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Characterizing psychosis-relevant phenomena and cognitive function in a unique population with isolated, chronic and very heavy cannabis exposure

Published online by Cambridge University Press:  16 October 2019

Deepak Cyril D'Souza ,
Suhas Ganesh ,
Jose Cortes-Briones ,
Michael H. Campbell  and
Maisha K. Emmanuel
Deepak Cyril D'Souza*
Affiliation:
Schizophrenia and Neuropharmacology Research Group, VA Connecticut Healthcare System, West Haven, CT, USA Abraham Ribicoff Research Facilities, Connecticut Mental Health Center, New Haven, CT, USA Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA
Suhas Ganesh
Affiliation:
Schizophrenia and Neuropharmacology Research Group, VA Connecticut Healthcare System, West Haven, CT, USA Abraham Ribicoff Research Facilities, Connecticut Mental Health Center, New Haven, CT, USA Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA
Jose Cortes-Briones
Affiliation:
Schizophrenia and Neuropharmacology Research Group, VA Connecticut Healthcare System, West Haven, CT, USA Abraham Ribicoff Research Facilities, Connecticut Mental Health Center, New Haven, CT, USA Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA
Michael H. Campbell
Affiliation:
Faculty of Medical Sciences, University of the West Indies, Kingston, Jamaica
Maisha K. Emmanuel
Affiliation:
Faculty of Medical Sciences, University of the West Indies, Kingston, Jamaica
*
Author for correspondence: Deepak Cyril D'Souza, E-mail: [email protected]
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Abstract

Background

The literature on psychosis-relevant outcomes in cannabis users does not adequately address the confounding effects of other substance use/misuse and psychiatric disorders.

Methods

We studied a unique population for whom cannabis use is central and necessary to their way of life. They are forbidden from using other substances, including tobacco and alcohol. Their use of cannabis is heavy, chronic, and begins early. The cases were compared with matched controls who did not use cannabis, alcohol, or drugs. The controls were from the same location and shared similar beliefs and lifestyle, except for cannabis use. Attenuated psychosis-relevant phenomena were assessed with the Schizotypal Personality Questionnaire (SPQ) and cognitive functioning with a culture-neutral computerized cognitive battery.

Results

Fifteen cases and 12 matched controls were studied. The cases averaged >30 000 lifetime cannabis exposures. Relative to controls, the cases had significantly higher mean (s.d.) SPQ scores 24 (14.32) v. 13 (8.92), p = 0.031; and poorer cognitive performance, reflected by a lower mean (s.d.) composite cognitive score −0.23 (0.32) v. +0.28 (0.52), p = 0.03. Moderate to large effect sizes were noted for differences in tests of attention, psychomotor speed, working memory, cognitive flexibility, visuo-spatial processing, and verbal memory. A subsample of cases had higher SPQ scores and worse cognitive performance than their siblings not using cannabis.

Conclusion

Heavy, chronic, and early cannabis use that is not confounded by other drug use is associated with psychosis-relevant phenomena and cognitive deficits. The findings are relevant to the evolving attitudes and laws about cannabis.

Keywords

Cannabischronicchronic-usecognitionpsychosisschizotypy
Type
Original Articles
Information
Psychological Medicine , Volume 50 , Issue 14 , October 2020 , pp. 2452 - 2459
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Copyright
Copyright © Cambridge University Press 2019

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Footnotes

*

Joint last authors.

References

Anglin, DM, Corcoran, CM, Brown, AS, Chen, H, Lighty, Q, Brook, JS and Cohen, PR (2012) Early cannabis use and schizotypal personality disorder symptoms from adolescence to middle adulthood. Schizophrenia Research 137, 45–49.CrossRefGoogle ScholarPubMed
Barron, D, Swami, V, Towell, T, Hutchinson, G and Morgan, KD (2015). Examination of the factor structure of the Schizotypal Personality Questionnaire among British and Trinidadian adults. Biomed Research International 2015, 258275.CrossRefGoogle ScholarPubMed
Bhattacharyya, S, Morrison, PD, Fusar-Poli, P, Martin-Santos, R, Borgwardt, S, Winton-Brown, T, Nosarti, C, CM, OC, Seal, M, Allen, P, Mehta, MA, Stone, JM, Tunstall, N, Giampietro, V, Kapur, S, Murray, RM, Zuardi, AW, Crippa, JA, Atakan, Z and McGuire, PK (2009) Opposite effects of Delta-9-tetrahydrocannabinol and cannabidiol on human brain function and psychopathology. Neuropsychopharmacology 35, 764–774.CrossRefGoogle ScholarPubMed
Borgwardt, SJ, Allen, P, Bhattacharyya, S, Fusar-Poli, P, Crippa, JA, Seal, ML, Fraccaro, V, Atakan, Z, Martin-Santos, R, O'Carroll, C, Rubia, K and McGuire, PK (2008) Neural basis of Delta-9-tetrahydrocannabinol and cannabidiol: effects during response inhibition. Biological Psychiatry 64, 966–973.CrossRefGoogle ScholarPubMed
Brandt, J (1991) The Hopkin's verbal learning test: development of a new memory test with six equivalent forms. Clinical Neuropsychologist 5, 125–142.CrossRefGoogle Scholar
Broyd, SJ, van Hell, HH, Beale, C, Yucel, M and Solowij, N (2016) Acute and chronic effects of cannabinoids on human cognition – a systematic review. Biological Psychiatry 79, 557–567.CrossRefGoogle ScholarPubMed
Campos, MW, Serebrisky, D and Castaldelli-Maia, JM (2016) Smoking and cognition. Current Drug Abuse Reviews 9, 76–79.CrossRefGoogle ScholarPubMed
Carbuto, M, Sewell, RA, Williams, A, Forselius-Bielen, K, Braley, G, Elander, J, Pittman, B, Schnakenberg, A, Bhakta, S, Perry, E, Ranganathan, M and D'Souza, DC (2011) The safety of studies with intravenous Delta(9)-tetrahydrocannabinol in humans, with case histories. Psychopharmacology (Berl) 219, 885–896.CrossRefGoogle ScholarPubMed
Chandra, S, Radwan, MM, Majumdar, CG, Church, JC, Freeman, TP and ElSohly, MA (2019) New trends in cannabis potency in USA and Europe during the last decade (2008–2017). European Archives of Psychiatry and Clinical Neuroscience 269, 5–15.CrossRefGoogle Scholar
Cogstate-Research (2017) Research Data Analysis Guidelines.Google Scholar
Cohen, J (1988). Statistical Power Analysis for the Behavioral Sciences. Hillsdale, NJ: L. Erlbaum Associates.Google Scholar
Cornblatt, BA, Risch, NJ, Faris, G, Friedman, D and Erlenmeyer-Kimling, L (1988) The Continuous Performance Test, identical pairs version (CPT-IP): I. New findings about sustained attention in normal families. Psychiatry Research 26, 223–238.CrossRefGoogle ScholarPubMed
Cortes-Briones, J, Skosnik, PD, Mathalon, D, Cahill, J, Pittman, B, Williams, A, Sewell, RA, Ranganathan, M, Roach, B, Ford, J and D'Souza, DC (2015 a) Delta9-THC disrupts gamma (gamma)-band neural oscillations in humans. Neuropsychopharmacology 40, 2124–2134.CrossRefGoogle ScholarPubMed
Cortes-Briones, JA, Cahill, JD, Skosnik, PD, Mathalon, DH, Williams, A, Sewell, RA, Roach, BJ, Ford, JM, Ranganathan, M and D'Souza, DC (2015 b) The psychosis-like effects of Delta-tetrahydrocannabinol Are associated with increased cortical noise in healthy humans. Biological Psychiatry 78, 805–813.CrossRefGoogle Scholar
Crane, NA, Schuster, RM, Fusar-Poli, P and Gonzalez, R (2013) Effects of cannabis on neurocognitive functioning: recent advances, neurodevelopmental influences, and sex differences. Neuropsychology Review 23, 117–137.CrossRefGoogle ScholarPubMed
Curran, C, Byrappa, N and McBride, A (2004) Stimulant psychosis: systematic review. British Journal of Psychiatry 185, 196–204.CrossRefGoogle ScholarPubMed
Davis, GP, Compton, MT, Wang, S, Levin, FR and Blanco, C (2013) Association between cannabis use, psychosis, and schizotypal personality disorder: findings from the national epidemiologic survey on alcohol and related conditions. Schizophrenia Research 151, 197–202.CrossRefGoogle ScholarPubMed
Di Forti, M, Morgan, C, Selten, J-P, Lynskey, M and Murray, RM (2019 a) High-potency cannabis and incident psychosis: correcting the causal assumption – authors’ reply. The Lancet Psychiatry 6, 466–467.CrossRefGoogle ScholarPubMed
Di Forti, M, Quattrone, D, Freeman, TP, Tripoli, G, Gayer-Anderson, C, Quigley, H, Rodriguez, V, Jongsma, HE, Ferraro, L, La Cascia, C, La Barbera, D, Tarricone, I, Berardi, D, Szoke, A, Arango, C, Tortelli, A, Velthorst, E, Bernardo, M, Del-Ben, CM, Menezes, PR, Selten, JP, Jones, PB, Kirkbride, JB, Rutten, BP, de Haan, L, Sham, PC, van Os, J, Lewis, CM, Lynskey, M, Morgan, C, Murray, RM and Group, E-GW (2019 b) The contribution of cannabis use to variation in the incidence of psychotic disorder across Europe (EU-GEI): a multicentre case-control study. The Lancet Psychiatry 6, 427–436.CrossRefGoogle ScholarPubMed
D'Souza, DC, Perry, E, MacDougall, L, Ammerman, Y, Cooper, T, Wu, YT, Braley, G, Gueorguieva, R and Krystal, JH (2004) The psychotomimetic effects of intravenous delta-9-tetrahydrocannabinol in healthy individuals: implications for psychosis. Neuropsychopharmacology 29, 1558–1572.CrossRefGoogle Scholar
D'Souza, DC, Braley, G, Blaise, R, Vendetti, M, Oliver, S, Pittman, B, Ranganathan, M, Bhakta, S, Zimolo, Z, Cooper, T and Perry, E (2008 a) Effects of haloperidol on the behavioral, subjective, cognitive, motor, and neuroendocrine effects of Delta-9-tetrahydrocannabinol in humans. Psychopharmacology (Berl) 198, 587–603.CrossRefGoogle ScholarPubMed
D'Souza, DC, Ranganathan, M, Braley, G, Gueorguieva, R, Zimolo, Z, Cooper, T, Perry, E and Krystal, J (2008 b) Blunted psychotomimetic and amnestic effects of delta-9-tetrahydrocannabinol in frequent users of cannabis. Neuropsychopharmacology 33, 2505–2516.CrossRefGoogle ScholarPubMed
D'Souza, DC, Sewell, RA and Ranganathan, M (2009) Cannabis and psychosis/schizophrenia: human studies. European Archives of Psychiatry and Clinical Neuroscience 259, 413–431.CrossRefGoogle ScholarPubMed
D'Souza, DC, Fridberg, DJ, Skosnik, PD, Williams, A, Roach, B, Singh, N, Carbuto, M, Elander, J, Schnakenberg, A, Pittman, B, Sewell, RA, Ranganathan, M and Mathalon, D (2012) Dose-related modulation of event-related potentials to novel and target stimuli by intravenous Delta(9)-THC in humans. Neuropsychopharmacology 37, 1632–1646.CrossRefGoogle ScholarPubMed
D'Souza, DC, Cortes-Briones, J, Creatura, G, Bluez, G, Thurnauer, H, Deaso, E, Bielen, K, Surti, T, Radhakrishnan, R and Gupta, A (2019) Efficacy and safety of a fatty acid amide hydrolase inhibitor (PF-04457845) in the treatment of cannabis withdrawal and dependence in men: a double-blind, placebo-controlled, parallel group, phase 2a single-site randomised controlled trial. The Lancet Psychiatry 6, 35–45.CrossRefGoogle ScholarPubMed
ElSohly, MA, Mehmedic, Z, Foster, S, Gon, C, Chandra, S and Church, JC (2016) Changes in cannabis potency over the last 2 decades (1995–2014): analysis of current data in the United States. Biological Psychiatry 79, 613–619.CrossRefGoogle ScholarPubMed
Englund, A, Morrison, PD, Nottage, J, Hague, D, Kane, F, Bonaccorso, S, Stone, JM, Reichenberg, A, Brenneisen, R, Holt, D, Feilding, A, Walker, L, Murray, RM and Kapur, S (2013) Cannabidiol inhibits THC-elicited paranoid symptoms and hippocampal-dependent memory impairment. Journal of Psychopharmacology 27, 19–27.CrossRefGoogle ScholarPubMed
Eren, F, Dilbaz, N, Önder Sönmez, E, Turan, Ö, Gündüz, N and Turan, H (2017) Evaluation of the effect of schizotypy on cannabis use predictors. Psychiatry and Clinical Psychopharmacology 27, 337–343.CrossRefGoogle Scholar
First, MB and Gibbon, M (2004) The structured clinical interview for DSM-IV axis I disorders (SCID-I) and the structured clinical interview for DSM-IV axis II disorders (SCID-II). In Hilsenroth, MJ and Segal, DL (eds), Comprehensive Handbook of Psychological Assessment, Vol. 2: Personality Assessment. Hoboken, NJ, USA: John Wiley & Sons Inc., pp. 134–143.Google Scholar
Fonseca-Pedrero, E, Debbane, M, Ortuno-Sierra, J, Chan, RCK, Cicero, DC, Zhang, LC, Brenner, C, Barkus, E, Linscott, RJ, Kwapil, T, Barrantes-Vidal, N, Cohen, A, Raine, A, Compton, MT, Tone, EB, Suhr, J, Muniz, J, Fumero, A, Giakoumaki, S, Tsaousis, I, Preti, A, Chmielewski, M, Laloyaux, J, Mechri, A, Lahmar, MA, Wuthrich, V, Laroi, F, Badcock, JC and Jablensky, A (2018) The structure of schizotypal personality traits: a cross-national study. Psychological Medicine 48, 451–462.CrossRefGoogle ScholarPubMed
Green, MF (1996) What are the functional consequences of neurocognitive deficits in schizophrenia? The American Journal of Psychiatry 153, 321–330.Google Scholar
Hasin, DS (2018) US epidemiology of cannabis use and associated problems. Neuropsychopharmacology 43, 195–212.CrossRefGoogle ScholarPubMed
Hasin, DS, Saha, TD, Kerridge, BT, Goldstein, RB, Chou, SP, Zhang, H, Jung, J, Pickering, RP, Ruan, WJ, Smith, SM, Huang, B and Grant, BF (2015) Prevalence of marijuana use disorders in the United States between 2001–2002 and 2012–2013. JAMA Psychiatry 72, 1235–1242.CrossRefGoogle ScholarPubMed
Heinrichs, RW and Zakzanis, KK (1998) Neurocognitive deficit in schizophrenia: a quantitative review of the evidence. Neuropsychology 12, 426–445.CrossRefGoogle Scholar
Hughes, C, Kumari, V, Soni, W, Das, M, Binneman, B, Drozd, S, O'Neil, S, Mathew, V and Sharma, T (2003) Longitudinal study of symptoms and cognitive function in chronic schizophrenia. Schizophrenia Research 59, 137–146.CrossRefGoogle ScholarPubMed
Keefe, RS, Bilder, RM, Harvey, PD, Davis, SM, Palmer, BW, Gold, JM, Meltzer, HY, Green, MF, Miller del, D, Canive, JM, Adler, LW, Manschreck, TC, Swartz, M, Rosenheck, R, Perkins, DO, Walker, TM, Stroup, TS, McEvoy, JP and Lieberman, JA (2006) Baseline neurocognitive deficits in the CATIE schizophrenia trial. Neuropsychopharmacology 31, 2033–2046.CrossRefGoogle ScholarPubMed
Leweke, FM, Piomelli, D, Pahlisch, F, Muhl, D, Gerth, CW, Hoyer, C, Klosterkotter, J, Hellmich, M and Koethe, D (2012) Cannabidiol enhances anandamide signaling and alleviates psychotic symptoms of schizophrenia. Translational Psychiatry 2, e94.CrossRefGoogle ScholarPubMed
McGuire, P, Robson, P, Cubala, WJ, Vasile, D, Morrison, PD, Barron, R, Taylor, A and Wright, S (2018) Cannabidiol (CBD) as an adjunctive therapy in schizophrenia: a multicenter randomized controlled trial. The American Journal of Psychiatry 175, 225–231.CrossRefGoogle ScholarPubMed
Meehl, PE (1989) Schizotaxia revisited. Archives Of General Psychiatry 46, 935–944.CrossRefGoogle ScholarPubMed
Morgan, CJ and Curran, HV (2008) Effects of cannabidiol on schizophrenia-like symptoms in people who use cannabis. British Journal of Psychiatry 192, 306–307.CrossRefGoogle ScholarPubMed
Morgan, CJ, Schafer, G, Freeman, TP and Curran, HV (2010) Impact of cannabidiol on the acute memory and psychotomimetic effects of smoked cannabis: naturalistic study. British Journal of Psychiatry 197, 285–290.CrossRefGoogle ScholarPubMed
National Academies of Sciences, Engineering and Medicine (2017) The health effects of Cannabis and cannabinoids: the current state of evidence and recommendations for research. Washington, DC: The National Academies Press.Google Scholar
Raine, A (1991) The SPQ: a scale for the assessment of schizotypal personality based on DSM-III-R criteria. Schizophrenia Bulletin 17, 555–564.CrossRefGoogle ScholarPubMed
Ranganathan, M and D'Souza, DC (2006) The acute effects of cannabinoids on memory in humans: a review. Psychopharmacology (Berl) 188, 425–444.CrossRefGoogle ScholarPubMed
Scott, JC, Slomiak, ST, Jones, JD, Rosen, AFG, Moore, TM and Gur, RC (2018) Association of cannabis with cognitive functioning in adolescents and young adults: a systematic review and meta-analysis. JAMA Psychiatry 75, 585–595.CrossRefGoogle Scholar
Sherif, M, Radhakrishnan, R, D'Souza, DC and Ranganathan, M (2016) Human laboratory studies on cannabinoids and psychosis. Biological Psychiatry 79, 526–538.CrossRefGoogle ScholarPubMed
Skosnik, PD, Park, S, Dobbs, L and Gardner, WL (2008) Affect processing and positive syndrome schizotypy in cannabis users. Psychiatry Research 157, 279–282.CrossRefGoogle ScholarPubMed
Solowij, N, Yücel, M, Respondek, C, Whittle, S, Lindsay, E, Pantelis, C and Lubman, D (2011) Cerebellar white-matter changes in cannabis users with and without schizophrenia. Psychological Medicine 41, 2349–2359.CrossRefGoogle ScholarPubMed
Solowij, N, Broyd, S, Greenwood, L-m, van Hell, H, Martelozzo, D, Rueb, K, Todd, J, Liu, Z, Galettis, P and Martin, J (2019) A randomised controlled trial of vaporised Δ9-tetrahydrocannabinol and cannabidiol alone and in combination in frequent and infrequent cannabis users: acute intoxication effects. European Archives of Psychiatry and Clinical Neuroscience 269, 17–35.CrossRefGoogle ScholarPubMed
Tikka, SK and D'Souza, DC (2019) The association between cannabinoids and psychosis. In Ivan, Montoya and Susan, Weiss (eds), Cannabis Use Disorders. Springer International Publishing, Springer Nature Switzerland, AG, pp. 127–155.CrossRefGoogle Scholar
Van Dam, NT, Earleywine, M and DiGiacomo, G (2008) Polydrug use, cannabis, and psychosis-like symptoms. Human Psychopharmacology 23, 475–485.CrossRefGoogle ScholarPubMed
Volkow, ND, Baler, RD, Compton, WM and Weiss, SR (2014) Adverse health effects of marijuana use. The New England Journal of Medicine 370, 2219–2227.CrossRefGoogle ScholarPubMed
Volkow, ND, Swanson, JM, Evins, AE, DeLisi, LE, Meier, MH, Gonzalez, R, Bloomfield, MA, Curran, HV and Baler, R (2016) Effects of cannabis use on human behavior, including cognition, motivation, and psychosis: a review. JAMA Psychiatry 73, 292–297.CrossRefGoogle ScholarPubMed
Winstock, A, Barratt, M, Maier, L and Ferris, J (2018) Global Drug Survey (2018) Key Findings Report.Google Scholar
Wu, LT, Zhu, H and Swartz, MS (2016) Trends in cannabis use disorders among racial/ethnic population groups in the United States. Drug and Alcohol Dependence 165, 181–190.CrossRefGoogle ScholarPubMed
Yücel, M, Lorenzetti, V, Suo, C, Zalesky, A, Fornito, A, Takagi, MJ, Lubman, D and Solowij, N (2016) Hippocampal harms, protection and recovery following regular cannabis use. Translational Psychiatry 6, e710.CrossRefGoogle ScholarPubMed