Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Fetal neurosonographic assessment of cortical development in late-onset Fetal growth restriction and small for gestational age fetuses

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

Buy this article

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

  1. 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.

    Article  PubMed  Google Scholar 

  2. 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.

    Article  CAS  PubMed  Google Scholar 

  3. Fetal Growth Restriction. ACOG practice bulletin, number 227. Obstet Gynecol. 2021;137:e16–e28. https://doi.org/10.1097/aog.0000000000004251.

    Article  Google Scholar 

  4. 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.

  5. 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.

    Article  CAS  PubMed  Google Scholar 

  6. 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.

    Article  CAS  PubMed  Google Scholar 

  7. 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.

  8. 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.

    Article  CAS  PubMed  Google Scholar 

  9. 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.

    Article  CAS  Google Scholar 

  10. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  11. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  12. 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.

    Article  CAS  PubMed  Google Scholar 

  13. Committee Opinion No 700. Methods for estimating the due date. Obstet Gynecol. 2017;129:e150–e4. https://doi.org/10.1097/aog.0000000000002046.

    Article  Google Scholar 

  14. 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.

    Article  CAS  PubMed  Google Scholar 

  15. 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.

    Article  CAS  PubMed  Google Scholar 

  16. 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.

    Article  CAS  PubMed  Google Scholar 

  17. 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.

    Article  CAS  PubMed  Google Scholar 

  18. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  19. 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.

    Article  CAS  PubMed  Google Scholar 

  20. 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.

    Article  CAS  PubMed  Google Scholar 

  21. 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.

  22. 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.

    Article  PubMed  Google Scholar 

  23. 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.

    Article  CAS  PubMed  Google Scholar 

  24. 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.

Download references

Author information

Authors and Affiliations

Authors

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

Correspondence to Murat İbrahim Toplu.

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Version of record:

  • DOI: https://doi.org/10.1038/s41372-026-02638-5

Search

Quick links