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Real-Life Impact of Executive Function Impairments in Adults Who Were Born Very Preterm

Published online by Cambridge University Press:  25 April 2017

Jasmin Kroll ,
Vyacheslav Karolis ,
Philip J. Brittain ,
Chieh-En Jane Tseng ,
Sean Froudist-Walsh ,
Robin M. Murray  and
Chiara Nosarti
Jasmin Kroll*
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, United Kingdom
Vyacheslav Karolis
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, United Kingdom
Philip J. Brittain
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, United Kingdom
Chieh-En Jane Tseng
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, United Kingdom
Sean Froudist-Walsh
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, United Kingdom
Robin M. Murray
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, United Kingdom
Chiara Nosarti
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, United Kingdom
*
Correspondence and reprint requests to: Jasmin Kroll, Department of Psychosis Studies, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, 16 De Crespigny Park, London SE5 8AF, UK. E-mail: jasmin.kroll@kcl.ac.uk
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Abstract

Objectives: Children and adolescents who were born very preterm (≤32 weeks’ gestation) are vulnerable to experiencing cognitive problems, including in executive function. However, it remains to be established whether cognitive deficits are evident in adulthood and whether these exert a significant effect on an individual’s real-lifeachievement. Methods: Using a cross-sectional design, we tested a range of neurocognitive abilities, with a focus on executive function, in a sample of 122 very preterm individuals and 89 term-born controls born between 1979 and 1984. Associations between executive function and a range of achievement measures, indicative of a successful transition to adulthood, were examined. Results: Very preterm adults performed worse compared to controls on measures of intellectual ability and executive function with moderate to large effect sizes. They also demonstrated significantly lower achievement levels in terms of years spent in education, employment status, and on a measure of functioning in work and social domains. Results of regression analysis indicated a stronger positive association between executive function and real-life achievement in the very preterm group compared to controls. Conclusions: Very preterm born adults demonstrate executive function impairments compared to full-term controls, and these are associated with lower achievement in several real-life domains. (JINS, 2017, 23, 381–389)

Keywords

Executive functionVery preterm adultAchievementIntelligenceNeuropsychologyPremature birth
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 23 , Issue 5 , May 2017 , pp. 381 - 389
Copyright
Copyright © The International Neuropsychological Society 2017 

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References

Aarnoudse-Moens, C.S., Duivenvoorden, H.J., Weisglas-Kuperus, N., Van Goudoever, J.B., & Oosterlaan, J. (2012). The profile of executive function in very preterm children at 4 to 12 years. Developmental Medicine and Child Neurology, 54(3), 247–253. doi: 10.1111/j.1469-8749.2011.04150.x Google Scholar
Aarnoudse-Moens, C.S., Smidts, D.P., Oosterlaan, J., Duivenvoorden, H.J., & Weisglas-Kuperus, N. (2009). Executive function in very preterm children at early school age. Journal of Abnormal Child Psychology, 37(7), 981–993. doi: 10.1007/s10802-009-9327-z Google Scholar
Aarnoudse-Moens, C.S., Weisglas-Kuperus, N., Duivenvoorden, H.J., van Goudoever, J.B., & Oosterlaan, J. (2013). Executive function and IQ predict mathematical and attention problems in very preterm children. PLoS One, 8(2), e55994. doi: 10.1371/journal.pone.0055994 Google Scholar
Aarnoudse-Moens, C.S., Weisglas-Kuperus, N., van Goudoever, J.B., & Oosterlaan, J. (2009). Meta-analysis of neurobehavioral outcomes in very preterm and/or very low birth weight children. Pediatrics, 124(2), 717–728. doi: 10.1542/peds.2008-2816 Google Scholar
Allen, M.C., Cristofalo, E., & Kim, C. (2010). Preterm birth: Transition to adulthood. Developmental Disabilities Research Reviews, 16(4), 323–335. doi: 10.1002/ddrr.128 Google Scholar
Anderson, P., & Doyle, L.W. (2003). Neurobehavioral outcomes of school-age children born extremely low birth weight or very preterm in the 1990s. The Journal of the American Medical Association, 289(24), 3264–3272.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(1), 50–57.Google Scholar
Basten, M., Jaekel, J., Johnson, S., Gilmore, C., & Wolke, D. (2015). Preterm birth and adult wealth: Mathematics skills count. Psychological Science, 26(10), 1608–1619. doi: 10.1177/0956797615596230 Google Scholar
Benton, A.L., & Hamsher, K.D. (1976). Multilingual Aphasia Examination. Iowa City: University of Iowa.Google Scholar
Breeman, L.D., Jaekel, J., Baumann, N., Bartmann, P., & Wolke, D. (2015). Preterm cognitive function into adulthood. Pediatrics, 136(3), 415–423. doi: 10.1542/peds.2015-0608 Google Scholar
Brown, T.T., Kuperman, J.M., Chung, Y., Erhart, M., McCabe, C., Hagler, D.J., & Dale, A.M. (2012). Neuroanatomical assessment of biological maturity. Current Biology, 22(18), 1693–1698.Google Scholar
Burgess, P.W., & Shallice, T. (1997). The Hayling and Brixton Tests. Bury St. Edmunds: Thames Valley Test Company.Google Scholar
Burnett, A.C., Scratch, S.E., & Anderson, P.J. (2013). Executive function outcome in preterm adolescents. Early Human Development, 89(4), 215–220. doi: 10.1016/j.earlhumdev.2013.01.013 Google Scholar
Cheong, J.L., Anderson, P.J., Roberts, G., Burnett, A.C., Lee, K.J., Thompson, D.K., & Doyle, L.W. (2013). Contribution of brain size to IQ and educational underperformance in extremely preterm adolescents. PLoS One, 8(10), e77475. doi: 10.1371/journal.pone.0077475 Google Scholar
Cheong, J.L., Thompson, D.K., Wang, H.X., Hunt, R.W., Anderson, P.J., Inder, T.E., & Doyle, L.W. (2009). Abnormal white matter signal on MR imaging is related to abnormal tissue microstructure. AJNR American Journal of Neuroradiology, 30(3), 623–628. doi: 10.3174/ajnr.A1399 Google Scholar
Cohen, J. (1992). A power primer. Psychological Bulletin, 112(1), 155–159.Google Scholar
Conners, C.K. (2000). Conners’ continuous performance test II: Technical guide. Toronto, Canada: Multi-Health Systems.Google Scholar
Cooke, R.W. (2004). Health, lifestyle, and quality of life for young adults born very preterm. Archives of Disease in Childhood, 89(3), 201–206.Google Scholar
Dahlin, E., Nyberg, L., Backman, L., & Neely, A.S. (2008). Plasticity of executive functioning in young and older adults: Immediate training gains, transfer, and long-term maintenance. Psychology and Aging, 23(4), 720–730. doi: 10.1037/a0014296 Google Scholar
De Luca, C.R., Wood, S.J., Anderson, V., Buchanan, J.A., Proffitt, T.M., Mahony, K., & Pantelis, C. (2003). Normative data from the CANTAB. I: Development of executive function over the lifespan. Journal of Clinical and Experimental Neuropsychology, 25(2), 242–254. doi: 10.1076/jcen.25.2.242.13639 Google Scholar
Delobel-Ayoub, M., Arnaud, C., White-Koning, M., Casper, C., Pierrat, V., Garel, M., & Group, E.S. (2009). Behavioral problems and cognitive performance at 5 years of age after very preterm birth: The EPIPAGE Study. Pediatrics, 123(6), 1485–1492. doi: 10.1542/peds.2008-1216 Google Scholar
Eryigit Madzwamuse, S., Baumann, N., Jaekel, J., Bartmann, P., & Wolke, D. (2015). Neuro-cognitive performance of very preterm or very low birth weight adults at 26 years. Journal of Child Psychology and Psychiatry, and allied disciplines, 56(8), 857–864. doi: 10.1111/jcpp.12358 Google Scholar
Fray, P.J., Robbins, T.W., & Sahakian, B.J. (1996). Neuorpsychiatyric applications of CANTAB International. Journal of Geriatric Psychiatry Volume 11, Issue 4. International Journal of Geriatric Psychiatry, 11(4), 329–336.Google Scholar
Froudist-Walsh, S., Karolis, V., Caldinelli, C., Brittain, P.J., Kroll, J., Rodriguez-Toscano, E., … Nosarti, C. (2015). Very early brain damage leads to remodeling of the working memory system in adulthood: A combined fMRI/tractography study. The Journal of Neuroscience, 35(48), 15787–15799. doi: 10.1523/JNEUROSCI.4769-14.2015 Google Scholar
Goodman, S.H., Sewell, D.R., Cooley, E.L., & Leavitt, N. (1993). Assessing levels of adaptive functioning: The Role Functioning Scale. Community Mental Health Journal, 29(2), 119–131.Google Scholar
Grunewaldt, K.H., Lohaugen, G.C., Austeng, D., Brubakk, A.M., & Skranes, J. (2013). Working memory training improves cognitive function in VLBW preschoolers. Pediatrics, 131(3), e747–e754. doi: 10.1542/peds.2012-1965 Google Scholar
Hack, M. (2009). Adult outcomes of preterm children. Journal of Developmental & Behavioral Pediatrics, 30(5), 460–470. doi: 10.1097/DBP.0b013e3181ba0fba Google Scholar
Hallin, A.-L., Hellström-Westas, L., & Stjernqvist, K. (2010). Follow-up of adolescents born extremely preterm cognitive function and health at 18 years of age. Acta Paediatrica, 99(9), 1401–1406.Google Scholar
Heinonen, K., Pesonen, A.K., Lahti, J., Pyhälä, R., Strang-Karlsson, S., Hovi, P., & Raikkonen, K. (2012). Self- and parent-rated executive functioning in young adults with very low birth weight. Pediatrics, 131(1), e243–250.Google Scholar
HMSO. (1991). Registrar General Office of Population Censuses and Surveys, Standard Occupational Classification. London: HMSO.Google Scholar
Hsu, N.S., Novick, J.M., & Jaeggi, S.M. (2014). The development and malleability of executive control abilities. Frontiers in Behavioral Neuroscience, 8, 221. doi: 10.3389/fnbeh.2014.00221 Google Scholar
Joseph, R.M., O–Shea, T.M., Allred, E.N., Heeren, T., Hirtz, D., Jara, H., & Kuban, K.C.K. for the ELGAN Study Investigators (2016). Neurocognitive and Academic Outcomes at Age 10 Years of Extremely Preterm Newborns. Pediatrics, 137(4), e20154343.CrossRefGoogle ScholarPubMed
Karolis, V.R., Froudist-Walsh, S., Brittain, P.J., Kroll, J., Ball, G., Edwards, A.D., & Nosarti, C. (2016). Reinforcement of the Brain’s Rich-Club architecture following early neurodevelopmental disruption caused by very preterm birth. Cerebral Cortex, 26(3), 1322–1335. doi: 10.1093/cercor/bhv305 Google Scholar
Kerr-Wilson, C.O., Mackay, D.F., Smith, G.C., & Pell, J.P. (2012). Meta-analysis of the association between preterm delivery and intelligence. Journal of Public Health (Oxford, England), 34(2), 209–216. doi: 10.1093/pubmed/fdr024 Google Scholar
Lindstrom, K., Lindblad, F., & Hjern, A. (2009). Psychiatric morbidity in adolescents and young adults born preterm: A Swedish national cohort study. Pediatrics, 123(1), e47–e53.Google Scholar
Lindstrom, K., Winbladh, B., Haglund, B., & Hjern, A. (2007). Preterm infants as young adults: A Swedish national cohort study. Pediatrics, 120(1), 70–77.Google Scholar
Lohaugen, G.C., Antonsen, I., Haberg, A., Gramstad, A., Vik, T., Brubakk, A.M., & Skranes, J. (2011). Computerized working memory training improves function in adolescents born at extremely low birth weight. Journal of Pediatrics, 158(4), 555–561 e554. doi:10.1016/j.jpeds.2010.09.060.Google Scholar
Lohaugen, G.C., Gramstad, A., Evensen, K.A., Martinussen, M., Lindqvist, S., Indredavik, M., & Skranes, J. (2010). Cognitive profile in young adults born preterm at very low birthweight. Developmental Medicine and Child Neurology, 52(12), 1133–1138. doi: 10.1111/j.1469-8749.2010.03743.x Google Scholar
Luu, T.M., Ment, L., Allan, W., Schneider, K., & Vohr, B.R. (2011). Executive and memory function in adolescents born very preterm. Pediatrics, 127(3), e639–e646. doi: 10.1542/peds.2010-1421 Google Scholar
Mathiasen, R., Hansen, B.M., Nybo Anderson, A.M., & Greisen, G. (2009). Socio-economic achievements of individuals born very preterm at the age of 27 to 29 years: A nationwide cohort study. Developmental Medicine & Child Neurology, 51(11), 901–908. doi: 10.1111/j.1469-8749.2009.03331.x Google Scholar
Moster, D., Lie, R.T., & Markestad, T. (2008). Long-term medical and social consequences of preterm birth. New England Journal of Medicine, 359(3), 262–273.Google Scholar
Mulder, H., Pitchford, N.J., Hagger, M.S., & Marlow, N. (2009). Development of executive function and attention in preterm children: A systematic review. Developmental Neuropsychology, 34(4), 393–421. doi: 10.1080/87565640902964524 Google Scholar
Nam, K.W., Castellanos, N., Simmons, A., Froudist-Walsh, S., Allin, M.P., Walshe, M., & Nosarti, C. (2015). Alterations in cortical thickness development in preterm-born individuals: Implications for high-order cognitive functions. Neuroimage, 115, 64–75. doi: 10.1016/j.neuroimage.2015.04.015 Google Scholar
Nosarti, C., & Froudist-Walsh, S. (2016). Alterations in development of hippocampal and cortical memory mechanisms following very preterm birth. Developmental Medicine and Child Neurology, 58(Suppl 4), 35–45. doi: doi:10.1111/dmcn.13042 CrossRefGoogle ScholarPubMed
Nosarti, C., Giouroukou, E., Micali, N., Rifkin, L., Morris, R.G., & Murray, R.M. (2007). Impaired executive functioning in young adults born very preterm. Journal of the International Neuropsychological Society, 13(4), 571–581. doi: 10.1017/S1355617707070725 Google Scholar
Nosarti, C., Murray, R.M., Reichenberg, A., Cnattingius, S., Lambe, M.P., Yin, L., & Hultman, C.M. (2012). Preterm birth and psychiatric disorders in young adult life. Archives of General Psychiatry, 69(6), 610–617.Google Scholar
Nosarti, C., Nam, K.W., Walshe, M., Murray, R.M., Cuddy, M., Rifkin, L., & Allin, M.P. (2014). Preterm birth and structural brain alterations in early adulthood. Neuroimage, Clinical, 6, 180–191. doi: 10.1016/j.nicl.2014.08.005 Google Scholar
Nosarti, C., Walshe, M., Rushe, T.M., Rifkin, L., Wyatt, J., Murray, R.M., & Allin, M.P. (2011). Neonatal ultrasound results following very preterm birth predict adolescent behavioral and cognitive outcome. Developmental Neuropsychology, 36(1), 118–135. doi: 10.1080/87565641.2011.540546 Google Scholar
Petanjek, Z., Judas, M., Simic, G., Rasin, M.R., Uylings, H.B., Rakic, P., & Kostovic, I. (2011). Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proceedings of the National Academy of Sciences of the United States of America, 108(32), 13281–13286. doi: 10.1073/pnas.1105108108 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(12), 1049–1062.Google Scholar
Saigal, S., Day, K.L., Van Lieshout, R.J., Schmidt, L.A., Morrison, K.M., & Boyle, M.H. (2016). Health, wealth, social integration, and sexuality of extremely low-birth-weight prematurely born adults in the fourth decade of life. JAMA Pediatrics, 170(7), 678–686. doi: 10.1001/jamapediatrics.2016.0289 Google Scholar
Saigal, S., Feeny, D., Rosenbaum, P., Furlong, W., Burrows, E., & Stoskopf, B. (1996). Self-perceived health status and health-related quality of life of extremely low-birth-weight infants at adolescence. The Journal of the American Medical Association, 276(6), 453–459.Google Scholar
Saigal, S., Stoskopf, B., Streiner, D., Boyle, M., Pinelli, J., Paneth, N., & Goddeeris, J. (2006). Transition of extremely low-birth-weight infants from adolescence to young adulthood. The Journal of the American Medical Association, 295, 667–675.Google Scholar
Salthouse, T. (2012). Consequences of age-related cognitive declines. Annual Review of Psychology, 63, 201–226. doi: 10.1146/annurev-psych-120710-100328 Google Scholar
Swamy, G.K., Ostbye, T., & Skjaerven, R. (2008). Association of preterm birth with long-term survival, reproduction, and next-generation preterm birth. The Journal of the American Medical Association, 299(12), 1429–1436. doi: 10.1001/jama.299.12.1429 Google Scholar
Tombaugh, T.N. (2004). Trail Making Test A and B: Normative data stratified by age and education. Archives of Clinical Neuropsychology, 19(2), 203–214. doi: 10.1016/S0887-6177(03)00039-8 Google Scholar
Van Lieshout, R.J., Boyle, M.H., Saigal, S., Morrison, K., & Schmidt, L.A. (2015). Mental health of extremely low birth weight survivors in their 30s. Pediatrics, 135(3), 452–459. doi: 10.1542/peds.2014-3143 Google Scholar
Wechsler, D. (1981). Wechsler Adult Intelligence Scale. New York: Psychological Corporation.Google Scholar
Wechsler, D. (1999). Wechsler Abbreviated Scale of Intelligence. New York: The Psychological Corporation.Google Scholar
Weissman, M.M., & Bothwell, S. (1976). Assessment of social adjustment by patient self-report. Archives of General Psychiatry, 33(9), 1111–1115.Google Scholar
Winstanley, A., Lamb, M.E., Ellis-Davies, K., & Rentfrow, P.J. (2015). The subjective well-being of adults born preterm. Journal of Research in Personality, 59, 23–30. doi: http://dx.doi.org/10.1016/j.jrp.2015.09.002 Google Scholar
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(2), 94–109.Google Scholar
Woodward, L.J., Clark, C.A., Bora, S., & Inder, T.E. (2012). Neonatal white matter abnormalities an important predictor of neurocognitive outcome for very preterm children. PLoS One, 7(12), e51879. doi: 10.1371/journal.pone.0051879 Google Scholar