Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-20T07:04:23.648Z Has data issue: false hasContentIssue false

The combined effects of prenatal drug exposure and early adversity on neurobehavioral disinhibition in childhood and adolescence

Published online by Cambridge University Press:  15 July 2011

Philip A. Fisher*
Affiliation:
Oregon Social Learning Center University of Oregon
Barry M. Lester
Affiliation:
Brown University
David S. DeGarmo
Affiliation:
Oregon Social Learning Center
Linda L. Lagasse
Affiliation:
Brown University
Hai Lin
Affiliation:
Brown University
Seetha Shankaran
Affiliation:
Wayne State University
Henrietta S. Bada
Affiliation:
University of Kentucky
Charles R. Bauer
Affiliation:
University of Miami
Jane Hammond
Affiliation:
Research Triangle Institute
Toni Whitaker
Affiliation:
University of Tennessee
Rosemary Higgins
Affiliation:
Eunice Kennedy Shriver National Institute of Child Health and Human Development
*
Address correspondence and reprint requests to: Philip A. Fisher, Oregon Social Learning Center, 10 Shelton McMurphey Boulevard, Eugene, OR 97401; E-mail: [email protected]

Abstract

The negative effects of prenatal substance exposure on neurobiological and psychological development and of early adversity are clear, but little is known about their combined effects. In this study, multilevel analyses of the effects of prenatal substance exposure and early adversity on the emergence of neurobehavioral disinhibition in adolescence were conducted. Neurobehavioral disinhibition has previously been observed to occur frequently in multiproblem youth from high-risk backgrounds. In the present study, neurobehavioral disinhibition was assessed via behavioral dysregulation and poor executive function composite measures. Data were drawn from a prospective longitudinal investigation of prenatal substance exposure that included 1,073 participants followed from birth through adolescence. The results from latent growth modeling analyses showed mean stability but significant individual differences in behavioral dysregulation and mean decline with individual differences in executive function difficulties. Prior behavioral dysregulation predicted increased executive function difficulties. Prenatal drug use predicted the emergence and growth in neurobehavioral disinhibition across adolescence (directly for behavioral dysregulation and indirectly for executive function difficulties via early adversity and behavioral dysregulation). Prenatal drug use and early adversity exhibited unique effects on growth in behavioral dysregulation; early adversity uniquely predicted executive function difficulties. These results are discussed in terms of implications for theory development, social policy, and prevention science.

Type
Articles
Copyright
Copyright © Cambridge University Press 2011

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.)

References

Achenbach, T. M. (1991). Integrative guide to the 1991 CBCL/4–18, YSR, and TRF profiles. Burlington, VT: University of Vermont, Department of Psychology.Google Scholar
Bada, H. S., Bann, C. M., Bauer, C. R., Shankaran, S., Lester, B., LaGasse, L., et al. (2011). Preadolescent behavior problems after prenatal cocaine exposure: Relationship between teacher and caretaker ratings (maternal lifestyle study). Neurotoxicology and Teratology, 33, 7887.CrossRefGoogle ScholarPubMed
Beck, A. T., Steer, R. A., & Brown, G. K. (1996). Manual for the Beck Depression Inventory—II. San Antonio, TX: Psychological Corporation.Google Scholar
Besinger, B., Garland, A., Litrownik, A., & Landsverk, J. (1999). Caretaker substance abuse among maltreated children placed in foster care. Child Welfare, 78, 221239.Google Scholar
Biesanz, J. C., Deeb-Sossa, N., Papadakis, A. A., Bollen, K. A., & Curran, P. J. (2004). The role of coding time in estimating and interpreting growth curve models. Psychological Methods, 9, 3052.CrossRefGoogle ScholarPubMed
Brown, H. C., Wang, W., Kellam, S. G., Muthén, B. O., Petras, H., Toyinbo, P., et al. (2008). Methods for testing theory and evaluating impact in randomized field trials: Intent-to-treat analyses for integrating the perspectives of person, place, and time. Drug and Alcohol Dependence, 95 (Suppl. 1), S74S104.CrossRefGoogle ScholarPubMed
Bruce, J., Fisher, P. A., Pears, K. C., & Levine, S. (2009). Morning cortisol levels in preschool-aged foster children: Differential effects of maltreatment type. Developmental Psychobiology, 51, 1423.CrossRefGoogle ScholarPubMed
Caldwell, B. M., & Bradley, R. H. (1984). Home Observation for Measurement of the Environment. Little Rock, AR: University of Arkansas at Little Rock Press.Google Scholar
Chapman, K., Tarter, R. E., Kirisci, L., & Cornelius, M. D. (2007). Childhood neurobehavior disinhibition amplifies the risk of substance use disorder: Interaction of parental history and prenatal alcohol exposure. Journal of Developmental and Behavioral Pediatrics, 28, 219224.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Curtis, W. J. (2007). Multilevel perspectives on pathways to resilient functioning. Development and Psychopathology, 19, 627629.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Dawson, G. (2002). Multiple levels of analysis [Editorial]. Development and Psychopathology, 14, 417420.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Gunnar, M. R. (2008). Integrating biological measures into the design and evaluation of preventive interventions. Development and Psychopathology, 20, 737743.CrossRefGoogle ScholarPubMed
Cicchetti, D., & Toth, S. L. (2009). The past achievements and future promises of developmental psychopathology: The coming of age of a discipline. Journal of Child Psychology and Psychiatry, 50, 1625.CrossRefGoogle ScholarPubMed
Clausen, J. M., Landsverk, J., Ganger, W., Chadwick, D., & Litrownik, A. (1998). Mental health problems of children in foster care. Journal of Child and Family Studies, 7, 283296.CrossRefGoogle Scholar
Conners, N. A., Bradley, R. H., Mansell, L. W., Liu, J. Y., Roberts, T. J., Burgdorf, K., et al. (2004). Children of mothers with serious substance abuse problems: An accumulation of risks. American Journal of Drug and Alcohol Abuse, 30, 85100.CrossRefGoogle ScholarPubMed
Dahl, T., Ceballo, R., & Huerta, M. (2010). In the eye of the beholder: Mothers’ perceptions of poor neighborhoods as places to raise children. Journal of Community Psychology, 38, 419434CrossRefGoogle Scholar
Derogatis, L. R., & Fitzpatrick, M. (2004). The SCL-90-R, the Brief Symptom Inventory (BSI), and the BSI-18. In Maruish, M. E. (Ed.), The use of psychological testing for treatment planning and outcomes assessment: Vol. 3. Instruments for adults (3rd ed., pp. 141). Mahwah, NJ: Erlbaum.Google Scholar
Edleson, J. L., Shin, N., & Armendariz, K. K. J. (2008). Measuring children's exposure to domestic violence: The development and testing of the Child Exposure to Domestic Violence (CEDV) Scale. Children and Youth Services Review, 30, 502521.CrossRefGoogle Scholar
Fisher, P. A., & Gunnar, M. R. (2010). Early life stress as a risk factor for disease in adulthood. In Lanius, R. A., Vermetten, E., & Pain, C. (Eds.), The impact of early life trauma on health and disease (pp. 133141). Cambridge: Cambridge University Press.Google Scholar
Franklin, T. B., Russig, H., Weiss, I. C., Gräff, J., Linder, N., Michalon, A., et al. (2010). Epigenetic transmission of the impact of early stress across generations. Biological Psychiatry, 68, 408415.Google Scholar
Gunnar, M. R., Fisher, P. A., & The Early Experience, Stress, and Prevention Science Network. (2006). Bringing basic research on early experience and stress neurobiology to bear on preventive interventions for neglected and maltreated children. Development and Psychopathology, 18, 651677.Google Scholar
Gunnar, M. R., Morison, S. J., Chisholm, K., & Schuder, M. (2001). Salivary cortisol levels in children adopted from Romanian orphanages. Development and Psychopathology, 13, 611628.CrossRefGoogle ScholarPubMed
Harden, B. J. (2004). Safety and stability for foster children: A developmental perspective. The Future of Children, 14, 3147.Google Scholar
Hollingshead, A. A. (1975). Four Factor Index of Social Status. Unpublished manuscript.Google Scholar
Iacono, W. G., Malone, S. M., & McGue, M. (2008). Behavioral disinhibition and the development of early-onset addiction: Common and specific influences. Annual Review of Clinical Psychology, 4, 325348.Google Scholar
Ingoldsby, E. M., Kohl, G. O., McMahon, R. J., Lengua, L., & The Conduct Problems Prevention Research Group. (2006). Conduct problems, depressive symptomatology and their co-occurring presentation in childhood as predictors of adjustment in early adolescence. Journal of Abnormal Child Psychology, 34, 603621.CrossRefGoogle ScholarPubMed
Jacobson, S. W., Bihun, J. T., & Chiodo, L. M. (1999). Effects of prenatal alcohol and cocaine exposure on infant cortisol levels. Development and Psychopathology, 11, 195208.CrossRefGoogle ScholarPubMed
Jacobson, S. W., Jacobson, J. L., & Nelson, C. A. (2000). Teratogenic insult and neurobehavioral function in infancy and childhood. In Nelson, C. A. (Ed.), Minnesota symposia on child psychology: Vol. 31. The effects of early adversity on neurobehavioral development (pp. 61112). Mahwah, NJ: Erlbaum.Google Scholar
Lester, B. M., Bagner, D. M., Liu, J., LaGasse, L. L., Seifer, R., Bauer, C. R., et al. (2009). Infant neurobehavioral dysregulation: Behavior problems in children with prenatal substance exposure. Pediatrics, 124, 13551362.CrossRefGoogle ScholarPubMed
Lester, B. M., LaGasse, L. L., Shankaran, S., Bada, H. S., Bauer, C. R., Lin, R., et al. (2010). Prenatal cocaine exposure related to cortisol stress reactivity in 11-year-old children. Journal of Pediatrics, 157, 288295.CrossRefGoogle ScholarPubMed
Lester, B. M., & Padbury, J. (2009). The third pathophysiology of prenatal cocaine exposure. Developmental Neuroscience, 31, 2335.CrossRefGoogle ScholarPubMed
Lewis, E. E., Dozier, M., Ackerman, J., & Sepulveda-Kozakowski, S. (2007). The effect of placement instability on adopted children's inhibitory control abilities and oppositional behavior. Developmental Psychology, 43, 14151427.CrossRefGoogle ScholarPubMed
Lopez-Duran, N. L., Kovacs, M., & George, C. J. (2009). Hypothalamic–pituitary–adrenal axis dysregulation in depressed children and adolescents: A meta-analysis. Psychoneuroendocrinology, 34, 12721283.Google Scholar
Luciana, M. (2003). Practitioner review: Computerized assessment of neuropsychological function in children: Clinical and research applications of the Cambridge Neuropsychological Testing Automated Battery (CANTAB). Journal of Child Psychology and Psychiatry, 44, 649663.Google Scholar
MacKinnon, D. P. (2008). Introduction to statistical mediation. New York: Psychology Press.Google Scholar
Magnano, C. L., Gardner, J. M., & Karmel, B. Z. (1992). Differences in salivary cortisol levels in cocaine-exposed and noncocaine-exposed NICU infants. Developmental Psychobiology, 25, 93103.Google Scholar
McEwen, B. S. (1998). Stress, adaptation, and disease: Allostasis and allostatic load. Annals of the New York Academy of Sciences, 840, 3344.CrossRefGoogle ScholarPubMed
McNamee, R. L., Dunfee, K. L., Luna, B., Clark, D. B., Eddy, W. F., & Tarter, R. E. (2008). Brain activation, response inhibition, and increased risk for substance use disorder. Alcoholism: Clinical and Experimental Research, 32, 405413.CrossRefGoogle ScholarPubMed
Muthén, L. K., & Muthén, B. O. (2010). Mplus user's guide (6th ed.). Los Angeles: Author.Google Scholar
Pears, K. C., & Fisher, P. A. (2005). Developmental, cognitive, and neuropsychological functioning in preschool-aged foster children: Associations with prior maltreatment and placement history. Journal of Developmental and Behavioral Pediatrics, 26, 112122.Google Scholar
Pears, K. C., Kim, H. K., & Fisher, P. A. (2008). Psychosocial and cognitive functioning of children with specific profiles of maltreatment. Child Abuse and Neglect, 32, 958971.Google Scholar
Pollak, S. D., Nelson, C. A., Schlaak, M. F., Roeber, B. J., Wewerka, S. S., Wiik, K. L., et al. (2010). Neurodevelopmental effects of early deprivation on postinstitutionalized children. Child Development, 81, 224236.CrossRefGoogle ScholarPubMed
Scafidi, F. A., Field, T. M., Wheeden, A., Schanberg, S., Kuhn, C., Symanski, R., et al. (1996). Cocaine-exposed preterm neonates show behavioral and hormonal differences. Pediatrics, 97, 851855.CrossRefGoogle ScholarPubMed
Schulkin, J., McEwen, B. S., & Gold, P. W. (1994). Allostasis, amygdala, and anticipatory angst. Neuroscience and Biobehavioral Reviews, 18, 385396.Google Scholar
Selye, H. (1978). The stress of life. Oxford: McGraw–Hill.Google Scholar
Shaffer, D., Fisher, P., Lucas, C. P., Dulcan, M. K., & Schwab-Stone, M. E. (2000). NIMH Diagnostic Interview Schedule for Children Version IV (NIMH DISC-IV): Description, differences from previous versions, and reliability of some common diagnoses. Journal of the American Academy of Child & Adolescent Psychiatry, 39, 2838.CrossRefGoogle ScholarPubMed
Shonkoff, J. P., Boyce, W. T., & McEwen, B. S. (2009). Neuroscience, molecular biology, and the childhood roots of health disparities: Building a new framework for health promotion and disease prevention. Journal of the American Medical Association, 301, 22522259.CrossRefGoogle ScholarPubMed
Simeon, D., Knutelska, M., Yehuda, R., Putnam, F., Schmeidler, J., & Smith, L. M. (2007). Hypothalamic–pituitary–adrenal axis function in dissociative disorders, post-traumatic stress disorder, and healthy volunteers. Biological Psychiatry, 61, 966973.CrossRefGoogle ScholarPubMed
Singer, J. D., & Willett, J. B. (2003). Applied longitudinal data analysis: Modeling change and event occurrence. New York: Oxford University Press.Google Scholar
Smith, D. K., Johnson, A. B., Pears, K. C., Fisher, P. A., & DeGarmo, D. S. (2007). Child maltreatment and foster care: Unpacking the effects of prenatal and postnatal parental substance use. Child Maltreatment, 12, 150160.CrossRefGoogle ScholarPubMed
Streissguth, A. P., Bookstein, F. L., Barr, H. M., Sampson, P. D., O’Malley, K., & Young, J. K. (2004). Risk factors for adverse life outcomes in fetal alcohol syndrome and fetal alcohol effects. Journal of Developmental and Behavioral Pediatrics, 25, 228238.CrossRefGoogle ScholarPubMed
Tarter, R. E., Kirisci, L., Mezzich, A., Cornelius, J. R., Pajer, K., Vanyukov, M., et al. (2003). Neurobehavior disinhibition in childhood predicts early age onset of substance use disorder. American Journal of Psychiatry, 160, 10781085.CrossRefGoogle ScholarPubMed
Thompson, B. L., Levitt, P., & Stanwood, G. D. (2009). Prenatal exposure to drugs: Effects on brain development and implications for policy and education. Nature Reviews Neuroscience, 10, 303312.CrossRefGoogle ScholarPubMed
Young, N. K., Boles, S. M., & Otero, C. (2007). Parental substance use disorders and child maltreatment: Overlap, gaps, and opportunities. Child Maltreatment, 12, 137149.CrossRefGoogle ScholarPubMed