Abstract
Objective
To evaluate whether late-onset fetal growth restriction (LO-FGR) is associated with distinct alterations in cortical sulcation and midline brain structures compared with small-for-gestational-age (SGA) and appropriately grown (AGA) fetuses, and to examine how these changes relate to cerebroplacental redistribution.
Study design
This prospective cross-sectional study included 84 LO-FGR, 64 SGA, and 120 AGA fetuses examined between 32 and 36 weeks’ gestation. Targeted neurosonography assessed cortical sulcation, corpus callosum length, and cranio-cortical width, together with Doppler evaluation of the cerebroplacental ratio (CPR).
Results
LO-FGR fetuses demonstrated shallower Sylvian fissures, shorter corpus callosum length, increased insular depth, and wider lateral cranio-cortical width compared with both SGA and AGA fetuses (all p < 0.001). These neurosonographic differences were more pronounced in the presence of abnormal CPR.
Conclusion
LO-FGR is associated with specific cortical and midline brain alterations distinct from both SGA and AGA, with the severity of these changes modulated by cerebroplacental redistribution.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to the full article PDF.
USD 39.95
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Data availability
Data supporting the findings of this study are available from the corresponding author upon reasonable request.
References
Martins JG, Biggio JR, Abuhamad A. Society for maternal-fetal medicine consult series #52: diagnosis and management of fetal growth restriction: (replaces clinical guideline number 3, April 2012). Am J Obstet Gynecol. 2020;223:B2–b17. https://doi.org/10.1016/j.ajog.2020.05.010.
Lees CC, Stampalija T, Baschat A, da Silva Costa F, Ferrazzi E, Figueras F, et al. ISUOG practice guidelines: diagnosis and management of small-for-gestational-age fetus and fetal growth restriction. Ultrasound Obstet Gynecol. 2020;56:298–312. https://doi.org/10.1002/uog.22134.
Fetal Growth Restriction. ACOG practice bulletin, number 227. Obstet Gynecol. 2021;137:e16–e28. https://doi.org/10.1097/aog.0000000000004251.
Yehuda B, Rabinowich A, Zilberman A, Wexler Y, Haratz KK, Miller E, et al. Reduced gyrification in fetal growth restriction with prenatal magnetic resonance images. Cereb Cortex. 2024;34. https://doi.org/10.1093/cercor/bhae250.
Malinger G, Paladini D, Haratz KK, Monteagudo A, Pilu GL, Timor-Tritsch IE. ISUOG practice guidelines (updated): sonographic examination of the fetal central nervous system. Part 1: performance of screening examination and indications for targeted neurosonography. Ultrasound Obstet Gynecol. 2020;56:476–84. https://doi.org/10.1002/uog.22145.
Eves R, Mendonça M, Bartmann P, Wolke D. Small for gestational age-cognitive performance from infancy to adulthood: an observational study. Bjog. 2020;127:1598–606. https://doi.org/10.1111/1471-0528.16341.
Çetin B, Madazli R. Assessment of normal fetal cortical sulcus development. Arch Gynecol Obstetrics. 2022;306. https://doi.org/10.1007/s00404-021-06334-x.
Mappa I, Marra MC, Pietrolucci ME, Lu JLA, D’Antonio F, Rizzo G. Midline structures and cortical development in late-onset fetal growth restriction according to Doppler status: prospective study. Ultrasound Obstet Gynecol. 2024;64:228–35. https://doi.org/10.1002/uog.27598.
Paules C, Miranda J, Policiano C, Crovetto F, Youssef L, Hahner N, et al. Fetal neurosonography detects differences in cortical development and corpus callosum in late-onset small fetuses. Ultrasound Obstetrics Gynecol. 2021;58:42–7. https://doi.org/10.1002/uog.23592.
Corbacioglu Esmer A, Yuksel A, Aksu Uzunhan T, Demir O, Sarac Sivrikoz T, Aydinli N. Evaluation of fetal subarachnoid space using transabdominal ultrasonography and normal values during pregnancy. Springerplus. 2016;5:1439. https://doi.org/10.1186/s40064-016-3121-5.
Sacchi C, Marino C, Nosarti C, Vieno A, Visentin S, Simonelli A. Association of intrauterine growth restriction and small for gestational age status with childhood cognitive outcomes: a systematic review and meta-analysis. JAMA Pediatr. 2020;174:772–81. https://doi.org/10.1001/jamapediatrics.2020.1097.
Gordijn SJ, Beune IM, Thilaganathan B, Papageorghiou A, Baschat AA, Baker PN, et al. Consensus definition of fetal growth restriction: a Delphi procedure. Ultrasound Obstet Gynecol. 2016;48:333–9. https://doi.org/10.1002/uog.15884.
Committee Opinion No 700. Methods for estimating the due date. Obstet Gynecol. 2017;129:e150–e4. https://doi.org/10.1097/aog.0000000000002046.
Hadlock FP, Harrist RB, Carpenter RJ, Deter RL, Park SK. Sonographic estimation of fetal weight. The value of femur length in addition to head and abdomen measurements. Radiology. 1984;150:535–40. https://doi.org/10.1148/radiology.150.2.6691115.
Kurmanavicius J, Wright EM, Royston P, Wisser J, Huch R, Huch A, et al. Fetal ultrasound biometry: 1. Head reference values. Br J Obstet Gynaecol. 1999;106:126–35. https://doi.org/10.1111/j.1471-0528.1999.tb08212.x.
Bhide A, Acharya G, Baschat A, Bilardo CM, Brezinka C, Cafici D, et al. ISUOG practice guidelines (updated): use of Doppler velocimetry in obstetrics. Ultrasound Obstet Gynecol. 2021;58:331–9. https://doi.org/10.1002/uog.23698.
Basso A, Youssef L, Nakaki A, Paules C, Miranda J, Casu G, et al. Fetal neurosonography at 31-35 weeks reveals altered cortical development in pre-eclampsia with and without small-for-gestational-age fetus. Ultrasound Obstet Gynecol. 2022;59:737–46. https://doi.org/10.1002/uog.24853.
Zheng W, Zhang X, Feng Y, Liu B, Zhu J, Zou Y, et al. Association of corpus callosum development with fetal growth restriction and maternal preeclampsia or gestational hypertension. JAMA Netw Open. 2022;5:e2226696. https://doi.org/10.1001/jamanetworkopen.2022.26696.
Napolitano R, Molloholli M, Donadono V, Ohuma EO, Wanyonyi SZ, Kemp B, et al. International standards for fetal brain structures based on serial ultrasound measurements from Fetal Growth Longitudinal Study of INTERGROWTH-21(st) Project. Ultrasound Obstet Gynecol. 2020;56:359–70. https://doi.org/10.1002/uog.21990.
Alonso I, Borenstein M, Grant G, Narbona I, Azumendi G. Depth of brain fissures in normal fetuses by prenatal ultrasound between 19 and 30 weeks of gestation. Ultrasound Obstet Gynecol. 2010;36:693–9. https://doi.org/10.1002/uog.7660.
Donadono V, Cavallaro A, Roberts NW, Ioannou C, Papageorghiou AT, Napolitano R. A systematic review of methodology used in studies aimed at creating charts of fetal brain structures. Diagnostics. 2021;11. https://doi.org/10.3390/diagnostics11060916.
Wu J, Sun T, Yu B, Li Z, Wu Q, Wang Y, et al. Age-specific structural fetal brain atlases construction and cortical development quantification for chinese population. Neuroimage. 2021;241:118412. https://doi.org/10.1016/j.neuroimage.2021.118412.
Lip-Sosa DL, Pérez-Cruz M, Ahumada-Droguett P, Ribas-Prats T, Puertollano M, García-Gómez MA, et al. Corpus callosum-fastigium and tectal lengths in late-onset small fetuses. Ultrasound Obstet Gynecol. 2023;62:226–33. https://doi.org/10.1002/uog.26169.
Simsek O, Manteghinejad A, Wannasarnmetha M, Kotha A, Teixeira SR, Zarnow D, et al. Subarachnoid space measurements in the second trimester using MR imaging. AJNR Am J Neuroradiol. 2025. https://doi.org/10.3174/ajnr.A8773.
Author information
Authors and Affiliations
Contributions
Miraç Özalp: Conceptualization; Methodology; Investigation; Data curation; Resources; Validation; Writing – review & editing; Supervision. Murat İbrahim Toplu: Methodology; Data curation; Formal analysis; Software; Writing – original draft; Writing – review & editing; Visualization; Project administration.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Ethics approval and consent to participate
This study was conducted in accordance with the principles of the Declaration of Helsinki. Ethical approval was obtained from the Institutional Review Board of Prof. Dr. Cemil Taşcıoğlu City Hospital (Approval No: 2024/69; Date: 01.04.2024). Written INFORMED consent was obtained from all participants prior to inclusion in the study.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Özalp, M., Toplu, M.İ. Fetal neurosonographic assessment of cortical development in late-onset Fetal growth restriction and small for gestational age fetuses. J Perinatol (2026). https://doi.org/10.1038/s41372-026-02638-5
Received:
Revised:
Accepted:
Published:
Version of record:
DOI: https://doi.org/10.1038/s41372-026-02638-5


