Long term neuromotor outcome in children born at term with asymmetrical intrauterine growth restriction
DOI:
https://doi.org/10.13112/pc.1102Keywords:
child; fetal growth retardation; motor skills disorders; neurodevelopmental disordersAbstract
Aim: Intrauterine growth restriction has an important influence on a child's neurological development. The aim of this study was a long-term follow up of a group of children born at term with asymmetrical intrauterine growth restriction until the age of 12 to 14.
Methods: Examinees were children born at term with asymmetrical intrauterine growth restriction matched to the control group according to age, gender, gestational age, and maternal education. Participants were between 12 and 14 years old at the time of examination. Exclusion criteria were central nervous system infections, congenital infections, major malformations, severe asphyxia, chromosomal disorders, and the presence of genetic syndromes. Neurological examination for minor neurological dysfunction according to Hadders-Algra was performed. The results were compared to their first neurological assessment at the age of 5 to 7.
Results: There were 43 participants (22 female and 21 male) in the IUGR group and 42 in the control group (21 female and 21 male). Children with intrauterine growth restriction had significantly lower values for associated movements (p 0.034) and coordination (p 0.001) than the control group. There was a positive correlation between birth weight and associated movements (0.015).
Conclusion: At pubertal age, examinees born at term with asymmetrical intrauterine growth restriction still show impairments in coordination and associated movements, which is an improvement when compared to the result from preschool age, but indicate that some neurological impairments are irreversible.
References
1. Roth S, Chang T.C, Robson S, Spencer JA, Wyatt JS, Stewart AL. The neurodevelopmental outcome of term infants with different intrauterine growth characteristics. Early Hum Dev 1999;55:39- 50. DOI: 10.1016/s0378-3782(99)00002-x
2. Kliegman RM. Intrauterine growth restriction. In: Martin RJFA, Walsh MC, eds. Fanaroff and Martin’s neonatal perinatal medicine. 9th edn. Louis (MO): Elsever Mosby; 2011:245–75.
3. Mandruzzato G, Antsaklis A, Botet F. Intrauterine restriction (IUGR). J Perinatal Med 2008; 36:277–81. DOI: 10.1515/JPM.2008.050
4. Fung C, Zinkhan E. Short and Long-Term Implications of Small for Gestational Age. Obstet Gynecol Clin N Am 2021;48:311–23. DOI: 10.1016/j.ogc.2021.02.004
5. Galjaard S, Devlieger R, Van Assche F.A. Fetal growth and developmental programming. J Perinat Med 2013;41:101–5. DOI: 10.1515/jpm-2012-0020
6. Rosenberg A. The IUGR Newborn. Semin Perinatol 2008;32:219-24. DOI: 10.1053/j.semperi.2007.11.003
7. Stellar JG, Gumina D, Driver C, Peek E, Galan HL, Reeves S, et al. Patterns of Brain Sparing in a Fetal Growth Restriction Cohort. J Clin Med 2022;11:4480. DOI: 10.3390/jcm11154480
8. Geva R, Eshel R, Leitner Y, Fattal Valevski A, Harel S. Neuropsychological outcome of children with intrauterine growth restriction: a 9-year prospective study. Pediatrics 2006;118:91-100. DOI: 10.1542/peds.2005-2343
9. Feldman R, Eidelman AI. Neonatal state organization, neuromaturation, mother-infant interaction and cognitive development in small-for-gestational-age premature infants. Pediatrics 2006;118:e869-78. DOI: 10.1542/peds.2005-2040
10. Eixarch E, Munoz-Moreno E, Bargallo N, Batalle D, Gratacos E. Motor and cortico-striatal-thalamic connectivity alterations in intrauterine growth restriction. Am J Obstet Gynecol 2016;214:725 e1–9. DOI: 10.1016/j.ajog.2015.12.028
11. Fischi-Gómez E, Vasung L, Meskaldji DE, Lazeyras F, Borradori-Tolsa C, Hagmann P, et al. Structural brain connectivity in school-age preterm infants provides evidence for impaired networks relevant for higher order cognitive skills and social cognition. Cerebral Cortex 2015; 25:2793–805. DOI: 10.1093/cercor/bhu073
12. Klarić AŠ, Galić S, Kolundžić Z, Bošnjak VM. Neuropsychological Development in Preschool Children Born After Asymmetrical Intrauterine Growth Restriction and Impact of Postnatal Head Growth. J Child Neurol 2013;28:867-73. DOI: 10.1177/0883073812452790
13. Leitner Y, Fattal-Valevski A, Geva R, Eshel R, Toledano-Alhadef H, Rotstein M, et al. Neurodevelopmental outcome of children a longitudinal, 10-year prospective study. J Child Neurol 2009;22:580–7. DOI: 10.1177/0883073807302605
14. Murray E, Fernandes M, Fazel M, Kennedy SH, Villar J, Stein A. Differential effect of intrauterine growth restriction on childhood neurodevelopment: A systematic review. BJOG 2015;122:1062-72. DOI: 10.1111/1471-0528.13435
15. Korzeniewski SJ, Allred EN, Joseph RM, Herren T, Kuban KCK, O' Shea TM, et al. Neurodevelopment at Age 10 Years of Children Born <28 Weeks With Fetal Growth Restriction. Pediatrics 2017;140:140. DOI:10.3390/ijerph191711043
16. Freire G, Shevell M, Oskoui M. Cerebral palsy: Phenotypes and risk factors in term singletons born small for gestational age. Eur J Paediatr Neurol 2015;19:218-25. DOI: 10.1016/j.ejpn.2014.12.005
17. Šimić Klarić A, Kolundžić Z, Galić S, Tomić Rajić M, Matoković D, Banožić Lj. The impact of neonatal complications on motor outcome in children with asymmetrical intrauterine growth restiction. Paediatr Croat. 2013;57:101-5. DOI:10.13112/pc.678
18. Šimić Klarić A, Kolundžić Z, Galić S, Mejaški Bošnjak V. Language development in preschool children born after asymmetrical intrauterine growth retardation. Eur J Paediatr Neurol 2012;16(2):132-7. DOI: 10.1016/j.ejpn.2011.06.003
19. Vollmer B, Edmonds CJ. School Age Neurological and Cognitive Outcomes of Fetal Growth Retardation or Small for Gestational Age Birth Weight. J Front Endocrinol (Lausanne) 2019; 10:186. DOI: 10.3389/fendo.2019.00186
20. Dražančić A. Obstetrics. Zagreb: School Newspaper; 1994. 125 (Croatian).
21. Hadders-Algra M. The neurological examination of the child with minor neurological dysfunction, 3rd edn. London: Mac Keith Press, 2010.
22. Olivier P, Baud O, Evrard P, Gressens P, Verney C. Prenatal ischemia and white matter damage in rats. J Neuropathol Exp Neurol 2005;64:998-1006. DOI: 10.1097/01.jnen.0000187052.81889.57
23. Olivier P, Baud O, Bouslama M, Evrard P, Gressens P, Verney C. Moderate growth restriction: Deleterious and protective effects on white matter damage. Neurobiol Dis 2007;26:253-63. DOI: 10.1016/j.nbd.2007.01.001
24. Strauss R.S. Adult functional outcome of those born small for gestational age : twenty-six-years follow-up of the 1970 British Birth Cohort. JAMA 2000;283:625-32. DOI: 10.1001/jama.283.5.625
25. Tanis JC, Van Braeckel KNJA, Kerstjens JM, Bocca-Tjeertes IFA, Reijneveld SA, Bos AF. Functional outcomes at age 7 years of moderate preterm and full term children born small for gestational age. J Pediatr 2015:166:552–8. DOI: 10.1016/j.jpeds.2014.11.043
26. Groene SG, Stegmeijer KJJ, Tan RNGB, Steggerda SJ, Haak MC, Slaghekke F, et al. Long-term effects of selective fetal growth restriction (LEMON): a cohort study of neurodevelopmental outcome in growth discordant identical twins in the Netherlands. Lancet Child Adolesc Health 2022;6:624–32. DOI: 10.1016/S2352-4642(22)00159-6
Downloads
Published
Issue
Section
License
Copyright (c) 2025 Andrea Šimić Klarić, Zdravko Kolundžić, Slavka Galić
This work is licensed under a Creative Commons Attribution 4.0 International License.
By publishing in Paediatria Croatica, authors retain the copyright to their work and grant others the right to use, reproduce, and share their research articles in accordance with the Creative Commons Attribution License (CC BY 4.0), which allows others to distribute and build upon the work as long as they credit the author for the original creation.
