Fetal cardiovascular remodeling persists at 6 months in infants with intrauterine growth restriction: Fetal cardiovascular remodeling persists in IUGR infants
Open accessAbstract
OBJECTIVES: Intrauterine growth restriction is associated with increased cardiovascular risk later in life but the link between fetal disease and postnatal risk is not well-documented. We evaluated longitudinally the association between cardiovascular remodeling in small-for-gestational-age (SGA) fetuses and at 6 months of age. METHODS: A cohort of 80 SGA fetuses (defined by estimated fetal and birth weights < 10(th) centile) delivered > 34 weeks' gestation was compared with 80 normally grown age-matched control fetuses, with follow-up at 6 months of corrected age (i.e. 6 months from estimated date of delivery according to first-trimester crown-rump length). Cardiovascular evaluation included a comprehensive echocardiographic assessment in both fetuses and infants and blood pressure and aortic intima-media thickness (aIMT) measurement in infants. Parameters were adjusted by linear regression analysis for gender, gestational age at delivery, pre-eclampsia, prenatal glucocorticoid exposure, Cesarean delivery, admission to neonatal intensive care unit and body surface area. RESULTS: Both pre- and postnatally, when compared with controls, the SGA group showed a more globular cardiac shape (left sphericity index: controls 2.06 vs SGA 1.87 (P = 0.022) prenatally and 1.92 vs 1.67 (P = 0.007) postnatally), as well as signs of systolic longitudinal dysfunction (systolic annular peak velocity (S'): 7.2 vs 6.3 cm/s (P = 0.003) prenatally and 7.9 vs 6.4 cm/s (P < 0.001) postnatally; tricuspid annular plane systolic excursion: 7.2 vs 6.8 mm (P = 0.015) prenatally and 16.0 vs 14.2 mm (P < 0.001) postnatally) and diastolic dysfunction (left isovolumetric relaxation time: 46 vs 52 ms (P < 0.001) prenatally and 50 vs 57 ms (P = 0.034) postnatally). In addition, infants in the SGA group had increased mean blood pressure (mean: 61 vs 70 mmHg, P < 0.001) and maximum aIMT (0.57 vs 0.66 mm; P < 0.001). CONCLUSIONS: Primary cardiovascular changes are already present in the SGA fetus and persist at 6 months of age. These data support prenatal cardiovascular remodeling as a mechanistic pathway of increased risk later in life in cases of SGA, regardless of Doppler abnormalities. Copyright © 2015 ISUOG. Published by John Wiley & Sons Ltd.
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Fetal growth restriction can contribute to cardiac remodeling, leading to cardiovascular dysfunction that can persist into childhood and adolescence.
“It also can contribute to cardiac remodeling, leading to cardiovascular dysfunction that can persist into childhood and adolescence.13,14”
From Society for Maternal-Fetal Medicine Consult Series #52: Diagnosis and management of fetal growth restriction (2020) · cites this paper as [13]
The Introduction and Discussion report that intrauterine growth restriction is associated with fetal cardiovascular remodeling and dysfunction, and the study found that the pattern persisted at six months. The Introduction also discusses cardiovascular changes in children and young adults, but the Strengths and limitations section says persistence of this study’s findings in the long term remains to be established. It therefore does not establish that the cardiac dysfunction persists into adolescence. (LLM, conf=0.86)
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BackgroundUtility of the modified myocardial performance index in growth‐restricted fetuses
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Langmia, I. M., Kräker, K., Weiss, S., Haase, N., Schütte, T., Herse, F., & Dechend, R. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00215 · Cited by 23 · see citing works
Bar, J., Weiner, E., Levy, M., & Gilboa, Y. (2021) · American Journal of Obstetrics & Gynecology MFM · doi:10.1016/j.ajogmf.2021.100473 · Cited by 23 · see citing works
DeVore, G. R., Portella, P. P., Hernandez‐Andrade, E. A., Yeo, L., & Romero, R. J. (2020) · Journal of Ultrasound in Medicine · doi:10.1002/jum.15532 · Cited by 20 · see citing works
“Except for a study by Channing et al,(44) all previous fetal studies computed the sphericity index by dividing the end-diastolic basal-apical length by the basal (segment 1) transverse width.(5,7,43,45) In utero changes in the sphericity index may be a precursor for postnatal changes in cardiac function.”
ResultÄnghagen, O., Engvall, J. E., Gottvall, T., Nelson, N., Nylander, E., & Bang, P. (2022) · Pediatric Cardiology · doi:10.1007/s00246-022-02850-y · Cited by 20 · see citing works
Vyas‐Read, S., Kanaan, U. B., Shankar, P. R. V., Stremming, J., Travers, C. D., Carlton, D. P., & Fitzpatrick, A. M. (2017) · BMC Pediatrics · doi:10.1186/s12887-017-0910-0 · Cited by 20 · see citing works
Briffa, C., Fabrizio, C. D., Kalafat, E., Giorgione, V., Bhate, R., Huddy, C., Richards, J., Shetty, S., & Khalil, A. A. (2021) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.23764 · Cited by 20 · see citing works
Guitart‐Mampel, M., González-Tendero, A., Niñerola, S., Morén, C., Catalán‐García, M., González‐Casacuberta, I., Juárez‐Flores, D. L., Ugarteburu, O., Matalonga, L., Cascajo, M. V., et al. (2018) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2018.02.006 · Cited by 18 · see citing works
Self-citationThoracic Aortic Intima-Media Thickness in Preschool Children Born Small for Gestational Age
Fontán, M. M., Erroz, I. O., Orias, D. R., Lozón, A. M., Rodríguez‐Núñez, A., & Lurbe, E. (2019) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2018.12.037 · Cited by 17 · see citing works
Song, Y., Yin, H., Wang, W., Zou, Y., Liu, D., Zhang, G., & Ji, X. (2021) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2021.07.004 · Cited by 17 · see citing works
Pépin, A.-S., Jazwiec, P. A., Dumeaux, V., Sloboda, D., & Kimmins, S. (2024) · eLife · doi:10.7554/elife.83288 · Cited by 10 · see citing works
“…coronary heart disease, and stroke, supporting a placental role in long-term health of offspring ( Brodszki et al., 2005 ; Crispi et al., 2010 ; Cruz-Lemini et al., 2016 ; Eriksson et al., 2016 ; Menendez-Castro et al., 2018 ; Mier-zynski et al., 2016 ; Morsing et al., 2014 ; Sarvari et al.,…”
Evaluation of 24-segment sphericity index of fetal heart using FetalHQ
Hata, T., Koyanagi, A., Yamanishi, T., Bouno, S., Takayoshi, R., AboEllail, M. A. M., & Miyake, T. M. (2020) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767058.2020.1856808 · Cited by 16 · see citing works
“Comparisons of mean SI values in each segment among our patients at 18–21 and 28–31weeks of gestation and those of DeVore’s study [1] in the left and”
BackgroundPost‐COVID‐19 fetal cardiac evaluation in moderate infection group of pregnant women
Ayhan, Ş. G., Turgut, E., Tokalıoğlu, E. Ö., Oluklu, D., Sakcak, B., Hendem, D. U., Tanaçan, A., Tekın, Ö. M., & Şahın, D. (2022) · Journal of Clinical Ultrasound · doi:10.1002/jcu.23220 · Cited by 16 · see citing works
“Fetal heart is one of the main organs in adaptation to hypoxia and placental insufficiency.(24) Oxygen deprivation displays circulatory changes to preserve vital organs (heart, brain, and kidney) and as a”
BackgroundSebastiani, G., García-Beltrán, C., Pie, S., Guerra, A., López‐Bermejo, A., Sánchez-de-Toledo, J., de Zegher, F., Rosés‐Noguer, F., & Ibáñez, L. (2018) · Pediatric Obesity · doi:10.1111/ijpo.12476 · Cited by 15 · see citing works
Sehgal, A., Allison, B. J., Crispi, F., & Menahem, S. (2023) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00134.2023 · Cited by 14 · see citing works
Self-citationOlander, R. F. W., Sundholm, J. K. M., Ojala, T. H., Andersson, S., & Sarkola, T. (2020) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.21972 · Cited by 14 · see citing works
Coats, L. E., Bakrania, B. A., Bamrick, D. R., Ariatti, A. M., Rawls, A. Z., Ojeda, N. B., & Alexander, B. T. (2021) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00033.2021 · Cited by 14 · see citing works
Transgenerational transmission of small‐for‐gestational age
Sepúlveda-Martínez, Á., Rodríguez‐López, M., y Miño, F. P., Casu, G., Crovetto, F., Gratacós, E., & Crispi, F. (2018) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.20119 · Cited by 13 · see citing works
Self-citationCoutinho, C. M., Giorgione, V., Thilaganathan, B., & Patey, O. V. (2024) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/1471-0528.17956 · Cited by 12 · see citing works
“The mechanisms for this developmental programming remain to be established, but fetal and neonatal abnormal cardiac remodelling and myocardial dysfunction demonstrated in this population, might play an important role [4–6].”
Ortigosa, N., Rodríguez‐López, M., Bailón, R., Sarvari, S. I., Sitges, M., Gratacós, E., Bijnens, B. H., Crispi, F., & Laguna, P. (2016) · Journal of Electrocardiology · doi:10.1016/j.jelectrocard.2016.03.011 · Cited by 12 · see citing works
Self-citationLongitudinal Behavior of Left-Ventricular Strain in Fetal Growth Restriction
Domínguez-Gallardo, C., Ginjaume-García, N., Ullmo, J., Fernández-Oliva, A., Parra, J., Vázquez, A., Cruz-Lemini, M., & Llurba, E. (2023) · Diagnostics · doi:10.3390/diagnostics13071252 · Cited by 11 · see citing works
Self-citationClarke, G. D., Li, J., Kuo, A. H., Moody, A. J., & Nathanielsz, P. W. (2020) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174420001233 · Cited by 11 · see citing works
Gonçalves, R., Wiertsema, C. J., Silva, C. C. V., Monasso, G. S., Gaillard, R., Steegers, E. A. P., Santos, S., & Jaddoe, V. W. V. (2022) · JAMA Network Open · doi:10.1001/jamanetworkopen.2022.19225 · Cited by 11 · see citing works
Varley, B. J., Nasir, R., Skilton, M. R., Craig, M. E., & Gow, M. L. (2022) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2022.08.033 · Cited by 11 · see citing works
Comparison of 2D versus M-mode echocardiography for assessing fetal myocardial wall thickness
Sepúlveda-Martínez, Á., García‐Otero, L., Soveral, I., Guirado, L., Valenzuela‐Alcaráz, B., Torres, X., Rodríguez‐López, M., Gratacós, E., Gómez, O., & Crispi, F. (2018) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767058.2018.1432041 · Cited by 10 · see citing works
“Several antenatal insults, such as hypoxia, lack of nutrients, infection or inflammation could affect the developing heart that adapts by changing its shape and function [17,38].”
BackgroundSelf-citationNormal fetal cardiac deformation values in pregnancy; a prospective cohort study protocol
van Oostrum, N. H. M., Oei, S. G., & van Laar, J. O. E. H. (2019) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-019-2662-3 · Cited by 10 · see citing works
Evaluation of the sphericity index of the fetal heart during middle and late pregnancy using fetalHQ
Luo, Y., Xiao, F., Long, C., Kuang, H., Jiang, M., Zhou, C., Cui, Q., Ye, Y., Zhang, S., & Zhang, M. (2021) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767058.2021.1940934 · Cited by 10 · see citing works
“There are few studies on the role of ventricular SI in fetal cardiac function, and the traditional methods for measuring the ventricular transverse diameter mainly focus on the basal or middle segment of the ventricle [4,5].”
Methodvan de Meent, M., Nijholt, K. T., Joemmanbaks, S. C. A., Kooiman, J., Schipper, H. S., Wever, K. E., Lely, A. T., & Terstappen, F. (2024) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00052.2024 · Cited by 10 · see citing works
Suciu, L. M., Giesinger, R. E., Mărginean, C., Muntean, M., Cucerea, M., Făgărășan, A., & McNamara, P. J. (2023) · Frontiers in Pediatrics · doi:10.3389/fped.2022.1045242 · Cited by 9 · see citing works
“Other authors have demonstrated higher systolic and diastolic BP in newborns (48, 38), infants (49), and adults (50)”
BackgroundFetal Cardiac Remodeling in Response to Anemia: Using Hemoglobin Bart’s Disease as a Study Model
Tongsong, T., Tongprasert, F., Srisupundit, K., Luewan, S., Traisrisilp, K., & Jatavan, P. (2018) · Ultraschall in der Medizin - European Journal of Ultrasound · doi:10.1055/s-0044-101253 · Cited by 9 · see citing works
The Assessment of Maternal and Fetal Intima-Media Thickness in Perinatology
Boroń, D., Kornacki, J., & Wender-Ożegowska, E. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11051168 · Cited by 8 · see citing works
“According to the research, vascular remodeling beginning in utero accounts for the risk factors for cardiovascular diseases and type 2 diabetes in adulthood, whereas cardiovascular changes observed in fetuses persist and are still present at six months of age [35,36].”
BackgroundDai, Y., Zhao, D., Chen, C. K., & Yap, C. H. (2021) · Pediatric Research · doi:10.1038/s41390-020-01356-8 · Cited by 8 · see citing works
Assessment of myocardial performance index in late-onset fetal growth restriction.
Nguyen, T. T. N., Kotani, T., Imai, K., Ushida, T., Moriyama, Y., Kobayashi, T., Niimi, K., Sumigama, S., Yamamoto, E., Vo, V. D., et al. (2021) · PubMed Central · doi:10.18999/nagjms.83.2.259 · Cited by 8 · see citing works
3D Fractional Limb Volume Identifies Reduced Subcutaneous and Lean Mass in Fetal Growth Restriction
Steller, J. G., Gumina, D. L., Driver, C., Palmer, C. E., Brown, L. D., Reeves, S. A., Hobbins, J. C., & Galan, H. L. (2021) · Journal of Ultrasound in Medicine · doi:10.1002/jum.15841 · Cited by 7 · see citing works
Ullmo, J., Cruz-Lemini, M., Sánchez‐Garcia, O., Real, L. B., Fernández‐Llama, P., Calero, F., Domínguez-Gallardo, C., Garrido‐Giménez, C., Trilla, C., Carreras, F., et al. (2021) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-021-04263-w · Cited by 7 · see citing works
“Recently, various studies have demonstrated the occurrence of a fetal cardiac programming in the growth-restricted fetus, which persists into childhood [19].”
BackgroundSelf-citationBertagnolli, M., Dartora, D. R., Lamata, P., Zacur, E., Mai-Vo, T.-A., He, Y., Beauchamp, L., Lewandowski, A. J., Cloutier, A., Sutherland, M. R., et al. (2022) · Hypertension · doi:10.1161/hypertensionaha.122.19115 · Cited by 7 · see citing works
Fetal Growth Restriction Impairs Lung Function and Neurodevelopment in an Early Preterm Rabbit Model
Valenzuela, I. J., Zapletalova, K., Greyling, M., Regin, Y., Gie, A. G., Basurto, D., Deprest, J. A., & van der Merwe, J. (2023) · Biomedicines · doi:10.3390/biomedicines11010139 · Cited by 7 · see citing works
Advances in fetal echocardiography
Gurson, S. C. (2018) · Current Opinion in Cardiology · doi:10.1097/hco.0000000000000584 · Cited by 6 · see citing works
Perlman, S., Messing, B., Salem, Y., Porat, S., Achiron, R., & Gilboa, Y. (2017) · Prenatal Diagnosis · doi:10.1002/pd.5087 · Cited by 6 · see citing works
Evaluation of cardiac sphericity index among intrauterine growth restriction and normal fetuses
Borna, S., Khanjani, S., Hantoushzade, S., Khazardoost, S., Mirzaeian, S., Ariana, S., & Hashemnezhad, M. (2021) · Journal of Obstetrics and Gynaecology · doi:10.1080/01443615.2021.1945005 · Cited by 6 · see citing works
“…in FGR foetuses, but recent studies have shown abnormal cardiac sphericity in FGR (Crispi et al. 2008; Cinar et al. 2015; P erezCruz et al. 2015; Cruz-Lemini et al. 2016; M€akikallio et al. 2016; Sehgal et al. 2016) and in other conditions including ART and maternal diabetes (Valenzuela-Alcaraz…”
BackgroundResultAzman, Z., Sehgal, A., Miller, S., Bubb, K. J., Polglase, G. R., & Allison, B. J. (2025) · The Journal of Physiology · doi:10.1113/jp289441 · Cited by 5 · see citing works
Bueno‐Palomeque, F. L., Mountris, K. A., Ortigosa, N., Bailón, R., Bijnens, B. H., Crispi, F., Pueyo, E., Mincholé, A., & Laguna, P. (2023) · IEEE Journal of Biomedical and Health Informatics · doi:10.1109/jbhi.2023.3297550 · Cited by 5 · see citing works
Self-citationDeVore, G. R., Cuneo, B. F., Satou, G. M., & Sklansky, M. (2018) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.20110 · Cited by 5 · see citing works
“The only requirements to use this approach are the following: (1) the data from which the mean and SD values are derived should be normally distributed; (2) the results should be symmetrical around the mean; and (3) the data should have a common variance.”
BackgroundBardin, R., Perlman, S., Hadar, E., Glassberg, Y. M., Bruckheimer, E., Silber, M., & Gilboa, Y. (2021) · Journal of Ultrasound in Medicine · doi:10.1002/jum.15629 · Cited by 5 · see citing works
“On further study, cardiovascular remodeling, noted prenatally in SGA neonates, persisted up to 6 months postnatally.(9) In order to better evaluate the shape of the ventricles, Devore et al described recently, a new technique to evaluate fetal cardiac diastolic shape by using an offline speckle tracking software that…”
MethodPostnatal persistence of cardiac remodelling and dysfunction in late fetal growth restriction
Crispi, F., Crovetto, F., Rodríguez‐López, M., Sepúlveda-Martínez, Á., Miranda, J., & Gratacós, E. (2021) · Minerva Obstetrics and Gynecology · doi:10.23736/s2724-606x.21.04823-5 · Cited by 5 · see citing works
Self-citationEffects of nifedipine on fetal cardiac function in preterm labor
Yılmaz, O., & Göncü, A. Ş. (2020) · Journal of Perinatal Medicine · doi:10.1515/jpm-2020-0160 · Cited by 5 · see citing works
Cardiac morphology in neonates with fetal growth restriction
Bjarkø, L., Fugelseth, D., Harsem, N. K., Kiserud, T., Haugen, G. N., & Nestaas, E. (2022) · Journal of Perinatology · doi:10.1038/s41372-022-01538-8 · Cited by 5 · see citing works
“Some studies report thinner ventricle septum in FGR [32, 33], whereas others report opposite findings [13, 31].”
BackgroundResultInfluentialIsa, N. I. M., Syafruddin, S. E., Mokhtar, M. H., Abidin, S. Z., Jaffar, F. H. F., Ugusman, A., & Hamid, A. A. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242316842 · Cited by 4 · see citing works
Lou, Y. L. G., Zhao, B., Pan, M., Huang, L., Lu, X., Zhang, X., & Peng, X. (2024) · Pediatric Cardiology · doi:10.1007/s00246-024-03454-4 · Cited by 4 · see citing works
“Cruz-Lemini et al. concluded that enlargement of the SI in the right ventricle of a normal fetus starts at segment 4, and the right ventricle gradually develops a rounded shape from the apex to the base [25].”
Nestaas, E., Bjarkø, L., Kiserud, T., Haugen, G. N., & Fugelseth, D. (2023) · Early Human Development · doi:10.1016/j.earlhumdev.2023.105809 · Cited by 4 · see citing works
Postnatal blood pressure in the preterm small for gestational age neonate
Dizon, S., & Hoffman, S. B. (2018) · Journal of Neonatal-Perinatal Medicine · doi:10.3233/npm-17141 · Cited by 4 · see citing works
Patey, O. V., Botting, K. J., Niu, Y., Zhang, L., Ma, J., Ford, S. G., Tong, W., Coutinho, C. M., Thilaganathan, B., & Giussani, D. A. (2025) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.29306 · Cited by 3 · see citing works
Hemodynamic evaluation of extremely low birth weight infants during the first 7 days of life
Tan, S., Nakanishi, H., Ishida, S., Kosaka, Y., Sekiya, R., Kawada, K., & Ooka, M. (2023) · Early Human Development · doi:10.1016/j.earlhumdev.2023.105900 · Cited by 3 · see citing works
Zhu, F., Zhao, Y., Wu, J., Wang, M., Zhu, Z., & Zhang, L. (2024) · Journal of Ultrasound in Medicine · doi:10.1002/jum.16444 · Cited by 3 · see citing works
Fetal cardiovascular function in a late-onset SGA and FGR cohort: CURIOSA study
Lobmaier, S. M., Graupner, O., Franke, C., Böss, N., Haller, B., Oberhoffer, R., Wacker‐Gussmann, A., & Ortiz, J. U. (2024) · Ultraschall in der Medizin - European Journal of Ultrasound · doi:10.1055/a-2390-2010 · Cited by 3 · see citing works
“These results are in agreement with previously published studies [21, 23, 24, 25].”
Bueno‐Palomeque, F. L., Mountris, K. A., Mincholé, A., Ortigosa, N., Bailón, R., Pueyo, E., & Laguna, P. (2020) · Computing in cardiology · doi:10.22489/cinc.2020.438 · Cited by 3 · see citing works
Fetal heart, brain and placenta: introducing a three‐way (patho)physiological pairing
Habib, P. A., Bucak, M., Crispi, F., Gomez, O., Turan, O. M., & Turan, S. (2025) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.29250 · Cited by 2 · see citing works
“In response to such flow changes, ventriculomegaly or suboptimal cortical development may be seen in the developing brain 52,81,102,120 .”
Self-citationHorgan, R., Sinkovskaya, E. S., Kalafat, E., Saade, G. A., & Abuhamad, A. Z. (2025) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.70110 · Cited by 2 · see citing works
“Previous studies have proposed reference ranges for fetal MPI using pulsed-wave Doppler 12–16 .”
Taksøe‐Vester, C., Mikolaj, K. W., Petersen, O. B., Ekelund, C. K., Vejlstrup, N. G., Vedel, C., Christensen, A. N., Feragen, A., Nielsen, M., & Tolsgaard, M. G. (2025) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.70123 · Cited by 2 · see citing works
“Research indicates that cardiac dysfunction is prevalent in cases of FGR 9 , persisting from the fetal stage through infancy 10,11 , childhood 12 and adolescence 13 , as a result of cardiac remodeling during fetal life.”
Maternal ozone exposure and differential cardiometabolic outcomes in aging male and female offspring
Yoo, B., Dye, J. A., Hazari, M. S., Farraj, A. K., Stewart, E. J., Thompson, L. C., Nguyen, H. H., Snow, S. J., Fiamingo, M. E., Fisher, A., et al. (2025) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2025.117669 · Cited by 2 · see citing works
Early nutritional influences of cardiovascular health
Drogalis-Kim, D. E., Cheifetz, I. M., & Robbins, N. (2021) · Expert Review of Cardiovascular Therapy · doi:10.1080/14779072.2021.2021070 · Cited by 2 · see citing works
“tion were present 6 months after birth [32].”
BackgroundLinking the Perinatal Environment to Neonatal Cardiovascular Outcomes
Korada, S., Jebbia, M. R., & Pavlek, L. R. (2022) · NeoReviews · doi:10.1542/neo.23-6-e400 · Cited by 2 · see citing works
Kurjak, A., Antsaklis, P. J., Barišić, L. S., Medjedović, E., Papamichail, M., & Malojčić, S. M. (2022) · Donald School Journal of Ultrasound in Obstetrics & Gynecology · doi:10.5005/jp-journals-10009-1928 · Cited by 2 · see citing works
Liefke, J., Sepúlveda-Martínez, Á., Shakya, S., Steding‐Ehrenborg, K., Arheden, H., Morsing, E., Ley, D., Heiberg, E., & Hedström, E. (2023) · Pediatric Cardiology · doi:10.1007/s00246-023-03265-z · Cited by 1 · see citing works
Assessing Coarctation of the Aorta With Fetal Heart Quantification Technology
Yang, J., Tan, F., Shen, Y., Zhao, Y., Xia, Y., Fan, S., & Ji, X. (2024) · Maternal-Fetal Medicine · doi:10.1097/fm9.0000000000000231 · Cited by 1 · see citing works
Groene, S. G., van Zwet, E. W., ten Harkel, A. D. J., Haak, M. C., van Klink, J. M. M., Lopriore, E., Heijmans, B. T., & Roest, A. A. W. (2025) · Pediatric Research · doi:10.1038/s41390-025-03916-2 · Cited by 1 · see citing works
Bueno‐Palomeque, F. L., Zacur, E., Pueyo, E., Crispi, F., Laguna, P., & Mincholé, A. (2025) · The Journal of Physiology · doi:10.1113/jp288197 · Cited by 1 · see citing works
“Among the consequences of IUGR, cardiac remodelling has been observed (Cruz-Lemini et al., 2016; Crispi et al., 2020; Sarvari et al., 2017), affecting the ventricular sphericity index (SpI), which is the ratio of apex-base length ( L ) to basal diameter ( φ ), SpI = L /φ , primarily in the left…”
Self-citation
- Authors
- Cruz-Lemini, M., Crispi, F., Valenzuela-Alcaraz, B., Figueras, F., Sitges, M., Bijnens, B., & Gratacós, E.
- Affiliations
- Consorci Institut D'Investigacions Biomediques August Pi I Sunyer (ES)
- BCNatal - Barcelona Center for Maternal-Fetal and Neonatal Medicine (Hospital Clínic and Hospital Sant Joan de Deu); Institut d'Investigacions Biomèdiques August Pi i Sunyer, Universitat de Barcelona, and Centre for Biomedical Research on Rare Diseases (CIBER-ER); Barcelona Spain
- Universitat de Barcelona (ES)
- Institució Catalana de Recerca i Estudis Avançats (ES)
- Corresponding author
- Gratacós, E.
- Venue
- Ultrasound in Obstetrics & Gynecology
- Publisher
- Wiley
- Published
- 2016-09
- Volume
- 48
- Issue
- 3
- Pages
- 349-356
- ISSN
- 0960-7692 (ISSN-L)
- OpenAlex
- W2520977127
- Semantic Scholar
- ed4ea8102affd6510f40170f5eafaf5ddc7b11bc
- Cited by
- 116
- References
- 46
- Citations by year
- 2026: 3 · 2025: 13 · 2024: 9 · 2023: 14 · 2022: 10 · 2021: 17 · 2020: 9 · 2019: 10 · 2018: 15 · 2017: 12 · 2016: 3 · 2014: 1
- FWCI
- 9.99
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Ultrasound in Obstetrics and Gynecology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Instituto de Salud Carlos III (PI11/00051, PI12/00801, PI11/01709)
- Ministerio de Economía y Competitividad (SAF2012-37196)
- Fondo Europeo de Desarrollo Regional de la Unión Europea ‘Una manera de hacer Europa’
- Fundación Mutua Madrileña
- Fundació Agrupació Premi Àmbit de la Infància
- Cerebra Foundation for the Brain Injured Child
- Programa de Ayudas Postdoctorales FI Agaur (2013FI_B 00667)
- Mexican National Council of Science and Technology
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Health Sciences › Medicine › Epidemiology › Congenital Heart Disease Studies
- Keywords
- fetal growth restriction, small-for-gestational-age fetuses, left ventricular diastolic dysfunction, left ventricular systolic dysfunction, left ventricular hypertrophy, aortic intima-media thickness, blood pressure, fetal echocardiography, tricuspid annular plane systolic excursion
- MeSH terms
- Adult, Cardiovascular Diseases, Cardiovascular System, Female, Fetal Growth Retardation, Gestational Age, Humans, Infant, Infant, Newborn, Infant, Small for Gestational Age, Longitudinal Studies, Male, Pregnancy, Prospective Studies, Risk Factors, Ultrasonography, Prenatal, Crown-Rump Length, Ventricular Remodeling, Carotid Intima-Media Thickness, Vascular Remodeling
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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