography, fetal hypoxia
- MeSH terms
- Adult, Diabetes Mellitus, Type 1, Female, Fetal Heart, Gestational Age, Glycated Hemoglobin, Humans, Hyperglycemia, Pregnancy, Pregnancy in Diabetics, Pregnancy Outcome, Pregnancy Trimester, First, Prospective Studies, Umbilical Arteries, Echocardiography, Doppler, Ultrasonography, Prenatal, Ventricular Function
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