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The effects of cannabis on memory function in users with and without a psychotic disorder: findings from a combined meta-analysis

Published online by Cambridge University Press:  10 September 2015

T. Schoeler
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King's College London, De Crespigny Park, London SE5 8AF, UK
J. Kambeitz
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King's College London, De Crespigny Park, London SE5 8AF, UK Department of Psychiatry, Ludwig-Maximilian-University Munich, Nuβbaumstr. 7, 80336 Munich, Germany
I. Behlke
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King's College London, De Crespigny Park, London SE5 8AF, UK Institute of Psychology, Univeristy of Osnabrueck, Seminarstr. 20, 49074 Osnabrueck, Germany
R. Murray
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King's College London, De Crespigny Park, London SE5 8AF, UK
S. Bhattacharyya*
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, Psychology & Neuroscience, King's College London, De Crespigny Park, London SE5 8AF, UK
*
*Address for correspondence: S. Bhattacharyya, M.B.B.S., M.D., Ph.D., Department of Psychosis Studies, Institute of Psychiatry, King's College London, De Crespigny Park, London SE5 8AF, UK. (Email: [email protected])

Abstract

Background.

Effect of cannabis use on memory function is a contentious issue, with effects being different in healthy individuals and patients with psychosis.

Method.

Employing a meta-analytic approach we investigated the effects of cannabis use on memory function in patients with psychosis and healthy individuals, and the effect of diagnosis, memory dimension and moderating factors. A total of 88 studies were identified through a systematic literature search, investigating healthy (n = 7697) and psychotic (n = 3261) individuals. Standardized mean differences between the cannabis user and non-user groups on memory tasks were estimated using random-effects models and the effect-size statistic Cohen's d. Effects of potential moderating factors were tested using mixed-effects models and subgroup analyses.

Results.

We found that cannabis use was associated with significantly (p ⩽ 0.05) impaired global (d = 0.27) and prospective memory (d = 0.61), verbal immediate (d = 0.40) and delayed (d = 0.36) recall as well as visual recognition (d = 0.41) in healthy individuals, but a better global memory (d = −0.11), visual immediate recall (d = −0.73) and recognition (d = −0.42) in patients. Lower depression scores and younger age appeared to attenuate the effects of cannabis on memory. Cannabis-using patients had lower levels of depression and were younger compared with non-using patients, whilst healthy cannabis-users had higher depression scores than age-matched non-users. Longer duration of abstinence from cannabis reduced the effects on memory in healthy and patient users.

Conclusions.

These results suggest that cannabis use is associated with a significant domain-specific impairment in memory in healthy individuals but not in cannabis-using patients, suggesting that they may represent a less developmentally impaired subgroup of psychotic patients.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2015 

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References

Bahorik, AL, Newhill, CE, Eack, SM (2013). Neurocognitive functioning of individuals with schizophrenia: using and not using drugs. Schizophrenia Bulletin 40, 856867.CrossRefGoogle Scholar
Beller, EM, Glasziou, PP, Altman, DG, Hopewell, S, Bastian, H, Chalmers, I, Gøtzsche, PC, Lasserson, T, Tovey, D (2013). PRISMA for abstracts: reporting systematic reviews in journal and conference abstracts. PLoS Medicine 10, e1001419.Google Scholar
Benedict, RHB, Schretlen, D, Groninger, L, Brandt, J (1998). Hopkins Verbal Learning Test–revised: normative data and analysis of inter-form and test–retest reliability. Clinical Neuropsychologist 12, 4355.Google Scholar
Bhattacharyya, S, Atakan, Z, Martin-Santos, R, Crippa, JA, Kambeitz, J, Prata, D, Williams, S, Brammer, M, Collier, DA, McGuire, PK (2012). Preliminary report of biological basis of sensitivity to the effects of cannabis on psychosis: AKT1 and DAT1 genotype modulates the effects of δ-9-tetrahydrocannabinol on midbrain and striatal function. Molecular Psychiatry 17, 11521155.Google Scholar
Bhattacharyya, S, Fusar-Poli, P, Borgwardt, S, Martin-Santos, R, Nosarti, C, O'Carroll, C, Allen, P, Seal, ML, Fletcher, PC, Crippa, JA, Giampietro, V, Mechelli, A, Atakan, Z, McGuire, P (2009). Modulation of mediotemporal and ventrostriatal function in humans by Δ9-tetrahydrocannabinol: a neural basis for the effects of Cannabis sativa on learning and psychosis. Archives of General Psychiatry 66, 442451.Google Scholar
Bolla, KI, Brown, K, Eldreth, D, Tate, K, Cadet, JL (2002). Dose-related neurocognitive effects of marijuana use. Neurology 59, 13371343.Google Scholar
Borenstein, M, Hedges, LV, Higgins, JP, Rothstein, HR (2011). Introduction to Meta-Analysis. Wiley: Chichester.Google Scholar
Bowman, M, Pihl, RO (1973). Cannabis: psychological effects of chronic heavy use. Psychopharmacologia 29, 159170.CrossRefGoogle ScholarPubMed
Bugra, H, Studerus, E, Rapp, C, Tamagni, C, Aston, J, Borgwardt, S, Riecher-Rössler, A (2013). Cannabis use and cognitive functions in at-risk mental state and first episode psychosis. Psychopharmacology (Berlin) 230, 299308.CrossRefGoogle ScholarPubMed
Burt, DB, Zembar, MJ, Niederehe, G (1995). Depression and memory impairment: a meta-analysis of the association, its pattern, and specificity. Psychological Bulletin 117, 285305.CrossRefGoogle ScholarPubMed
Carey, KB, Carey, MP, Simons, JS (2003). Correlates of substance use disorder among psychiatric outpatients: focus on cognition, social role functioning and psychiatric status. Journal of Nervous and Mental Disease 191, 300308.CrossRefGoogle ScholarPubMed
Cunha, PJ, Rosa, PGP, Ayres, Ade M, Duran, FLS, Santos, LC, Scazufca, M, Menezes, PR, dos Santos, B, Murray, RM, Crippa, JAS, Busatto, GF, Schaufelberger, MS (2013). Cannabis use, cognition and brain structure in first-episode psychosis. Schizophrenia Research 147, 209215.CrossRefGoogle ScholarPubMed
Curran, VH, Brignell, C, Fletcher, S, Middleton, P, Henry, J (2002). Cognitive and subjective dose–response effects of acute oral Δ9-tetrahydrocannabinol (THC) in infrequent cannabis users. Psychopharmacology (Berlin) 164, 6170.CrossRefGoogle ScholarPubMed
D'Souza, DC, Abi-Saab, WM, Madonick, S, Forselius-Bielen, K, Doersch, A, Braley, G, Gueorguieva, R, Cooper, TB, Krystal, JH (2005). Δ−9-Tetrahydrocannabinol effects in schizophrenia: implications for cognition, psychosis, and addiction. Biological Psychiatry 57, 594608.CrossRefGoogle ScholarPubMed
D'Souza, DC, Perry, E, MacDougall, L, Ammerman, Y, Cooper, T, Wu, YT, Braley, G, Gueorguieva, R, Krystal, JH (2004). The psychotomimetic effects of intravenous Δ−9-tetrahydrocannabinol in healthy individuals: implications for psychosis. Neuropsychopharmacology 29, 15581572.Google Scholar
Donoghue, K, Doody, GA (2012). Effect of illegal substance use on cognitive function in individuals with a psychotic disorder, a review and meta-analysis. Neuropsychology 26, 785801.CrossRefGoogle ScholarPubMed
Donoghue, K, Mazzoncini, R, Hart, J, Zanelli, J, Morgan, C, Dazzan, P, Morgan, KD, Murray, RM, Jones, PB, Doody, GA (2012). The differential effect of illicit drug use on cognitive function in first-episode psychosis and healthy controls. Acta Psychiatrica Scandinavica 125, 400411.Google Scholar
Eichenbaum, H (1993). Memory, Amnesia, and the Hippocampal System. The MIT Press: Cambridge, MA.Google Scholar
Englund, A, Morrison, PD, Nottage, J, Hague, D, Kane, F, Bonaccorso, S, Stone, JM, Reichenberg, A, Brenneisen, R, Holt, D (2013). Cannabidiol inhibits THC-elicited paranoid symptoms and hippocampal-dependent memory impairment. Journal of Psychopharmacology 27, 1927.CrossRefGoogle ScholarPubMed
Ferraro, L, Russo, M, O'Connor, J, Wiffen, BDR, Falcone, MA, Sideli, L, Gardner-Sood, P, Stilo, S, Trotta, A, Dazzan, P, Mondelli, V, Taylor, H, Friedman, B, Sallis, H, La Cascia, C, La Barbera, D, David, AS, Reichenberg, A, Murray, R, Di Forti, M (2013). Cannabis users have higher premorbid IQ than other patients with first onset psychosis. Schizophrenia Research 150, 129135.Google Scholar
Fletcher, PC, Honey, GD (2006). Schizophrenia, ketamine and cannabis: evidence of overlapping memory deficits. Trends in Cognitive Sciences 10, 167174.CrossRefGoogle ScholarPubMed
Fried, PA, Watkinson, B, Gray, R (2005). Neurocognitive consequences of marihuana – a comparison with pre-drug performance. Neurotoxicology and Teratology 27, 231239.CrossRefGoogle ScholarPubMed
Gonzalez, R, Carey, C, Grant, I (2002). Nonacute (residual) neuropsychological effects of cannabis use: a qualitative analysis and systematic review. Journal of Clinical Pharmacology 42 (11 Suppl.), 48S57S.Google Scholar
Grant, I, Gonzales, R, Carey, CL, Natarajan, L, Wolfson, T (2003). Non-acute (residual) neurocognitive effects of cannabis use: a meta-analytic study. Journal of the International Neuropsychological Society 9, 679689.Google Scholar
Gruber, SA, Sagar, KA, Dahlgren, MK, Racine, M, Lukas, SE (2012). Age of onset of marijuana use and executive function. Psychology of Addictive Behaviors 26, 496506.Google Scholar
Hardwick, S, King, LA (2008). Home Office Cannabis Potency Study 2008. United Kingdom: Home Office Scientific Development Branch: St Albans.Google Scholar
Herkenham, M, Lynn, AB, Little, MD, Johnson, MR, Melvin, LS, De Costa, BR, Rice, KC (1990). Cannabinoid receptor localization in brain. Proceedings of the National Academy of Sciences of the USA 87, 19321936.Google Scholar
Higgins, JP, Green, S (editors) (2008). Cochrane Handbook for Systematic Reviews of Interventions. Wiley Online Library: Chichester.Google Scholar
Hulicka, IM (1966). Age differences in Wechsler Memory Scale scores. Journal of Genetic Psychology 109, 135145.Google Scholar
Iversen, L (2003). Cannabis and the brain. Brain 126, 12521270.Google Scholar
Jager, G, Kahn, RS, Van Den Brink, W, Van Ree, JM, Ramsey, NF (2006). Long-term effects of frequent cannabis use on working memory and attention: an fMRI study. Psychopharmacology (Berlin) 185, 358368.Google Scholar
Jockers-Scherubl, MC, Wolf, T, Radzei, N, Schlattmann, P, Rentzsch, J, Gomez-Carrillo de Castro, A, Kuhl, KP (2007). Cannabis induces different cognitive changes in schizophrenic patients and in healthy controls. Progress in Neuro-Psychopharmacology and Biological Psychiatry 31, 10541063.Google Scholar
Kambeitz, JP, Bhattacharyya, S, Kambeitz-Ilankovic, LM, Valli, I, Collier, DA, McGuire, P (2012). Effect of BDNF val66met polymorphism on declarative memory and its neural substrate: a meta-analysis. Neuroscience and Biobehavioral Reviews 36, 21652177.Google Scholar
Kanayama, G, Rogowska, J, Pope, HG, Gruber, SA, Yurgelun-Todd, DA (2004). Spatial working memory in heavy cannabis users: a functional magnetic resonance imaging study. Psychopharmacology (Berlin) 176, 239247.Google Scholar
Korver, N, Nieman, DH, Becker, HE, van de Fliert, JR, Dingemans, PH, de Haan, L, Spiering, M, Schmitz, N, Linszen, DH (2010). Symptomatology and neuropsychological functioning in cannabis using subjects at ultra-high risk for developing psychosis and healthy controls. Australian and New Zealand Journal of Psychiatry 44, 230236.Google Scholar
Koskinen, J, Löhönen, J, Koponen, H, Isohanni, M, Miettunen, J (2010). Rate of cannabis use disorders in clinical samples of patients with schizophrenia: a meta-analysis. Schizophrenia Bulletin 36, 11151130.Google Scholar
Lane, SD, Cherek, DR, Lieving, LM, Tcheremissine, OV (2005). Marijuana effects on human forgetting functions. Journal of the Experimental Analysis of Behavior 83, 6783.CrossRefGoogle ScholarPubMed
Leeson, VC, Harrison, I, Ron, MA, Barnes, TR, Joyce, EM (2012). The effect of cannabis use and cognitive reserve on age at onset and psychosis outcomes in first-episode schizophrenia. Schizophrenia Bulletin 38, 873880.CrossRefGoogle ScholarPubMed
Linszen, DH, Dingemans, PM, Nugter, MA, Van der Does, AJ, Scholte, WF, Lenior, MA (1997). Patient attributes and expressed emotion as risk factors for psychotic relapse. Schizophrenia Bulletin 23, 119130.Google Scholar
Løberg, E-M, Hugdahl, K (2009). Cannabis use and cognition in schizophrenia. Frontiers in Human Neuroscience 3, 53.Google Scholar
Løberg, EM, Hugdahl, K, Jørgensen, HA (2008). Lower neurocognitive vulnerability in schizophrenia with a history of cannabis abuse? Schizophrenia Research 98, 73.Google Scholar
Lutgens, D, Lepage, M, Iyer, S, Malla, A (2014). Predictors of cognition in first episode psychosis. Schizophrenia Research 152, 164169.Google Scholar
Matochik, JA, Eldreth, DA, Cadet, JL, Bolla, KI (2005). Altered brain tissue composition in heavy marijuana users. Drug and Alcohol Dependence 77, 2330.CrossRefGoogle ScholarPubMed
McDermott, LM, Ebmeier, KP (2009). A meta-analysis of depression severity and cognitive function. Journal of Affective Disorders 119, 18.Google Scholar
Meier, MH, Caspi, A, Ambler, A, Harrington, H, Houts, R, Keefe, RS, McDonald, K, Ward, A, Poulton, R, Moffitt, TE (2012). Persistent cannabis users show neuropsychological decline from childhood to midlife. Proceedings of the National Academy of Sciences of the USA 109, E2657E2664.Google Scholar
Miles, H, Johnson, S, Amponsah-Afuwape, S, Finch, E, Leese, M, Thornicroft, G (2003). Characteristics of subgroups of individuals with psychotic illness and a comorbid substance use disorder. Psychiatric Services 54, 554561.Google Scholar
Moreno-Granados, JM, Ferrín, M, Salcedo-Marín, DM, Ruiz-Veguilla, M (2014). Neuropsychological assessment of memory in child and adolescent first episode psychosis: cannabis and the «paradox effect». Revista Brasileira de Psiquiatria 7, 1324.Google ScholarPubMed
Morrison, PD, Zois, V, McKeown, DA, Lee, TD, Holt, DW, Powell, JF, Kapur, S, Murray, RM (2009). The acute effects of synthetic intravenous Δ9-tetrahydrocannabinol on psychosis, mood and cognitive functioning. Psychological Medicine 39, 16071616.Google Scholar
Moss, HB, Chen, CM, Yi, HY (2013). Early adolescent patterns of alcohol, cigarettes, and marijuana polysubstance use and young adult substance use outcomes in a nationally representative sample. Drug and Alcohol Dependence 136, 5162.Google Scholar
Murray, RM, Lewis, SW (1987). Is schizophrenia a neurodevelopmental disorder? British Medical Journal (Clinical Research ed.) 295, 681682.Google Scholar
Murray, RM, Paparelli, A, Morrison, PD, Marconi, A, Di Forti, M (2013). What can we learn about schizophrenia from studying the human model, drug-induced psychosis? American Journal of Medical Genetics Part B: Neuropsychiatric Genetics 162B, 661670.Google Scholar
Nakamura, EM, Da Silva, EA, Concilio, GV, Adrian Wilkinson, D, Masur, J (1991). Reversible effects of acute and long-term administration of Δ−9-tetrahydrocannabinol (THC) on memory in the rat. Drug and Alcohol Dependence 28, 167175.CrossRefGoogle ScholarPubMed
Packard, MG, Knowlton, BJ (2002). Learning and memory functions of the basal ganglia. Annual Review of Neuroscience 25, 563593.Google Scholar
Pencer, A, Addington, J (2003). Substance use and cognition in early psychosis. Journal of Psychiatry and Neuroscience 28, 4854.Google Scholar
Penk, WE, Flannery, RB Jr, Irvin, E, Geller, J, Fisher, W, Hanson, MA (2000). Characteristics of substance-abusing persons with schizophrenia: the paradox of the dually diagnosed. Journal of Addictive Diseases 19, 2330.CrossRefGoogle ScholarPubMed
Pertwee, RG (2008). Ligands that target cannabinoid receptors in the brain: from THC to anandamide and beyond. Addiction Biology 13, 147159.CrossRefGoogle ScholarPubMed
Pezdek, K, Evans, GW (1979). Visual and verbal memory for objects and their spatial locations. Journal of Experimental Psychology Human Learning and Memory 5, 360373.Google Scholar
Pope, HG, Gruber, AJ, Hudson, JI, Cohane, G, Huestis, MA, Yurgelun-Todd, D (2003). Early-onset cannabis use and cognitive deficits: what is the nature of the association? Drug and Alcohol Dependence 69, 303310.CrossRefGoogle ScholarPubMed
Pope, HG, Gruber, AJ, Hudson, JI, Huestis, MA, Yurgelun-Todd, D (2001). Neuropsychological performance in long-term cannabis users. Archives of General Psychiatry 58, 909915.Google Scholar
Potvin, S, Joyal, CC, Pelletier, J, Stip, E (2008). Contradictory cognitive capacities among substance-abusing patients with schizophrenia: a meta-analysis. Schizophrenia Research 100, 242251.Google Scholar
Poulsen, HA, Sutherland, GJ (2000). The potency of cannabis in New Zealand from 1976 to 1996. Science and Justice 40, 171176.Google Scholar
Rabin, RA, Zakzanis, KK, Daskalakis, ZJ, George, TP (2012). Effects of cannabis use status on cognitive function, in males with schizophrenia. Psychiatry Research 206, 158165.Google Scholar
Rabin, RA, Zakzanis, KK, George, TP (2011). The effects of cannabis use on neurocognition in schizophrenia: a meta-analysis. Schizophrenia Research 128, 111116.Google Scholar
Ranganathan, M, D'Souza, DC (2006). The acute effects of cannabinoids on memory in humans: a review. Psychopharmacology 188, 425444.Google Scholar
Ruiz-Veguilla, M, Callado, LF, Ferrin, M (2012). Neurological soft signs in patients with psychosis and cannabis abuse: a systematic review and meta-analysis of paradox. Current Pharmaceutical Design 18, 51565164.Google Scholar
Salyers, MP, Mueser, KT (2001). Social functioning, psychopathology, and medication side effects in relation to substance use and abuse in schizophrenia. Schizophrenia Research 48, 109123.Google Scholar
Schnell, T, Koethe, D, Daumann, J, Gouzoulis-Mayfrank, E (2009). The role of cannabis in cognitive functioning of patients with schizophrenia. Psychopharmacology (Berlin) 205, 4552.Google Scholar
Schoeler, T, Bhattacharyya, S (2013). The effect of cannabis use on memory function: an update. Journal of Substance Abuse and Rehabilitation 4, 1127.Google Scholar
Schreiner, AM, Dunn, ME (2012). Residual effects of cannabis use on neurocognitive performance after prolonged abstinence: a meta-analysis. Experimental and Clinical Psychopharmacology 20, 409420.Google Scholar
Smith, K, Flatley, J (2011). Drug misuse declared: findings from the 2010/11 British Crime Survey England and Wales. Home Office Statistical Bulletin 12/11 (https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/116333/hosb1211.pdf). Accessed August 2015.Google Scholar
Smith, MJ, Cobia, DJ, Wang, L, Alpert, KI, Cronenwett, WJ, Goldman, MB, Mamah, D, Barch, DM, Breiter, HC, Csernansky, JG (2014). Cannabis-related working memory deficits and associated subcortical morphological differences in healthy individuals and schizophrenia subjects. Schizophrenia Bulletin 40, 287299.Google Scholar
Sneider, JT, Pope, HG Jr, Silveri, MM, Simpson, NS, Gruber, SA, Yurgelun-Todd, DA (2008). Differences in regional blood volume during a 28-day period of abstinence in chronic cannabis smokers. European Neuropsychopharmacology 18, 612619.Google Scholar
Solowij, N, Battisti, R (2008). The chronic effects of cannabis on memory in humans: a review. Current Drug Abuse Reviews 1, 8198.Google Scholar
Solowij, N, Pesa, N (2010). Cognitive abnormalities and cannabis use. Revista Brasileira de Psiquiatria 32 (Suppl. 1), S31S40.Google Scholar
Song, F, Sheldon, TA, Sutton, AJ, Abrams, KR, Jones, DR (2001). Methods for exploring heterogeneity in meta-analysis. Evaluation and the Health Professions 24, 126151.Google Scholar
Soueif, MI (1976). Differential association between chronic cannabis use and brain function deficits. Annals of the New York Academy of Sciences 282, 323343.Google Scholar
Tait, RJ, Mackinnon, A, Christensen, H (2011). Cannabis use and cognitive function: 8-year trajectory in a young adult cohort. Addiction 106, 21952203.CrossRefGoogle Scholar
UN Office on Drugs and Crime (2010). World Drug Report 2010. United Nations Publications: New York.Google Scholar
Vakil, E, Blachstein, H (1997). Rey AVLT: developmental norms for adults and the sensitivity of different memory measures to age. Clinical Neuropsychologist 11, 356369.Google Scholar
Viechtbauer, W (2010). Conducting meta-analyses in R with the metafor package. Journal of Statistical Software 36, 148.Google Scholar
Wadsworth, EJK, Moss, SC, Simpson, SA, Smith, AP (2006). Cannabis use, cognitive performance and mood in a sample of workers. Journal of Psychopharmacology 20, 1423.Google Scholar
Wagner, D, Becker, B, Gouzoulis-Mayfrank, E, Daumann, J (2010). Interactions between specific parameters of cannabis use and verbal memory. Progress in Neuro-Psychopharmacology and Biological Psychiatry 34, 871876.Google Scholar
Wobrock, T, Falkai, P, Schneider-Axmann, T, Hasan, A, Galderisi, S, Davidson, M, Kahn, RS, Derks, EM, Boter, H, Rybakowski, JK (2013). Comorbid substance abuse in first-episode schizophrenia: effects on cognition and psychopathology in the EUFEST study. Schizophrenia Research 147, 132139.Google Scholar
Wojtalik, JA, Barch, DM (2014). An fMRI study of the influence of a history of substance abuse on working memory-related brain activation in schizophrenia. Frontiers in Psychiatry 5, 1.Google Scholar
Yücel, M, Bora, E, Lubman, DI, Solowij, N, Brewer, WJ, Cotton, SM, Conus, P, Takagi, MJ, Fornito, A, Wood, SJ (2012). The impact of cannabis use on cognitive functioning in patients with schizophrenia: a meta-analysis of existing findings and new data in a first-episode sample. Schizophrenia Bulletin 38, 316330.Google Scholar
Yucel, M, Solowij, N, Respondek, C, Whittle, S, Fornito, A, Pantelis, C, Lubman, DI (2008). Regional brain abnormalities associated with long-term heavy cannabis use. Archives of General Psychiatry 65, 694701.Google Scholar
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