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Am J Perinatol 2014; 31(04): 305-314
DOI: 10.1055/s-0033-1348950
Original Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

The Impact of Late Preterm Birth on Executive Function at Preschool Age

Jane E. Brumbaugh
1   Department of Pediatrics, University of Iowa Hospitals and Clinics, Iowa City, Iowa
,
Amanda S. Hodel
2   Institute of Child Development, University of Minnesota, Minneapolis, Minnesota
,
Kathleen M. Thomas
2   Institute of Child Development, University of Minnesota, Minneapolis, Minnesota
› Author Affiliations
Further Information

Publication History

17 March 2013

20 May 2013

Publication Date:
17 June 2013 (online)

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Abstract

Objective Very preterm birth (< 32 weeks' gestation) affects cognitive development. The impact of late preterm birth (34 to 36 weeks' gestation) on cognition, specifically executive function, is not fully characterized. The aim of this study was to assess whether late preterm children demonstrate impaired executive function compared with full-term children (38 to 42 weeks' gestation).

Study Design This was a prospective cohort study of 4-year-old children. Preterm (n = 39) and full-term children (n = 44) completed a battery of executive function tasks and the Peabody Picture Vocabulary Test-4. Parents completed the Behavior Rating Inventory of Executive Function–Preschool version.

Results Preterm children performed worse on the verbal inhibitory control (p = 0.02) and short-term verbal memory (p = 0.01) tasks. Gestational age predicted performance on the verbal inhibitory control (p = 0.02) and short-term verbal memory (p = 0.04) tasks. There was no group difference in nonverbal inhibitory control (p = 0.45) or spatial memory (p = 0.60). Parents of preterm and full-term children rated their children's behavior similarly (p = 0.79).

Conclusion Late preterm children demonstrated compromised verbal inhibitory control and short-term verbal memory compared with full-term peers. Late preterm children may not be spared from altered brain development. Further research is indicated to determine whether to screen late preterm children for executive function deficits.

Keywords

late preterm - premature birth - executive function - inhibitory control - memory
 

  • References

  • 1 Martin JA, Hamilton BE, Ventura SJ , et al. Births: final data for 2009. Natl Vital Stat Rep 2011; 60: 1-70
    PubMedGoogle Scholar
  • 2 Hüppi PS, Warfield S, Kikinis R , et al. Quantitative magnetic resonance imaging of brain development in premature and mature newborns. Ann Neurol 1998; 43: 224-235
    CrossrefPubMedGoogle Scholar
  • 3 Burns CM, Rutherford MA, Boardman JP, Cowan FM. Patterns of cerebral injury and neurodevelopmental outcomes after symptomatic neonatal hypoglycemia. Pediatrics 2008; 122: 65-74
    CrossrefPubMedGoogle Scholar
  • 4 Hansen TW. Prevention of neurodevelopmental sequelae of jaundice in the newborn. Dev Med Child Neurol 2011; 53 (Suppl. 04) 24-28
    CrossrefPubMedGoogle Scholar
  • 5 Mishra OP, Delivoria-Papadopoulos M. Cellular mechanisms of hypoxic injury in the developing brain. Brain Res Bull 1999; 48: 233-238
    CrossrefPubMedGoogle Scholar
  • 6 Welsh MC, Pennington BF, Groisser DB. A normative-developmental study of executive function: a window on prefrontal function in children. Dev Neuropsychol 1991; 7: 131-149
    CrossrefPubMedGoogle Scholar
  • 7 Aarnoudse-Moens CS, Smidts DP, Oosterlaan J, Duivenvoorden HJ, Weisglas-Kuperus N. Executive function in very preterm children at early school age. J Abnorm Child Psychol 2009; 37: 981-993
    CrossrefPubMedGoogle Scholar
  • 8 Marlow N, Hennessy EM, Bracewell MA, Wolke D. EPICure Study Group. Motor and executive function at 6 years of age after extremely preterm birth. Pediatrics 2007; 120: 793-804
    CrossrefPubMedGoogle Scholar
  • 9 Anderson PJ, Doyle LW. Victorian Infant Collaborative Study Group. Executive functioning in school-aged children who were born very preterm or with extremely low birth weight in the 1990s. Pediatrics 2004; 114: 50-57
    CrossrefPubMedGoogle Scholar
  • 10 Sun J, Mohay H, O'Callaghan M. A comparison of executive function in very preterm and term infants at 8 months corrected age. Early Hum Dev 2009; 85: 225-230
    CrossrefPubMedGoogle Scholar
  • 11 Narberhaus A, Segarra D, Caldú X , et al. Corpus callosum and prefrontal functions in adolescents with history of very preterm birth. Neuropsychologia 2008; 46: 111-116
    CrossrefPubMedGoogle Scholar
  • 12 Nosarti C, Giouroukou E, Micali N, Rifkin L, Morris RG, Murray RM. Impaired executive functioning in young adults born very preterm. J Int Neuropsychol Soc 2007; 13: 571-581
    PubMedGoogle Scholar
  • 13 Johnson S, Hennessy E, Smith R, Trikic R, Wolke D, Marlow N. Academic attainment and special educational needs in extremely preterm children at 11 years of age: the EPICure study. Arch Dis Child Fetal Neonatal Ed 2009; 94: F283-F289
    CrossrefPubMedGoogle Scholar
  • 14 Grunau RE, Whitfield MF, Davis C. Pattern of learning disabilities in children with extremely low birth weight and broadly average intelligence. Arch Pediatr Adolesc Med 2002; 156: 615-620
    CrossrefPubMedGoogle Scholar
  • 15 Saigal S, Hoult LA, Streiner DL, Stoskopf BL, Rosenbaum PL. School difficulties at adolescence in a regional cohort of children who were extremely low birth weight. Pediatrics 2000; 105: 325-331
    CrossrefPubMedGoogle Scholar
  • 16 Carlson SM, Wang TS. Inhibitory control and emotion regulation in preschool children. Cognitive Dev 2007; 22: 489-510
    PubMedGoogle Scholar
  • 17 Kerstjens JM, de Winter AF, Bocca-Tjeertes IF, ten Vergert EM, Reijneveld SA, Bos AF. Developmental delay in moderately preterm-born children at school entry. J Pediatr 2011; 159: 92-98
    CrossrefPubMedGoogle Scholar
  • 18 Clark C, Prior M, Kinsella G. The relationship between executive function abilities, adaptive behaviour, and academic achievement in children with externalising behaviour problems. J Child Psychol Psychiatry 2002; 43: 785-796
    CrossrefPubMedGoogle Scholar
  • 19 Altemeier L, Jones J, Abbott RD, Berninger VW. Executive functions in becoming writing readers and reading writers: note taking and report writing in third and fifth graders. Dev Neuropsychol 2006; 29: 161-173
    CrossrefPubMedGoogle Scholar
  • 20 Delobel-Ayoub M, Arnaud C, White-Koning M , et al; EPIPAGE Study Group. Behavioral problems and cognitive performance at 5 years of age after very preterm birth: the EPIPAGE Study. Pediatrics 2009; 123: 1485-1492
    CrossrefPubMedGoogle Scholar
  • 21 Romer D, Betancourt L, Giannetta JM, Brodsky NL, Farah M, Hurt H. Executive cognitive functions and impulsivity as correlates of risk taking and problem behavior in preadolescents. Neuropsychologia 2009; 47: 2916-2926
    CrossrefPubMedGoogle Scholar
  • 22 Latzman RD, Elkovitch N, Young J, Clark LA. The contribution of executive functioning to academic achievement among male adolescents. J Clin Exp Neuropsychol 2010; 32: 455-462
    CrossrefPubMedGoogle Scholar
  • 23 Clark CA, Pritchard VE, Woodward LJ. Preschool executive functioning abilities predict early mathematics achievement. Dev Psychol 2010; 46: 1176-1191
    CrossrefPubMedGoogle Scholar
  • 24 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
    CrossrefPubMedGoogle Scholar
  • 25 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: 251-257
    CrossrefPubMedGoogle Scholar
  • 26 Morse SB, Zheng H, Tang Y, Roth J. Early school-age outcomes of late preterm infants. Pediatrics 2009; 123: e622-e629
    CrossrefPubMedGoogle Scholar
  • 27 Anderson DE, Flax ML. A comparison of the Peabody Picture Vocabulary Test with the Wechsler Intelligence Scale for Children. J Educ Res 1968; 62: 114-116
    CrossrefPubMedGoogle Scholar
  • 28 Sherman EMS, Brooks BL. Behavior Rating Inventory of Executive Function—Preschool Version (BRIEF-P): test review and clinical guidelines for use. Child Neuropsychol 2010; 16: 503-519
    CrossrefPubMedGoogle Scholar
  • 29 Carlson SM. Developmentally sensitive measures of executive function in preschool children. Dev Neuropsychol 2005; 28: 595-616
    CrossrefPubMedGoogle Scholar
  • 30 Gerstadt CL, Hong YJ, Diamond A. The relationship between cognition and action: performance of children 3 1/2-7 years old on a Stroop-like day-night test. Cognition 1994; 53: 129-153
    CrossrefPubMedGoogle Scholar
  • 31 Carlson SM, Moses LJ. Individual differences in inhibitory control and children's theory of mind. Child Dev 2001; 72: 1032-1053
    CrossrefPubMedGoogle Scholar
  • 32 Kaufman AS, Kaufman NL , Eds. Kaufman Assessment Battery for Children, Second Edition. Circle Pines, MN: American Guidance Services; 2004
    Google Scholar
  • 33 Corsi PM. Human memory and the medial temporal region of the brain. Dissertation Abstracts International. 1972; 34: 819B
    PubMedGoogle Scholar
  • 34 Mischel W, Shoda Y, Rodriguez MI. Delay of gratification in children. Science 1989; 244: 933-938
    CrossrefPubMedGoogle Scholar
  • 35 Berwid OG, Curko Kera EA, Marks DJ, Santra A, Bender HA, Halperin JM. Sustained attention and response inhibition in young children at risk for Attention Deficit/Hyperactivity Disorder. J Child Psychol Psychiatry 2005; 46: 1219-1229
    CrossrefPubMedGoogle Scholar
  • 36 Zelazo PD. The Dimensional Change Card Sort (DCCS): a method of assessing executive function in children. Nat Protoc 2006; 1: 297-301
    CrossrefPubMedGoogle Scholar
  • 37 Lee ES, Yeatman JD, Luna B, Feldman HM. Specific language and reading skills in school-aged children and adolescents are associated with prematurity after controlling for IQ. Neuropsychologia 2011; 49: 906-913
    CrossrefPubMedGoogle Scholar
  • 38 Barre N, Morgan A, Doyle LW, Anderson PJ. Language abilities in children who were very preterm and/or very low birth weight: a meta-analysis. J Pediatr 2011; 158: 766-774 , e1
    CrossrefPubMedGoogle Scholar
  • 39 Foster-Cohen SH, Friesen MD, Champion PR, Woodward LJ. High prevalence/low severity language delay in preschool children born very preterm. J Dev Behav Pediatr 2010; 31: 658-667
    CrossrefPubMedGoogle Scholar
  • 40 Briscoe J, Gathercole SE, Marlow N. Short-term memory and language outcomes after extreme prematurity at birth. J Speech Lang Hear Res 1998; 41: 654-666
    CrossrefPubMedGoogle Scholar
  • 41 Taylor GH, Klein NM, Minich NM, Hack M. Verbal memory deficits in children with less than 750 g birth weight. Child Neuropsychol 2000; 6: 49-63
    CrossrefPubMedGoogle Scholar
  • 42 Saavalainen P, Luoma L, Bowler D , et al. Spatial span in very prematurely born adolescents. Dev Neuropsychol 2007; 32: 769-785
    CrossrefPubMedGoogle Scholar
  • 43 Luciana M, Lindeke L, Georgieff M, Mills M, Nelson CA. Neurobehavioral evidence for working-memory deficits in school-aged children with histories of prematurity. Dev Med Child Neurol 1999; 41: 521-533
    CrossrefPubMedGoogle Scholar
  • 44 Espy KA, Stalets MM, McDiarmid MM, Senn TE, Cwik MF, Hamby A. Executive functions in preschool children born preterm: application of cognitive neuroscience paradigms. Child Neuropsychol 2002; 8: 83-92
    CrossrefPubMedGoogle Scholar
  • 45 Böhm B, Smedler AC, Forssberg H. Impulse control, working memory and other executive functions in preterm children when starting school. Acta Paediatr 2004; 93: 1363-1371
    CrossrefPubMedGoogle Scholar
  • 46 Friedman NP, Miyake A, Corley RP, Young SE, Defries JC, Hewitt JK. Not all executive functions are related to intelligence. Psychol Sci 2006; 17: 172-179
    CrossrefPubMedGoogle Scholar
  • 47 Gross SJ, Mettelman BB, Dye TD, Slagle TA. Impact of family structure and stability on academic outcome in preterm children at 10 years of age. J Pediatr 2001; 138: 169-175
    CrossrefPubMedGoogle Scholar
  • 48 Patrianakos-Hoobler AI, Msall ME, Marks JD, Huo D, Schreiber MD. Risk factors affecting school readiness in premature infants with respiratory distress syndrome. Pediatrics 2009; 124: 258-267
    CrossrefPubMedGoogle Scholar
  • 49 Noble KG, Norman MF, Farah MJ. Neurocognitive correlates of socioeconomic status in kindergarten children. Dev Sci 2005; 8: 74-87
    CrossrefPubMedGoogle Scholar
  • 50 Parker S, Greer S, Zuckerman B. Double jeopardy: the impact of poverty on early child development. Pediatr Clin North Am 1988; 35: 1227-1240
    PubMedGoogle Scholar
  • 51 Huizinga M, Dolan CV, van der Molen MW. Age-related change in executive function: developmental trends and a latent variable analysis. Neuropsychologia 2006; 44: 2017-2036
    CrossrefPubMedGoogle Scholar
  • 52 Luna B, Garver KE, Urban TA, Lazar NA, Sweeney JA. Maturation of cognitive processes from late childhood to adulthood. Child Dev 2004; 75: 1357-1372
    CrossrefPubMedGoogle Scholar
  • 53 Aarnoudse-Moens CS, Duivenvoorden HJ, Weisglas-Kuperus N, Van Goudoever JB, Oosterlaan J. The profile of executive function in very preterm children at 4 to 12 years. Dev Med Child Neurol 2012; 54: 247-253
    CrossrefPubMedGoogle Scholar
  • 54 Luu TM, Ment L, Allan W, Schneider K, Vohr BR. Executive and memory function in adolescents born very preterm. Pediatrics 2011; 127: e639-e646
    CrossrefPubMedGoogle Scholar
  • 55 Pyhälä R, Lahti J, Heinonen K , et al. Neurocognitive abilities in young adults with very low birth weight. Neurology 2011; 77: 2052-2060
    CrossrefPubMedGoogle Scholar
  • 56 Allin M, Walshe M, Fern A , et al. Cognitive maturation in preterm and term born adolescents. J Neurol Neurosurg Psychiatry 2008; 79: 381-386
    CrossrefPubMedGoogle Scholar
  • 57 Farooqi A, Hägglöf B, Serenius F. Behaviours related to executive functions and learning skills at 11 years of age after extremely preterm birth: a Swedish national prospective follow-up study. Acta Paediatr 2013; 102: 625-634
    CrossrefPubMedGoogle Scholar
  • 58 Burnett AC, Scratch SE, Anderson PJ. Executive function outcome in preterm adolescents. Early Hum Dev 2013; 89: 215-220
    CrossrefPubMedGoogle Scholar
  • 59 Rezaie P, Dean A. Periventricular leukomalacia, inflammation and white matter lesions within the developing nervous system. Neuropathology 2002; 22: 106-132
    CrossrefPubMedGoogle Scholar
  • 60 Løhaugen GC, Antonsen I, Håberg A , et al. Computerized working memory training improves function in adolescents born at extremely low birth weight. J Pediatr 2011; 158: 555-561 , e4
    CrossrefPubMedGoogle Scholar
  • 61 Diamond A, Lee K. Interventions shown to aid executive function development in children 4 to 12 years old. Science 2011; 333: 959-964
    CrossrefPubMedGoogle Scholar