Impact of congenital heart disease on cerebrovascular blood flow dynamics in the fetus
Open accessAbstract
Objectives: Neurological abnormalities are present in some children after repair of congenital heart disease (CHD). Recently, structural brain abnormalities have been identified in infants prior to cardiac surgery. By altering in utero blood flow patterns, the type of CHD may impact upon cerebrovascular flow dynamics prior to birth. We sought to determine whether left‐ and right‐sided obstructive congenital heart lesions modify cerebrovascular flow dynamics in the fetus. Methods: Pulsed Doppler was used to measure blood flow velocities in the umbilical (UA) and middle cerebral (MCA) arteries in 172 fetuses from 20 to 39 weeks' gestational age referred for fetal echocardiography. Pulsatility index (PI), an indicator of downstream vascular resistance, was determined by (peak systolic velocity—end‐diastolic velocity)/mean velocity. Results: Fetuses with hypoplastic left heart syndrome (HLHS; n = 28) had decreased MCA‐PI ( P = 0.009) compared to normal fetuses ( n = 114). Fetuses with right‐sided obstructive lesions (RSOL; n = 17) had increased MCA‐PI ( P = 0.001) when compared to fetuses with HLHS. The UA‐PI was elevated in fetuses with RSOLs ( P = 0.045). Conclusions: Cerebrovascular resistance is lower than normal in fetuses with HLHS, a condition in which cerebral perfusion occurs retrograde via the ductus arteriosus. Fetuses with RSOL had significantly higher cerebrovascular resistance compared to fetuses with HLHS. The type of CHD impacts upon fetal cerebrovascular blood flow distribution and this may have implications for later development of neurological sequelae. Copyright © 2004 ISUOG. Published by John Wiley & Sons, Ltd.
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Abnormal cerebral blood flow has been documented in fetuses and newborns with complex anomalies such as hypoplastic left heart syndrome.
“Several studies have documented abnormal cerebral blood flow in fetuses and newborns with complex anomalies such as hypoplastic left heart syndrome (HLHS) [12,20,21].”
From Brain Volume and Metabolism in Fetuses With Congenital Heart Disease: Evaluation With Quantitative Magnetic Resonance Imaging and Spectroscopy (2010) · cites this paper as [21]
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Bellinger, D. C., Jonas, R. A., Rappaport, L., Wypij, D., Wernovsky, G., Kuban, K., Barnes, P. D., Holmes, G. L., Hickey, P. R., Strand, R. D., et al. (1995) · New England Journal of Medicine · doi:10.1056/nejm199503023320901 · Cited by 803 · see citing works
Cardiovascular responses to hypoxemia and acidemia in fetal lambs
Cohn, H. E., Sacks, E. J., Heymann, M. A., & Rudolph, A. M. (1974) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(74)90587-0 · Cited by 800 · see citing works
Newburger, J. W., Jonas, R. A., Wernovsky, G., Wypij, D., Hickey, P. R., Kuban, K., Farrell, D. M., Holmes, G. L., Helmers, S. L., Constantinou, J., et al. (1993) · New England Journal of Medicine · doi:10.1056/nejm199310073291501 · Cited by 702 · see citing works
Bellinger, D. C., Wypij, D., Kuban, K. C. K., Rappaport, L. A., Hickey, P. R., Wernovsky, G., Jonas, R. A., & Newburger, J. W. (1999) · Circulation · doi:10.1161/01.cir.100.5.526 · Cited by 579 · see citing works
An MRI Study of Neurological Injury Before and After Congenital Heart Surgery
Mahle, W. T., Tavani, F., Zimmerman, R. A., Nicolson, S. C., Galli, K. K., Gaynor, J. W., Clancy, R. R., Montenegro, L. M., Spray, T. L., Chiavacci, R. M., et al. (2002) · Circulation · doi:10.1161/01.cir.0000032908.33237.b1 · Cited by 541 · see citing works
Cerebral-Umbilical Doppler Ratio As a Predictor of Adverse Perinatal Outcome
Gramellini, D., FOLLI, M. C., Raboni, S., Vadora, E., & Merialdi, A. (1992) · Obstetrics and Gynecology · doi:10.1097/00006250-199203000-00018 · Cited by 480 · see citing works
Arduini, D., & Rizzo, G. (1990) · Journal of Perinatal Medicine · doi:10.1515/jpme.1990.18.3.165 · Cited by 480 · see citing works
Mahle, W. T., Clancy, R. R., Moss, E., Gerdes, M., Jobes, D. R., & Wernovsky, G. (2000) · PEDIATRICS · doi:10.1542/peds.105.5.1082 · Cited by 463 · see citing works
Doppler ultrasound assessment of cerebral blood flow in the human fetus
Wladimiroff, J. W., Tonge, H. M., & Stewart, P. A. (1986) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1986.tb08656.x · Cited by 444 · see citing works
Donofrio, M. T., Bremer, Y. A., Schieken, R. M., Gennings, C., Morton, L. D., Eidem, B. W., Cetta, F., Falkensammer, C. B., Huhta, J. C., & Kleinman, C. S. (2003) · Pediatric Cardiology · doi:10.1007/s00246-002-0404-0 · Cited by 364 · see citing works
Wladimiroff, J. W., van den Wijngaard, J. A. G. W., Degani, S., Noordam, M. J., van Eyck, J., & Tonge, H. M. (1987) · PubMed · Cited by 348 · see citing works
Middle cerebral artery flow velocity waveforms in fetal hypoxaemia
Vyas, S. K., Nicolaides, K. H., Bower, S. J., & Campbell, S. C. (1990) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1990.tb02573.x · Cited by 314 · see citing works
Cognitive Development After the Fontan Operation
Wernovsky, G., Stiles, K. M., Gauvreau, K., Gentles, T. L., duPlessis, A. J., Bellinger, D. C., Walsh, A. Z., Burnett, J. T., Jonas, R. A., Mayer, J. E., et al. (2000) · Circulation · doi:10.1161/01.cir.102.8.883 · Cited by 272 · see citing works
Congenital Brain Anomalies Associated With the Hypoplastic Left Heart Syndrome
Glauser, T. A., RORKE, L. B., Weinberg, P. M., & Clancy, R. R. (1990) · PEDIATRICS · doi:10.1542/peds.85.6.984 · Cited by 270 · see citing works
Neurologic status of newborns with congenital heart defects before open heart surgery
Limperopoulos, C., Majnemer, A., Shevell, M. I., Rosenblatt, B., Rohlicek, C., & Tchervenkov, C. (1999) · PEDIATRICS · doi:10.1542/peds.103.2.402 · Cited by 249 · see citing works
Goldberg, C. S., Schwartz, E. M., Brunberg, J. A., Mosca, R. S., Bove, E. L., Schork, M. A., Stetz, S. P., Cheatham, J. P., & Kulik, T. J. (2000) · The Journal of Pediatrics · doi:10.1067/mpd.2000.108952 · Cited by 220 · see citing works
Preferential streaming of ductus venosus blood to the brain and heart in fetal lambs
Edelstone, D. I., & Rudolph, A. M. (1979) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1979.237.6.h724 · Cited by 191 · see citing works
Doppler ultrasound assessment of cerebral blood flow in the human fetus
Wladimiroff, J. W., Tonge, H. M., & Stewart, P. A. (1986) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1986.tb07932.x · Cited by 170 · see citing works
Scherjon, S. A., Haas, H. S., Kok, J. H., & Zondervan, H. A. (1993) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(93)90156-d · Cited by 129 · see citing works
Reuss, M. L., & Rudolph, A. M. (1981) · PubMed · Cited by 109 · see citing works
van Houten, J., Rothman, A., & Bejar, R. F. (1996) · American Journal of Perinatology · doi:10.1055/s-2007-994202 · Cited by 89 · see citing works
Iklé, L., Hale, K., Fashaw, L. M., Boucek, M. M., & Rosenberg, A. A. (2003) · The Journal of Pediatrics · doi:10.1067/mpd.2003.mpd0340 · Cited by 79 · see citing works
Kjellmer, I., Karlsson, K., Olsson, T., et al. (1974) · Pediatric Research · doi:10.1203/00006450-197401000-00009 · Cited by 70 · see citing works
Neurologic and developmental morbidity in children with complex congenital heart disease
Wernovsky, G., & Newburger, J. W. (2003) · The Journal of Pediatrics · doi:10.1067/mpd.2003.mpd0354 · Cited by 61 · see citing works
CHAN, F., Pun, T. C., Lam, P., et al. (1996) · Obstetrics and Gynecology · doi:10.1016/0029-7844(96)00062-2 · Cited by 51 · see citing works
Arterial Doppler ultrasound in 115 second‐ and third‐trimester fetuses with congenital heart disease
Meise, C., Germer, U., & Gembruch, U. (2001) · Ultrasound in Obstetrics and Gynecology · doi:10.1046/j.1469-0705.2001.00397.x · Cited by 39 · see citing works
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Marino, B. S., Lipkin, P. H., Newburger, J. W., Peacock, G., Gerdes, M., Gaynor, J. W., Mussatto, K. A., Uzark, K., Goldberg, C. S., Johnson, W. H., et al. (2012) · Circulation · doi:10.1161/cir.0b013e318265ee8a · Cited by 1,608 · see citing works
Donofrio, M. T., Moon-Grady, A. J., Hornberger, L. K., Copel, J. A., Sklansky, M. S., Abuhamad, A., Cuneo, B. F., Huhta, J. C., Jonas, R. A., Krishnan, A., et al. (2014) · Circulation · doi:10.1161/01.cir.0000437597.44550.5d · Cited by 1,275 · see citing works
Self-citationLimperopoulos, C., Tworetzky, W., McElhinney, D. B., Newburger, J. W., Brown, D. W., Robertson, R. L., Guizard, N., McGrath, E., Geva, J., Annese, D., et al. (2010) · Circulation · doi:10.1161/circulationaha.109.865568 · Cited by 663 · see citing works
Brain maturation is delayed in infants with complex congenital heart defects
Licht, D. J., Shera, D. M., Clancy, R. R., Wernovsky, G., Montenegro, L. M., Nicolson, S. C., Zimmerman, R. A., Spray, T. L., Gaynor, J. W., & Vossough, A. (2009) · The Journal of Thoracic and Cardiovascular Surgery · doi:10.1016/j.jtcvs.2008.10.025 · Cited by 629 · see citing works
Shillingford, A. J., Glanzman, M. M., Ittenbach, R. F., Clancy, R. R., Gaynor, J. W., & Wernovsky, G. (2008) · Pediatrics · doi:10.1542/peds.2007-1066 · Cited by 348 · see citing works
Wernovsky, G. (2006) · Cardiology in the Young · doi:10.1017/s1047951105002398 · Cited by 335 · see citing works
Petit, C. J., Rome, J. J., Wernovsky, G., Mason, S. E., Shera, D. M., Nicolson, S. C., Montenegro, L. M., Tabbutt, S., Zimmerman, R. A., & Licht, D. J. (2009) · Circulation · doi:10.1161/circulationaha.107.760819 · Cited by 282 · see citing works
Sood, E., Newburger, J. W., Anixt, J. S., Cassidy, A. R., Jackson, J. L., Jonas, R. A., Lisanti, A. J., Lopez, K. N., Peyvandi, S., Marino, B. S., et al. (2024) · Circulation · doi:10.1161/cir.0000000000001211 · Cited by 266 · see citing works
Brain Volume and Neurobehavior in Newborns with Complex Congenital Heart Defects
Owen, M., Shevell, M., Donofrio, M., Majnemer, A., McCarter, R., Vezina, G., Bouyssi-Kobar, M., Evangelou, I., Freeman, D., Weisenfeld, N., et al. (2014) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2013.11.033 · Cited by 115 · see citing works
Masoller, N., Martínez, J. M., Gómez, O., Bennasar, M., Crispi, F., Sanz‐Cortés, M., Egaña‐Ugrinovic, G., Bartrons, J., Puerto, B., & Gratacós, E. (2014) · Ultrasound in Obstetrics & Gynecology · doi:10.1002/uog.13373 · Cited by 89 · see citing works
Fetal MRI detects early alterations of brain development in tetralogy of fallot
Schellen, C., Ernst, S., Gruber, G. M., Mlczoch, E., Weber, M., Brugger, P. C., Ulm, B., Langs, G., Salzer-Muhar, U., Prayer, D., et al. (2015) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2015.05.046 · Cited by 79 · see citing works
Delayed cortical gray matter development in neonates with severe congenital heart disease
; on behalf of the Research Group Heart and Brain, Claessens, N. H. P., Moeskops, P., Buchmann, A., Latal, B., Knirsch, W., Scheer, I., Išgum, I., de Vries, L. S., Benders, M. J. N. L., et al. (2016) · Pediatric Research · doi:10.1038/pr.2016.145 · Cited by 66 · see citing works
The Paradigm Shift Toward Surgical Intervention for Neonates With Hypoplastic Left Heart Syndrome
Wernovsky, G. (2008) · Archives of Pediatrics & Adolescent Medicine · doi:10.1001/archpedi.162.9.849 · Cited by 71 · see citing works
Goff, D. A., Shera, D. M., Tang, S., Lavin, N. A., Durning, S. M., Nicolson, S. C., Montenegro, L. M., Rome, J. J., Gaynor, J. W., Spray, T. L., et al. (2014) · The Journal of Thoracic and Cardiovascular Surgery · doi:10.1016/j.jtcvs.2013.06.021 · Cited by 65 · see citing works
Ibuki, K., Watanabe, K., Yoshimura, N., Kakimoto, T., Matsui, M., Yoshida, T., Origasa, H., & Ichida, F. (2012) · The Journal of Thoracic and Cardiovascular Surgery · doi:10.1016/j.jtcvs.2011.08.042 · Cited by 46 · see citing works
Multi-Tiered Analysis of Brain Injury in Neonates With Congenital Heart Disease
Mulkey, S. B., Swearingen, C. J., Melguizo, M. S., Schmitz, M. L., Ou, X., Ramakrishnaiah, R. H., Glasier, C. M., Bradley Schaefer, G., & Bhutta, A. T. (2013) · Pediatric Cardiology · doi:10.1007/s00246-013-0712-6 · Cited by 34 · see citing works
- Authors
- Kaltman, J. R., Di, H., Tian, Z., & Rychik, J.
- Affiliations
- Children's Hospital of Philadelphia (US)
- Corresponding author
- Rychik, J.
- Venue
- Ultrasound in Obstetrics & Gynecology
- Publisher
- Wiley
- Published
- 2004-12-08
- Volume
- 25
- Issue
- 1
- Pages
- 32-36
- ISSN
- 0960-7692 (ISSN-L)
- 1469-0705
- OpenAlex
- W2082589628
- Cited by
- 296
- References
- 26
- Citations by year
- 2026: 11 · 2025: 10 · 2024: 12 · 2023: 11 · 2022: 21 · 2021: 16 · 2020: 15 · 2019: 15 · 2018: 15 · 2017: 16 · 2016: 18 · 2015: 10 · 2014: 12 · 2013: 17 · 2012: 15
- FWCI
- 6.23
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Ultrasound in Obstetrics and Gynecology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- U.S. Public Health Service (T32 07915)
- Topics
- Health Sciences › Medicine › Epidemiology › Congenital Heart Disease Studies
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Cardiovascular Conditions and Treatments
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Fetal and Pediatric Neurological Disorders
- Keywords
- congenital heart disease, hypoplastic left heart syndrome, middle cerebral artery pulsatility index, umbilical artery pulsatility index, cerebrovascular resistance, ductus arteriosus, fetal neurological development, fetal echocardiography
- MeSH terms
- Blood Flow Velocity, Cerebrovascular Circulation, Cross-Sectional Studies, Fetal Diseases, Gestational Age, Heart Defects, Congenital, Humans, Pulsatile Flow, Umbilical Arteries, Vascular Resistance, Ultrasonography, Doppler, Pulsed, Middle Cerebral Artery
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