Altered white matter integrity in adolescent binge drinkers.

BACKGROUND White matter integrity has been found to be compromised in adult alcoholics, but it is unclear when in the course of alcohol exposure white matter abnormalities become apparent. This study assessed microstructural white matter integrity among adolescent binge drinkers with no history of an alcohol use disorder. METHODS We used diffusion tensor imaging to examine fractional anisotropy (FA), a measure of directional coherence of white matter tracts, among teens with (n = 14) and without (n = 14) histories of binge drinking but no history of alcohol use disorder, matched on age, gender, and education. RESULTS Binge drinkers had lower FA than controls in 18 white matter areas (clusters > or =27 contiguous voxels, each with p < 0.01) throughout the brain, including the corpus callosum, superior longitudinal fasciculus, corona radiata, internal and external capsules, and commissural, limbic, brainstem, and cortical projection fibers, while exhibiting no areas of higher FA. Among binge drinkers, lower FA in 6 of these regions was linked to significantly greater lifetime hangover symptoms and/or higher estimated peak blood alcohol concentrations. CONCLUSIONS Binge drinking adolescents demonstrated widespread reductions of FA in major white matter pathways. Although preliminary, these results could indicate that infrequent exposure to large doses of alcohol during youth may compromise white matter fiber coherence.

[1]  C. Spielberger,et al.  Manual for the State-Trait Anxiety Inventory , 1970 .

[2]  Terry M. Peters,et al.  3D statistical neuroanatomical models from 305 MRI volumes , 1993, 1993 IEEE Conference Record Nuclear Science Symposium and Medical Imaging Conference.

[3]  June Yoshii,et al.  Age-related changes in prefrontal white matter volume across adolescence , 2006, Neuroreport.

[4]  T. Jernigan,et al.  Development of cortical and subcortical brain structures in childhood and adolescence: a structural MRI study , 2002, Developmental medicine and child neurology.

[5]  J. MacFall,et al.  Diffusion tensor measures of the corpus callosum in adolescents with adolescent onset alcohol use disorders. , 2008, Alcoholism, clinical and experimental research.

[6]  S. Tapert,et al.  Depressive symptoms in adolescents: associations with white matter volume and marijuana use. , 2007, Journal of child psychology and psychiatry, and allied disciplines.

[7]  J E Desmond,et al.  Thinning of the corpus callosum in older alcoholic men: a magnetic resonance imaging study. , 1996, Alcoholism, clinical and experimental research.

[8]  E. Sacanella,et al.  Atrophy of the corpus callosum in chronic alcoholism , 1997, Journal of the Neurological Sciences.

[9]  A. Pfefferbaum,et al.  Disruption of Brain White Matter Microstructure by Excessive Intracellular and Extracellular Fluid in Alcoholism: Evidence from Diffusion Tensor Imaging , 2005, Neuropsychopharmacology.

[10]  John A Matochik,et al.  Altered brain tissue composition in heavy marijuana users. , 2005, Drug and alcohol dependence.

[11]  August B. Hollingshead,et al.  Two Factor Index of Social Position , 1957 .

[12]  A. Petersen,et al.  A self-report measure of pubertal status: Reliability, validity, and initial norms , 1988, Journal of youth and adolescence.

[13]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

[14]  John Suckling,et al.  Mapping brain structure in attention deficit-hyperactivity disorder: A voxel-based MRI study of regional grey and white matter volume , 2007, Psychiatry Research: Neuroimaging.

[15]  H. Breiter,et al.  Decreased Volume of the Brain Reward System in Alcoholism , 2008, Biological Psychiatry.

[16]  F. Crews,et al.  Binge ethanol consumption causes differential brain damage in young adolescent rats compared with adult rats. , 2000, Alcoholism, clinical and experimental research.

[17]  C. Harper,et al.  The Neuropathology of Alcohol‐specific Brain Damage, or Does Alcohol Damage the Brain? , 1998, Journal of neuropathology and experimental neurology.

[18]  H. Wechsler,et al.  Health and behavioral consequences of binge drinking in college. A national survey of students at 140 campuses. , 1994, JAMA.

[19]  Daniel Rueckert,et al.  Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data , 2006, NeuroImage.

[20]  P. Basser,et al.  Diffusion tensor MR imaging of the human brain. , 1996, Radiology.

[21]  E. Sullivan,et al.  Corpus callosal microstructural integrity influences interhemispheric processing: a diffusion tensor imaging study. , 2005, Cerebral cortex.

[22]  Alan C. Evans,et al.  Structural maturation of neural pathways in children and adolescents: in vivo study. , 1999, Science.

[23]  S. Tapert,et al.  Psychometric evaluation of the Customary Drinking and Drug Use Record (CDDR): a measure of adolescent alcohol and drug involvement. , 1998, Journal of studies on alcohol.

[24]  A. Pfefferbaum,et al.  Neurocircuitry in alcoholism: a substrate of disruption and repair , 2005, Psychopharmacology.

[25]  S. Tapert,et al.  Prefrontal cortex volumes in adolescents with alcohol use disorders: unique gender effects. , 2008, Alcoholism, clinical and experimental research.

[26]  Linda C. Sobell,et al.  Timeline Follow-Back A Technique for Assessing Self-Reported Alcohol Consumption , 1992 .

[27]  P. Renshaw,et al.  Smaller frontal lobe white matter volumes in depressed adolescents , 2002, Biological Psychiatry.

[28]  R. Catalano,et al.  Risk and protective factors for alcohol and other drug problems in adolescence and early adulthood: implications for substance abuse prevention. , 1992, Psychological bulletin.

[29]  G. Douaud,et al.  Brain Morphometry and Cognitive Performance in Detoxified Alcohol-Dependents with Preserved Psychosocial Functioning , 2007, Neuropsychopharmacology.

[30]  D A Dawson,et al.  Age at onset of alcohol use and its association with DSM-IV alcohol abuse and dependence: results from the National Longitudinal Alcohol Epidemiologic Survey. , 1997, Journal of substance abuse.

[31]  L. Frank,et al.  Reduced Fractional Anisotropy in the Splenium of Adolescents with Alcohol Use Disorder , 2003 .

[32]  R. Viner,et al.  Adult outcomes of binge drinking in adolescence: findings from a UK national birth cohort , 2007, Journal of Epidemiology & Community Health.

[33]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[34]  K O Lim,et al.  Relationship between alcohol withdrawal seizures and temporal lobe white matter volume deficits. , 1996, Alcoholism, clinical and experimental research.

[35]  L L Chao,et al.  Effects of heavy drinking, binge drinking, and family history of alcoholism on regional brain metabolites. , 2004, Alcoholism, clinical and experimental research.

[36]  A. Pfefferbaum,et al.  Effects of alcohol dependence comorbidity and antipsychotic medication on volumes of the thalamus and pons in schizophrenia. , 2003, The American journal of psychiatry.

[37]  E. Neafsey,et al.  Brain damage due to episodic alcohol exposure in vivo and in vitro: furosemide neuroprotection implicates edema‐based mechanism , 1998, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[38]  A Pfefferbaum,et al.  Frontal lobe volume loss observed with magnetic resonance imaging in older chronic alcoholics. , 1997, Alcoholism, clinical and experimental research.

[39]  E. Granholm,et al.  Substance use and withdrawal: Neuropsychological functioning over 8 years in youth , 2002, Journal of the International Neuropsychological Society.

[40]  M. Cohen-Zion,et al.  Effects of alcohol and combined marijuana and alcohol use during adolescence on hippocampal volume and asymmetry. , 2007, Neurotoxicology and teratology.

[41]  Matcheri S Keshavan,et al.  Prefrontal cortex, thalamus, and cerebellar volumes in adolescents and young adults with adolescent-onset alcohol use disorders and comorbid mental disorders. , 2005, Alcoholism, clinical and experimental research.

[42]  Edith V. Sullivan,et al.  Dysmorphology and microstructural degradation of the corpus callosum: Interaction of age and alcoholism , 2006, Neurobiology of Aging.

[43]  S. Tapert,et al.  Reduced hippocampal volume among adolescents with alcohol use disorders without psychiatric comorbidity , 2005, Psychiatry Research: Neuroimaging.

[44]  M. Paulus,et al.  Functional MRI of inhibitory processing in abstinent adolescent marijuana users , 2007, Psychopharmacology.

[45]  G. Canino,et al.  The DISC Predictive Scales (DPS): efficiently screening for diagnoses. , 2001, Journal of the American Academy of Child and Adolescent Psychiatry.

[46]  J. Brick Intoxication Test Evidence , 1998 .

[47]  T. Achenbach Manual for ASEBA School-Age Forms & Profiles , 2001 .

[48]  Adolf Pfefferbaum,et al.  Using Magnetic Resonance Imaging and Diffusion Tensor Imaging to Assess Brain Damage in Alcoholics , 2003, Alcohol research & health : the journal of the National Institute on Alcohol Abuse and Alcoholism.

[49]  Nikos Makris,et al.  Frontal white matter and cingulum diffusion tensor imaging deficits in alcoholism. , 2008, Alcoholism, clinical and experimental research.

[50]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[51]  L. Johnston,et al.  Monitoring the Future national survey results on drug use, 1975-2017: Volume I, secondary school students , 2005 .

[52]  Khader M Hasan,et al.  Development and organization of the human brain tissue compartments across the lifespan using diffusion tensor imaging , 2007, Neuroreport.

[53]  S. Wakana,et al.  Fiber tract-based atlas of human white matter anatomy. , 2004, Radiology.

[54]  D. Clark,et al.  Gender and comorbid psychopathology in adolescents with alcohol dependence. , 1997, Journal of the American Academy of Child and Adolescent Psychiatry.

[55]  Heidi Johansen-Berg,et al.  Changes in white matter microstructure during adolescence , 2008, NeuroImage.

[56]  Edith V. Sullivan,et al.  Supratentorial Profile of White Matter Microstructural Integrity in Recovering Alcoholic Men and Women , 2006, Biological Psychiatry.

[57]  T. Patterson,et al.  Chemical pathology in brain white matter of recently detoxified alcoholics: a 1H magnetic resonance spectroscopy investigation of alcohol-associated frontal lobe injury. , 2001, Alcoholism, clinical and experimental research.

[58]  Michele A. Schottenbauer,et al.  Relationships among aging, IQ, and intracranial volume in alcoholics and control subjects. , 2007, Neuropsychology.

[59]  J. Kril,et al.  The cerebral cortex is damaged in chronic alcoholics , 1997, Neuroscience.