Abstract
The purpose of this review was to study the Russian and foreign literature on the effect of congenital heart disease on the developing fetal brain, assessing the degree of risk of developing neurological pathology in such a child in the future. The results obtained are confirmed both by instrumental methods of studying the brain (in particular, magnetic resonance imaging) and by clinical manifestations and indicate that in a large percentage of cases, newborns with heart disease also have a pathology of the central nervous system, which radically changes parent counseling concept. They also indicate the need for a more detailed study of the fetal brain in the presence of a heart defect.
References
- Marzoeva O.V., Grishaeva O.M., Gasanova R.M., Bartagova M.N., Bespalova E.D. Doppler study of cerebral hemodynamics in fetuses with congenital heart defects. The Bulletin of Bakoulev Center. Cardiovascular Diseases. 2015; 16 (S3): 162 (in Russ.).
- Ruiz A., Cruz-Lemini M., Masoller N., Sanz-Cortes M., Ferrer Q., Ribera I. et al. Longitudinal changes in fetal biometry and cerebroplacental hemodynamics in fetuses with congenital heart disease. Ultrasound. Obstet. Gynecol. 2017; 49: 379–86. DOI: 10.1002/uog.15970
- Hahn E., Szwast A., Cnota J., Levine J.C., Fifer C.G., Jaeggi E. et al. Association between fetal growth, cerebral blood flow and neurodevelopmental outcome in univentricular fetuses. Ultrasound. Obstet. Gynecol. 2016; 47: 460–5. DOI: 10.1002/uog.14881
- Zeng S., Zhou Q.C., Zhou J.W., Li M., Long C., Peng Q.H. Volume of intracranial structures on three-dimensional ultrasound in fetuses with congenital heart disease. Ultrasound. Obstet. Gynecol. 2015; 46: 174–81. DOI: 10.1002/uog.14677
- Masoller N., Martinez J.M., Gomez O., Bennasar M., Crispi F., Sanz-Cortés M. et al. Evidence of second-trimester changes in head biometry and brain perfusion in fetuses with congenital heart disease. Ultrasound. Obstet. Gynecol. 2014; 44: 182–7. DOI: 10.1002/uog.13373
- Yamamoto Y., Khoo N.S., Brooks P.A., Savard W., Hirose A., Hornberger L.K. Severe left heart obstruction with retrograde arch flow influences fetal cerebral and placental blood flow. Ultrasound. Obstet. Gynecol. 2013; 42: 294–9. DOI: 10.1002/uog.12572
- Arduini M., Rosati P., Caforio L., Guariglia L., Clerici G., Di Renzo G.C. et al. Cerebral blood flow autoregulation and congenital heart disease: possible causes of abnormal prenatal neurologic development. J. Matern. Fetal. Neonatal. Med. 2011; 24: 1208–11. DOI: 10.3109/14767058.2010.547961
- Itsukaichi M., Kikuchi A., Yoshihara K., Serikawa T., Takakuwa K., Tanaka K. Changes in fetal circulation associated with congenital heart disease and their effects on fetal growth. Fetal. Diagn. Ther. 2011; 30: 219–4. DOI: 10.1159/000330202
- Wallenstein M.B., Harper L.M., Odibo A.O., Roehl K.A., Longman R.E., Macones G.A. et al. Fetal congenital heart disease and intrauterine growth restriction: a retrospective cohort study. J. Matern. Fetal. Neonatal. Med. 2012; 25: 662–5. DOI: 10.3109/14767058.2011.597900
- Paladini D., Alfirevic Z., Carvalho J.S., Khalil A., Malinger G., Martinez J.M. et al. ISUOG Clinical Standards Committee. ISUOG consensus statement on current understanding of the association of neurodevelopmental delay and congenital heart disease: impact on prenatal counseling. Ultrasound. Obstet. Gynecol. 2017; 49: 287–8. DOI: 10.1002/uog.17324
- Marino B.S., Lipkin P.H., Newburger J.W., Peacock G., Gerdes M., Gaynor J.W. et al. American Heart Association Congenital Heart Defects Committee, Council on Cardiovascular Disease in the Young, Council on Cardiovascular Nursing, and Stroke Council. Neurodevelopmental outcomes in children with congenital heart disease: evaluation and management: a scientific statement from the American Heart Association. Children’s Heart and Vascular Diseases. 2022; 19 (1) DOI: 10.24022/1810-0686-2022-19-1-34-41
- Sun L., Macgowan C.K., Sled J.G., Yoo S.J., Manlhiot C., Porayette P. et al. Reduced fetal cerebral oxygen consumption is associated with smaller brain size in fetuses with congenital heart disease. Circulation. 2015; 131: 1313–23. DOI: 10.1161/CIRCULATIONAHA.114.013051
- Massaro A.N., Glass P., Brown J., Chang T., Krishnan A., Jonas R.A. et al. Neurobehavioral abnormalities in newborns with congenital heart disease requiring open-heart surgery. J. Pediatr. 2011; 158 (4): 678–81.e2. DOI: 10.1016/j.jpeds.2010.11.060
- Mebius M.J., Clur S.A.B., Vink A.S., Pajkrt E., Kalteren W.S., Kooi E.M.W. et al. Growth patterns and cerebroplacental hemodynamics in fetuses with congenital heart disease. Ultrasound. Obstet. Gynecol. 2019; 53 (6): 769–78. DOI: 10.1002/uog.19102
- Karamlou T., Najm H.K. Evolution of care pathways for babies with hypoplastic left heart syndrome: integrating mechanistic and clinical process investigation, standardization, and collaborative study. J. Thorac. Dis. 2020; 12 (3): 1174–83. DOI: 10.21037/jtd.2019.10.75
- Barkhuizen M., Abella R., Vles J.S.H., Zimmermann L.J.I., Gazzolo D., Gavilanes A.W.D. Antenatal and Perioperative Mechanisms of Global Neurological Injury in Congenital Heart Disease. Pediatr. Cardiol. 2021; 42 (1): 1–18. DOI: 10.1007/s00246-020-02440-w
- Khalil A., Bennet S., Thilaganathan B., Paladini D., Griffiths P., Carvalho J.S. Prevalence of prenatal brain abnormalities in fetuses with congenital heart disease: a systematic review. Ultrasound. Obstet. Gynecol. 2016; 48 (3): 296–307. DOI: 10.1002/uog.15932
- Peyvandi S., Latal B., Miller S.P., McQuillen P.S. The neonatal brain in critical congenital heart disease: Insights and future directions. Neuroimage. 2019; 185: 776–82. DOI: 10.1016/j.neuroimage.2018.05.045
- Liamlahi R., Latal B. Neurodevelopmental outcome of children with congenital heart disease. Handb. Clin. Neurol. 2019; 162: 329–45. DOI: 10.1016/B978-0-444-64029-1.00016-3
- DeVore G.R. Computing the Z-score and centiles for crosssectional analysis: a practical approach. J. Ultrasound. Med. 2017; 36 (3): 459–73. DOI: 10.7863/ultra.16.03025
- van Nisselrooij A.E.L., Jansen F.A.R., van Geloven N., Linskens I.H., Pajkrt E., Clur S.A. et al. Impact of extracardiac pathology on head growth in fetuses with congenital heart defect. Ultrasound. Obstet. Gynecol. 2020; 55 (2): 217–25. DOI: 10.1002/uog.20260
- Limperopoulos C., Tworetzky W., McElhinney D.B., Newburger J.W., Brown D.W., Robertson R.L. Jr. et al. Brain volume and metabolism in fetuses with congenital heart disease: evaluation with quantitative magnetic resonance imaging and spectroscopy. Circulation. 2010; 121 (1): 26–33. DOI: 10.1161/CIRCULATIONAHA.109.865568
- Chock V.Y., Reddy V.M., Bernstein D., Madan A. Neurologic events in neonates treated surgically for congenital heart disease. J. Perinatol. 2006; 26 (4): 237–42. DOI: 10.1038/sj.jp.7211459
- Glauser T., Ben-Menachem E., Bourgeois B., Cnaan A., Guerreiro C., Kälviäinen R. et al. Updated ILAE evidence review of antiepileptic drug efficacy and effectiveness as initial monotherapy for epileptic seizures and syndromes. Epilepsia. 2013; 54 (3): 551–63. DOI: 10.1111/epi.12074
- Donofrio M.T., Massaro A.N. Impact of congenital heart disease on brain development and neurodevelopmental outcome. Int. J. Pediatr. 2010; 19 (4): 2010. pii: 359390. DOI: 10.1155/2010/359390
- Griffiths P.D., Mousa H.A., Finney C., Mooney C., Mandefield L., Timothy J. et al. An integrated in utero MR method for assessing structural brain abnormalities and measuring intracranial volumes in fetuses with congenital heart disease: results of a prospective case-control feasibility study. Neuroradiology. 2019; 61 (5): 603–11. DOI: 10.1007/s00234-019-02184-2
- Rudolph A.M. Impaired cerebral development in fetuses with congenital cardiovascular malformations; Is it the result of inadequate glucose supply? Pediatr. Res. 2016; 80: 172–7. DOI: 10.1038/pr.2016.65
- Vollgraff Heidweiller-Schreurs C.A., De Boer M.A., Heymans M.W., Schoonmade L.J., Bossuyt P.M.M., Mol B.W.J. et al. Prognostic accuracy of cerebroplacental ratio and middle cerebral artery Doppler for adverse perinatal outcome: systematic review and meta-analysis. Ultrasound. Obstet. Gynecol. 2018; 51 (3): 313–22. DOI: 10.1002/uog.18809
- Husen S.C., Koning I.V., Go A.T.J.I., van Graafeiland A.W., Willemsen S.P., Groenenberg I.A.L. et al. Three-dimensional ultrasound imaging of fetal brain fissures in the growth restricted fetus. PLoS One. 2019; 14 (5): e0217538. DOI: 10.1371/journal.pone.0217538. eCollection 2019.
- Szwast A., Putt M., Gaynor J.W., Licht D.J., Rychik J. Cerebrovascular response to maternal hyperoxygenation in fetuses with hypoplastic left heart syndrome depends on gestational age and baseline cerebrovascular resistance. Ultrasound. Obstet. Gynecol. 2018; 52 (4): 473–8. DOI: 10.1002/uog.18919
- Tanis J.C., Boelen M.R., Schmitz D.M., Casarella L., van der Laan M.E., Bos A.F. et al. Correlation between Doppler flow patterns in growth-restricted fetuses and neonatal circulation. Ultrasound. Obstet. Gynecol. 2016; 48 (2): 210–6. DOI: 10.1002/uog.15744
- Tanis J.C., Schmitz D.M., Boelen M.R., Casarella L., van den Berg P.P., Bilardo C.M. et al. Relationship between general movements in neonates who were growth restricted in utero and prenatal Doppler flow patterns. Ultrasound. Obstet. Gynecol. 2016; 48 (6): 772–8. DOI: 10.1002/uog.15903
- Masoller N., Sanz-Cortés M., Crispi F., Gómez O., Bennasar M., Egaña-Ugrinovic G. et al. Mid-gestation brain Doppler and head biometry in fetuses with congenital heart disease predict abnormal brain development at birth. Ultrasound. Obstet. Gynecol. 2016; 47 (1): 65–73. DOI: 10.1002/uog.14919
- Ribera I., Ruiz A., Sánchez O., Eixarch E., Antolín E., GómezMontes E. et al. Multicenter prospective clinical study to evaluate children short-term neurodevelopmental outcome in congenital heart disease (children NEURO-HEART): study protocol. BMC Pediatr. 2019; 19 (1): 326. DOI: 10.1186/s12887-019-1689-y
- Mulkey S.B., Govindan R., Metzler M., Swisher C.B., Hitchings L., Wang Y. et al. Heart rate variability is depressed in the early transitional period for newborns with complex congenital heart disease. Clin. Auton. Res. 2020; 30 (2): 165–72. DOI: 10.1007/s10286-019-00616-w
- Zeng S., Zhou J., Peng Q., Tian L., Xu G., Zhao Y., et al. Doppler ultrasound of cerebral blood flow perfusion in fetuses with congenital heart disease. Ultrasound. Obstet. Gynecol. 2015; 45 (6): 649–56. DOI: 10.1002/uog.14798
- Dominguez T.E., Wernovsky G., Gaynor J.W. Cause and prevention of central nervous system injury in neonates undergoing cardiac surgery. Semin. Thorac. Cardiovasc. Surg. 2007; 19 (3): 269–77. DOI: 10.1053/j.semtcvs.2007.07.005
- Jansen F.A.R., van Zwet E.W., Everwijn S.M.P., Teunissen A.K.K., Rozendaal L., van Lith J.M.M. et al. Fetuses with isolated congenital heart defects show normal cerebral and extracerebral fluid volume growth: a 3D-sonographic study in the second and third trimester. Fetal. Diagn. Ther. 2019; 45 (4): 212–20. DOI: 10.1159/000488674
- Bonthrone A.F., Kelly C.J., Ng I.H.X., Counsell S.J. MRI studies of brain size and growth in individuals with congenital heart disease. Transl. Pediatr. 2021; 10 (8): 2171–81. DOI: 10.21037/tp-20-282
- Ren J.Y., Zhu M., Dong S.Z. Three-dimensional volumetric magnetic resonance imaging detects early alterations of the brain growth in fetuses with congenital heart disease. J. Magn. Reson. Imaging. 2021; 54 (1): 263–72. DOI: 10.1002/jmri.27526
- Claessens N.H.P., Khalili N., Isgum I., Ter Heide H., Steenhuis T.J., Turk E. et al. Brain and CSF volumes in fetuses and neonates with antenatal diagnosis of critical congenital heart disease: a longitudinal MRI study. Am. J. Neuroradiol. 2019; 40 (5): 885–91. DOI: 10.3174/ajnr.A6021
- Jarvis D.A., Finney C.R., Griffiths P.D. Normative volume measurements of the fetal intra-cranial compartments using 3D volume in utero MR imaging. Eur. Radiol. 2019; 29 (7): 3488–95. DOI: 10.1007/s00330-018-5938-5
- Rampun A., Jarvis D., Griffiths P.D., Zwiggelaar R., Scotney B.W., Armitage P.A. Single-input multi-output U-net for automated 2D foetal brain segmentation of MR images. J. Imaging. 2021; 7 (10): 200. DOI: 10.3390/jimaging7100200
- Xia F., Guo Y., He H., Chen P., Shao J., Xia W. Reference biometry of foetal brain by prenatal MRI and the distribution of measurements in foetuses with ventricular septal defect. Ann. Med. 2021; 53 (1): 1428–37. DOI: 10.1080/07853890.2021.1969590
- Lee F.T., Seed M., Sun L., Marini D. Fetal brain issues in congenital heart disease. Transl. Pediatr. 2021; 10 (8): 2182–96. DOI: 10.21037/tp-20-224
- Meuwly E., Feldmann M., Knirsch W., von Rhein M., Payette K., Hitendu D. et al. Research Group Heart and Brain. Postoperative brain volumes are associated with one-year neurodevelopmental outcome in children with severe congenital heart disease. Sci. Rep. 2019; 9 (1): 10885. DOI: 10.1038/s41598-019-47328-9
- Desnous B., Lenoir M., Doussau A., Marandyuk B., BeaulieuGenest L., Poirier N. et al. CINC multidisciplinary team. Epilepsy and seizures in children with congenital heart disease: A prospective study. Seizure. 2019; 64: 50–3. DOI: 10.1016/j.seizure.2018.11.011
- Andropoulos D.B., Easley R.B., Gottlieb E.A., Brady K. Neurologic injury in neonates undergoing cardiac surgery. Clin. Perinatol. 2019; 46 (4): 657–71. DOI: 10.1016/j.clp.2019.08.003
About the authors
- Ol’ga V. Marzoeva, Cand. Med. Sci., Ultrasound Doctor; ORCID
- Elena V. Sypchenko, Cand. Med. Sci., Ultrasound Doctor; ORCID
- Elena I. Leonova, Ultrasound Doctor; ORCID
- Rena M. Gasanova, Dr. Med. Sci., Research Associate, Cardiologist; ORCID
- Tamara A. Yarygina, Cand. Med. Sci., Ultrasound Doctor; ORCID