Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-28T12:57:03.102Z Has data issue: false hasContentIssue false
  • English
  • Français

Problematic alcohol use and reduced hippocampal volume: a meta-analytic review

Published online by Cambridge University Press:  04 April 2017

S. Wilson ,
J. L. Bair ,
K. M. Thomas  and
W. G. Iacono
S. Wilson*
Affiliation:
Department of Psychology, University of Minnesota, 75 E River Rd, Minneapolis, MN, USA
J. L. Bair
Affiliation:
Department of Psychology, University of Minnesota, 75 E River Rd, Minneapolis, MN, USA
K. M. Thomas
Affiliation:
Institute of Child Development, 51 E River Rd, Minneapolis, MN, USA
W. G. Iacono
Affiliation:
Department of Psychology, University of Minnesota, 75 E River Rd, Minneapolis, MN, USA
*
*Address for correspondence: S. Wilson, Department of Psychology, University of Minnesota, 75 E River Rd, Minneapolis, MN 55455, USA. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

A number of studies reports reduced hippocampal volume in individuals who engage in problematic alcohol use. However, the magnitude of the difference in hippocampal volume between individuals with v. without problematic alcohol use has varied widely, and there have been null findings. Moreover, the studies comprise diverse alcohol use constructs and samples, including clinically significant alcohol use disorders and subclinical but problematic alcohol use (e.g. binge drinking), adults and adolescents, and males and females.

Methods

We conducted the first quantitative synthesis of the published empirical research on associations between problematic alcohol use and hippocampal volume. In total, 23 studies were identified and selected for inclusion in the meta-analysis; effects sizes were aggregated using a random-effects model.

Results

Problematic alcohol use was associated with significantly smaller hippocampal volume (d = −0.53). Moderator analyses indicated that effects were stronger for clinically significant v. subclinical alcohol use and among adults relative to adolescents; effects did not differ among males and females.

Conclusions

Problematic alcohol use is associated with reduced hippocampal volume. The moderate overall effect size suggests the need for larger samples than are typically included in studies of alcohol use and hippocampal volume. Because the existing literature is almost entirely cross-sectional, future research using causally informative study designs is needed to determine whether this association reflects premorbid risk for the development of problematic alcohol use and/or whether alcohol has a neurotoxic effect on the hippocampus.

Keywords

Alcohol usehippocampal volumemeta-analysis
Type
Original Articles
Information
Psychological Medicine , Volume 47 , Issue 13 , October 2017 , pp. 2288 - 2301
Copyright
Copyright © Cambridge University Press 2017 

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

Abrous, DN, Koehl, M, Le Moal, M (2005). Adult neurogenesis: from precursors to network and physiology. Physiological Reviews 85, 523–569.Google Scholar
Agartz, I, Shoaf, S, Rawlings, RR, Momenan, R, Hommer, DW (2003). CSF monoamine metabolites and MRI brain volumes in alcohol dependence. Psychiatry Research: Neuroimaging 122, 21–35.Google Scholar
Bartels, C, Kunert, H-J, Stawicki, S, Kröner-Herwig, B, Ehrenreich, H, Krampe, H (2007). Recovery of hippocampus-related functions in chronic alcoholics during monitored long-term abstinence. Alcohol and Alcoholism 42, 92–102.Google Scholar
Benegal, V, Antony, G, Venkatasubramanian, G, Jayakumar, PN (2007). Gray matter volume abnormalities and externalizing symptoms in subjects at high risk for alcohol dependence. Addiction Biology 12, 122–132.Google Scholar
Beresford, TP, Arciniegas, DB, Alfers, J, Clapp, L, Martin, B, Lie, YDD, Shen, D, Davatzikos, C (2006). Hippocampus volume loss due to chronic heavy drinking. Alcoholism: Clinical and Experimental Research 30, 1866–1870.Google Scholar
Bjork, JM, Grant, SJ, Hommer, DW (2003). Cross-sectional volumetric analysis of brain atrophy in alcohol dependence: effects of drinking history and comorbid substance use disorder. American Journal of Psychiatry 160, 1–8.Google Scholar
Bleich, S, Sperling, W, Degner, D, Graesel, E, Bleich, K, Wilhelm, J, Havemann-Reinecke, U, Javaheripour, K, Kornhuber, J (2003). Lack of association between hippocampal volume reduction and first-onset alcohol withdrawal seizure: a volumetric MRI study. Alcohol and Alcoholism 38, 40–44.CrossRefGoogle ScholarPubMed
Borenstein, M, Hedges, L, Higgins, J, Rothstein, H (2014). Comprehensive Meta-Analysis Version 3. Biostat: Englewood, NJ.Google Scholar
Campbell, S, Marriott, M, Nahmias, C, MacQueen, GM (2004). Lower hippocampal volume in patients suffering from depression: a meta-analysis. American Journal of Psychiatry 161, 598–607.Google Scholar
Cardenas, VA, Studholme, C, Gazdzinski, S, Durazzo, TC, Meyerhoff, DJ (2007). Deformation-based morphometry of brain changes in alcohol dependence and abstinence. NeuroImage 34, 879–887.Google Scholar
Cardenas, VA, Studholme, C, Meyerhoff, DJ, Song, E, Weiner, MW (2005). Chronic active heavy drinking and family history of problem drinking modulate regional brain tissue volumes. Psychiatry Research: Neuroimaging 138, 115–130.Google Scholar
Cheetham, A, Allen, NB, Whittle, S, Simmons, J, Yücel, M, Lubman, DI (2014). Volumetric differences in the anterior cingulate cortex prospectively predict alcohol-related problems in adolescence. Psychopharmacology 231, 1731–1742.Google Scholar
Cipolotti, L, Bird, CM (2006). Amnesia and the hippocampus. Current Opinion in Neurology 19, 593–598.CrossRefGoogle ScholarPubMed
Cohen, J (1988). Statistical Power Analysis for the Behavioral Sciences. Erlbaum: Hillsdale, NJ.Google Scholar
Crews, FT, Nixon, K (2009). Mechanisms of neurodegeneration and regeneration in alcoholism. Alcohol and Alcoholism 44, 115–127.Google Scholar
De Bellis, MD, Clark, DB, Beers, SR, Soloff, PH, Boring, AM, Hall, J, Kersh, A, Keshavan, MS (2000). Hippocampal volume in adolescent-onset alcohol use disorders. American Journal of Psychiatry 157, 737–744.CrossRefGoogle ScholarPubMed
de Kloet, ER, Joëls, M, Holsboer, F (2005). Stress and the brain: from adaptation to disease. Nature Reviews Neuroscience 6, 463–475.Google Scholar
den Heijer, T, Vermeer, SE, van Dijk, EJ, Prins, ND, Koudstaal, PJ, van Duijn, CM, Hofman, A, Breteler, MMB (2004). Alcohol intake in relation to brain magnetic resonance imaging findings in older persons without dementia. American Journal of Clinical Nutrition 80, 992–997.Google Scholar
Durazzo, TC, Tosun, D, Buckley, S, Gazdzinski, S, Mon, A, Fryer, SL, Meyerhoff, DJ (2011). Cortical thickness, surface area, and volume of the brain reward system in alcohol dependence: relationships to relapse and extended abstinence. Alcoholism: Clinical and Experimental Research 35, 1187–1200.Google Scholar
Duval, S, Tweedie, R (2000). Trim and fill: a simple funnel-plot–based method of testing and adjusting for publication bias in meta-analysis. Biometrics 56, 455–463.Google Scholar
Egger, M, Smith, GD, Schneider, M, Minder, C (1997). Bias in meta-analysis detected by a simple, graphical test. British Medical Journal 315, 629–634.Google Scholar
Eriksson, PS, Perfilieva, E, Björk-Eriksson, T, Alborn, A-M, Nordborg, C, Peterson, DA, Gage, FH (1998). Neurogenesis in the adult human hippocampus. Nature Medicine 4, 1313–1317.Google Scholar
Faul, F, Erdfelder, E, Lang, A-G, Buchner, A (2007). G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods 39, 175–191.Google Scholar
Fein, G, Fein, D (2013). Subcortical volumes are reduced in short-term and long-term abstinent alcoholics but not those with a comorbid stimulant disorder. NeuroImage: Clinical 3, 47–53.CrossRefGoogle Scholar
Fein, G, Greenstein, D, Cardenas, VA, Cuzen, NL, Fouche, J-P, Ferrett, H, Thomas, K, Stein, DJ (2013). Cortical and subcortical volumes in adolescents with alcohol dependence but without substance or psychiatric comorbidities. Psychiatry Research: Neuroimaging 214, 1–8.Google Scholar
Gazdzinski, S, Durazzo, TC, Yeh, P-H, Hardin, D, Banys, P, Meyerhoff, DJ (2008). Chronic cigarette smoking modulates injury and short-term recovery of the medial temporal lobe in alcoholics. Psychiatry Research: Neuroimaging 162, 133–145.CrossRefGoogle ScholarPubMed
Gross, CM, Spiegelhalder, K, Mercak, J, Feige, B, Langosch, JM (2013). Predictability of alcohol relapse by hippocampal volumetry and psychometric variables. Psychiatry Research: Neuroimaging 212, 14–18.CrossRefGoogle ScholarPubMed
Hanson, KL, Medina, KL, Nagel, BJ, Spadoni, AD, Gorlick, A, Tapert, SF (2010). Hippocampal volumes in adolescents with and without a family history of alcoholism. American Journal of Drug and Alcohol Abuse 36, 161–167.Google Scholar
He, J, Nixon, K, Shetty, AK, Crews, FT (2005). Chronic alcohol exposure reduces hippocampal neurogenesis and dendritic growth of newborn neurons. European Journal of Neuroscience 21, 2711–2720.Google Scholar
Herrera, DG, Yagüe, AG, Johnsen-Soriano, S, Bosch-Morell, F, Collado-Morente, L, Muriach, M, Romero, FJ, García-Verdugo, JM (2003). Selective impairment of hippocampal neurogenesis by chronic alcoholism: protective effects of an antioxidant. Proceedings of the National Academy of Sciences 100, 7919–7924.Google Scholar
Hill, SY, De Bellis, MD, Keshavan, MS, Lowers, L, Shen, S, Hall, J, Pitts, T (2001). Right amygdala volume in adolescent and young adult offspring from families at high risk for developing alcoholism. Biological Psychiatry 49, 894–905.Google Scholar
Hommer, DW (2003). Male and female sensitivity to alcohol-induced brain damage. Alcohol Research and Health 27, 181–185.Google Scholar
Honey, GD, Fletcher, PC, Bullmore, ET (2002). Functional brain mapping of psychopathology. Journal of Neurology, Neurosurgery and Psychiatry 72, 432–439.Google Scholar
Ieraci, A, Herrera, DG (2007). Single alcohol exposure in early life damages hippocampal stem/progenitor cells and reduces adult neurogenesis. Neurobiology of Disease 26, 597–605.Google Scholar
Jacobus, J, Tapert, SF (2013). Neurotoxic effects of alcohol in adolescence. Annual Review of Clinical Psychology 9, 703–721.Google Scholar
Karl, A, Schaefer, M, Malta, LS, Dörfel, D, Rohleder, N, Werner, A (2006). A meta-analysis of structural brain abnormalities in PTSD. Neuroscience and Biobehavioral Reviews 30, 1004–1031.Google Scholar
Kim, JJ, Diamond, DM (2002). The stressed hippocampus, synaptic plasticity and lost memories. Nature Reviews Neuroscience 3, 453–462.Google Scholar
Kitayama, N, Vaccarino, V, Kutner, M, Weiss, P, Bremner, JD (2005). Magnetic resonance imaging (MRI) measurement of hippocampal volume in posttraumatic stress disorder: a meta-analysis. Journal of Affective Disorders 88, 79–86.Google Scholar
Koolschijn, P, van Haren, NE, Lensvelt-Mulders, GJ, Pol, H, Hilleke, E, Kahn, RS (2009). Brain volume abnormalities in major depressive disorder: a meta-analysis of magnetic resonance imaging studies. Human Brain Mapping 30, 3719–3735.CrossRefGoogle ScholarPubMed
Laakso, MP, Vaurio, O, Savolainen, L, Repo, E, Soininen, H, Aronen, HJ, Tiihonen, J (2000). A volumetric MRI study of the hippocampus in type 1 and 2 alcoholism. Behavioural Brain Research 109, 177–186.Google Scholar
LaBar, KS, Cabeza, R (2006). Cognitive neuroscience of emotional memory. Nature Reviews Neuroscience 7, 54–64.Google Scholar
Le Berre, A-P, Pitel, A-L, Chanraud, S, Beaunieux, H, Eustache, F, Martinot, J-L, Reynaud, M, Martelli, C, Rohlfing, T, Sullivan, EV, Pfefferbaum, A (2014). Chronic alcohol consumption and its effect on nodes of frontocerebellar and limbic circuitry: comparison of effects in France and the United States. Human Brain Mapping 35, 4635–4653.CrossRefGoogle ScholarPubMed
Lee, E, Jang, D-P, Kim, J-J, An, SK, Park, S, Kim, I-Y, Kim, SI, Yoon, K-J, Namkoong, K (2007). Alteration of brain metabolites in young alcoholics without structural changes. NeuroReport 18, 1511–1514.Google Scholar
Light, R, Pillemer, DB (1984). Summing Up. Harvard University Press: Cambridge, MA.Google Scholar
Lipsey, MW, Wilson, DB (2001). Practical Meta-analysis. Sage: Thousand Oaks, CA.Google Scholar
Makris, N, Oscar-Berman, M, Jaffin, SK, Hodge, SM, Kennedy, DN, Caviness, VS, Marinkovic, K, Breiter, HC, Gasic, GP, Harris, GJ (2008). Decreased volume of the brain reward system in alcoholism. Biological Psychiatry 64, 192–202.CrossRefGoogle ScholarPubMed
Malone, SM, Luciana, M, Wilson, S, Sparks, JC, Hunt, RH, Thomas, KM, Iacono, WG (2014). Adolescent drinking and motivated decision-making: a cotwin-control investigation with monozygotic twins. Behavior Genetics 44, 407–418.Google Scholar
McEwen, BS (2007). Physiology and neurobiology of stress and adaptation: central role of the brain. Physiological Reviews 87, 873–904.Google Scholar
Medina, KL, Schweinsburg, AD, Cohen-Zion, M, Nagel, BJ, Tapert, SF (2007). Effects of alcohol and combined marijuana and alcohol use during adolescence on hippocampal volume and asymmetry. Neurotoxicology and Teratology 29, 141–152.CrossRefGoogle ScholarPubMed
Miller, G (2010). Beyond DSM: seeking a brain-based classification of mental illness. Science 327, 1437–1437.Google Scholar
Nagel, BJ, Schweinsburg, AD, Phan, V, Tapert, SF (2005). Reduced hippocampal volume among adolescents with alcohol use disorders without psychiatric comorbidity. Psychiatry Research: Neuroimaging 139, 181–190.Google Scholar
Nixon, K (2006). Alcohol and adult neurogenesis: roles in neurodegeneration and recovery in chronic alcoholism. Hippocampus 16, 287–295.Google Scholar
Nixon, K, Crews, FT (2002). Binge ethanol exposure decreases neurogenesis in adult rat hippocampus. Journal of Neurochemistry 83, 1087–1093.Google Scholar
Nixon, K, Crews, FT (2004). Temporally specific burst in cell proliferation increases hippocampal neurogenesis in protracted abstinence from alcohol. Journal of Neuroscience 24, 9714–9722.Google Scholar
Oscar-Berman, M, Marinković, K (2007). Alcohol: effects on neurobehavioral functions and the brain. Neuropsychology Review 17, 239–257.CrossRefGoogle ScholarPubMed
Ozsoy, S, Durak, AC, Esel, E (2013). Hippocampal volumes and cognitive functions in adult alcoholic patients with adolescent-onset. Alcohol 47, 9–14.Google Scholar
Schuff, N, Neylan, TC, Fox-Bosetti, S, Lenoci, M, Samuelson, KW, Studholme, C, Kornak, J, Marmar, CR, Weiner, MW (2008). Abnormal N-acetylaspartate in hippocampus and anterior cingulate in posttraumatic stress disorder. Psychiatry Research: Neuroimaging 162, 147–157.Google Scholar
Smith, ME (2005). Bilateral hippocampal volume reduction in adults with post-traumatic stress disorder: a meta-analysis of structural MRI studies. Hippocampus 15, 798–807.Google Scholar
Smith, MJ, Wang, L, Cronenwett, W, Goldman, MB, Mamah, D, Barch, DM, Csernansky, JG (2011). Alcohol use disorders contribute to hippocampal and subcortical shape differences in schizophrenia. Schizophrenia Research 131, 174–183.Google Scholar
Starcevic, A, Dimitrijevic, I, Aksic, M, Stijak, L, Radonjic, V, Aleksic, D, Filipovic, B (2015). Brain changes in patients with posttraumatic stress disorder and associated alcoholism: MRI based study. Psychiatria Danubina 27, 78–83.Google Scholar
Sullivan, EV, Marsh, L, Mathalon, DH, Lim, KO, Pfefferbaum, A (1995). Anterior hippocampal volume deficits in nonamnesic, aging chronic alcoholics. Alcoholism: Clinical and Experimental Research 19, 110–122.Google Scholar
Taffe, MA, Kotzebue, RW, Crean, RD, Crawford, EF, Edwards, S, Mandyam, CD (2010). Long-lasting reduction in hippocampal neurogenesis by alcohol consumption in adolescent nonhuman primates. Proceedings of the National Academy of Sciences 107, 11104–11109.Google Scholar
van Praag, H, Schinder, AF, Christie, BR, Toni, N, Palmer, TD, Gage, FH (2002). Functional neurogenesis in the adult hippocampus. Nature 415, 1030–1034.Google Scholar
Videbech, P, Ravnkilde, B (2004). Hippocampal volume and depression: a meta-analysis of MRI studies. American Journal of Psychiatry 161, 1957–1966.Google Scholar
White, AM, Matthews, DB, Best, PJ (2000). Ethanol, memory, and hippocampal function: a review of recent findings. Hippocampus 10, 88–93.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
White, AM, Swartzwelder, HS (2005). Age-related effects of alcohol on memory and memory-related brain function in adolescents and adults. In Recent Developments in Alcoholism (ed. Galanter, M.), pp. 161–176. Springer: New York, NY.Google Scholar
Wilson, S, Malone, SM, Thomas, KM, Iacono, WG (2015 a). Adolescent drinking and brain morphometry: a co-twin control analysis. Developmental Cognitive Neuroscience 16, 130–138.Google Scholar
Wilson, S, Thomas, KM, Iacono, WG (2015 b). Neurological risk factors for the development of problematic substance use. In Handbook of Cognitive Neuroscience (ed. Wilson, S. J.), pp. 269–291. Wiley-Blackwell: Hoboken, NJ.Google Scholar
Wrase, J, Makris, N, Braus, DF, Mann, K, Smolka, MN, Kennedy, DN, Caviness, VS, Hodge, SM, Tang, L, Albaugh, M (2008). Amygdala volume associated with alcohol abuse relapse and craving. American Journal of Psychiatry 165, 1179–1184.Google Scholar
Wright, IC, Rabe-Hesketh, S, Woodruff, PW, David, AS, Murray, RM, Bullmore, ET (2000). Meta-analysis of regional brain volumes in schizophrenia. American Journal of Psychiatry 157, 16–25.CrossRefGoogle ScholarPubMed
Zeigler, DW, Wang, CC, Yoast, RA, Dickinson, BD, McCaffree, MA, Rominowitz, CB, Sterling, ML (2005). The neurocognitive effects of alcohol on adolescents and college students. Preventive Medicine 40, 23–32.Google Scholar