Evidence of second‐trimester changes in head biometry and brain perfusion in fetuses with congenital heart disease
Abstract
Objectives: To evaluate the associations between congenital heart disease (CHD) and head biometry and cerebrovascular blood flow dynamics at the time of diagnosis of CHD in the second trimester of pregnancy. Methods: This was a study of 95 consecutive fetuses diagnosed with CHD. At the time of diagnosis, fetal biometry was performed and brain perfusion was assessed by middle cerebral artery pulsatility index (MCA‐PI), cerebroplacental ratio (CPR) and fractional moving blood volume (FMBV). The results were compared with those of 95 normal fetuses matched for gestational age. Results: Median gestational age at diagnosis was 22 + 3 (range, 20 + 0 to 23 + 5) weeks. Fetuses with CHD showed significantly lower MCA‐PI and CPR Z‐scores (−0.23 vs 0.34 and −0.37 vs 0.30, respectively; both P < 0.001) and higher FMBV Z‐scores (2.35 vs 0.15; P < 0.001). FMBV > 95 th percentile was observed in 81.1% of cases as compared with 10.5% in controls (P < 0.001). Moreover, cases showed significantly smaller biparietal diameter (BPD) and head circumference (HC) Z‐scores (−1.61 vs −0.43 and −0.89 vs 0.09, respectively; both P < 0.001), with a higher proportion of BPD and HC measurements below the 5 th percentile compared with controls (51.6% vs 13.7% and 26.3% vs 4.2%, respectively; both P < 0.001). These findings were more pronounced in those cases with types of CHD associated with compromised oxygenated blood delivery to the brain, such as left outflow tract obstruction and transposition of the great arteries. Conclusions: A high proportion of fetuses with CHD have a smaller head and increased brain perfusion already in the second trimester, suggesting an early onset of the mechanisms leading to poorer neurodevelopment later in life. Copyright © 2014 ISUOG. Published by John Wiley & Sons Ltd
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Birth head circumferences and z-scores are decreased in congenital heart disease as a result of affected antenatal cerebral circulation.
“As a result of affected antenatal cerebral circulation, birth head circumferences and z-scores are decreased in CHD.31,32”
From Neuroimaging, cardiovascular physiology, and functional outcomes in infants with congenital heart disease (2017) · cites this paper as [32]
Cites
The incidence of congenital heart disease.
Hoffman, J. I. E., & Kaplan, S. (2002) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(02)01886-7 · Cited by 6,099 · see citing works
Abnormal brain development in newborns with congenital heart disease
Miller, S. P., McQuillen, P. S., Hamrick, S., Xu, D., Glidden, D. V., Charlton, N., Karl, T., Azakie, A., Ferriero, D. M., Barkovich, A. J., et al. (2007) · New England Journal of Medicine · doi:10.1056/nejmoa067393 · Cited by 860 · see citing works
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
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
The cerebroplacental Doppler ratio revisited
Baschat, A., & Gembruch, U. (2003) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.20 · Cited by 505 · 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
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
Impact of congenital heart disease on cerebrovascular blood flow dynamics in the fetus
Kaltman, J. R., Di, H., Tian, Z., & Rychik, J. (2005) · Ultrasound in Obstetrics & Gynecology · doi:10.1002/uog.1785 · Cited by 296 · see citing works
Limperopoulos, C., Majnemer, A., Shevell, M. I., Rosenblatt, B., Rohlicek, C., & Tchervenkov, C. (2000) · The Journal of Pediatrics · doi:10.1067/mpd.2000.109152 · Cited by 274 · see citing works
(2005) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.2677 · Cited by 254 · see citing works
Majnemer, A., Limperopoulos, C., Shevell, M., Rosenblatt, B., Rohlicek, C., & Tchervenkov, C. (2006) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2005.08.036 · Cited by 193 · see citing works
Khalil, A. A., Suff, N., Thilaganathan, B., Hurrell, A., Cooper, D., & Carvalho, J. S. (2013) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.12526 · Cited by 190 · see citing works
Congenital heart disease and brain development
McQuillen, P. S., & Miller, S. P. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.05116.x · Cited by 164 · see citing works
Impact of Congenital Heart Disease on Brain Development and Neurodevelopmental Outcome
Donofrio, M. T., & Massaro, A. N. (2010) · International Journal of Pediatrics · doi:10.1155/2010/359390 · Cited by 144 · see citing works
Fetal ultrasound biometry: 1. Head reference values
Kurmanavičius, J., Wright, E. M., Royston, P. J., Wisser, J., Huch, R., Huch, A., & Zimmermann, R. (1999) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1999.tb08212.x · Cited by 137 · see citing works
Hernandez‐Andrade, E. A., Horacio Figueroa, D., Jansson, T. T., Rangel-Nava, H. A., & Gratacós, E. (2008) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.5377 · Cited by 129 · see citing works
Self-citationAortic morphometry and microcephaly in hypoplastic left heart syndrome
Shillingford, A. J., Ittenbach, R. F., Marino, B. S., Rychik, J., Clancy, R. R., Spray, T. L., Gaynor, J. W., & Wernovsky, G. (2007) · Cardiology in the Young · doi:10.1017/s1047951107000248 · Cited by 129 · see citing works
Preoperative brain injury in newborns with transposition of the great arteries
Miller, S. P., McQuillen, P. S., Vigneron, D. B., Glidden, D. V., Barkovich, A. J., Ferriero, D. M., Hamrick, S. E. G., Azakie, A., & Karl, T. R. (2004) · The Annals of Thoracic Surgery · doi:10.1016/j.athoracsur.2003.10.084 · Cited by 124 · see citing works
Prenatal Head Growth and White Matter Injury in Hypoplastic Left Heart Syndrome
Hinton, R. B., Andelfinger, G., Sekar, P., Hinton, A. C., Gendron, R. L., Michelfelder, E. C., Robitaille, Y., & Benson, D. W. (2008) · Pediatric Research · doi:10.1203/pdr.0b013e3181827bf4 · Cited by 118 · see citing works
Fetal ultrasound biometry: 2. Abdomen and femur length reference values
Kurmanavičius, J., Wright, E. M., Royston, P. J., Zimmermann, R., Huch, R., Huch, A., & Wisser, J. (1999) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1999.tb08213.x · Cited by 109 · see citing works
Berg, C., Gembruch, O., Gembruch, U., & Geipel, A. (2009) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.7474 · Cited by 90 · see citing works
Williams, I. A., Tarullo, A. R., Grieve, P. G., Wilpers, A. B., Vignola, E. F., Myers, M. M., & Fifer, W. P. (2012) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.11144 · Cited by 85 · see citing works
Arduini, M., Rosati, P., Caforio, L., Guariglia, L., Clerici, G., Renzo, G. C. D., & Scambia, G. (2011) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.3109/14767058.2010.547961 · Cited by 63 · see citing works
Szwast, A. L., Tian, Z., McCann, M., Soffer, D., & Rychik, J. R. (2012) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.11147 · Cited by 60 · see citing works
Accuracy of Prenatal Diagnosis of Congenital Heart Disease with Fetal Echocardiography
Bakiler, A. R., Özer, E. A., Kanık, A., Kanit, H., & Aktaş, F. N. (2007) · Fetal Diagnosis and Therapy · doi:10.1159/000100782 · Cited by 49 · see citing works
Hernandez‐Andrade, E. A., Jansson, T. G., Horacio Figueroa, D., Rangel-Nava, H. A., Acosta‐Rojas, R., & Gratacós, E. (2007) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.4005 · Cited by 47 · see citing works
Self-citationFetuses with congenital heart disease demonstrate signs of decreased cerebral impedance
Modena, A. B., Horan, C., Visintine, J. F., Chanthasenanont, A., WOOD, D. C., & Weiner, S. (2006) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2006.05.045 · Cited by 43 · see citing works
Cruz-Martínez, R., Figueras, F., Hernandez‐Andrade, E. A., Benavides-Serralde, A., & Gratacós, E. (2010) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.7722 · Cited by 27 · see citing works
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Masoller, N., Sanz‐Cortés, M., Crispi, F., Gómez, O., Bennasar, M., Egaña‐Ugrinovic, G., Bargalló, N., Martínez, J. M., & Gratacós, E. (2016) · Ultrasound in Obstetrics & Gynecology · doi:10.1002/uog.14919 · Cited by 84 · see citing works
Self-citationClaessens, N. H. P., Kelly, C. J., Counsell, S. J., & Benders, M. J. N. L. (2017) · Developmental Medicine & Child Neurology · doi:10.1111/dmcn.13461 · Cited by 59 · see citing works
Congenital cardiac anomalies and white matter injury
Morton, P. D., Ishibashi, N., Jonas, R. A., & Gallo, V. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.04.001 · Cited by 55 · see citing works
- Authors
- Masoller, N., Martínez, J. M., Gómez, O., Bennasar, M., Crispi, F., Sanz‐Cortés, M., Egaña‐Ugrinovic, G., Bartrons, J., Puerto, B., & Gratacós, E.
- Affiliations
- Hospital Sant Joan de Déu Barcelona (ES)
- BCNatal – Barcelona Center for Maternal–Fetal and Neonatal Medicine (Hospital Clínic and Hospital Sant Joan de Déu), IDIBAPS University of Barcelona, and Centre for Biomedical Research on Rare Diseases (CIBER‐ER) Barcelona Spain
- Corresponding author
- Masoller, N.
- Venue
- Ultrasound in Obstetrics & Gynecology
- Publisher
- Wiley
- Published
- 2014-07-08
- Volume
- 44
- Issue
- 2
- Pages
- 182-187
- ISSN
- 0960-7692 (ISSN-L)
- 1469-0705
- OpenAlex
- W2092565569
- Cited by
- 89
- References
- 28
- Citations by year
- 2026: 1 · 2025: 7 · 2024: 6 · 2023: 6 · 2022: 8 · 2021: 6 · 2020: 5 · 2019: 14 · 2018: 10 · 2017: 12 · 2016: 8 · 2015: 5 · 2014: 1
- FWCI
- 6.54
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Ultrasound in Obstetrics and Gynecology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Fondo Europeo de Desarrollo Regional de la Uni�n Europea Una manera de hacer
- Instituto de Salud Carlos III (PI12/02230)
- Topics
- Health Sciences › Medicine › Epidemiology › Congenital Heart Disease Studies
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Fetal and Pediatric Neurological Disorders
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Screening and Diagnostics
- Keywords
- congenital heart disease, second trimester, middle cerebral artery pulsatility index, cerebroplacental ratio, fractional moving blood volume, biparietal diameter, head circumference, transposition of the great arteries, fetal brain development, fetal growth restriction
- MeSH terms
- Adult, Biometry, Blood Flow Velocity, Brain, Cerebrovascular Circulation, Female, Fetal Diseases, Head, Heart Defects, Congenital, Hemodynamics, Humans, Pregnancy, Pregnancy Trimester, Second, Case-Control Studies, Echocardiography, Doppler, Pulsed, Middle Cerebral Artery
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