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Fetal Cardiac Function and Ventricular Volumes Determined by Three-Dimensional Ultrasound Using STIC and VOCAL Methods in Fetuses from Pre-gestational Diabetic Women

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Abstract

To assess the fetal cardiac function and ventricular volumes by three-dimensional (3D) ultrasound using spatio-temporal image correlation (STIC) and virtual organ computer-aided analysis (VOCAL) methods in fetuses from pre-gestational diabetic women. This was a prospective and cross-sectional study that evaluated 53 fetuses from pre-gestational diabetic women and 53 fetuses from healthy mothers between 20 and 34 weeks of gestation. Only fetuses with no structural or genetic abnormalities and singleton pregnant women were included in this study. The fetal cardiac volumes were assessed by STIC and VOCAL methods. The ejection fraction, stroke volume, and cardiac output were calculated from these measurements to evaluate fetal cardiac function. The Mann–Whitney U test was performed to compare the two groups. For calculation of intra- and interobserver reproducibility’s, we used concordance correlation coefficients. The mean differences in the right atrial volumes between the diabetic and normal groups ranged from 0.05 mL to 0.1 mL (p = 0.917 and 0.355, respectively). The median of left atrium (LA) volume measurement in pre-gestational diabetic group was significantly lower than healthy mothers (LA: 0.62 vs. 0.68 mL; p < 0.001). The fetal right and left ventricular volumes were similar in both groups. No significant differences in ejection fraction, stroke volume and cardiac output were observed (p value range 0.086–0.815). The majority of fetal atrial/ventricular volumes showed good intra- and interobserver reliabilities. Conversely, the majority cardiac function parameters showed poor intra- and interobserver agreements. STIC and VOCAL methods gave reproducible quantitative results for fetal atrial and ventricular volumes. Significant differences in fetal left atrial volumes were observed between the two groups, which be related to LA atrial dysfunction and /or left ventricle (LV) compliance, reflecting earlier stages of cardiac dysfunction.

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References

  1. Van Mieghem T, Hodges R, Jaeggi E, Ryan G (2014) Functional echocardiography in the fetus with non-cardiac disease. Prenat Diagn 34:23–32

    Article  Google Scholar 

  2. Bravo-Valenzuela NJ, Peixoto AB, Nardozza LM, Souza AS, Araujo JE (2017) Applicability and technical aspects of two-dimensional ultrasonography for assessment of fetal heart function. Med Ultrason 19:94–101

    Article  Google Scholar 

  3. Crispi F, Gratacós E (2012) Fetal cardiac function: technical considerations and potential research and clinical applications. Fetal Diagn Ther 32:47–64

    Article  Google Scholar 

  4. Hofstaetter C, Hansmann M, Eik-Nes SH, Huhta JC, Luther SL (2006) A cardiovascular profile score in the surveillance of fetal hydrops. J Matern Fetal Neonatal Med 19:407–413

    Article  Google Scholar 

  5. Turan S, Turan OM, Miller J, Harman C, Reece EA, Baschat AA (2011) Decreased fetal cardiac performance in the first trimester correlates with hyperglycemia in pregestational maternal diabetes. Ultrasound Obstet Gynecol 38:325–331

    Article  CAS  Google Scholar 

  6. Passarella G, Trifirò G, Gasparetto M, Moreolo GS, Milanesi O (2013) Disorders in glucidic metabolism and congenital heart diseases: detection and prevention. Pediatr Cardiol 34:931–937

    Article  CAS  Google Scholar 

  7. Rizzo G, Arduini D, Capponi A, Romanini C (1995) Cardiac and venous blood flow in fetuses of insulin-dependent diabetic mothers: evidence of abnormal hemodynamics in early gestation. Am J Obstet Gynecol 173:1775–1781

    Article  CAS  Google Scholar 

  8. Hunter LE, Sharland GK (2015) Maternal gestational diabetes and fetal congenital heart disease: an observational study. J Preg Child Health 2:132

    Google Scholar 

  9. Han S, Wang G, Jin Y, Ma ZL, Jia WJ, Wu X et al (2015) Investigating the mechanism of hyperglycemia-induced fetal cardiac hypertrophy. PLoS ONE 10:e0139141

    Article  Google Scholar 

  10. Russell NE, Foley M, Kinsley BT, Firth RG, Coffey M, McAuliffe FM (2008) Effect of pregestational diabetes mellitus on fetal cardiac function and structure. Am J Obstet Gynecol 199:311–312

    Google Scholar 

  11. Fouda UM, Abou ElKassem MM, Hefny SM, Fouda RM, Hashem AT (2013) Role of fetal echocardiography in the evaluation of structure and function of fetal heart in diabetic pregnancies. J Matern Fetal Neonatal Med 26:571–575

    Article  Google Scholar 

  12. Devore GR, Falkensammer P, Sklansky MS, Platt LD (2003) Spatio-temporal image correlation (STIC): new technology for evaluation of the fetal heart. Ultrasound Obstet Gynecol 22:380–387

    Article  CAS  Google Scholar 

  13. Uittenbogaard LB, Haak MC, Peters RJ, van Couwelaar GM, Van Vugt JM (2010) Validation of volume measurements for fetal echocardiography using four-dimensional ultrasound imaging and spatiotemporal image correlation. Ultrasound Obstet Gynecol 35:324–331

    Article  CAS  Google Scholar 

  14. Melo Júnior JF, Bravo-Valenzuela NJ, Nardozza LM, Peixoto AB, Mattar R, Martins WP et al (2019) Reference range of fetal myocardial area by three-dimensional ultrasonography and its applicability in fetuses of pre-gestational diabetic women. J Perinat Med 47:422–428

    Article  Google Scholar 

  15. Hadlock FP, Harrist RB, Marinez-Poyer J (1991) In utero analysis of fetal growth: a sonographic weight standard. Radiology 181:129–133

    Article  CAS  Google Scholar 

  16. Gonçalves LF, Lee W, Espinoza J, Romero R (2006) Examination of the fetal heart by four-dimensional (4D) ultrasound with spatio-temporal image correlation (STIC). Ultrasound Obstet Gynecol 27:336–348

    Article  Google Scholar 

  17. Paladini D (2007) Standardization of on-screen fetal heart orientation prior to storage of spatio-temporal image correlation (STIC) volume datasets. Ultrasound Obstet Gynecol 29:605–611

    Article  CAS  Google Scholar 

  18. Cohen J (1988) Statistical power analysis for the behavioral sciences. Routledge Academic, New York

    Google Scholar 

  19. Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1:307–310

    Article  CAS  Google Scholar 

  20. Martins WP, Nastri CO (2014) Interpreting reproducibility results for ultrasound measurements. Ultrasound Obstet Gynecol 43:479–480

    Article  CAS  Google Scholar 

  21. Dervisoglu P, Kosecik M, Kumbasar S (2018) Effects of gestational and pregestational diabetes mellitus on the foetal heart: a cross-sectional study. J Obstet Gynaecol 38:408–412

    Article  Google Scholar 

  22. Garcia-Flores J, Jañez M, Gonzalez MC, Martinez N, Espada M, Gonzalez A (2011) Fetal myocardial morphological and functional changes associated with well-controlled gestational diabetes. Eur J Obstet Gynecol Reprod Biol 154:24–26

    Article  Google Scholar 

  23. Balli S, Pac FA, Ece I, Oflaz MB, Kibar AE, Kandemir Ö (2014) Assessment of cardiac functions in fetuses of gestational diabetic mothers. Pediatr Cardiol 35:30–37

    Article  Google Scholar 

  24. Barros FS, Rolo LC, Rocha LA, Martins WP, Nardozza LM, Moron AF et al (2015) Reference ranges for the volumes of fetal cardiac ventricular walls by three-dimensional ultrasound using spatiotemporal image correlation and virtual organ computer-aided analysis and its validation in fetuses with congenital heart diseases. Prenat Diagn 35:65–73

    Article  Google Scholar 

  25. Zielinsky P, Piccoli AL Jr, Teixeira L, Gus EI, Mânica JL, Satler F et al (2003) Pulmonary vein pulsatility in fetuses of diabetic mothers: Prenatal Doppler echocardiographic study. Arq Bras Cardiol 81:600–603

    Article  Google Scholar 

  26. Rizzo G, Arduini D, Romanini C (1992) Accelerated cardiac growth and abnormal cardiac flow in fetuses of type I diabetic mothers. Obstet Gynecol 80:369–376

    CAS  PubMed  Google Scholar 

  27. Zielinsky P, Piccoli AL Jr (2012) Myocardial hypertrophy and dysfunction in maternal diabetes. Early Hum Dev 88:273–278

    Article  Google Scholar 

  28. Messing B, Cohen SM, Valsky DV, Rosenak D, Hochner-Celnikier D, Savchev S et al (2007) Fetal cardiac ventricle volumetry in the second half of gestation assessed by 4D ultrasound using STIC combined with inversion mode. Ultrasound Obstet Gynecol 30:142–151

    Article  CAS  Google Scholar 

  29. Simioni C, Nardozza LM, Araujo Júnior E, Rolo LC, Terasaka OA, Zamith MM et al (2011) Fetal cardiac function assessed by spatio-temporal image correlation. Arch Gynecol Obstet 284:253–260

    Article  Google Scholar 

  30. Gutgesell HP, Speer ME, Rosenberg HS (1980) Characterization of the cardiomyopathy in infants of diabetic mothers. Circulation 61:441–450

    Article  CAS  Google Scholar 

  31. Elmekkawi SF, Mansour GM, Elsafty MS, Hassanin AS, Laban M, Elsayed HM (2015) Prediction of fetal hypertrophic cardiomyopathy in diabetic pregnancies compared with postnatal outcome. Clin Med Insights Womens Health 8:39–43

    PubMed  PubMed Central  Google Scholar 

  32. Rolo LC, Santana EF, da Silva PH, Costa FS, Nardozza LM, Tonni G et al (2015) Fetal cardiac interventricular septum: volume assessment by 3D/4D ultrasound using spatio-temporal image correlation (STIC) and virtual organ computer-aided analysis (VOCAL). J Matern Fetal Neonatal Med 28:1388–1393

    Article  Google Scholar 

  33. Araujo Júnior E, Novoa Y, Novoa VA, Barros FS, Rocha LA, Peixoto AB, Martins WP et al (2016) Reference values for the volumes of foetal heart atrial wall by three-dimensional ultrasound using STIC and VOCAL methods between 20w0d and 33w6d weeks of gestation. J Matern Fetal Neonatal Med 29:3076–3083

    Article  Google Scholar 

  34. Bravo-Valenzuela NJM, Zielinsky P, Zurita-Peralta J, Nicoloso LH, Piccoli A Jr, Van der Ferreira Sand L et al (2019) Pulmonary vein flow impedance: an early predictor of cardiac dysfunction in intrauterine growth restriction. Fetal Diagn Ther 45:205–211

    Article  Google Scholar 

  35. Naujorks AA, Zielinsky P, Klein C, Nicoloso LH, Piccoli AL Jr, Becker E et al (2014) Myocardial velocities, dynamics of the septum primum, and placental dysfunction in fetuses with growth restriction. Congenit Heart Dis 9:138–143

    Article  Google Scholar 

  36. Molina FS, Faro C, Sotiriadis A, Dagklis T, Nicolaides KH (2008) Heart stroke volume and cardiac output by four-dimensional ultrasound in normal fetuses. Ultrasound Obstet Gynecol 32:181–187

    Article  CAS  Google Scholar 

  37. Schoonderwaldt EM, Groenenberg IA, Hop WC, Wladimiroff JW, Steegers EA (2012) Reproducibility of echocardiographic measurements of human fetal left ventricular volumes and ejection fractions using four-dimensional ultrasound with the spatio-temporal image correlation modality. Eur J Obstet Gynecol Reprod Biol 160:22–29

    Article  Google Scholar 

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Correspondence to Edward Araujo Júnior.

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Bravo-Valenzuela, N.J., Peixoto, A.B., Mattar, R. et al. Fetal Cardiac Function and Ventricular Volumes Determined by Three-Dimensional Ultrasound Using STIC and VOCAL Methods in Fetuses from Pre-gestational Diabetic Women. Pediatr Cardiol 41, 1125–1134 (2020). https://doi.org/10.1007/s00246-020-02362-7

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