Long-term cognitive, executive, and behavioral outcomes of moderate and late preterm at school age

Abstract

Background

There is increasing concern that moderate preterm (32–33 weeks’ gestation) and late preterm (34–36 weeks’ gestation) birth may be associated with minor neurodevelopmental problems affecting poor school performance.

Purpose

We explored the cognitive function, cognitive visual function, executive function, and behavioral problems at schoolage in moderate to late preterm infants.

Methods

Children aged 7–10 years who were born at 32+0 to 36+6 weeks of gestation and admitted to the neonatal intensive care unit from August 2006 to July 2011 at the National Health Insurance Service Ilsan Hospital were included. We excluded children with severe neurologic impairments, congenital malformations, or chromosomal abnormalities. Neuropsychological assessments consisted of 5 neuropsychological tests and 3 questionnaires.

Results

A total of 37 children (mean age, 9.1±1.2 years) participated. The mean gestational age at birth was 34.6±7.5 weeks, while the mean birth weight was 2,229.2±472.8 g. The mean full-scale intelligence quotient was 92.89±11.90; 24.3% scored between 70 and 85 (borderline intelligence functioning). An abnormal score was noted for at least one of the variables on the attention deficit hyperactivity disorder diagnostic system for 65% of the children. Scores below borderline function for executive quotient and memory quotient were 32.4% and 24.3%, respectively. Borderline or clinically relevant internalizing problems were noted in 13.5% on the Child Behavior Check List. There were no significant associations between perinatal factors or socioeconomic status and cognitive, visual perception, executive function, or behavior outcomes.

Conclusion

Moderate to late preterm infants are at risk of developing borderline intelligence functioning and attention problems at early school age. Cognitive and executive functions that are important for academic performance must be carefully monitored and continuously followed up in moderate to late preterm infants.

Alternate abstract:

Question: Infants born at moderate to late preterm gestations are known to have little problem later on, but is that really true

Finding: At school age, cognitive problem was observed in about a quarter of the children. In addition, more than half of the children was suspected of having attention problems.

Meaning: Moderate to late preterm infants are at risk of developing abnormal intelligence and attention problems at early school age, therefore they should not be neglected on longterm follow-up evaluation.

A major strength of our study is that we investigated a wide range of neurodevelopmental outcomes, including various domains of cognitive and executive function in school-aged children using direct, objective, standardized assessments.

In conclusion, moderate to late preterm infants are at risk for developing borderline intelligence at school age. Executive function deficits, especially attention problems, were prominent. Our study supports the importance of periodic assessments and long-term follow-up in moderate to late preterm children, even if they have no signs of disabilities in early life, as these subtle or minor problems tend to become more obvious as the child grows to school age. Because minor neurodevelopmental problems such as borderline intelligence, and behavioral and adaptive functioning problems are more responsive to early interventions [23], closer follow-up monitoring of neurodevelopment after discharge for early detection and referral to early intervention is needed. The impact of this large and growing population of moderate to late preterm infants should not be underestimated or neglected on long-term follow-up evaluation.

References

1. Voss W, Neubauer AP, Wachtendorf M, Verhey JF, Kattner E. Neurodevelopmental outcome in extremely low birth weight infants: what is the minimum age for reliable developmental prognosis? Acta Paediatr 2007;96:342–7.

2. Foulder-Hughes LA, Cooke RW. Motor, cognitive, and behavioural disorders in children born very preterm. Dev Med Child Neurol 2003;45:97–103.

3. Lee HJ, Park HK. Neurodevelopmental outcome of preterm infants at childhood: cognition and language. Hanyang Med Rev 2016;36:55–8.

4. Talge NM, Holzman C, Wang J, Lucia V, Gardiner J, Breslau N. Late-preterm birth and its association with cognitive and socioemotional outcomes at 6 years of age. Pediatrics 2010;126:1124–31.

5. McGowan JE, Alderdice FA, Holmes VA, Johnston L. Early childhood development of late-preterm infants: a systematic review. Pediatrics 2011;127:1111–24.

6. van Baar AL, Vermaas J, Knots E, de Kleine MJ, Soons P. Functioning at school age of moderately preterm children born at 32 to 36 weeks' gestational age. Pediatrics 2009;124:251–7.

7. Huddy CL, Johnson A, Hope PL. Educational and behavioural problems in babies of 32-35 weeks gestation. Arch Dis Child Fetal Neonatal Ed 2001;85:F23–8.

9. Cserjesi R, Van Braeckel KN, Butcher PR, Kerstjens JM, Reijneveld SA, Bouma A, et al. Functioning of 7-year-old children born at 32 to 35 weeks' gestational age. Pediatrics 2012;130:e838–46.

10. Odd DE, Emond A, Whitelaw A. Long-term cognitive outcomes of infants born moderately and late preterm. Dev Med Child Neurol 2012;54:704–9.

11. de Jong M, Verhoeven M, van Baar AL. School outcome, cognitive functioning, and behaviour problems in moderate and late preterm children and adults: a review. Semin Fetal Neonatal Med 2012;17:163–9.

12. Kwak GJ, Oh SH, Kim CT. K-WISC-IV manual for professionals. 4th ed. Seoul: Hakjisa Publisher, 2011.

13. Hammill DD, Pearson NA, Voress JK, Frostig M. Developmental test of visual perception: DTVP-2. 2nd ed. Austin (TX): Pro-Ed, 1993.

14. Hammill DD, Pearson NA, Voress JK, Frostig M. Developmental test of visual perception: DTVP-3. 3rd ed. Austin (TX): Pro-Ed, 2014.

15. Shin MS, Cho SZ, Chun SY, Hong KE. A study of the development and standardization of ADHD diagnostic system. Korean J Child Adol Psychiatr 2000;11:91–9.

16. Kim HG. Children's Rey-Kim memory test: manual. Daegu: Neuropsy Pub, 2005.

17. Kim HG. Children's kims frontal-executive function test; manual. Daegu: Neuropsy Pub, 2005.

18. Achenbach TM, Edelbrock CS. Manual for the child behavior checklist and revised child behavior profile. Burlington (VT): University of Vermont, Department of Psychiatry, 1983.

19. Cho SC, Lee YS. Development of the Korean form of the Kovacs' children's depression inventory. J Korean Neuropsychiatr Assoc 1990;29:943–56.

20. Choi JS, Cho SC. Assessment of anxiety in children: reliability and validity of revised children's manifest anxiety scale. J Korean Neuropsychiatr Assoc 1990;29:691–702.

21. Korean Statistical Information Service [Internet]. Daejeon (Korea), Statistics Korea. 2018;[cited 2019 Sep 20]. Available from: http://kosis.kr/eng/statisticsList/statisticsListIndex.do?menuId=M_01_01&vwcd=MT_TITLE&parmTabId=M_01_01.

22. Wieland J, Zitman FG. It is time to bring borderline intellectual functioning back into the main fold of classification systems. BJPsych Bull 2016;40:204–6.

27. Chyi LJ, Lee HC, Hintz SR, Gould JB, Sutcliffe TL. School outcomes of late preterm infants: special needs and challenges for infants born at 32 to 36 weeks gestation. J Pediatr 2008;153:25–31.

28. Lipkind HS, Slopen ME, Pfeiffer MR, McVeigh KH. School-age outcomes of late preterm infants in New York City. Am J Obstet Gynecol 2012;206:222e1-6.

32. Caravale B, Tozzi C, Albino G, Vicari S. Cognitive development in low risk preterm infants at 3-4 years of life. Arch Dis Child Fetal Neonatal Ed 2005;90:F474–9.

34. Atkinson J, Braddick O. Visual and visuocognitive development in children born very prematurely. Prog Brain Res 2007;164:123–49.

35. Taylor HG, Clark CA. Executive function in children born preterm: risk factors and implications for outcome. Semin Perinatol 2016;40:520–9.