Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-18T18:45:35.810Z Has data issue: false hasContentIssue false

Effect of alcohol use disorder family history on cognitive function

Published online by Cambridge University Press:  14 July 2020

Lotfi Khemiri*
Affiliation:
Centre for Psychiatry Research, Karolinska Institutet & Stockholm Health Care Services, Stockholm County Council, Stockholm, Sweden
Johan Franck
Affiliation:
Centre for Psychiatry Research, Karolinska Institutet & Stockholm Health Care Services, Stockholm County Council, Stockholm, Sweden
Nitya Jayaram-Lindström
Affiliation:
Centre for Psychiatry Research, Karolinska Institutet & Stockholm Health Care Services, Stockholm County Council, Stockholm, Sweden
*
Author for correspondence: Lotfi Khemiri, E-mail: [email protected]

Abstract

Background

Alcohol use disorder (AUD) is associated with cognitive deficits but little is known to what degree this is caused by genetically influenced traits, i.e. endophenotypes, present before the onset of the disorder. The aim of the current study was to investigate to what degree family history (FH) of AUD is associated with cognitive functions.

Methods

Case-control cross-sectional study at an outpatient addiction research clinic. Treatment-seeking AUD patients (n = 106) were compared to healthy controls (HC; n = 90), matched for age and sex. The HC group was further subdivided into AUD FH positive (FH+; n = 47) or negative (FH−; n = 39) based on the Family Tree Questionnaire. Participants underwent psychiatric and substance use assessments, completed the Barratt Impulsiveness Scale and performed a comprehensive battery of neuropsychological tests assessing response inhibition, decision making, attention, working memory, and emotional recognition.

Results

Compared to HC, AUD patients exhibited elevated self-rated impulsivity (p < 0.001; d = 0.62), as well as significantly poorer response inhibition (p = 0.001; d = 0.51), attention (p = 0.021; d = 0.38) and information gathering in decision making (p = 0.073; d = 0.34). Similar to AUD patients, FH+ individuals exhibited elevated self-rated impulsivity (p = 0.096; d = 0.46), and in addition significantly worse future planning capacity (p < 0.001; d = 0.76) and prolonged emotional recognition response time (p = 0.010; d = 0.60) compared to FH−, while no other significant differences were found between FH+ and FH−.

Conclusions

Elevated impulsivity, poor performance in future planning and emotional processing speed may be potential cognitive endophenotypes in AUD. These cognitive domains represent putative targets for prevention strategies and treatment of AUD.

Type
Original Article
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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

Acheson, A., Lake, S. L., Bray, B. C., Liang, Y., Mathias, C. W., Ryan, S. R., … Dougherty, D. M. (2016). Early adolescent trajectories of impulsiveness and sensation seeking in children of fathers with histories of alcohol and other substance use disorders. Alcoholism, Clinical and Experimental Research, 40(12), 26222630. https://doi.org/10.1111/acer.13235CrossRefGoogle ScholarPubMed
Acheson, A., Richard, D. M., Mathias, C. W., & Dougherty, D. M. (2011). Adults with a family history of alcohol related problems are more impulsive on measures of response initiation and response inhibition. Drug and Alcohol Dependence, 117(2–3), 198203. https://doi.org/10.1016/j.drugalcdep.2011.02.001CrossRefGoogle ScholarPubMed
American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed., text rev.). Washington, DC: American Psychiatric Association.Google Scholar
Anton, R. F., Moak, D. H., & Latham, P. (1995). The obsessive compulsive drinking scale: A self-rated instrument for the quantification of thoughts about alcohol and drinking behavior. Alcoholism. Clinical and Experimental Research, 19(1), 9299.CrossRefGoogle Scholar
Anton, R. F., Schacht, J. P., Voronin, K. E., & Randall, P. K. (2017). Aripiprazole suppression of drinking in a clinical laboratory paradigm: Influence of impulsivity and self-control. Alcoholism, Clinical and Experimental Research, 41(7), 13701380. https://doi.org/10.1111/acer.13417CrossRefGoogle Scholar
Beatty, W. W., Katzung, V. M., Nixon, S. J., & Moreland, V. J. (1993). Problem-solving deficits in alcoholics: Evidence from the California Card Sorting Test. Journal of Studies on Alcohol, 54(6), 687692. https://doi.org/10.15288/jsa.1993.54.687CrossRefGoogle ScholarPubMed
Bickel, W. K., Jarmolowicz, D. P., Mueller, E. T., Gatchalian, K. M., & McClure, S. M. (2012). Are executive function and impulsivity antipodes? A conceptual reconstruction with special reference to addiction. Psychopharmacology, 221(3), 361387. https://doi.org/10.1007/s00213-012-2689-xCrossRefGoogle ScholarPubMed
Bjork, J. M., Hommer, D. W., Grant, S. J., & Danube, C. (2004). Impulsivity in abstinent alcohol-dependent patients: Relation to control subjects and type 1-/type 2-like traits. Alcohol (Fayetteville, N.Y.), 34(2–3), 133150.CrossRefGoogle ScholarPubMed
Bora, E., & Zorlu, N. (2017). Social cognition in alcohol use disorder: A meta-analysis: Social cognition in AUD. Addiction, 112(1), 4048. https://doi.org/10.1111/add.13486CrossRefGoogle Scholar
Bowden-Jones, H., McPhillips, M., Rogers, R., Hutton, S., & Joyce, E. (2005). Risk-taking on tests sensitive to ventromedial prefrontal cortex dysfunction predicts early relapse in alcohol dependency: A pilot study. The Journal of Neuropsychiatry and Clinical Neurosciences, 17(3), 417420. https://doi.org/10.1176/appi.neuropsych.17.3.417CrossRefGoogle ScholarPubMed
Buckholtz, J. W., Treadway, M. T., Cowan, R. L., Woodward, N. D., Li, R., Ansari, M. S., … Zald, D. H. (2010). Dopaminergic network differences in human impulsivity. Science (New York, N.Y.), 329(5991), 532. https://doi.org/10.1126/science.1185778CrossRefGoogle ScholarPubMed
Clark, L., Robbins, T. W., Ersche, K. D., & Sahakian, B. J. (2006). Reflection impulsivity in current and former substance users. Biological Psychiatry, 60(5), 515522. https://doi.org/10.1016/j.biopsych.2005.11.007CrossRefGoogle ScholarPubMed
Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). Hillsdale, NJ: L. Erlbaum Associates.Google Scholar
Cordovil De Sousa Uva, M., Luminet, O., Cortesi, M., Constant, E., Derely, M., & De Timary, P. (2010). Distinct effects of protracted withdrawal on affect, craving, selective attention and executive functions among alcohol-dependent patients. Alcohol and Alcoholism (Oxford, Oxfordshire), 45(3), 241246. https://doi.org/10.1093/alcalc/agq012CrossRefGoogle ScholarPubMed
Corral, M. M., Holguín, S. R., & Cadaveira, F. (1999). Neuropsychological characteristics in children of alcoholics: Familial density. Journal of Studies on Alcohol, 60(4), 509513.CrossRefGoogle ScholarPubMed
Coull, J. T., Middleton, H. C., Robbins, T. W., & Sahakian, B. J. (1995). Clonidine and diazepam have differential effects on tests of attention and learning. Psychopharmacology, 120(3), 322332.CrossRefGoogle ScholarPubMed
DeVito, E. E., Blackwell, A. D., Clark, L., Kent, L., Dezsery, A. M., Turner, D. C., … Sahakian, B. J. (2009). Methylphenidate improves response inhibition but not reflection-impulsivity in children with attention deficit hyperactivity disorder (ADHD). Psychopharmacology, 202(1–3), 531539. https://doi.org/10.1007/s00213-008-1337-yCrossRefGoogle Scholar
de Wit, H., Enggasser, J. L., & Richards, J. B. (2002). Acute administration of d-amphetamine decreases impulsivity in healthy volunteers. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 27(5), 813825. https://doi.org/10.1016/S0893-133X(02)00343-3CrossRefGoogle ScholarPubMed
Dick, D. M., Smith, G., Olausson, P., Mitchell, S. H., Leeman, R. F., O'Malley, S. S., & Sher, K. (2010). Understanding the construct of impulsivity and its relationship to alcohol use disorders. Addiction Biology, 15(2), 217226. https://doi.org/10.1111/j.1369-1600.2009.00190.xCrossRefGoogle ScholarPubMed
Ersche, K. D., Clark, L., London, M., Robbins, T. W., & Sahakian, B. J. (2006). Profile of executive and memory function associated with amphetamine and opiate dependence. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 31(5), 10361047. https://doi.org/10.1038/sj.npp.1300889CrossRefGoogle ScholarPubMed
Ersche, K. D., Jones, P. S., Williams, G. B., Turton, A. J., Robbins, T. W., & Bullmore, E. T. (2012). Abnormal brain structure implicated in stimulant drug addiction. Science, 335(6068), 601604. https://doi.org/10.1126/science.1214463CrossRefGoogle ScholarPubMed
Ersche, K. D., Turton, A. J., Pradhan, S., Bullmore, E. T., & Robbins, T. W. (2010). Drug addiction endophenotypes: Impulsive versus sensation-seeking personality traits. Biological Psychiatry, 68(8), 770773. https://doi.org/10.1016/j.biopsych.2010.06.015CrossRefGoogle ScholarPubMed
Gierski, F., Hubsch, B., Stefaniak, N., Benzerouk, F., Cuervo-Lombard, C., Bera-Potelle, C., … Limosin, F. (2013). Executive functions in adult offspring of alcohol-dependent probands: Toward a cognitive endophenotype? Alcoholism, Clinical and Experimental Research, 37(Suppl 1), E356E363. https://doi.org/10.1111/j.1530-0277.2012.01903.xCrossRefGoogle Scholar
Gottesman, I. I., & Gould, T. D. (2003). The endophenotype concept in psychiatry: Etymology and strategic intentions. The American Journal of Psychiatry, 160(4), 636645.CrossRefGoogle ScholarPubMed
Goudriaan, A. E., Oosterlaan, J., de Beurs, E., & van den Brink, W. (2006). Neurocognitive functions in pathological gambling: A comparison with alcohol dependence, Tourette syndrome and normal controls. Addiction (Abingdon, England), 101(4), 534547. https://doi.org/10.1111/j.1360-0443.2006.01380.xCrossRefGoogle ScholarPubMed
Joos, L., Goudriaan, A. E., Schmaal, L., Fransen, E., van den Brink, W., Sabbe, B. G. C., & Dom, G. (2013). Effect of modafinil on impulsivity and relapse in alcohol dependent patients: A randomized, placebo-controlled trial. European Neuropsychopharmacology: The Journal of the European College of Neuropsychopharmacology, 23(8), 948955. https://doi.org/10.1016/j.euroneuro.2012.10.004CrossRefGoogle ScholarPubMed
Kareken, D. A., Dzemidzic, M., Wetherill, L., Eiler, W II.., Oberlin, B. G., Harezlak, J., … O'Connor, S. J. (2013). Family history of alcoholism interacts with alcohol to affect brain regions involved in behavioral inhibition. Psychopharmacology, 228(2), 335345. https://doi.org/10.1007/s00213-013-3038-4CrossRefGoogle ScholarPubMed
Kehagia, A. A., Housden, C. R., Regenthal, R., Barker, R. A., Müller, U., Rowe, J., … Robbins, T. W. (2014). Targeting impulsivity in Parkinson's disease using atomoxetine. Brain: A Journal of Neurology, 137(Pt 7), 19861997. https://doi.org/10.1093/brain/awu117CrossRefGoogle ScholarPubMed
Ketzenberger, K. E., & Forrest, L. (2000). Impulsiveness and compulsiveness in alcoholics and nonalcoholics. Addictive Behaviors, 25(5), 791795.CrossRefGoogle ScholarPubMed
Khemiri, L., Brynte, C., Stunkel, A., Klingberg, T., & Jayaram-Lindström, N. (2019a). Working memory training in alcohol use disorder: A randomized controlled trial. Alcoholism, Clinical and Experimental Research, 43(1), 135146. https://doi.org/10.1111/acer.13910CrossRefGoogle ScholarPubMed
Khemiri, L., Kuja-Halkola, R., Larsson, H., & Jayaram-Lindström, N. (2015a). Genetic overlap between impulsivity and alcohol dependence: A large-scale national twin study. Psychological Medicine, 46(5), 10911102. https://doi.org/10.1017/S0033291715002652CrossRefGoogle ScholarPubMed
Khemiri, L., Larsson, H., Kuja-Halkola, R., D'Onofrio, B. M., Lichtenstein, P., Jayaram-Lindström, N., & Latvala, A. (2019b). Association of parental substance use disorder with offspring cognition: A population family-based study. Addiction (Abingdon, England), 115(2), 326336. https://doi.org/10.1111/add.14813CrossRefGoogle ScholarPubMed
Khemiri, L., Steensland, P., Guterstam, J., Beck, O., Carlsson, A., Franck, J., & Jayaram-Lindström, N. (2015b). The effects of the monoamine stabilizer (-)-OSU6162 on craving in alcohol dependent individuals: A human laboratory study. European Neuropsychopharmacology: The Journal of the European College of Neuropsychopharmacology, 25(12), 22402251. https://doi.org/10.1016/j.euroneuro.2015.09.018CrossRefGoogle ScholarPubMed
Korponay, C., Dentico, D., Kral, T., Ly, M., Kruis, A., Goldman, R., … Davidson, R. J. (2017). Neurobiological correlates of impulsivity in healthy adults: Lower prefrontal gray matter volume and spontaneous eye-blink rate but greater resting-state functional connectivity in basal ganglia-thalamo-cortical circuitry. NeuroImage, 157, 288296. https://doi.org/10.1016/j.neuroimage.2017.06.015CrossRefGoogle ScholarPubMed
Kraemer, H. C. (2019). Is it time to ban the p value? JAMA Psychiatry, 76(12), 12191220. https://doi.org/10.1001/jamapsychiatry.2019.1965CrossRefGoogle ScholarPubMed
Lawrence, A. J., Luty, J., Bogdan, N. A., Sahakian, B. J., & Clark, L. (2009a). Impulsivity and response inhibition in alcohol dependence and problem gambling. Psychopharmacology, 207(1), 163172. https://doi.org/10.1007/s00213-009-1645-xCrossRefGoogle ScholarPubMed
Lawrence, A. J., Luty, J., Bogdan, N. A., Sahakian, B. J., & Clark, L. (2009b). Problem gamblers share deficits in impulsive decision-making with alcohol-dependent individuals. Addiction (Abingdon, England), 104(6), 10061015. https://doi.org/10.1111/j.1360-0443.2009.02533.xCrossRefGoogle ScholarPubMed
Le Berre, A.-P., Fama, R., & Sullivan, E. V. (2017). Executive functions, memory, and social cognitive deficits and recovery in chronic alcoholism: A critical review to inform future research. Alcoholism, Clinical and Experimental Research, 41(8), 14321443. https://doi.org/10.1111/acer.13431CrossRefGoogle ScholarPubMed
Lee, B., London, E. D., Poldrack, R. A., Farahi, J., Nacca, A., Monterosso, J. R., … Mandelkern, M. A. (2009). Striatal dopamine d2/d3 receptor availability is reduced in methamphetamine dependence and is linked to impulsivity. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 29(47), 1473414740. https://doi.org/10.1523/JNEUROSCI.3765-09.2009CrossRefGoogle ScholarPubMed
Lees, J., Michalopoulou, P. G., Lewis, S. W., Preston, S., Bamford, C., Collier, T., … Drake, R. J. (2017). Modafinil and cognitive enhancement in schizophrenia and healthy volunteers: The effects of test battery in a randomised controlled trial. Psychological Medicine, 47(13), 23582368. https://doi.org/10.1017/S0033291717000885CrossRefGoogle Scholar
Logan, G. D., Cowan, W. B., & Davis, K. A. (1984). On the ability to inhibit simple and choice reaction time responses: A model and a method. Journal of Experimental Psychology. Human Perception and Performance, 10(2), 276291.CrossRefGoogle Scholar
Mann, R. E., Sobell, L. C., Sobell, M. B., & Pavan, D. (1985). Reliability of a family tree questionnaire for assessing family history of alcohol problems. Drug and Alcohol Dependence, 15(1–2), 6167.CrossRefGoogle ScholarPubMed
Matsuo, K., Nicoletti, M., Nemoto, K., Hatch, J. P., Peluso, M. A. M., Nery, F. G., & Soares, J. C. (2009). A voxel-based morphometry study of frontal gray matter correlates of impulsivity. Human Brain Mapping, 30(4), 11881195. https://doi.org/10.1002/hbm.20588CrossRefGoogle ScholarPubMed
Moorman, D. E. (2018). The role of the orbitofrontal cortex in alcohol use, abuse, and dependence. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 87(Pt A), 85107. https://doi.org/10.1016/j.pnpbp.2018.01.010CrossRefGoogle ScholarPubMed
Morgan, C. J. A., Muetzelfeldt, L., & Curran, H. V. (2009). Ketamine use, cognition and psychological wellbeing: A comparison of frequent, infrequent and ex-users with polydrug and non-using controls. Addiction (Abingdon, England), 104(1), 7787. https://doi.org/10.1111/j.1360-0443.2008.02394.xCrossRefGoogle ScholarPubMed
Müller, S. E., Weijers, H.-G., Böning, J., & Wiesbeck, G. A. (2008). Personality traits predict treatment outcome in alcohol-dependent patients. Neuropsychobiology, 57(4), 159164. https://doi.org/10.1159/000147469CrossRefGoogle ScholarPubMed
Noël, X., Van der Linden, M., Brevers, D., Campanella, S., Hanak, C., Kornreich, C., & Verbanck, P. (2012). The contribution of executive functions deficits to impaired episodic memory in individuals with alcoholism. Psychiatry Research, 198(1), 116122. https://doi.org/10.1016/j.psychres.2011.10.007CrossRefGoogle ScholarPubMed
Noël, X., Van der Linden, M., Schmidt, N., Sferrazza, R., Hanak, C., Le Bon, O., … Verbanck, P. (2001). Supervisory attentional system in nonamnesic alcoholic men. Archives of General Psychiatry, 58(12), 11521158. https://doi.org/10.1001/archpsyc.58.12.1152CrossRefGoogle ScholarPubMed
Owen, A. M., Downes, J. J., Sahakian, B. J., Polkey, C. E., & Robbins, T. W. (1990). Planning and spatial working memory following frontal lobe lesions in man. Neuropsychologia, 28(10), 10211034.CrossRefGoogle ScholarPubMed
Patton, J. H., Stanford, M. S., & Barratt, E. S. (1995). Factor structure of the Barratt impulsiveness scale. Journal of Clinical Psychology, 51(6), 768774.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
Robbins, T. W., Gillan, C. M., Smith, D. G., de Wit, S., & Ersche, K. D. (2012). Neurocognitive endophenotypes of impulsivity and compulsivity: Towards dimensional psychiatry. Trends in Cognitive Sciences, 16(1), 8191. https://doi.org/10.1016/j.tics.2011.11.009CrossRefGoogle ScholarPubMed
Rogers, R. D., Owen, A. M., Middleton, H. C., Williams, E. J., Pickard, J. D., Sahakian, B. J., & Robbins, T. W. (1999). Choosing between small, likely rewards and large, unlikely rewards activates inferior and orbital prefrontal cortex. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 19(20), 90299038.CrossRefGoogle ScholarPubMed
Rupp, C. I., Beck, J. K., Heinz, A., Kemmler, G., Manz, S., Tempel, K., & Fleischhacker, W. W. (2016). Impulsivity and alcohol dependence treatment completion: Is there a neurocognitive risk factor at treatment entry? Alcoholism, Clinical and Experimental Research, 40(1), 152160. https://doi.org/10.1111/acer.12924CrossRefGoogle Scholar
Rupp, C. I., Derntl, B., Osthaus, F., Kemmler, G., & Fleischhacker, W. W. (2017). Impact of social cognition on alcohol dependence treatment outcome: Poorer facial emotion recognition predicts relapse/dropout. Alcoholism, Clinical and Experimental Research, 41(12), 21972206. https://doi.org/10.1111/acer.13522CrossRefGoogle ScholarPubMed
Salgado, J. V., Malloy-Diniz, L. F., Campos, V. R., Abrantes, S. S. C., Fuentes, D., Bechara, A., & Correa, H. (2009). Neuropsychological assessment of impulsive behavior in abstinent alcohol-dependent subjects. Revista Brasileira De Psiquiatria (Sao Paulo, Brazil: 1999), 31(1), 49.CrossRefGoogle ScholarPubMed
Schaeffer, K. W., Parsons, O. A., & Yohman, J. R. (1984). Neuropsychological differences between male familial and nonfamilial alcoholics and nonalcoholics. Alcoholism, Clinical and Experimental Research, 8(4), 347351. https://doi.org/10.1111/j.1530-0277.1984.tb05678.xCrossRefGoogle ScholarPubMed
Schmaal, L., Joos, L., Koeleman, M., Veltman, D. J., van den Brink, W., & Goudriaan, A. E. (2013). Effects of modafinil on neural correlates of response inhibition in alcohol-dependent patients. Biological Psychiatry, 73(3), 211218. https://doi.org/10.1016/j.biopsych.2012.06.032CrossRefGoogle ScholarPubMed
Schweizer, T. A., Vogel-Sprott, M., Danckert, J., Roy, E. A., Skakum, A., & Broderick, C. E. (2006). Neuropsychological profile of acute alcohol intoxication during ascending and descending blood alcohol concentrations. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 31(6), 13011309. https://doi.org/10.1038/sj.npp.1300941CrossRefGoogle ScholarPubMed
Sheehan, D. V., Lecrubier, Y., Sheehan, K. H., Amorim, P., Janavs, J., Weiller, E., … Dunbar, G. C. (1998). The Mini-International Neuropsychiatric Interview (M.I.N.I.): The development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. The Journal of Clinical Psychiatry, 59(Suppl 20), 2233, quiz 34–57.Google ScholarPubMed
Sobell, L., & Sobell, M. (1992). Timeline follow-back: A technique for assessing self-reported ethanol consumption. In Litten, R. & Allen, J. (Eds.), Measuring alcohol consumption: Psychosocial and biological methods (pp. 4172). Totowa, NJ: Humana Press.CrossRefGoogle Scholar
Stavro, K., Pelletier, J., & Potvin, S. (2013). Widespread and sustained cognitive deficits in alcoholism: A meta-analysis. Addiction Biology, 18(2), 203213. https://doi.org/10.1111/j.1369-1600.2011.00418.xCrossRefGoogle ScholarPubMed
Svanborg, P., & Asberg, M. (2001). A comparison between the Beck Depression Inventory (BDI) and the self-rating version of the Montgomery Asberg Depression Rating Scale (MADRS). Journal of Affective Disorders, 64(2–3), 203216.CrossRefGoogle ScholarPubMed
Verhulst, B., Neale, M. C., & Kendler, K. S. (2015). The heritability of alcohol use disorders: A meta-analysis of twin and adoption studies. Psychological Medicine, 45(5), 10611072. https://doi.org/10.1017/S0033291714002165CrossRefGoogle ScholarPubMed
Volkow, N. D., Wang, G.-J., Telang, F., Fowler, J. S., Logan, J., Jayne, M., … Wong, C. (2007). Profound decreases in dopamine release in striatum in detoxified alcoholics: Possible orbitofrontal involvement. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 27(46), 1270012706. https://doi.org/10.1523/JNEUROSCI.3371-07.2007CrossRefGoogle ScholarPubMed
Supplementary material: File

Khemiri et al. supplementary material

Tables S1-S2

Download Khemiri et al. supplementary material(File)
File 25.7 KB