Prenatal cocaine effects on brain structure in early infancy

NeuroImage

Volumn 101, Issue , 2014, Pages 114-123

  Grewen, Karen ^a   Burchinal, Margaret ^b   Vachet, Clement ^c   Gouttard, Sylvain ^c   Gilmore, John H ^a   Lin, Weili ^b   Johns, Josephine ^a   Elam, Mala ^a   Gerig, Guido ^c  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c UNIVERSITY OF UTAH   (United States)

Author keywords

Cortical gray matter; CSF enlargement; Infant brain development; Magnetic resonance imaging; Prenatal cocaine; Prenatal substance abuse

Indexed keywords

ALCOHOL; CANNABIS; COCAINE; NICOTINE; OPIATE; SEROTONIN UPTAKE INHIBITOR; DOPAMINE UPTAKE INHIBITOR; NARCOTIC AGENT;

ARTICLE; BRAIN DEVELOPMENT; BRAIN REGION; BRAIN SIZE; CEREBROSPINAL FLUID; CLINICAL ARTICLE; COMORBIDITY; CONTROLLED STUDY; EXECUTIVE FUNCTION; FEMALE; FOLLOW UP; GESTATIONAL AGE; GRAY MATTER; HEAD CIRCUMFERENCE; HUMAN; HUMAN TISSUE; INFANT; LONGITUDINAL STUDY; MATERNAL AGE; NUCLEAR MAGNETIC RESONANCE IMAGING; PREFRONTAL CORTEX; PRENATAL COCAINE EXPOSURE; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; WHITE MATTER; ADVERSE EFFECTS; ANATOMY AND HISTOLOGY; BRAIN; CHEMICALLY INDUCED; DRINKING BEHAVIOR; DRUG EFFECTS; FRONTAL LOBE; GROWTH, DEVELOPMENT AND AGING; MALE; NEWBORN; PREGNANCY; PRENATAL EXPOSURE; SMOKING; COGNITION; FRONTAL CORTEX; INHIBITORY CONTROL; MOTHER CHILD RELATION; PARIETAL CORTEX; RISK FACTOR;

ALCOHOL DRINKING; BRAIN; CANNABIS; CEREBROSPINAL FLUID; COCAINE; DOPAMINE UPTAKE INHIBITORS; FEMALE; FRONTAL LOBE; GRAY MATTER; HUMANS; INFANT, NEWBORN; MAGNETIC RESONANCE IMAGING; MALE; NARCOTICS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SEROTONIN UPTAKE INHIBITORS; SMOKING;

EID: 84904726485     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.06.070     Document Type: Article

References (99)

1. Accornero V.H., Amado A.J., et al. Impact of prenatal cocaine exposure on attention and response inhibition as assessed by continuous performance tests. J. Dev. Behav. Pediatr. 2007, 28(3):195-205.
2. Alia-Klein N., Parvaz M.A., et al. Gene×disease interaction on orbitofrontal gray matter in cocaine addiction. Arch. Gen. Psychiatry 2011, 68(3):283-294.
3. Avants B.B., Hurt H., et al. Effects of heavy in utero cocaine exposure on adolescent caudate morphology. Pediatr. Neurol. 2007, 37(4):275-279.
4. Balaraman S., Winzer-Serhan U.H., et al. Opposing actions of ethanol and nicotine on microRNAs are mediated by nicotinic acetylcholine receptors in fetal cerebral cortical-derived neural progenitor cells. Alcohol. Clin. Exp. Res. 2012, 36(10):1669-1677.
5. Bandstra E.S., Morrow C.E., et al. Longitudinal investigation of task persistence and sustained attention in children with prenatal cocaine exposure. Neurotoxicol. Teratol. 2001, 23(6):545-559.
6. Bandstra E.S., Morrow C.E., et al. Prenatal drug exposure: infant and toddler outcomes. J. Addict. Dis. 2010, 29(2):245-258.
7. Barros-Loscertales A., Garavan H., et al. Reduced striatal volume in cocaine-dependent patients. Neuroimage 2011, 56(3):1021-1026.
8. Bartzokis G., Beckson M., et al. Increased CSF volumes are associated with diminished subjective responses to cocaine infusion. Neuropsychopharmacology 2000, 23(4):468-473.
9. Bendersky M., Lewis M. Arousal modulation in cocaine-exposed infants. Dev. Psychol. 1998, 34:555-564.
10. Benjamini Y., Hochberg Y. On the adaptive control of the false discovery rate in multiple testing with independent statistics. J. Educ. Behav. Stat. 2000, 25:60-83.
11. Benveniste H., Fowler J.S., et al. Cocaine is pharmacologically active in the nonhuman primate fetal brain. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(4):1582-1587.
12. Betancourt L.M., Yang W., et al. Adolescents with and without gestational cocaine exposure: longitudinal analysis of inhibitory control, memory and receptive language. Neurotoxicol. Teratol. 2011, 33(1):36-46.
13. Bridgett D.J., Mayes L.C. Development of inhibitory control among prenatally cocaine exposed and non-cocaine exposed youths from late childhood to early adolescence: the effects of gender and risk and subsequent aggressive behavior. Neurotoxicol. Teratol. 2011, 33(1):47-60.
14. CDC Pediatric and Pregnancy Nutrition Surveillance System from. http://www.cdc.gov/pednss/what_is/pednss_health_indicators.htm.
15. Chaplin T.M., Freiburger M.B., et al. Prenatal cocaine exposure, gender, and adolescent stress response: a prospective longitudinal study. Neurotoxicol. Teratol. 2010, 32(6):595-604.
16. Cortese B., Moore G., et al. Magnetic resonance and spectroscopic imaging of prenatal alcohol-exposed children: preliminary findings in the caudate nucleus. Neurotoxicol. Teratol. 2006, 28:597-606.
17. Covert R.F., Schreiber M.D., et al. Hemodynamic and cerebral blood flow effects of cocaine, cocethylene and benzoylecgonine in conscious and anesthetized fetal lambs. J. Pharmacol. Exp. Ther. 1994, 270:118-126.
18. Coyle J.T. Brain structural alterations induced by fetal exposure to cocaine persist into adolescence and affect behavior. JAMA Psychiatry 2013, 167(4):348-354.
19. de Kieviet J.F., Zoetebier L., et al. Brain development of very preterm and very low-birthweight children in childhood and adolescence: a meta-analysis. Dev. Med. Child Neurol. 2012, 54(4):313-323.
20. Delaney-Black V., Chiodo L.M., et al. Prenatal and postnatal cocaine exposure predict teen cocaine use. Neurotoxicol. Teratol. 2011, 33(1):110-119.
21. Demirakca T., Ende G., et al. Effects of alcoholism and continued abstinence on brain volumes in both genders. Alcohol. Clin. Exp. Res. 2011, 35(9):1678-1685.
22. Dow-Edwards D. Fetal and maternal cocaine levels peak rapidly following intragastric administration in the rat. J. Subst. Abuse 1990, 2(4):427-437.
23. Dow-Edwards D. Translational issues for prenatal cocaine studies and the role of environment. Neurotoxicol. Teratol. 2011, 33(1):9-16.
24. Dow-Edwards D.L., Benveniste H., et al. Neuroimaging of prenatal drug exposure. Neurotoxicol. Teratol. 2006, 28:386-402.
25. Dwyer J.B., Broide R.S., et al. Nicotine and brain development. Birth Defects Res. C Embryo Today 2008, 84(1):30-44.
26. Eiden R.D., McAuliffe S., et al. Effects of prenatal cocaine exposure on infant reactivity and regulation. Neurotoxicol. Teratol. 2009, 31(1):60-68.
27. Eiden R.D., Schuetze P., et al. Maternal cocaine use and mother-infant interactions: direct and moderated associations. Neurotoxicol. Teratol. 2011, 33(1):120-128.
28. Eiden R.D., Schuetze P., et al. Cocaine exposure and children's self-regulation: indirect association via maternal harshness. Front. Psychiatry 2011, 2:31.
29. Ersche K.D., Barnes A., et al. Abnormal structure of frontostriatal brain systems is associated with aspects of impulsivity and compulsivity in cocaine dependence. Brain 2011, 134(Pt 7):2013-2024.
30. Ersche K.D., Jones P.S., et al. Abnormal brain structure implicated in stimulant drug addiction. Science 2012, 335(6068):601-604.
31. Fein G., Di Sclafani V., et al. Prefrontal cortical volume reduction associated with frontal cortex function deficit in 6-week abstinent crack-cocaine dependent men. Drug Alcohol Depend. 2002, 68(1):87-93.
32. Fox N.C., Schott J.M. Imaging cerebral atrophy: normal ageing to Alzheimer's disease. Lancet 2004, 363(9406):392-394.
33. Frank D.A., McCarten K.M., et al. Level of in utero cocaine exposure and neonatal ultrasound findings. Pediatrics 1999, 104:1101-1105.
34. Frank D.A., Augustyn M., et al. Growth, development, and behavior in early childhood following prenatal cocaine exposure: a systematic review. JAMA 2001, 285(12):1613-1625.
35. Frankfurt M., Wang H.Y., et al. Prenatal cocaine increases dendritic spine density in cortical and subcortical brain regions of the rat. Dev. Neurosci. 2009, 31(1-2):71-75.
36. Frankfurt M., Salas-Ramirez K., et al. Cocaine alters dendritic spine density in cortical and subcortical brain regions of the postpartum and virgin female rat. Synapse 2011, 65(9):955-961.
37. Franklin T.R., Acton P.D., et al. Decreased gray matter concentration in the insular, orbitofrontal, cingulate, and temporal cortices of cocaine patients. Biol. Psychiatry 2002, 51(2):134-142.
38. Gan X., Zhang L., et al. Cocaine enhances brain endothelial adhesion molecules and leukocyte migration. Clin. Immunol. 1999, 91(1):68-76.
39. Gao W., Zhu H., et al. Evidence on the emergence of the brain's default network from 2-week-old to 2-year-old healthy pediatric subjects. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(16):6790-6795.
40. Gilmore J.H., Lin W., et al. Regional gray matter growth, sexual dimorphism, and cerebral asymmetry in the neonatal brain. J. Neurosci. 2007, 27(6):1255-1260.
41. Gilmore J.H., Schmitt J.E., et al. Genetic and environmental contributions to neonatal brain structure: a twin study. Hum. Brain Mapp. 2010, 31(8):1174-1182.
42. Gilmore J.H., Shi F., et al. Longitudinal development of cortical and subcortical gray matter from birth to 2years. Cereb. Cortex 2012, 22(11):2478-2485.
43. Gomez-Anson B., Ramsey R.G. Pachygyria in a neonate with prenatal cocaine exposure: MR features. J. Comput. Assist. Tomogr. 1994, 18(4):637-639.
44. Gouin K., Murphy K., et al. Effects of cocaine use during pregnancy on low birthweight and preterm birth: systematic review and metaanalyses. Am. J. Obstet. Gynecol. 2011, 204(4):340. (e341-312).
45. Hanlon C.A., Dufault D.L., et al. Elevated gray and white matter densities in cocaine abstainers compared to current users. Psychopharmacology (Berl) 2011, 218(4):681-692.
46. Irner T.B. Substance exposure in utero and developmental consequences in adolescence: a systematic review. Child Neuropsychol. 2012, 18(6):521-549.
47. Knickmeyer R.C., Gouttard S., et al. A structural MRI study of human brain development from birth to 2years. J. Neurosci. 2008, 28(47):12176-12182.
48. Knickmeyer R.C., Kang C., et al. Twin-singleton differences in neonatal brain structure. Twin Res. Hum. Genet. 2011, 14(3):268-276.
49. Knowles J.K., Penn A.A. Perinatal Brain, Development, Malformation, and Injury 2012, M. M. McCarthy, Morgan Claypool Life Sciences.
50. Landi N., Crowley M.J., et al. Deviant ERP response to spoken non-words among adolescents exposed to cocaine in utero. Brain Lang. 2012, 120(3):209-216.
51. Lane S.D., Steinberg J.L., et al. Diffusion tensor imaging and decision making in cocaine dependence. PLoS One 2010, 5(7):e11591.
52. Lauder J.M. Neurotransmitters as growth regulatory signals: role of receptors and second messengers. Trends Neurosci. 1993, 16(6):233-240.
53. Lester B.M., Lagasse L., et al. The Maternal Lifestyle Study (MLS): effects of prenatal cocaine and/or opiate exposure on auditory brain response at one month. J. Pediatr. 2003, 142(3):279-285.
54. Lewis B.A., Minnes S., et al. The effects of prenatal cocaine on language development at 10years of age. Neurotoxicol. Teratol. 2011, 33(1):17-24.
55. Li Z., Coles C.D., et al. Prenatal cocaine exposure alters emotional arousal regulation and its effects on working memory. Neurotoxicol. Teratol. 2009, 31(6):342-348.
56. Li Z., Santhanam P., et al. Increased "default mode" activity in adolescents prenatally exposed to cocaine. Hum. Brain Mapp. 2011, 32(5):759-770.
57. Lin W., Zhu Q., et al. Functional connectivity MR imaging reveals cortical functional connectivity in the developing brain. AJNR Am. J. Neuroradiol. 2008, 29(10):1883-1889.
58. Link E.A., Weese-Mayer D.W., et al. Magnetic resonance imaging in infants exposed to cocaine prenatally: a preliminary report. Clin. Pediatr. (Phila) 1991, 30(8):506-508.
59. Liu J., Lester B.M., et al. Regional brain morphometry and impulsivity in adolescents following prenatal exposure to cocaine and tobacco. JAMA Pediatr. 2013, 167(4):348-354.
60. Lowe J.R., Maclean P.C., et al. Comparison of cerebral volume in children aged 18-22 and 36-47 months born preterm and term. J. Child Neurol. 2012, 27(2):172-177.
61. Lumeng J.C., Cabral H.J., et al. Pre-natal exposures to cocaine and alcohol and physical growth patterns to age 8years. Neurotoxicol. Teratol. 2007, 29(4):446-457.
62. Matochik J.A., London E.D., et al. Frontal cortical tissue composition in abstinent cocaine abusers: a magnetic resonance imaging study. Neuroimage 2003, 19(3):1095-1102.
63. Mayes L., Snyder P.J., et al. Visuospatial working memory in school-aged children exposed in utero to cocaine. Child Neuropsychol. 2007, 13(3):205-218.
64. Meyer J.S., Quenzer L.F. Psychopharmacology: Drugs, the Brain and Behavior 2005, Sinauer Associates, Sunderland, MA.
65. Minnes S., Singer L., et al. Effects of prenatal cocaine/polydrug use on maternal-infant feeding interactions during the first year of life. Dev. Behav. Pediatr. 2005, 26(3):194-200.
66. Moreno-Lopez L., Catena A., et al. Trait impulsivity and prefrontal gray matter reductions in cocaine dependent individuals. Drug Alcohol Depend. 2012, 125(3):208-214.
67. Morrow C.E., Culbertson J.L., et al. Learning disabilities and intellectual functioning in school-aged children with prenatal cocaine exposure. Dev. Neuropsychol. 2006, 30(3):905-931.
68. Noland J.S., Singer L.T., et al. Prenatal drug exposure and selective attention in preschoolers. Neurotoxicol. Teratol. 2005, 27(3):429-438.
69. Pfefferbaum A., Mathalon D.H., et al. A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. Arch. Neurol. 1994, 51(9):874-887.
70. Phillips J.P., Montague E.Q., et al. Prematurity affects cortical maturation in early childhood. Pediatr. Neurol. 2011, 45(4):213-219.
71. Popolo M., McCarthy D.M., et al. Influence of dopamine on precursor cell proliferation and differentiation in the embryonic mouse telencephalon. Dev. Neurosci. 2004, 26(2-4):229-244.
72. Prastawa M., Gilmore J.H., et al. Automatic segmentation of MR images of the developing newborn brain. Med. Image Anal. 2005, 9(5):457-466.
73. Rao H., Wang J., et al. Altered resting cerebral blood flow in adolescents with in utero cocaine exposure revealed by perfusion functional MRI. Pediatrics 2007, 120(5):e1245-e1254.
74. Raznahan A., Shaw P., et al. How does your cortex grow?. J. Neurosci. 2011, 31(19):7174-7177.
75. Ren J.Q., Malanga C.J., et al. Neuropathological consequences of prenatal cocaine exposure in the mouse. Int. J. Dev. Neurosci. 2004, 22(5-6):309-320.
76. Riccio O., Hurni N., et al. Alpha2-adrenergic receptor activation regulates cortical interneuron migration. Eur. J. Neurosci. 2012, 36(7):2879-2887.
77. Rivkin M.J., Davis P.E., et al. Volumetric MRI study of brain in children with intrauterine exposure to cocaine, alcohol, tobacco, and marijuana. Pediatrics 2008, 121(4):741-750.
78. Rogers C.E., Anderson P.J., et al. Regional cerebral development at term relates to school-age social-emotional development in very preterm children. J. Am. Acad. Child Adolesc. Psychiatry 2012, 51(2):181-191.
79. Roussotte F., Soderberg L., et al. Structural, metabolic, and functional brain abnormalities as a result of prenatal exposure to drugs of abuse: evidence from neuroimaging. Neuropsychol. Rev. 2010, 20(4):376-397.
80. Savage J., Brodsky N.L., et al. Attentional functioning and impulse control in cocaine-exposed and control children at age ten years. J. Dev. Behav. Pediatr. 2005, 26(1):42-47.
81. Schenker S., Yang Y., et al. The transfer of cocaine and its metabolites across the term human placenta. Clin. Pharmacol. Ther. 1993, 53(3):329-339.
82. Scher M.S., Richardson G.A., et al. Effects of prenatal cocaine/crack and other drug exposure on electroencephalographic sleep studies at birth and one year. Pediatrics 2000, 105(1 Pt 1):39-48.
83. Schroder M.D., Snyder P.J., et al. Impaired performance of children exposed in utero to cocaine on a novel test of visuospatial working memory. Brain Cogn. 2004, 55(2):409-412.
84. Sim M.E., Lyoo I.K., et al. Cerebellar gray matter volume correlates with duration of cocaine use in cocaine-dependent subjects. Neuropsychopharmacology 2007, 32(10):2229-2237.
85. Singer L.T., Arendt R., et al. Developing language skills of cocaine-exposed infants. Pediatrics 2001, 107(5):1057-1064.
86. Singer L.T., Eisengart L.J., et al. Prenatal cocaine exposure and infant cognition. Infant Behav. Dev. 2005, 28(4):431-444.
87. Smith L.M., Chang L., et al. Brain proton magnetic resonance spectroscopy and imaging in children exposed to cocaine in utero. Pediatrics 2001, 107(2):227-231.
88. Sobell L.C., Sobell M.B. Alcohol Timeline Followback Users' Manual 1995, A. R. Foundation, (Toronto, Canada, Addiction Research Foundation).
89. Song Z.M., Undie A.S., et al. D1 dopamine receptor regulation of microtubule-associated protein-2 phosphorylation in developing cerebral cortical neurons. J. Neurosci. 2002, 22(14):6092-6105.
90. Song Z.M., Abou-Zeid O., et al. Alpha2a adrenoceptors regulate phosphorylation of microtubule-associated protein-2 in cultured cortical neurons. Neuroscience 2004, 123(2):405-418.
91. Squitieri F., Cannella M., et al. Distinct brain volume changes correlating with clinical stage, disease progression rate, mutation size, and age at onset prediction as early biomarkers of brain atrophy in Huntington's disease. CNS Neurosci. Ther. 2009, 15(1):1-11.
92. Stanwood G.D., Levitt P. Prenatal exposure to cocaine produces unique developmental and long-term adaptive changes in dopamine D1 receptor activity and subcellular distribution. J. Neurosci. 2007, 27(1):152-157.
93. Tronick E.Z., Messinger D.S., et al. Cocaine exposure is associated with subtle compromises of infants' and mothers' social-emotional behavior and dyadic features of their interaction in the face-to-face still-face paradigm. Dev. Psychol. 2005, 41(5):711-722.
94. Tzarouchi L.C., Astrakas L.G., et al. Periventricular leukomalacia in preterm children: assessment of grey and white matter and cerebrospinal fluid changes by MRI. Pediatr. Radiol. 2009, 39(12):1327-1332.
95. Vitalis T., Parnavelas J.G. The role of serotonin in early cortical development. Dev. Neurosci. 2003, 25(2-4):245-256.
96. Warner T.D., Behnke M., et al. Diffusion tensor imaging of frontal white matter and executive functioning in cocaine-exposed children. Pediatrics 2006, 118(5):2014-2024.
97. Whitaker-Azmitia P.M., Druse M., et al. Serotonin as a developmental signal. Behav. Brain Res. 1996, 73(1-2):19-29.
98. Yao H., Kim K., et al. Cocaine hijacks sigma1 receptor to initiate induction of activated leukocyte cell adhesion molecule: implication for increased monocyte adhesion and migration in the CNS. J. Neurosci. 2011, 31(16):5942-5955.
99. Yap P.T., Fan Y., et al. Development trends of white matter connectivity in the first years of life. PLoS One 2011, 6(9):e24678.