Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-05T22:09:04.580Z Has data issue: false hasContentIssue false
  • English
  • Français

Extremely low birth weight babies grown up: Gene–environment interaction predicts internalizing problems in the third and fourth decades of life

Published online by Cambridge University Press:  15 July 2016

Ayelet Lahat ,
Ryan J. van Lieshout ,
Karen J. Mathewson ,
James Mackillop ,
Saroj Saigal ,
Katherine M. Morrison ,
Michael H. Boyle  and
Louis A. Schmidt
Ayelet Lahat*
Affiliation:
McMaster University
Ryan J. van Lieshout
Affiliation:
McMaster University
Karen J. Mathewson
Affiliation:
McMaster University
James Mackillop
Affiliation:
McMaster University
Saroj Saigal
Affiliation:
McMaster University
Katherine M. Morrison
Affiliation:
McMaster University
Michael H. Boyle
Affiliation:
McMaster University
Louis A. Schmidt
Affiliation:
McMaster University
*
Address correspondence and reprint requests to: Ayelet Lahat, Department of Psychology, Neuroscience & Behaviour, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4K1, Canada; E-mail: lahata@mcmaster.ca.
Get access Rights & Permissions [Opens in a new window]

Abstract

Extremely low birth weight (ELBW; <1000 g) infants have been exposed to stressful intrauterine and early postnatal environments. Even greater early adversity has been experienced by ELBW survivors who were also born small for gestational age (SGA; <10th percentile for GA) compared to those born appropriate for GA (AGA). ELBW survivors, particularly those born SGA, face increased risk for internalizing problems compared to normal BW (NBW; ≥2500 g) controls. Internalizing problems are related to allelic variations in the promoter region of the serotonin transporter linked polymorphic region gene (5-HTTLPR). We followed the oldest longitudinal cohort of ELBW survivors to adulthood. Participants provided buccal cells and reported on internalizing problems, using the Young Adult Self-Report when they were in their mid-20s (ELBW/SGA, N = 28; ELBW/AGA, N = 60; NBW, N = 81) and mid-30s (ELBW/SGA, N = 27; ELBW/AGA, N = 58; NBW, N = 76). The findings indicate that ELBW/SGAs carrying the 5-HTTLPR short allele reported increased internalizing problems, particularly depression, during the third and fourth decades of life. This is the first known report on gene–environment interactions predicting psychopathology among ELBW survivors. Our findings elucidate putative neurobiological pathways that underlie risk for psychopathology.

Type
Regular Articles
Information
Development and Psychopathology , Volume 29 , Issue 3 , August 2017 , pp. 837 - 843
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

This research was supported by Canadian Institutes of Health Research Grants CIHR:TMH-103145 (to L.A.S) and CIHR:MOP42536 (to S.S.) and National Institute of Child Health and Human Development Grant NICHD:1-R01HD40219 (to S.S.). This research was also supported by a Social Sciences and Humanities Research Council Banting Post-Doctoral Fellowship (to A.L.) and the Peter Boris Chair in Addictions Research (to J.M.). We thank the study participants and their families for their continued participation in this work and Paz Fortier, Sue McKee, Vladimir Miskovic, Jordana Waxman, and Shirien Yunus for their help with data collection and data entry. We also thank Jane Foster for performing the genotyping.

References

Achenbach, T. M. (1997). Manual for the Young Adult Self-Report and Young Adult Behavior Checklist. Burlington, VT: University of Vermont, Department of Psychiatry.Google Scholar
Achenbach, T. M., Bernstein, A., & Dumenci, L. (2005). DSM-oriented scales and statistically based syndromes for ages 18 to 59: Linking taxonomic paradigms to facilitate multitaxonomic approaches. Journal of Personality Assessment, 84, 49–63.Google Scholar
Achenbach, T. M., & Rescorla, L. A. (2001). Manual for the ASEBA School-Age Forms & Profiles: An integrated system of multi-informant assessment. Burlington, VT: University of Vermont, Department of Psychiatry.Google Scholar
American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders (4th ed.). Washington, DC: Author.Google Scholar
Anderson, P., Doyle, L. W., & Group, V. I. C. S. (2003). Neurobehavioral outcomes of school-age children born extremely low birth weight or very preterm in the 1990s. Journal of the American Medical Association, 289, 3264–3272.CrossRefGoogle ScholarPubMed
Benjet, C., Thompson, R. J., & Gotlib, I. H. (2010). 5-HTTLPR moderates the effect of relational peer victimization on depressive symptoms in adolescent girls. Journal of Child Psychology and Psychiatry, 51, 173–179.CrossRefGoogle ScholarPubMed
Botting, N., Powls, A., Cooke, R. W., & Marlow, N. (1997). Attention deficit hyperactivity disorders and other psychiatric outcomes in very low birthweight children at 12 years. Journal of Child Psychology and Psychiatry, 38, 931–941.CrossRefGoogle Scholar
Boyle, M. H., Miskovic, V., Van Lieshout, R. J., Duncan, L., Schmidt, L. A., Hoult, L., et al. (2011). Psychopathology in young adults born at extremely low birth weight. Psychological Medicine, 41, 1763–1774.Google Scholar
Caspi, A., Hariri, A. R., Holmes, A., Uher, R., & Moffitt, T. E. (2010). Genetic sensitivity to the environment: The case of the serotonin transporter gene and its implications for studying complex diseases and traits. American Journal of Psychiatry, 167, 509–527.Google Scholar
Caspi, A., Sugden, K., Moffitt, T. E., Taylor, A., Craig, I. W., Harrington, H., et al. (2003). Influence of life stress on depression: Moderation by a polymorphism in the 5-HTT gene. Science, 301, 386–389.Google Scholar
Chau, C. M. Y., Ranger, M., Sulistyoningrum, D., Devlin, A. M., Oberlander, T., & Grunau, R. E. (2014). Neonatal pain and COMT Val158Met genotype in relation to serotonin transporter (SLC6A4) promoter methylation in very preterm children at school age. Frontiers in Behavioral Neuroscience. Retrieved from http://dx.doi.org/10.3389/fnbeh.2014.00409 Google Scholar
Conrad, A. L., Richman, L., Lindgren, S., & Nopoulos, P. (2010). Biological and environmental predictors of behavioral sequelae in children born preterm. Pediatrics, 125, e83–e89.Google Scholar
Engle, W. A., Tomashek, K. M., & Wallman, C. (2007). “Late-preterm” infants: A population at risk. Pediatrics, 120, 1390–1401.CrossRefGoogle ScholarPubMed
Farooqi, A., Hägglöf, B., Sedin, G., Gothefors, L., & Serenius, F. (2007). Mental health and social competencies of 10- to 12-year-old children born at 23 to 25 weeks of gestation in the 1990s: A Swedish national prospective follow-up study. Pediatrics, 120, 118–133.Google Scholar
Hack, M., Taylor, H. G., Schluchter, M., Andreias, L., Drotar, D., & Klein, N. (2009). Behavioral outcomes of extremely low birth weight children at age 8 years. Journal of Developmental and Behavioral Pediatrics, 30, 122–130.Google Scholar
Hariri, A. R., Mattay, V. S., Tessitore, A., Kolachana, B., Fera, F., Goldman, D., et al. (2002). Serotonin transporter genetic variation and the response of the human amygdala. Science, 297, 400–403.CrossRefGoogle ScholarPubMed
Heils, A., Teufel, A., Petri, S., Stöber, G., Riederer, P., Bengel, D., et al. (1996). Allelic variation of human serotonin transporter gene expression. Journal of Neurochemistry, 66, 2621–2624.Google Scholar
Hollingshead, A. B. (1969). Two Factor Index of Social Position. Unpublished manuscript, Yale University.Google Scholar
Hu, X.-Z., Lipsky, R. H., Zhu, G., Akhtar, L. A., Taubman, J., Greenberg, B. D., et al. (2006). Serotonin transporter promoter gain-of-function genotypes are linked to obsessive-compulsive disorder. American Journal of Human Genetics, 78, 815–826.Google Scholar
Indredavik, M. S., Vik, T., Heyerdahl, S., Kulseng, S., & Brubakk, A.-M. (2005). Psychiatric symptoms in low birth weight adolescents, assessed by screening questionnaires. European Child and Adolescent Psychiatry, 14, 226–236.Google Scholar
Indredavik, M. S., Vik, T., Heyerdahl, S., Kulseng, S., Fayers, P., & Brubakk, A. (2004). Psychiatric symptoms and disorders in adolescents with low birth weight. Archives of Disease in Childhood: Fetal and Neonatal Edition, 89, F445–F450.Google Scholar
Johnson, S., Hollis, C., Kochhar, P., Hennessy, E., Wolke, D., & Marlow, N. (2010). Psychiatric disorders in extremely preterm children: Longitudinal finding at age 11 years in the EPICure study. Journal of the American Academy of Child & Adolescent Psychiatry, 49, 453–463.Google Scholar
Kramer, M. S., Platt, R. W., Wen, S. W., Joseph, K. S., Allen, A., Abrahamowicz, M., et al. (2001). A new and improved population-based Canadian reference for birth weight for gestational age. Pediatrics, 108, E35.Google Scholar
Lesch, K.-P., Bengel, D., Heils, A., Sabol, S. Z., Greenberg, B. D., Petri, S., et al. (1996). Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science, 274, 1527–1531.CrossRefGoogle ScholarPubMed
Levy-Shiff, R., Einat, G., Har-Even, D., Mogilner, M., Mogilner, S., Lerman, M., et al. (1994). Emotional and behavioral adjustment in children born prematurely. Journal of Clinical Child Psychology, 23, 323–333.CrossRefGoogle Scholar
Methúsalemsdóttir, H. F., Egilson, S. Þ., Guðmundsdóttir, R., Valdimarsdóttir, U. A., & Georgsdóttir, I. (2013). Quality of life of adolescents born with extremely low birth weight. Acta Paediatrica, 102, 597–601.Google Scholar
Munafo, M. R., Clark, T. G., Moore, L. R., Payne, E., Walton, R., & Flint, J. (2003). Genetic polymorphisms and personality in healthy adults: A systematic review and meta-analysis. Molecular Psychiatry, 8, 471–484.Google Scholar
Praschak-Rieder, N., Kennedy, J., Wilson, A. A., Hussey, D., Boovariwala, A., Willeit, M., et al. (2007). Novel 5-HTTLPR allele associates with higher serotonin transporter binding in putamen: A [11 C] DASB positron emission tomography study. Biological Psychiatry, 62, 327–331.Google Scholar
Raikkonen, K., Pesonen, A.-K., Heinonen, K., Kajantie, E., Hovi, P., Jarvenpaa, A.-L., et al. (2008). Depression in young adults with very low birth weight: The Helsinki study of very low-birth-weight adults. Archives of General Psychiatry, 65, 290–296.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
Saigal, S., & Doyle, L. W. (2008). An overview of mortality and sequelae of preterm birth from infancy to adulthood. Lancet, 371, 261–269.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. Journal of the American Medical Association, 276, 453–459.CrossRefGoogle ScholarPubMed
Saigal, S., Hoult, L. A., Streiner, D. L., Stoskopf, B. L., & Rosenbaum, P. L. (2000). School difficulties at adolescence in a regional cohort of children who were extremely low birth weight. Pediatrics, 105, 325–331.CrossRefGoogle Scholar
Saigal, S., Pinelli, J., Hoult, L., Kim, M. M., & Boyle, M. H. (2003). Psychopathology and social competencies of adolescents who were extremely low birth weight. Pediatrics, 111, 969–975.Google Scholar
Saigal, S., Rosenbaum, P. L., Szatmari, P., & Campbell, D. (1991). Learning disabilities and school problems in a regional cohort of extremely low birth weight (<1000 g) children: A comparison with term controls. Journal of Developmental and Behavioral Pediatrics, 12, 294–300.Google Scholar
Saigal, S., Szatmari, P., Rosenbaum, P., Campbell, D., & King, S. (1990). Intellectual and functional status at school entry of children who weighed 1000 grams or less at birth: A regional perspective of births in the 1980s. Journal of Pediatrics, 116, 409–416.Google Scholar
Saigal, S., Szatmari, P., Rosenbaum, P., Campbell, D., & King, S. (1991). Cognitive abilities and school performance of extremely low birth weight children and matched term control children at age 8 years: A regional study. Journal of Pediatrics, 118, 751–760.CrossRefGoogle Scholar
Schmidt, L. A., Miskovic, V., Boyle, M. H., & Saigal, S. (2008). Shyness and timidity in young adults who were born at extremely low birth weight. Pediatrics, 122, e181–e187.Google Scholar
Stevenson, C., Blackburn, P., & Pharoah, P. (1999). Longitudinal study of behaviour disorders in low birthweight infants. Archives of Disease in Childhood: Fetal and Neonatal Edition, 81, F5–F9.Google Scholar
Strang-Karlsson, S., Räikkönen, K., Pesonen, A.-K., Kajantie, E., Paavonen, E., Lahti, J., et al. (2008). Very low birth weight and behavioral symptoms of attention deficit hyperactivity disorder in young adulthood: The Helsinki study of very-low-birth-weight adults. American Journal of Psychiatry, 165, 1345–1353.Google Scholar
Szatmari, P., Saigal, S., Rosenbaum, P., & Campbell, D. (1993). Psychopathology and adaptive functioning among extremely low birthweight children at eight years of age. Development and Psychopathology, 5, 345–357.CrossRefGoogle Scholar
Szatmari, P., Saigal, S., Rosenbaum, P., Campbell, D., & King, S. (1990). Psychiatric disorders at five years among children with birthweights <1000 g: A regional perspective. Developmental Medicine and Child Neurology, 32, 954–962.Google Scholar
Taylor, H. G., Margevicius, S., Schluchter, M., Andreias, L., & Hack, M. (2015). Persisting behavior problems in extremely low birth weight adolescents. Journal of Developmental & Behavioral Pediatrics, 36, 178–187.Google Scholar
Taylor, S. E., Way, B. M., Welch, W. T., Hilmert, C. J., Lehman, B. J., & Eisenberger, N. I. (2006). Early family environment, current adversity, the serotonin transporter promoter polymorphism, and depressive symptomatology. Biological Psychiatry, 60, 671–676.Google Scholar
Uher, R., & McGuffin, P. (2008). The moderation by the serotonin transporter gene of environmental adversity in the aetiology of mental illness: Review and methodological analysis. Molecular Psychiatry, 13, 131–146.Google Scholar
van Baar, A. L., Vermaas, J., Knots, E., de Kleine, M. J., & Soons, P. (2009). Functioning at school age of moderately preterm children born at 32 to 36 weeks’ gestational age. Pediatrics, 124, 251–257.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, 452–459.Google Scholar
Waxman, J., Van Lieshout, R. J., Saigal, S., Boyle, M. H., & Schmidt, L. A. (2013). Still cautious: Personality characteristics of extremely low birth weight adults in their early 30s. Personality and Individual Differences, 55, 967–971.Google Scholar