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

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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·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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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
“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., Costantini, E., Jagarlapoodi, S., Khan, H., Belwal, T., & Cichelli, A. (2020) · Nutrients · doi:10.3390/nu12010206 · Cited by 56
“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
Bernheim, A., Halfon, O., & Boutrel, B. (2013) · Frontiers in Pharmacology · doi:10.3389/fphar.2013.00118 · Cited by 49
Alcohol-related neurodegeneration and recovery: mechanisms from animal models.
Crews, F. T. (2008) · Europe PMC (PubMed Central) · Cited by 49
Protection against alcohol-induced neuronal and cognitive damage by the PPARγ receptor agonist pioglitazone
Cippitelli, A., Domi, E., Ubaldi, M., Douglas, J. C., Li, H. W., Demopulos, G. A., Gaitanaris, G., Roberto, M., Drew, P. D., Kane, C. J. M., et al. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.02.001 · Cited by 47
Vitamin E protects developing rat hippocampus and cerebellum against ethanol-induced oxidative stress and apoptosis
Shirpoor, A., Minassian, S., Salami, S., Ansari, M. H. K., Pakdel, F. G., & Yeghiazaryan, M. (2008) · Food Chemistry · doi:10.1016/j.foodchem.2008.07.034 · Cited by 45
“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
“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
Izco, M., Orío, L., O’Shea, E., & Colado, M. I. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0602-1 · Cited by 43
“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
Perry, C. J. (2016) · Journal of Molecular Neuroscience · doi:10.1007/s12031-016-0798-4 · Cited by 42
“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
Alcohol-Induced Blood-Brain Barrier Impairment: An In Vitro Study
Carrino, D., Branca, J. J. V., Becatti, M., Paternostro, F., Morucci, G., Gulisano, M., Mannelli, L. D. C., & Pacini, A. (2021) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph18052683 · Cited by 43
Are treated alcoholics representative of the entire population with alcohol use disorders? A magnetic resonance study of brain injury
Gazdzinski, S. P., Durazzo, T. C., Weiner, M. W., & Meyerhoff, D. J. (2008) · Alcohol · doi:10.1016/j.alcohol.2008.01.002 · Cited by 41
Binge ethanol effects on prefrontal cortex neurons, spatial working memory and task-induced neuronal activation in male and female rats
West, R. K., Maynard, M. E., & Leasure, J. L. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2018.01.027 · Cited by 39
Structural and Functional Modifications in Glutamateric Synapses Following Prolonged Ethanol Exposure
Chandler, L. J., Carpenter‐Hyland, E. P., Hendricson, A. W., Maldve, R. E., Morrisett, R. A., Zhou, F., Sari, Y., Bell, R. L., & Szumlinski, K. K. (2006) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2006.00041.x · Cited by 38
The protective effect of vitamin E against prenatal and early postnatal ethanol treatment-induced heart abnormality in rats: A 3-month follow-up study
Shirpoor, A., Nemati, S., Ansari, M. H. K., & Ilkhanizadeh, B. (2015) · International Immunopharmacology · doi:10.1016/j.intimp.2015.03.008 · Cited by 35
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
Motaghinejad, M., Safari, S., Feizipour, S., & Sadr, S. (2019) · Medical Hypotheses · doi:10.1016/j.mehy.2019.01.017 · Cited by 34
Chemokines, cytokines and substance use disorders
Ahearn, O., Watson, M. N., & Rawls, S. M. (2021) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2021.108511 · Cited by 33
Binge drinking is associated with attenuated frontal and parietal activation during successful response inhibition in fearful context
Herman, A. M., Critchley, H., & Duka, T. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14108 · Cited by 36
Alcohol use and brain morphology in adolescence: A longitudinal study in three different cohorts
Marroun, H. E., Klapwijk, E. T., Koevoets, M., Brouwer, R. M., Peters, S., Ent, D. V. ‘., Boomsma, D. I., Muetzel, R. L., Crone, E. A., Pol, H. E. H., et al. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15411 · Cited by 31
“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
“…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
“Studies have shown that the forebrain regions in adolescent rats are especially sensitive to alcohol-induced neurodegeneration and inhibition of neurogenesis [19,20].”
Background
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
“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
Effects of Ethanol Exposure on Nervous System Development in Zebrafish
Cole, G. J., Zhang, C., Ojiaku, P., Bell, V., Devkota, S., & Mukhopadhyay, S. (2012) · International review of cytology · doi:10.1016/b978-0-12-394310-1.00007-2 · Cited by 30
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
Association Between Reduced Brain Glucose Metabolism and Cortical Thickness in Alcoholics: Evidence of Neurotoxicity
Tomasi, D. G., Wiers, C. E., Kojori, E. S., Zehra, A., Ramirez, V., Freeman, C. R., Burns, J. A., Liu, C. K., Manza, P., Kim, S. W., et al. (2019) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyz036 · Cited by 26
“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.”
Background
Botulinum Neurotoxin: The Ugly Duckling
Koussoulakos, S. L. (2009) · European Neurology · doi:10.1159/000210545 · Cited by 26
Volumetric Reductions of Subcortical Structures and Their Localizations in Alcohol-Dependent Patients
Shim, J., Kim, Y., Kim, S., & Baek, H. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.00247 · Cited by 25
“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
Marcos, M., Pastor, I., González‐Sarmiento, R., & Laso, F. J. (2009) · Cytokine · doi:10.1016/j.cyto.2008.11.003 · Cited by 25
“The relationship of cytokines with ethanol-induced brain damage is receiving increasing attention [7,13] but still there are little data supporting this association.”
Background
Ceramide metabolism analysis in a model of binge drinking reveals both neuroprotective and toxic effects of ethanol
Bae, M. H., Bandaru, V. V. R., Patel, N., & Haughey, N. J. (2014) · Journal of Neurochemistry · doi:10.1111/jnc.12834 · Cited by 25
L-Type Calcium Channel Blockers: A Potential Novel Therapeutic Approach to Drug Dependence
Little, H. J. (2021) · Pharmacological Reviews · doi:10.1124/pharmrev.120.000245 · Cited by 24
“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
“As demonstrated before (Crews et al. 2004), these brain structures are very susceptible to ethanol-induced neurodegeneration.”
Background
Alcohol's Burden on Immunity Following Burn, Hemorrhagic Shock, or Traumatic Brain Injury
Molina, P. E. (2015) · Alcohol research · doi:10.35946/arcr.v37.2.10 · Cited by 23
Sleep–wakefulness in alcohol preferring and non-preferring rats following binge alcohol administration
Thakkar, M. M., Engemann, S. C., Sharma, R., Mohan, R. R., & Sahota, P. K. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.07.005 · Cited by 22
Sex and Age Effects on Neurobehavioral Toxicity Induced by Binge Alcohol
Cortez, I., Rodgers, S. P., Kosten, T. A., & Leasure, J. L. (2020) · Brain Plasticity · doi:10.3233/bpl-190094 · Cited by 22
Neuropsychological Dysfunction among HIV Infected Drug Abusers
Durvasula, R., & Hinkin, C. H. (2006) · American Journal of Infectious Diseases · doi:10.3844/ajidsp.2006.67.73 · Cited by 21
Ethanol Induction of Innate Immune Signals Across BV2 Microglia and SH-SY5Y Neuroblastoma Involves Induction of IL-4 and IL-13
Lawrimore, C. J., Coleman, L. G., Zou, J., & Crews, F. T. (2019) · Brain Sciences · doi:10.3390/brainsci9090228 · Cited by 21
“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
Grønkjær, M. S., Flensborg‐Madsen, T., Osler, M., Sørensen, H. J., Becker, U., & Mortensen, E. L. (2019) · Alcohol and Alcoholism · doi:10.1093/alcalc/agz038 · Cited by 21
Comparative effects of EtOH consumption and thiamine deficiency on cognitive impairment, oxidative damage, and β-amyloid peptide overproduction in the brain
Gong, Y.-S., Hu, K., Yang, L., Guo, J., Gao, Y., Song, F., Hou, F., & Liang, C.-Y. (2017) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2017.03.019 · Cited by 19
Polyamine Modulation of NMDARs as a Mechanism to Reduce Effects of Alcohol Dependence
Barron, S., Lewis, B., Wellmann, K. A., Carter, M., Farook, J. M., Ring, J., Rogers, D. T., Holley, R. C., Crooks, P. A., & Littleton, J. M. (2012) · Recent Patents on CNS Drug Discovery · doi:10.2174/157488912800673128 · Cited by 18
“Alcohol acutely reduces neuronal viability and neurogenesis [164], but neurotoxicity also occurs during alcohol withdrawal [see 11].”
Background
DUI Offenders Who Delay Relicensing: A Quantitative and Qualitative Investigation
Brown, T., Ouimet, M., Nadeau, L., Lepage, M., Tremblay, J., Dongier, M., & Kin, N. (2008) · Traffic Injury Prevention · doi:10.1080/15389580801907908 · Cited by 20
“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
Hinton, D. J., Lee, M. R., Jang, J. S., & Choi, D. (2014) · Brain and Behavior · doi:10.1002/brb3.283 · Cited by 17
Cell Death is Associated with Reduced Base Excision Repair During Chronic Alcohol Administration in Adult Rat Brain
Sunkesula, S. R. B., Swain, U., & Babu, P. P. (2008) · Neurochemical Research · doi:10.1007/s11064-007-9560-1 · Cited by 17
“Neurodegeneration has been demonstrated during ethanol intoxication (in vivo and in vitro) and it is suggested that there is difference in the pattern of degeneration [3].”
Background
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

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 › Clinical 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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