Alcohol-induced neurodegeneration: when, where and why?

Crews, Fulton T.; Collins, Michael A.; Dlugos, Cynthia; Littleton, John; Wilkins, Lincoln; Neafsey, Edward J.; Pentney, Roberta; Snell, Lawrence D.; Tabakoff, Boris; Zou, Jian; Noronha, Antonio

doi:10.1097/01.alc.0000113416.65546.01

Cited by 181Alcoholism and Thiamine DeficiencyAlcohol Consumption and Health EffectsNeuroscience and Neuropharmacology Research

Alcohol-induced neurodegeneration: when, where and why?

Crews, Fulton T., Collins, Michael A., Dlugos, Cynthia, Littleton, John, Wilkins, Lincoln, Neafsey, Edward J., Pentney, Roberta, Snell, Lawrence D. +3 more·2004·Alcoholism Clinical and Experimental Research

DOI 10.1097/01.alc.0000113416.65546.01

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Abstract

This manuscript reviews the proceedings of a symposium organized by Drs. Antonio Noronha and Fulton Crews presented at the 2003 Research Society on Alcoholism meeting. The purpose of the symposium was to examine recent findings on when alcohol induced brain damage occurs, e.g., during intoxication and/or during alcohol withdrawal. Further studies investigate specific brain regions (where) and the mechanisms (why) of alcoholic neurodegeneration. The presentations were (1) Characterization of Synaptic Loss in Cerebella of Mature and Senescent Rats after Lengthy Chronic Ethanol Consumption, (2) Ethanol Withdrawal Both Causes Neurotoxicity and Inhibits Neuronal Recovery Processes in Rat Organotypic Hippocampal Cultures, (3) Binge Drinking-Induced Brain Damage: Genetic and Age Related Effects, (4) Binge Ethanol-Induced Brain Damage: Involvement of Edema, Arachidonic Acid and Tissue Necrosis Factor alpha (TNFalpha), and (5) Cyclic AMP Cascade, Stem Cells and Ethanol. Taken together these studies suggest that alcoholic neurodegeneration occurs through multiple mechanisms and in multiple brain regions both during intoxication and withdrawal.

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Progressive increases in ethanol consumption lead to brain structure alterations that reduce behavioral control, promoting further alcohol abuse and neurodegeneration.
“It has been proposed that progressive increases in ethanol consumption lead to alterations in brain structure that reduce behavioral control promoting further alcohol abuse and neurodegeneration (Crews et al., 2004).”
From Impulsivity, frontal lobes and risk for addiction (2009) · cites this paper as Crews et al., 2004
High blood alcohol levels can induce brain damage in animal models.
“Basic animal model studies have established that high blood levels of alcohol can induce brain damage (Crews et al., 2004).”
From Impulsivity, frontal lobes and risk for addiction (2009) · cites this paper as Crews et al., 2004

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Pentney, R. J. (1995) · Alcohol and Alcoholism · doi:10.1093/oxfordjournals.alcalc.a045705 · Cited by 35 · see citing works
The organotypic entorhinal-hippocampal complex slice culture of adolescent rats. A model to study transcellular changes in a circuit particularly vulnerable in neurodegenerative disorders
Diekmann, S., Nitsch, R., & Ohm, T. G. (1994) · Springer eBooks · doi:10.1007/978-3-7091-9350-1_5 · Cited by 34 · see citing works
Drinking restraint and alcohol-related outcomes: exploring the contributions of beverage instructions, beverage content and self-monitoring.
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Ethanol Pretreatment Enhances NMDA Excitotoxicity in Biogenic Amine Neurons: Protection by Brain Derived Neurotrophic Factor
Crews, F. T., Waage, H. G., Wilkie, M. B., & Lauder, J. M. (1999) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1999.tb04080.x · Cited by 30 · see citing works
9 Adenylyl cyclases and alcohol
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The Number of Granule Cells and Spine Density on Purkinje Cells in Aged, Ethanol-fed Rats
Tabbaa, S., Dlugos, C. A., & Pentney, R. J. (1999) · Alcohol · doi:10.1016/s0741-8329(98)00059-7 · Cited by 23 · see citing works
Transection of intrinsic polysynaptic pathways reduces N-methyl-d-aspartate neurotoxicity in hippocampal slice cultures
Mulholland, P. J., & Prendergast, M. (2003) · Neuroscience Research · doi:10.1016/s0168-0102(03)00102-0 · Cited by 19 · see citing works
Length Changes in Dendritic Networks of Cerebellar Purkinje Cells of Old Rats after Chronic Ethanol Treatment
Pentney, R. J., Quackenbush, L. J., & O’Neill, M. C. (1989) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1989.tb00346.x · Cited by 17 · see citing works
Mechanisms of arachidonic acid induced glial swelling
Winkler, A. S., Baethmann, A. J., Peters, J., Kempski, O. S., & Staub, F. (2000) · Molecular Brain Research · doi:10.1016/s0169-328x(00)00017-6 · Cited by 14 · see citing works
Quantitative Immunocytochemistry of GABA and Synaptophysin in the Cerebellar Cortex of Old Ethanol‐Fed Rats
Dlugos, C. A., & Pentney, R. J. (2002) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2002.tb02477.x · Cited by 12 · see citing works
Quantitative immunocytochemistry of GABA and synaptophysin in the cerebellar cortex of old ethanol-fed rats.
Dlugos, C. A., & Pentney, R. J. (2002) · PubMed · doi:10.1097/01.alc.0000037139.60009.2d · Cited by 10 · see citing works
Synapses Call the Shots
Barinaga, M. (2000) · Science · doi:10.1126/science.290.5492.736 · Cited by 8 · see citing works
Alcohol toxicity in the cerebellum: fundamental aspects
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Untitled work
(1997) · doi:10.1002/(sici)1098-1063(1997)7:1

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Adolescent cortical development: A critical period of vulnerability for addiction
Crews, F., He, J., & Hodge, C. (2007) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.12.001 · Cited by 1,091 · see citing works
“Studies of binge drinking induced brain damage in rats have found that adolescent forebrain is particularly sensitive to ethanol induced neurodegeneration (Crews et al., 2004).”
Background
Impulsivity, frontal lobes and risk for addiction
Crews, F. T., & Boettiger, C. A. (2009) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2009.04.018 · Cited by 679 · see citing works
“Basic animal model studies have established that high blood levels of alcohol can induce brain damage (Crews et al., 2004).”
BackgroundInfluential
Mechanisms of Neurodegeneration and Regeneration in Alcoholism
Crews, F. T., & Nixon, K. (2008) · Alcohol and Alcoholism · doi:10.1093/alcalc/agn079 · Cited by 576 · see citing works
Cytokines and Alcohol
Crews, F. T., Bechara, R. I., Brown, L. A. S., Guidot, D. M., Mandrekar, P., Oak, S. A., Qin, L., Szabó, G., Wheeler, M. D., & Zou, J. (2006) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2006.00084.x · Cited by 414 · see citing works
Intermittent ethanol exposure induces inflammatory brain damage and causes long‐term behavioural alterations in adolescent rats
Pascual, M., Blanco, A. M., Cauli, O., Miñarro, J., & Guerri, C. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05298.x · Cited by 385 · see citing works
“During adolescence, the brain undergoes neuromaturation, which involves changes in neurotransmission and plasticity that are associated with structural modifications in some brain regions, including the hippocampus, prefrontal cortex and the limbic system structures (Dahl, 2004).”
Background
Oxidative stress in anxiety and comorbid disorders
Hovatta, I., Juhila, J., & Donner, J. (2010) · Neuroscience Research · doi:10.1016/j.neures.2010.08.007 · Cited by 365 · see citing works
Alcohol-related dementia: an update of the evidence
Ridley, N. J., Draper, B., & Withall, A. (2013) · Alzheimer's Research & Therapy · doi:10.1186/alzrt157 · Cited by 335 · see citing works
“Support for the neurotoxicity hypothesis emerges from animal studies, which have demonstrated doserelated ethanol-induced damage to brain struc tures – including the hippocampus, hypothalamus, and cerebellum – that correspond with impairments in memory and learning [14,15].”
Background
NADPH oxidase and reactive oxygen species contribute to alcohol-induced microglial activation and neurodegeneration
Qin, L., & Crews, F. T. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-5 · Cited by 290 · see citing works
“Binge ethanol administration in adult rats is known to cause brain damage reduced by anti-oxidants [6-8].”
Background
Molecular and behavioral aspects of the actions of alcohol on the adult and developing brain
Alfonso-Loeches, S., & Guerri, C. (2011) · Critical Reviews in Clinical Laboratory Sciences · doi:10.3109/10408363.2011.580567 · Cited by 254 · see citing works
Butyrate ameliorates chronic alcoholic central nervous damage by suppressing microglia-mediated neuroinflammation and modulating the microbiome-gut-brain axis
Wei, H., Yu, C., Zhang, C., Ren, Y., Guo, L., Wang, T., Chen, F., Li, Y., Zhang, X., Wang, H., et al. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.114308 · Cited by 231 · see citing works
Glial and glutamatergic markers in depression, alcoholism, and their comorbidity
Miguel-Hidalgo, J. J., Waltzer, R., Whittom, A. A., Austin, M. C., Rajkowska, G., & Stockmeier, C. A. (2010) · Journal of Affective Disorders · doi:10.1016/j.jad.2010.06.003 · Cited by 218 · see citing works
“In addition, acute alcohol exposure or alcohol-induced brain damage can result in gliosis (enlargement of astrocytes and their processes) and increased GFAP synthesis (Crews et al., 2004; Evrard et al., 2006).”
Background
Comparison of Cannabidiol, Antioxidants, and Diuretics in Reversing Binge Ethanol-Induced Neurotoxicity
Hamelink, C., Hampson, A. J., Wink, D. A., Eiden, L. E., & Eskay, R. L. (2005) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.105.085779 · Cited by 190 · see citing works
“These include excitotoxicity associated with excessive neurotransmitter release, oxidative stress leading to free radical damage (Eskay et al., 1995; Crews et al., 2004), and edema caused by alterations in cellular control of ion transport (Collins et al., 1998).”
Background
BHT Blocks NF‐κB activation and Ethanol‐Induced Brain Damage
Crews, F. T., Nixon, K., Kim, D., Joseph, J. A., Shukitt‐Hale, B., Qin, L., & Zou, J. (2006) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2006.00239.x · Cited by 184 · see citing works
CREB and NF-κB Transcription Factors Regulate Sensitivity to Excitotoxic and Oxidative Stress Induced Neuronal Cell Death
Zou, J., & Crews, F. T. (2006) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-006-9045-9 · Cited by 164 · see citing works
“Alcoholism is associated with neurodegeneration (Crews et al., 2004) consistent with ethanol induced neurotoxicity.”
Alcohol Use Disorder, Neurodegeneration, Alzheimer’s and Parkinson’s Disease: Interplay Between Oxidative Stress, Neuroimmune Response and Excitotoxicity
Kamal, H., Tan, G. C., Ibrahim, S. F., Shaikh, M. F., Mohamed, I. N., Mohamed, R. M. P., Hamid, A. A., Ugusman, A., & Kumar, J. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00282 · Cited by 164 · see citing works
Neuroimmune Basis of Alcoholic Brain Damage
Crews, F. T., & Vetreno, R. P. (2014) · International review of neurobiology · doi:10.1016/b978-0-12-801284-0.00010-5 · Cited by 160 · see citing works
“…find neurodegeneration in multiple cortical areas that extend from frontal to perirhinal, piriform, and entorhinal cortex (Collins, Zou, & Neafsey, 1998; Corso, Mostafa, Collins, & Neafsey, 1998; Crews et al., 2004; Hamelink, Hampson, Wink, Eiden, & Eskay, 2005; Obernier, Bouldin, & Crews, 2002).”
Background
Induction of Innate Immune Gene Expression Cascades in Brain Slice Cultures by Ethanol: Key Role of NF‐κB and Proinflammatory Cytokines
Zou, J., & Crews, F. T. (2010) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2010.01150.x · Cited by 158 · see citing works
“These studies suggest that ethanol increases NF-jB–DNA binding in brain that could contribute to ethanol-induced neurotoxicity (Crews et al., 2004).”
Background
Differential regional gray matter volumes in patients with on-line game addiction and professional gamers
Han, D. H., Lyoo, I. K., & Renshaw, P. F. (2012) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2012.01.004 · Cited by 156 · see citing works
“Early adolescence has consistently been reported to be a critical period for the maturation of visual cortex (Prusky and Douglas, 2003; Crews et al., 2004).”
Background
Toll-like receptor signaling and stages of addiction
Crews, F. T., Walter, T. J., Coleman, L. G., & Vetreno, R. P. (2017) · Psychopharmacology · doi:10.1007/s00213-017-4560-6 · Cited by 159 · see citing works
“While innate immune activation contributes to alcohol consumptive behaviors, it also contributes to alcohol-induced neurodegeneration (Crews et al. 2004, 2006b; Obernier et al. 2002a, b; Qin et al. 2013).”
Alcohol and adult neurogenesis: Roles in neurodegeneration and recovery in chronic alcoholism
Nixon, K. (2006) · Hippocampus · doi:10.1002/hipo.20162 · Cited by 156 · see citing works
“Many proliferative events, growth factors, cytokines, and other signaling cascades (as detailed elsewhere see Crews et al., 1998, 2004) are shared by these neurodegenerative events.”
Alcoholic neurobiology: changes in dependence and recovery
Crews, F. T., Buckley, T., Dodd, P. R., Ende, G., Foley, N., Harper, C., He, J., Innes, D., Loh, E.-W., Pfefferbaum, A., et al. (2005) · Alcoholism: Clinical & Experimental Research · doi:10.1097/01.alc.0000175013.50644.61 · Cited by 154 · see citing works
Self-citation
Alcohol-Related Dementia and Neurocognitive Impairment: A Review Study
Sachdeva, A., Chandra, M., Choudhary, M., Dayal, P., & Anand, K. S. (2016) · international journal high risk behaviors & addiction · doi:10.5812/ijhrba.27976 · Cited by 142 · see citing works
“Dose related damage has been observed in the hippocampus, hypothalamus, and cerebellum in animal studies (43, 44).”
Background
Dementia associated with alcohol and other drug use
Hulse, G. K., Lautenschlager, N. T., Tait, R. J., & Almeida, O. P. (2005) · International Psychogeriatrics · doi:10.1017/s1041610205001985 · Cited by 134 · see citing works
Biochemical and Neurotransmitter Changes Implicated in Alcohol-Induced Brain Damage in Chronic or 'Binge Drinking' Alcohol Abuse
Ward, R. J., Lallemand, F., & de Witte, P. A. M. (2009) · Alcohol and Alcoholism · doi:10.1093/alcalc/agn100 · Cited by 133 · see citing works
“Although one study did show some benefit of specific anti-oxidants, i.e. furosemide and butylated hydroxytoluene, in preventing neurodegeneration in binge drinking animal models (Crews et al., 2004), no results for NF κ B activation were presented.”
BackgroundInfluential
Facets of impulsivity and alcohol use: What role do emotions play?
Herman, A. M., & Duka, T. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.08.011 · Cited by 131 · see citing works
Research on alcohol and adolescent brain development: opportunities and future directions
Witt, E. D. (2010) · Alcohol · doi:10.1016/j.alcohol.2009.08.011 · Cited by 125 · see citing works
Inflammasome-IL-1β Signaling Mediates Ethanol Inhibition of Hippocampal Neurogenesis
Zou, J., & Crews, F. T. (2012) · Frontiers in Neuroscience · doi:10.3389/fnins.2012.00077 · Cited by 124 · see citing works
Distinct cell proliferation events during abstinence after alcohol dependence: Microglia proliferation precedes neurogenesis
Nixon, K., Kim, D. H., Potts, E. N., He, J., & Crews, F. T. (2008) · Neurobiology of Disease · doi:10.1016/j.nbd.2008.04.009 · Cited by 117 · see citing works
“Further, stereological estimations, profile counts and/or densitometric analyses show identical results in percent change, the measure of interest (Crews et al., 2004).”
BackgroundMethodResultInfluential
Chronic alcohol-induced neuroinflammation involves CCR2/5-dependent peripheral macrophage infiltration and microglia alterations
Lowe, P., Morel, C., Ambade, A., Iracheta‐Vellve, A., Kwiatkowski, E. R., Satishchandran, A., Fűri, I., Cho, Y., Gyöngyösi, B., Catalano, D. E., et al. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-01972-5 · Cited by 114 · see citing works
The neurotoxicity of alcohol
Harper, C. G. (2007) · Human & Experimental Toxicology · doi:10.1177/0960327107070499 · Cited by 112 · see citing works
Suppression of neuro-inflammatory signaling cascade by tocotrienol can prevent chronic alcohol-induced cognitive dysfunction in rats
Tiwari, V., Kuhad, A., & Chopra, K. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.05.016 · Cited by 94 · see citing works
Peroxiredoxin II Maintains the Mitochondrial Membrane Potential against Alcohol-Induced Apoptosis in HT22 Cells
Jin, M., Yu, J., Sun, H., Jin, Y.-H., Shen, G., Jin, C., Cui, Y., Lee, D., Kim, S.-U., Kim, J.-S., et al. (2019) · Antioxidants · doi:10.3390/antiox9010001 · Cited by 87 · see citing works
Fluctuating Disinhibition: Implications for the Understanding and Treatment of Alcohol and Other Substance Use Disorders
Jones, A., Christiansen, P., Nederkoorn, C., Houben, K., & Field, M. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00140 · Cited by 87 · see citing works
“In support of the first explanation, it is well-established that chronic alcoholics present with structural brain damage, with prefrontal areas showing the greatest damage associated with heavy drinking (22, 23).”
Background
Short-Term Supplementation with Plant Extracts Rich in Flavonoids Protect Nigrostriatal Dopaminergic Neurons in a Rat Model of Parkinson's Disease
Datla, K. P., Zbarsky, V., Rai, D., Parkar, S., Osakabe, N., Aruoma, O. I., & Dexter, D. T. (2007) · Journal of the American College of Nutrition · doi:10.1080/07315724.2007.10719621 · Cited by 83 · see citing works
“Studies on rats fed ethanol demonstrate increased lipid peroxidation, TNF- expression, necrosis and mild-inflammation in the brain [69,70].”
Background
Changes in neuropsychological functioning over 10 years following adolescent substance abuse treatment.
Hanson, K. L., Cummins, K. M., Tapert, S. F., & Brown, S. A. (2011) · Psychology of Addictive Behaviors · doi:10.1037/a0022350 · Cited by 78 · see citing works
“For example, rapid cell death and reduced neuro- and gliogenesis appear to occur within the hippocampus both during exposure to high levels of alcohol (i.e., binge drinking) and acute alcohol withdrawal (Crews et al., 2004).”
BackgroundInfluential
Adolescent Intermittent Ethanol Exposure Is Associated with Increased Risky Choice and Decreased Dopaminergic and Cholinergic Neuron Markers in Adult Rats
Boutros, N., Semenova, S., Liu, W., Crews, F. T., & Markou, A. (2015) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyu003 · Cited by 80 · see citing works
Adolescent binge ethanol-induced loss of basal forebrain cholinergic neurons and neuroimmune activation are prevented by exercise and indomethacin
Vetreno, R. P., & Crews, F. T. (2018) · PLoS ONE · doi:10.1371/journal.pone.0204500 · Cited by 78 · see citing works
A low chronic ethanol exposure induces morphological changes in the adolescent rat brain that are not fully recovered even after a long abstinence: An immunohistochemical study
Evrard, S. G., Vega, M. D., Tagliaferro, P. A., Mirochnic, S., Caltana, L. R., & Brusco, A. (2006) · Experimental Neurology · doi:10.1016/j.expneurol.2006.03.001 · Cited by 78 · see citing works
Sex differences in hippocampal damage, cognitive impairment, and trophic factor expression in an animal model of an alcohol use disorder
Maynard, M. E., Barton, E. A., Robinson, C. R., Wooden, J. I., & Leasure, J. L. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1482-3 · Cited by 77 · see citing works
“And while men remain more likely to drink and to drink heavily (Dwyer-Lindgren et al. 2015; Erol and Karpyak 2015), it is concerning that women are beginning to narrow the gender gap in prevalence of alcohol use disorders (AUD) (Holmila and Raitasalo 2005; Wilsnack et al. 2013; Erol and Karpyak 2015).”
Influential
Role of adenosine and wake‐promoting basal forebrain in insomnia and associated sleep disruptions caused by ethanol dependence
Sharma, R., Engemann, S. C., Sahota, P. K., & Thakkar, M. M. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.06980.x · Cited by 75 · see citing works
Alterations of serum brain-derived neurotrophic factor levels in early alcohol withdrawal
Huang, M., Chen, C., Chen, C., Liu, S., Ho, C., Shen, W. W., & Leu, S. (2008) · Alcohol and Alcoholism · doi:10.1093/alcalc/agm172 · Cited by 75 · see citing works
“ture was shown to prevent NMDA excitotoxicity sensitized by ethanol (Crews et al., 2004).”
Hippocampal Dysfunction Provoked by Mercury Chloride Exposure: Evaluation of Cognitive Impairment, Oxidative Stress, Tissue Injury and Nature of Cell Death
Aragão, W. A. B., Teixeira, F. B., Fagundes, N. C. F., Fernandes, R. M., Fernandes, L. M. P., da Silva, M. C. F., Amado, L. L., Sagica, F. D. E. S., de Oliveira, E. H. C., Lopez, M. E. C., et al. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/7878050 · Cited by 75 · see citing works
“Another factor associated with this reduction of neuronal cells may be a notable reduction in their replacement due to the reduction of neurogenesis and gliogenesis [54].”
Background
Ethanol, TLR 3, and TLR 4 Agonists Have Unique Innate Immune Responses in Neuron‐Like SH ‐ SY 5Y and Microglia‐Like BV 2
Lawrimore, C. J., & Crews, F. T. (2017) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.13368 · Cited by 73 · see citing works
“ETHANOL (ETOH) CONSUMPTION causes increasedproinflammatory signaling in brain that is linked with neurodegeneration (Collins et al., 1996; Crews et al., 2004, 2006; Qin et al., 2008; Reynolds et al., 2015), alcoholism (He and Crews, 2008; Vetreno et al., 2013), fetal alcohol syndrome disorder (Drew…”
Background
Alcohol-Mediated Organ Damages: Heart and Brain
Obad, A. S., Peeran, A. A., Little, J. I., Haddad, G. E., & Tarzami, S. T. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00081 · Cited by 73 · see citing works
“…animal models have demonstrated that heavy alcohol use is associated with an increased incidence of myopathy and neuropathy suggesting heart and brain changes (Crews et al., 2004; Liu et al., 2004, 2006; Remick, 2013; Fernandez-Sola and FIGURE 1 | Mechanisms of alcohol-induced tissue injuries.”
Background
Acetyl-l-carnitine protects neuronal function from alcohol-induced oxidative damage in the brain
Rump, T. J., Muneer, P. M. A., Szlachetka, A. M., Lamb, A., Haorei, C., Alikunju, S., Xiong, H., Keblesh, J. P., Liu, J., Zimmerman, M. C., et al. (2010) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2010.08.011 · Cited by 70 · see citing works
“There are multiple mechanisms of alcohol-induced neurotoxicity and neuronal degeneration in various brain regions [6].”
Background
Role of microglia in ethanol-induced neurodegenerative disease: Pathological and behavioral dysfunction at different developmental stages
Yang, J., Xue, X., Tian, H., Wang, X., Dong, Y., Wang, F., Zhao, Y., Yao, X., Cui, W., & Wu, C. (2014) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2014.07.002 · Cited by 72 · see citing works
“Crews and colleagues have proposed that progressive increases in EtOH consumption lead to alterations in brain structures that reduce behavioral control, promoting further alcohol abuse and neurodegeneration (Crews et al., 2004).”
Background
Current hypotheses on the mechanisms of alcoholism
Vetreno, R. P., & Crews, F. T. (2014) · Handbook of clinical neurology · doi:10.1016/b978-0-444-62619-6.00027-6 · Cited by 71 · see citing works
“It has been proposed that progressive increases in alcohol consumption, a common feature of alcoholism, lead to PFC alterations that reduce executive functioning that promote further alcohol abuse and neurodegeneration (Crews et al., 2004).”
BackgroundMethod
Ethanol-Induced Neurodegeneration and Glial Activation in the Developing Brain
Saito, M., Chakraborty, G., Hui, M., Masiello, K., & Saito, M. (2016) · Brain Sciences · doi:10.3390/brainsci6030031 · Cited by 69 · see citing works
“Studies using MRI have shown that brain structural changes associated with alcoholism are enlargement of the ventricles and shrinkage of the frontal cortex, the underlying white matter, and the cerebellum [38,81,82].”
Background
Determining the Threshold for Alcohol‐Induced Brain Damage: New Evidence with Gliosis Markers
Hayes, D. M., Deeny, M. A., Shaner, C. A., & Nixon, K. (2013) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2012.01955.x · Cited by 68 · see citing works
Chronic ethanol exposure during adolescence through early adulthood in female rats induces emotional and memory deficits associated with morphological and molecular alterations in hippocampus
Oliveira, A. C., Pereira, M. C., Santana, L. N. D. S., Fernandes, R. M., Teixeira, F. B., de Oliveira, G. B., Fernandes, L. M. P., Fontes-Júnior, E. A., Prediger, R. D., Lopez, M. E. C., et al. (2015) · Journal of Psychopharmacology · doi:10.1177/0269881115581960 · Cited by 65 · see citing works
“Ethanol is a widely used psychoactive drug (Crews et al., 2004) and adolescence is a critical stage of life in which ethanol exposure usually begins.”
Background
Chronic Alcohol Consumption, Abstinence and Relapse: Brain Proton Magnetic Resonance Spectroscopy Studies in Animals and Humans
Meyerhoff, D. J., Durazzo, T. C., & Ende, G. (2011) · Current topics in behavioral neurosciences · doi:10.1007/7854_2011_131 · Cited by 64 · see citing works
Alcohol-Induced Neurodegeneration, Suppression of Transforming Growth Factor-β, and Cognitive Impairment in Rats: Prevention by Group II Metabotropic Glutamate Receptor Activation
Cippitelli, A., Damadzic, R., Frankola, K., Goldstein, A., Thorsell, A., Singley, E., Eskay, R. L., & Heilig, M. A. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.12.018 · Cited by 62 · see citing works
CREB Gene Transcription Factors: Role in Molecular Mechanisms of Alcohol and Drug Addiction
Pandey, S. C., Chartoff, E. H., Carlezon, W. A., Zou, J., Zhang, H., Kreibich, A. S., Blendy, J. A., & Crews, F. T. (2005) · Alcoholism Clinical and Experimental Research · doi:10.1097/01.alc.0000153550.31168.1d · Cited by 58 · see citing works
The relationship between alcohol use and long-term cognitive decline in middle and late life: a longitudinal analysis using UK Biobank
Piumatti, G., Moore, S. C., Berridge, D. M., Sarkar, C., & Gallacher, J. (2018) · Journal of Public Health · doi:10.1093/pubmed/fdx186 · Cited by 51 · see citing works
Increased Oxidative DNA Damage in Patients With Alcohol Dependence and Its Correlation With Alcohol Withdrawal Severity
Chen, C.-H., Pan, C., Chen, C., & Huang, M. (2010) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2010.01349.x · Cited by 54 · see citing works
“Specifically, oxidative stress and glutamate overactivation are regarded as sequential as well as interacting processes (Coyle and Puttfarcken, 1993) for a variety of neurodegenerative diseases, including chronic alcoholism (Crews et al., 2004).”
Background
Psychological changes and cognitive impairments in adolescent heavy drinkers
Peeters, M., Vollebergh, W. A. M., Wiers, R. W., & Field, M. (2014) · Alcohol and Alcoholism · doi:10.1093/alcalc/agt162 · Cited by 53 · see citing works
“Repeated experience of alcohol withdrawal has been associated with impairments in cognitive functioning (Duka et al., 2002, 2004; Crews et al., 2004) and it is suggested that repeated cycles of binge-withdrawal might lead to deficits in cognition as a consequence of glutamatergic adaptations, which are analogous to th…”
BackgroundResult
Adolescent Intermittent ethanol exposure enhances ethanol activation of the nucleus accumbens while blunting the prefrontal cortex responses in adult rat
Liu, W., & Crews, F. T. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.02.014 · Cited by 53 · see citing works
“Quantification The number of single c-Fos, EGR1, and pERK1/2-positive neurons was quantified by image analysis software as previously described (Crews et al., 2004).”
Method
Relationship of Wine Consumption with Alzheimer’s Disease
Reale, M., Costantini, E., Jagarlapoodi, S., Khan, H. Z., Belwal, T., & Cichelli, A. (2020) · Nutrients · doi:10.3390/nu12010206 · Cited by 53 · see citing works
“showed that, during adolescence, intermittent ethanol intake induces inflammation and cell death in the neocortex, hippocampus, and cerebellum, and cognitive impairment, supporting the role of inflammation in ethanol-induced brain damage [96].”
Background
Controversies about the enhanced vulnerability of the adolescent brain to develop addiction
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Protection against alcohol-induced neuronal and cognitive damage by the PPARγ receptor agonist pioglitazone
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Vitamin E protects developing rat hippocampus and cerebellum against ethanol-induced oxidative stress and apoptosis
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“These include excitotoxicity associated with excessive neurotransmitter release, oxidative stress leading to free radical damage (Andreoli & Mallett, 1997; Eskay, Chautard, Torda, Daoud, & Hamelink, 1995) and edema caused by alterations in cellular control of ion transport (Crews et al., 2004).”
Background
Linking Binge Alcohol-Induced Neurodamage to Brain Edema and Potential Aquaporin-4 Upregulation: Evidence in Rat Organotypic Brain Slice Cultures and In Vivo
Sripathirathan, K., Brown, J. A., Neafsey, E. J., & Collins, M. A. (2009) · Journal of Neurotrauma · doi:10.1089/neu.2008.0682 · Cited by 43 · see citing works
“As such, the neurodamage could ultimately result from oxidative stress arising in part from pro-inﬂammatory, edema-dependent processes such as phospholipase 2 (PLA 2 ) activation and arachidonic acid (AA) mobilization (Crews et al., 2004; Brown et al., 2008).”
Binge ethanol administration enhances the MDMA-induced long-term 5-HT neurotoxicity in rat brain
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“1995), increased intracellular calcium (Lovinger 1993) and an oxidative stress process (Bondy et al. 1996; Crews et al. 2004) mediated by a rise in oxygen and nitrogen-derived reactive species (Lancaster 1992; Reddy et al.”
Background
Cognitive Decline and Recovery in Alcohol Abuse
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“In vitro models show that alcohol impairs the ability of neural stem cells to form, colonize, proliferate, differentiate, and survive (Crews et al. 2004a; Hao et al. 2003; Tateno et al. 2005).”
BackgroundInfluential
The correlation between early alcohol withdrawal severity and oxidative stress in patients with alcohol dependence
Huang, M., Chen, C., Peng, F.-C., Tang, S.-H., & Chen, C.-H. (2008) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2008.10.009 · Cited by 42 · see citing works
Alcohol-Induced Blood-Brain Barrier Impairment: An In Vitro Study
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Are treated alcoholics representative of the entire population with alcohol use disorders? A magnetic resonance study of brain injury
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Structural and Functional Modifications in Glutamateric Synapses Following Prolonged Ethanol Exposure
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The protective effect of vitamin E against prenatal and early postnatal ethanol treatment-induced heart abnormality in rats: A 3-month follow-up study
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Crocin may be useful to prevent or treatment of alcohol induced neurodegeneration and neurobehavioral sequels via modulation of CREB/BDNF and Akt/GSK signaling pathway
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Chemokines, cytokines and substance use disorders
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Binge drinking is associated with attenuated frontal and parietal activation during successful response inhibition in fearful context
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Alcohol use and brain morphology in adolescence: A longitudinal study in three different cohorts
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“Although animal studies have demonstrated that alcohol use in adolescence induces neurodegeneration (Crews et al., 2000, 2004; Pascual et al., 2007) and inhibition of neurogenesis (Crews et al., 2006), it remains to be determined to what extent alcohol use in human adolescents relates to changes in…”
Background
Genetic aspects of behavioral neurotoxicology
Levin, E. D., Aschner, M., Heberlein, U., Ruden, D. M., Welsh-Bohmer, K. A., Bartlett, S. E., Berger, K. H., Chen, L., Corl, A. B., Eddins, D. M., et al. (2009) · NeuroToxicology · doi:10.1016/j.neuro.2009.07.014 · Cited by 32 · see citing works
“…clearly affected by genetic background (Martin et al., 1986; Becker et al., 1996; Gilliam et al., 1997; Olney et al., 2002; Crews and Braun, 2003; Crews et al., 2004; Goodlett et al., 2005; Warren and Li, 2005), there has been limited success identifying the genes involved, due to the limited…”
Background
Effects of Voluntary Alcohol Intake on Risk Preference and Behavioral Flexibility during Rat Adolescence
McMurray, M. S., Amodeo, L. R., & Roitman, J. D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0100697 · Cited by 32 · see citing works
“Studies have shown that the forebrain regions in adolescent rats are especially sensitive to alcohol-induced neurodegeneration and inhibition of neurogenesis [19,20].”
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Binge Ethanol-induced Neurodegeneration in Rat Organotypic Brain Slice Cultures: Effects of PLA2 Inhibitor Mepacrine and Docosahexaenoic Acid (DHA)
Brown, J. A., Achille, N. J., Neafsey, E. J., & Collins, M. A. (2008) · Neurochemical Research · doi:10.1007/s11064-008-9765-y · Cited by 31 · see citing works
“These results are consistent with binge or episodic ethanol-induced brain damage involving to an appreciable extent neuroinflammatory PLA2 activation, excess AA mobilization and oxidative stress that are conceivably downstream of neuroglial edema/electrolyte dysregulation [7, 34].”
Result
Potential Value of Changes in Cell Markers in Organotypic Hippocampal Cultures Associated With Chronic EtOH Exposure and Withdrawal: Comparison with NMDA‐Induced Changes
Wilkins, L. H., Prendergast, M., Blanchard, J. A., Holley, R. C., Chambers, E. R., & Littleton, J. M. (2006) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2006.00210.x · Cited by 31 · see citing works
Effects of Ethanol Exposure on Nervous System Development in Zebrafish
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Identifying a novel biological mechanism for alcohol addiction associated with circRNA networks acting as potential miRNA sponges
Vornholt, E., Drake, J. W., Mamdani, M., McMichael, G. O., Taylor, Z. N., Bacanu, S., Miles, M. F., & Vladimirov, V. I. (2021) · Addiction Biology · doi:10.1111/adb.13071 · Cited by 26 · see citing works
Association Between Reduced Brain Glucose Metabolism and Cortical Thickness in Alcoholics: Evidence of Neurotoxicity
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“This cortical GM loss in people with AUD likely reflects reversible neurodegeneration (Crews et al., 2004; Bartsch et al., 2007), although there is also evidence of long-lasting neuropathology particularly in frontal regions (Volkow et al.”
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Botulinum Neurotoxin: The Ugly Duckling
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Volumetric Reductions of Subcortical Structures and Their Localizations in Alcohol-Dependent Patients
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“It has also been considered that certain portions of the brain experience different rates of degeneration in chronic exposure to alcohol depending on how each structure reacts to loss of nutrition and to inhibition of neuroregeneration (12).”
Background
Common polymorphisms in interleukin genes (IL4, IL6, IL8 and IL12) are not associated with alcoholic liver disease or alcoholism in Spanish men
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Ceramide metabolism analysis in a model of binge drinking reveals both neuroprotective and toxic effects of ethanol
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“L-channel blockers have been found to have some neuroprotective actions that may contribute to their beneﬁcial effects, for example, against brain damage caused by alcohol withdrawal (Chandler et al., 1993; Crews et al., 2004).”
Background
Effects of the Positive Allosteric Modulator of Metabotropic Glutamate Receptor 5, VU-29, on Impairment of Novel Object Recognition Induced by Acute Ethanol and Ethanol Withdrawal in Rats
Marszałek‐Grabska, M., Gibuła‐Tarłowska, E., Bodzoń‐Kułakowska, A., Suder, P., Gaweł, K., Filarowska, J., Listos, J., Danysz, W., & Kotlinska, J. H. (2018) · Neurotoxicity Research · doi:10.1007/s12640-017-9857-z · Cited by 23 · see citing works
“As demonstrated before (Crews et al. 2004), these brain structures are very susceptible to ethanol-induced neurodegeneration.”
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Alcohol's Burden on Immunity Following Burn, Hemorrhagic Shock, or Traumatic Brain Injury
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Neuropsychological Dysfunction among HIV Infected Drug Abusers
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Ethanol Induction of Innate Immune Signals Across BV2 Microglia and SH-SY5Y Neuroblastoma Involves Induction of IL-4 and IL-13
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“However, we observed a significant main effect of co-culture (F [1,17] = 9.”
BackgroundInfluential
Adult-Life Alcohol Consumption and Age-Related Cognitive Decline from Early Adulthood to Late Midlife
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Comparative effects of EtOH consumption and thiamine deficiency on cognitive impairment, oxidative damage, and β-amyloid peptide overproduction in the brain
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DUI Offenders Who Delay Relicensing: A Quantitative and Qualitative Investigation
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“Alcohol abuse–related neurotoxicity is well documented and commonly involves impair ment to executive functioning, declarative memory, language skills, and visuospatial, motor, and perceptual abilities (Crews et al., 2004, 2005; Parsons & Nixon, 1998).”
Type 1 equilibrative nucleoside transporter regulates astrocyte‐specific glial fibrillary acidic protein expression in the striatum
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Zonisamide Ameliorated the Apoptosis and Inflammation in Cerebellar Tissue of Induced Alcohol Addiction Animal Model
Aşir, F., Erdemci, F., Çankırı, Z., Korak, T., Başaran, S. Ö., Kaplan, Ö., Yükselmiş, Ö., Dönmezdil, N., Ayaz, H., Kaplan, Ş., et al. (2024) · Life · doi:10.3390/life14070795 · Cited by 16 · see citing works

Mechanisms of Neurodegeneration and Regeneration in Alcoholism
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Advance Access publication 21 October 2008 Mechanisms of Neurodegeneration and Regeneration in Alcoholism
Crews, F. T., & Nixon, K. (2016)
Binge Ethanol Exposure in Adult Rats Causes Necrotic Cell Death
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Does chronic alcohol exposure induce neurodegeneration in the central nervous system of rats
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Glutamate Receptor-Mediated Neurotoxicity in a Model of Ethanol Dependence and Withdrawal in Rat Organotypic Hippocampal Slice Cultures
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Authors: Crews, F. T., Collins, M. A., Dlugos, C., Littleton, J., Wilkins, L., Neafsey, E. J., Pentney, R., Snell, L. D., Tabakoff, B., Zou, J., & Noronha, A.
Affiliations: University of North Carolina at Chapel Hill (US)
Corresponding author: Crews, Fulton T.
ORCID: Crews, Fulton T.
Collins, Michael A.
Tabakoff, Boris
Zou, Jian
Venue: Alcoholism Clinical and Experimental Research
Publisher: Wiley
Published: 2004-02
Volume: 28
Issue: 2
Pages: 350-364
ISSN: 0145-6008 (ISSN-L)
1530-0277
DOI: 10.1097/01.alc.0000113416.65546.01
OpenAlex: W2086810773
Cited by: 181
References: 98
Citations by year: 2026: 3 · 2025: 7 · 2024: 5 · 2023: 7 · 2022: 3 · 2021: 9 · 2020: 9 · 2019: 11 · 2018: 9 · 2017: 7 · 2016: 8 · 2015: 12 · 2014: 14 · 2013: 6 · 2012: 9
FWCI: 4.92
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 822 d)
Locations: Alcoholism Clinical and Experimental Research (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Neurology › Alcoholism and Thiamine Deficiency
Health Sciences › Medicine › Pathology and Forensic Medicine › Alcohol Consumption and Health Effects
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: ethanol neurotoxicity, alcohol withdrawal, binge drinking, chronic alcohol consumption, hippocampal cultures, neuronal recovery, cerebral edema, arachidonic acid, TNF-α, cyclic AMP, stem cells, aging, genetic susceptibility
MeSH terms: Alcohol Drinking, Ethanol, Animals, Cell Differentiation, Humans, Nerve Degeneration, Neurons, Societies, Medical, United States

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Alcohol-induced neurodegeneration: when, where and why?

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