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Impaired executive functioning in young adults born very preterm

Published online by Cambridge University Press:  18 May 2007

CHIARA NOSARTI ,
ELENA GIOUROUKOU ,
NADIA MICALI ,
LARRY RIFKIN ,
ROBIN G. MORRIS  and
ROBIN M. MURRAY
CHIARA NOSARTI
Affiliation:
Division of Psychological Medicine and Psychiatry, Section of General Psychiatry, Institute of Psychiatry and Kings College London, London, United Kingdom
ELENA GIOUROUKOU
Affiliation:
Division of Psychological Medicine and Psychiatry, Section of General Psychiatry, Institute of Psychiatry and Kings College London, London, United Kingdom
NADIA MICALI
Affiliation:
Department of Child & Adolescent Psychiatry, Institute of Psychiatry and Kings College London, London, United Kingdom
LARRY RIFKIN
Affiliation:
Division of Psychological Medicine and Psychiatry, Section of General Psychiatry, Institute of Psychiatry and Kings College London, London, United Kingdom
ROBIN G. MORRIS
Affiliation:
Department of Neurodegeneration & Brain Injury and Department of Psychology, Institute of Psychiatry and Kings College London, London, United Kingdom
ROBIN M. MURRAY
Affiliation:
Division of Psychological Medicine and Psychiatry, Section of General Psychiatry, Institute of Psychiatry and Kings College London, London, United Kingdom
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Abstract

Individuals born very preterm (VPT) are at increased risk of perinatal brain injury and long-term cognitive and behavioral problems. Executive functioning, in particular, has been shown to be impaired in VPT children and adolescents. This study prospectively assessed executive function in young adults who were born VPT (<33 weeks of gestation) [n = 61; mean age, 22.25 (±1.07) years; range, 20.62–24.78 years] and controls [n = 64; mean age, 23.20 (±1.48) years; range, 19.97–25.46 years]. Tests used comprised the Wechsler Abbreviated Scale of Intelligence (WASI), the Hayling Sentence Completion Test (HSCT), the Controlled Oral Word Association Test (COWAT), the Animal and Object test, the Trail-Making Test (TMT), and the Test of Attentional Performance (TAP). VPT participants showed specific executive function impairments in tasks involving response inhibition and mental flexibility, even when adjusting for IQ, gender, and age. No significant associations were observed between executive function test scores and perinatal variables or neonatal ultrasound classification. The results suggest that, although free from major physical disability, VPT young adults perform worse than controls on tasks involving selective aspects of executive processing, such as mental flexibility and response inhibition. (JINS, 2007, 13, 571–581.)

Keywords

Premature birthGestational ageNeuropsychologyWechsler ScalesInhibition (Psychology)Cognition
Type
Research Article
Information
Journal of the International Neuropsychological Society , Volume 13 , Issue 4 , July 2007 , pp. 571 - 581
Copyright
© 2007 The International Neuropsychological Society

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References

REFERENCES

Abernethy, L.J., Cooke, R.W., & Foulder-Hughes, L. (2004). Caudate and hippocampal volumes, intelligence, and motor impairment in 7-year-old children who were born preterm. Pediatric Research, 55, 884–893.Google Scholar
Abrahams, S., Leigh, P.N., Harvey, A., Vythelingum, G.N., Grise, D., & Goldstein, L.H. (2000). Verbal fluency and executive dysfunction in amyotrophic lateral sclerosis (ALS). Neuropsychologia, 38, 734–747.Google Scholar
Allin, M., Matsumoto, H., Santhouse, A.M., Nosarti, C., Al-Asady, M.H., Stewart, A.L., Rifkin, L., & Murray, R.M. (2001). Cognitive and motor function and the size of the cerebellum in adolescents born very pre-term. Brain, 124(Pt. 1), 60–66.Google Scholar
Allin, M., Nosarti, C., Rifkin, L., & Murray, R.M. (2004). Brain plasticity and long term function after early cerebral insult: The example of very preterm birth. In M.S. Keshavan, J.L. Kennedy, & R.M. Murray (Eds.), Neurodevelopment and schizophrenia. Cambridge: Cambridge University Press.
Allin, M., Rooney, M., Cuddy, M., Wyatt, J., Walshe, M., Rifkin, L., & Murray, R. (2006a). Personality in young adults who are born preterm. Pediatrics, 117, 309–316.Google Scholar
Allin, M., Rooney, M., Griffiths, T., Cuddy, M., Wyatt, J., Rifkin, L., & Murray, R. (2006b). Neurological abnormalities in young adults born preterm. Journal of Neurology, Neurosurgery and Psychiatry, 77, 495–499.Google Scholar
Anderson, P.J. & Doyle, L.W. (2004). Executive functioning in school-aged children who were born very preterm or with extremely low birth weight in the 1990s. Pediatrics, 114, 50–57.Google Scholar
Aylward, G.P. (2002). Cognitive and neuropsychological outcomes: More than IQ scores. Mental Retardation and Developmental Disabilities Research Reviews, 8, 234–240.Google Scholar
Bayless, S. & Stevenson, J. (2006). Executive functions in school-age children born very prematurely. Early Human Development, Jul 10 [Epub ahead of print].Google Scholar
Benton, A.L. & Hamsher, K.D. (1976). Multilingual aphasia examination. Iowa City: University of Iowa.
Bland, M. (1995). An introduction to medical statistics. Oxford: Oxford University Press.
Bohm, B., Smedler, A.C., & Forssberg, H. (2004). Impulse control, working memory and other executive functions in preterm children when starting school. Acta Paediatrica, 93, 1363–1371.Google Scholar
Breslau, N., Chilcoat, H., DelDotto, J., Andreski, P., & Brown, G. (1996). Low birth weight and neurocognitive status at six years of age. Biological Psychiatry, 40, 389–397.Google Scholar
Breslau, N., Chilcoat, H.D., Johnson, E.O., Andreski, P., & Lucia, V.C. (2000). Neurologic soft signs and low birthweight: Their association and neuropsychiatric implications. Biological Psychiatry, 47, 71–79.Google Scholar
Burgess, P.W. & Shallice, T. (1996). Response suppression, initiation and strategy use following frontal lobe lesions. Neuropsychologia, 34, 263–272.Google Scholar
Burgess, P.W. & Shallice, T. (1997). The Hayling and Brixton Tests. Bury St. Edmunds: Thames Valley Test Company.
Cooke, R.W. (2004). Health, lifestyle, and quality of life for young adults born very preterm. Archives of Disease in Childhood, 89, 201–206.Google Scholar
Cooke, R.W. (2005). Perinatal and postnatal factors in very preterm infants and subsequent cognitive and motor abilities. Archives of Disease in Childhood. Fetal and Neonatal Edition, 90, F60–F63.Google Scholar
Curtis, W.J., Lindeke, L.L., Georgieff, M.K., & Nelson, C.A. (2002). Neurobehavioural functioning in neonatal intensive care unit graduates in late childhood and early adolescence. Brain, 125(Pt. 7), 1646–1659.Google Scholar
Espy, K.A., Stalets, M.M., McDiarmid, M.M., Senn, T.E., Cwik, M.F., & Hamby, A. (2002). Executive functions in preschool children born preterm: Application of cognitive neuroscience paradigms. Neuropsychology, Development, and Cognition. Section C, Child Neuropsychology, 8, 83–92.Google Scholar
Faust, M.E., Balota, D.A., Spieler, D.H., & Ferraro, F.R. (1999). Individual differences in information-processing rate and amount: Implications for group differences in response latency. Psychological Bulletin, 125, 777–799.Google Scholar
Fawer, C.L., Besnier, S., Forcada, M., Buclin, T., & Calame, A. (1995). Influence of perinatal, developmental and environmental factors on cognitive abilities of preterm children without major impairments at 5 years. Early Human Development, 43, 151–164.Google Scholar
Feingold, E., Sheir-Neiss, G., Melnychuk, J., Bachrach, S., & Paul, D. (2002). HRQL and severity of brain ultrasound findings in a cohort of adolescents who were born preterm. Journal of Adolescent Health, 31, 234–239.Google Scholar
Foulder-Hughes, L.A. & Cooke, R.W. (2003). Motor, cognitive, and behavioural disorders in children born very preterm. Developmental Medicine and Child Neurology, 45, 97–103.Google Scholar
Gabrielson, J., Hard, A.L., Ek, U., Svensson, E., Carlsson, G., & Hellstrom, A. (2002). Large variability in performance IQ associated with postnatal morbidity, and reduced verbal IQ among school-aged children born preterm. Acta Paediatrica, 91, 1371–1378.Google Scholar
Gale, C.R. & Martyn, C.N. (2004). Birth weight and later risk of depression in a national birth cohort. The British Journal of Psychiatry, 184, 28–33.Google Scholar
Goodglass, H. & Kaplan, E. (1972). Assessment of aphasia and related disorders. Philadelphia: Lippincott Williams & Wilkins.
Hack, M. & Fanaroff, A.A. (1999). Outcomes of children of extremely low birthweight and gestational age in the 1990's. Early Human Development, 53, 193–218.Google Scholar
Hack, M., Flannery, D.J., Schluchter, M., Cartar, L., Borawski, E., & Klein, N. (2002). Outcomes in young adulthood for very-low-birth-weight infants. The New England Journal of Medicine, 346, 149–157.Google Scholar
Hack, M. & Taylor, H.G. (2000). Perinatal brain injury in preterm infants and later neurobehavioral function. Journal of the American Medical Association, 284, 1973–1974.Google Scholar
Harvey, J.M., O'Callaghan, M.J., & Mohay, H. (1999). Executive function of children with extremely low birthweight: A case control study. Developmental Medicine and Child Neurology, 41, 292–297.Google Scholar
Her Majesty's Stationary Office (HMSO). (1991). Office of Population Censuses and Surveys, Standard Occupational Classification. London: HMSO.
Hertzig, M.E. (1981). Neurological ‘soft’ signs in low-birthweight children. Developmental Medicine and Child Neurology, 23, 778–791.Google Scholar
Inder, T.E., Wells, S.J., Mogridge, N.B., Spencer, C., & Volpe, J.J. (2003). Defining the nature of the cerebral abnormalities in the premature infant: A qualitative magnetic resonance imaging study. The Journal of Pediatrics, 143, 171–179.Google Scholar
Jefferis, B.J., Power, C., & Hertzman, C. (2002). Birth weight, childhood socioeconomic environment, and cognitive development in the 1958 British birth cohort study. British Medical Journal, 325, 305.Google Scholar
Klein, N., Hack, M., Gallagher, J., & Fanaroff, A.A. (1985). Preschool performance of children with normal intelligence who were very low-birth-weight infants. Pediatrics, 75, 531–537.Google Scholar
Luciana, M., Lindeke, L., Georgieff, M., Mills, M., & Nelson, C.A. (1999). Neurobehavioral evidence for working-memory deficits in school-aged children with histories of prematurity. Developmental Medicine and Child Neurology, 41, 521–533.Google Scholar
Nosarti, C., Al Asady, M.H., Frangou, S., Stewart, A.L., Rifkin, L., & Murray, R.M. (2002). Adolescents who were born very preterm have decreased brain volumes. Brain, 125(Pt. 7), 1616–1623.Google Scholar
Nosarti, C., Allin, M., Frangou, S., Rifkin, L., & Murray, R. (2005). Decreased caudate volume is associated with hyperactivity in adolescents born very preterm. Biological Psychiatry, 13, 339.Google Scholar
Nosarti, C., Rubia, K., Smith, A., Frearson, S., Williams, S.C., Rifkin, L., & Murray, K.M. (2006). Altered functional neuroanatomy of response inhibition in adolescent males who were born very preterm. Developmental Medicine and Child Neurology, 48, 265–271.Google Scholar
Nosarti, C., Rushe, T.M., Woodruff, P.W., Stewart, A.L., Rifkin, L., & Murray, R.M. (2004). Corpus callosum size and very preterm birth: Relationship to neuropsychological outcome. Brain, 127, 2080–2089.Google Scholar
Olsen, P., Vainionpaa, L., Paakko, E., Korkman, M., Pyhtinen, J., & Jarvelin, M.R. (1998). Psychological findings in preterm children related to neurologic status and magnetic resonance imaging. Pediatrics, 102(Pt. 1), 329–336.Google Scholar
Patra, K., Wilson-Costello, D., Taylor, H.G, Mercuri-Minich, N., & Hack, M. (2006). Grades I-II intraventricular hemorrhage in extremely low birth weight infants. Effects on neurodevelopment. Journal of Pediatrics, 149, 169–173.Google Scholar
Peng, Y., Huang, B., Biro, F., Feng, L., Guo, Z., & Slap, G. (2005). Outcome of low birthweight in China: A 16-year longitudinal study. Acta Paediatrica, 94, 843–849.Google Scholar
Peterson, B.S., Anderson, A.W., Ehrenkranz, R., Staib, L.H., Tageldin, M., Colson, E., Gore, J.C., Duncan, C.C., Makuch, R., & Ment, L.R. (2003). Regional brain volumes and their later neurodevelopmental correlates in term and preterm infants. Pediatrics, 111(Pt 1), 939–948.Google Scholar
Peterson, B.S., Vohr, B., Staib, L.H., Cannistraci, C.J., Dolberg, A., Schneider, K.C., Katz, K.H., Westerveld, M., Sparrow, S., Anderson, A.W., Duncan, C.C., Makuch, R.W., Gore, J.C., & Ment, L.R. (2000). Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. Journal of the American Medical Association, 284, 1939–1947.Google Scholar
Pharoah, P.O., Stevenson, C.J., & West, C.R. (2003). General certificate of secondary education performance in very low birthweight infants. Archives of Disease in Childhood, 88, 295–298.Google Scholar
Reitan, R.M. & Wolfson, D. (1985). The Halstead-Reitan neuropsychological test battery. Tucson: Neuropsychology Press.
Rickards, A.L., Ford, G.W., Kitchen, W.H., Doyle, L.W., Lissenden, J.V., & Keith, C.G. (1987). Extremely-low-birthweight infants: Neurological, psychological, growth and health status beyond five years of age. Medical Journal of Australia, 147, 476–481.Google Scholar
Rickards, A.L., Kelly, E.A., Doyle, L.W., & Callanan, C. (2001). Cognition, academic progress, behavior and self-concept at 14 years of very low birth weight children. Journal of Developmental & Behavioral Pediatrics, 22, 11–18.Google Scholar
Roth, S.C., Baudin, J., McCormick, D.C., Edwards, A.D., Townsend, J., Stewart, A.L., & Reynolds, E.O.R. (1993). Relation between ultrasound appearance of the brain of very preterm infants and neurodevelopmental impairment at eight years. Developmental Medicine and Child Neurology, 35, 755–768.Google Scholar
Roth, S.C., Baudin, J., Pezzani-Goldsmith, M., Townsend, J., Reynolds, E.O., & Stewart, A.L. (1994). Relation between neurodevelopmental status of very preterm infants at one and eight years. Developmental Medicine and Child Neurology, 36, 1049–1062.Google Scholar
Rose, S.A. & Feldman, J.F. (1996). Memory and processing speed in preterm children at eleven years: A comparison with full-terms. Child Development, 67, 2005–2021.Google Scholar
Rose, S.A., Feldman, J.F., & Jankowski, J.J. (2002). Processing speed in the 1st year of life: A longitudinal study of preterm and full-term infants. Developmental Psychology, 38, 895–902.Google Scholar
Rubia, K., Smith, A.B., Woolley, J., Nosarti, C., Heyman, I., Taylor, E., & Brammer, M. (2006). Progressive increase of frontostriatal brain activation from childhood to adulthood during event-related tasks of cognitive control. Human Brain Mapping, 27, 973–993.Google Scholar
Rushe, T.M., Rifkin, L., Stewart, A.L., Townsend, J.P., Roth, S.C., Wyatt, J.S., & Murray, R.M. (2001). Neuropsychological outcome at adolescence of very preterm birth and its relation to brain structure. Developmental Medicine and Child Neurology, 43, 226–233.Google Scholar
Saigal, S. (2000). Follow-up of very low birthweight babies to adolescence. Seminars in Neonatology, 5, 107–118.Google Scholar
Sherlock, R.L., Anderson, P.J., & Doyle, L.W. (2005). Neurodevelopmental sequelae of intraventricular haemorrhage at 8 years of age in a regional cohort of ELBW/very preterm infants. Early Human Development, 81, 909–916.Google Scholar
Spreen, O. & Strauss, E. (1991). A compendium of neuropsychological tests. New York: Oxford University Press.
St. Clair-Thompson, H.L. & Gathercole, S.E. (2006). Executive functions and achievements in school: Shifting, updating, inhibition, and working memory. The Quarterly Journal of Experimental Psychology, 59, 745–759.Google Scholar
Stewart, A.L., Rifkin, L., Amess, P.N., Kirkbride, V., Townsend, J.P., Miller, D.H., Lewis, S.W., Kingsley, D.P.E., Moseley, I.F., Foster, O., & Murray, R.M. (1999). Brain structure and neurocognitive and behavioural function in adolescents who were born very preterm. Lancet, 353, 1653–1657.Google Scholar
Stewart, A.L., Thorburn, R.J., Hope, P.L., Goldsmith, M., Lipscomb, A.P., & Reynolds, E.O. (1983). Ultrasound appearance of the brain in very preterm infants and neurodevelopmental outcome at 18 months of age. Archives of Disease in Childhood, 58, 598–604.Google Scholar
Stiles, J., Reilly, J., Paul, B., & Moses, P. (2005). Cognitive development following early brain injury: Evidence for neural adaptation. Trends in Cognitive Sciences, 9, 136–143.Google Scholar
Sullivan, M.C. & Margaret, M.M. (2003). Perinatal morbidity, mild motor delay, and later school outcomes. Developmental Medicine and Child Neurology, 45, 104–112.Google Scholar
Taylor, H., Hack, M., & Klein, N. (1998). Attention deficits in children with < 750 gm birth weight. Child Neuropsychologia, 4, 21–34.Google Scholar
Taylor, H.G., Minich, N., Bangert, B., Filipek, P.A., & Hack, M. (2004b). Long-term neuropsychological outcomes of very low birth weight: Associations with early risks for periventricular brain insults. Journal of the International Neuropsychological Society, 10, 987–1004.Google Scholar
Taylor, H.G., Minich, N.M., Klein, N., & Hack, M. (2004a). Longitudinal outcomes of very low birth weight: Neuropsychological findings. Journal of the International Neuropsychological Society, 10, 149–163.Google Scholar
Tideman, E. (2000). Longitudinal follow-up of children born preterm: Cognitive development at age 19. Early Human Development, 58, 81–90.Google Scholar
United Nations Children's Fund and World Health Organization. (2004). Low birthweight: Country, regional and global estimates. New York: UNICEF.
Vohr, B.R., Garcia-Coll, C., & Oh, W. (1989). Language and neurodevelopmental outcome of low-birthweight infants at three years. Developmental Medicine and Child Neurology, 31, 582–590.Google Scholar
Vollmer, B., Roth, S., Baudin, J., Stewart, A.L., Neville, B.G., & Wyatt, J.S. (2003). Predictors of long-term outcome in very preterm infants: Gestational age versus neonatal cranial ultrasound. Pediatrics, 112, 1108–1114.Google Scholar
Volpe, J.J. (1995). Neurological evaluation; Hypoxic-ischemic encephalopathy; and Intracranial hemorrhage. In J.J. Volpe (Ed.), Neurology of the newborn. Philadelphia: Saunders.
Volpe, J.J. (2003). Cerebral white matter injury of the premature infant-more common than you think. Pediatrics, 112(Pt. 1), 176–180.Google Scholar
Waber, D.P. & McCormick, M.C. (1995). Late neuropsychological outcomes in preterm infants of normal IQ: Selective vulnerability of the visual system. Journal of Pediatric Psychology, 20, 721–735.Google Scholar
Wechsler, D. (1974). Manual for the Wechsler Intelligence Scale for Children–Revised. New York: The Psychological Cooperation.
Wechsler, D. (1999). Wechsler Abbreviated Scale of Intelligence. New York: The Psychological Corporation.
Wolke, D. & Meyer, R. (1999). Cognitive status, language attainment, and prereading skills of 6-year-old very preterm children and their peers: The Bavarian Longitudinal Study. Developmental Medicine and Child Neurology, 41, 94–109.Google Scholar
Woodward, L.J., Anderson, P.J., Austin, N.C., Howard, K., & Inder, T.E. (2006). Neonatal MRI to predict neurodevelopmental outcomes in preterm infants. The New England Journal of Medicine, 355, 685–694.Google Scholar
Woodward, L.J., Edgin, J.O., Thompson, D., & Inder, T.E. (2005). Object working memory deficits predicted by early brain injury and development in the preterm infant. Brain, 128(Pt. 11), 2578–2587.Google Scholar
Yliherva, A., Olsen, P., & Jarvelin, M.R. (2001). Linguistic skills in relation to neurological findings at 8 years of age in children born preterm. Logopedics, Phoniatrics, Vocology, 26, 66–75.Google Scholar
Zimmerman, P. & Fimm, B. (1995). Test of Attentional Performance (TAP). Wurselen: Psytest.