Cannabinoids and Brain Damage: A Systematic Review on a Frequently Overlooked Issue

Page: [741 - 757] Pages: 17

  • * (Excluding Mailing and Handling)

Abstract

Background: Although cannabinoid consumption represents a current social and health problem, especially in a historical context characterized by an open orientation for recreational and therapeutic purposes, risks regarding the neurotoxicity of such substances are frequently overlooked.

Objective: The present systematic review aims to summarize the available evidence regarding the mechanism of cannabinoids-induced brain damage as a substrate of neurological, psychiatric, and behavioral effects. Another objective is to provide support for future investigations and legislative choices.

Methods: The systematic literature search through PubMed and Scopus and a critical appraisal of the collected studies were conducted. Search terms were “(("Cannabinoids" OR "THC" OR "CBD") AND "Brain” AND ("Damage" OR "Toxicity"))” in the title and abstracts. Studies were included examining toxic effects on the brain potentially induced by cannabinoids on human subjects.

Results: At the end of the literature selection process, 30 papers were considered for the present review. The consumption of cannabinoids is associated with the development of psychiatric, neurocognitive, neurological disorders and, in some cases of acute consumption, even death. In this sense, the greatest risks have been related to the consumption of high-potency synthetic cannabinoids, although the consumption of phytocannabinoids is not devoid of risks.

Conclusion: The research carried out has allowed to highlight some critical points to focus on, such as the need to reinforce the toxic-epidemiologic monitor of new substances market and the importance of information for both medical personnel and general population, with particular attention to the mostly involved age groups.

Keywords: Toxicology, cannabinoids, cannabis, brain damage, toxicity, THC, CBD.

Graphical Abstract

[1]
Kabelik, J.; Krejci, Z.; Santavy, F. Cannabis as a medicament. Bull. Narc., 1960, 12(3), 5-23.
[2]
Moffat, A.C.; Osselton, M.D.; Widdop, B.; Watts, J. Clarke’s analysis of drugs and poisons, 4th ed; Pharmaceutical press: London, 2011.
[3]
Ligresti, A.; De Petrocellis, L.; Di Marzo, V. From phytocannabinoids to cannabinoid receptors and endocannabinoids: Pleiotropic physiological and pathological roles through complex pharmacology. Physiol. Rev., 2016, 96(4), 1593-1659.
[http://dx.doi.org/10.1152/physrev.00002.2016] [PMID: 27630175]
[4]
Russo, E.B.; Grotenhermen, F. The Handbook of Cannabis Therapeutics: From Bench to Bedside, 1st ed; Taylor & Francis Inc: New York, 2006.
[5]
Andre, C.M.; Hausman, J.F.; Guerriero, G. Cannabis sativa: The plant of the thousand and one molecules. Front. Plant Sci., 2016, 7, 19.
[http://dx.doi.org/10.3389/fpls.2016.00019] [PMID: 26870049]
[6]
Jacob, A.; Todd, A.R. Cannabis indica. Part II. Isolation of cannabidiol from Egyptian hashish. Observations on the structure of cannabinol. J. Chem. Soc., 1940, 119, 649-653.
[http://dx.doi.org/10.1039/jr9400000649]
[7]
Adams, R.; Hunt, M.; Clark, J.H. Structure of cannabidiol, a product isolated from the marihuana extract of Minnesota wild hemp. J. Am. Chem. Soc., 1940, 62(1), 196-200.
[http://dx.doi.org/10.1021/ja01858a058]
[8]
Gaoni, Y.; Mechoulam, R. Isolation, structure, and partial synthesis of an active constituent of hashish. J. Am. Chem. Soc., 1964, 86(8), 1646-1647.
[http://dx.doi.org/10.1021/ja01062a046]
[9]
Munro, S.; Thomas, K.L.; Abu-Shaar, M. Molecular characterization of a peripheral receptor for cannabinoids. Nature, 1993, 365(6441), 61-65.
[http://dx.doi.org/10.1038/365061a0] [PMID: 7689702]
[10]
MacCallum, C.A.; Russo, E.B. Practical considerations in medical cannabis administration and dosing. Eur. J. Intern. Med., 2018, 49, 12-19.
[http://dx.doi.org/10.1016/j.ejim.2018.01.004] [PMID: 29307505]
[12]
Devane, W.A.; Hanus, L.; Breuer, A.; Pertwee, R.G.; Stevenson, L.A.; Griffin, G.; Gibson, D.; Mandelbaum, A.; Etinger, A.; Mechoulam, R. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science, 1992, 258(5090), 1946-1949.
[http://dx.doi.org/10.1126/science.1470919] [PMID: 1470919]
[13]
Lu, H.C.; Mackie, K. Review of the endocannabinoid system. Biol. Psychiatry Cogn. Neurosci. Neuroimaging, 2021, 6(6), 607-615.
[PMID: 32980261]
[14]
Di Marzo, V. Targeting the endocannabinoid system: To enhance or reduce? Nat. Rev. Drug Discov., 2008, 7(5), 438-455.
[http://dx.doi.org/10.1038/nrd2553] [PMID: 18446159]
[15]
De Petrocellis, L.; Di Marzo, V. Non-CB1, non-CB2 receptors for endocannabinoids, plant cannabinoids, and synthetic cannabimimetics: Focus on G-protein-coupled receptors and transient receptor potential channels. J. Neuroimmune Pharmacol., 2010, 5(1), 103-121.
[http://dx.doi.org/10.1007/s11481-009-9177-z] [PMID: 19847654]
[16]
Madras, B.K. Update of cannabis and its medical use; World Health Organization: Geneva, 2015. Available from:. https://www.who.int/medicines/access/controlled-substances/6_2_cannabis_update.pdf (Accessed May 26, 2022)
[17]
Laprairie, R.B.; Bagher, A.M.; Kelly, M.E.M.; Denovan-Wright, E.M. Cannabidiol is a negative allosteric modulator of the cannabinoid CB1 receptor. Br. J. Pharmacol., 2015, 172(20), 4790-4805.
[http://dx.doi.org/10.1111/bph.13250] [PMID: 26218440]
[18]
McPartland, J.M.; Duncan, M.; Di Marzo, V.; Pertwee, R.G. Are cannabidiol and Δ(9) -tetrahydrocannabivarin negative modulators of the endocannabinoid system? A systematic review. Br. J. Pharmacol., 2015, 172(3), 737-753.
[http://dx.doi.org/10.1111/bph.12944] [PMID: 25257544]
[19]
Tham, M.; Yilmaz, O.; Alaverdashvili, M.; Kelly, M.E.M.; Denovan-Wright, E.M.; Laprairie, R.B. Allosteric and orthosteric pharmacology of cannabidiol and cannabidiol-dimethylheptyl at the type 1 and type 2 cannabinoid receptors. Br. J. Pharmacol., 2019, 176(10), 1455-1469.
[http://dx.doi.org/10.1111/bph.14440] [PMID: 29981240]
[20]
Straiker, A.; Dvorakova, M.; Zimmowitch, A.; Mackie, K. Cannabidiol inhibits endocannabinoid signaling in autaptic hippocampal neurons. Mol. Pharmacol., 2018, 94(1), 743-748.
[http://dx.doi.org/10.1124/mol.118.111864] [PMID: 29669714]
[21]
Davidson, C.; Opacka-Juffry, J.; Arevalo-Martin, A.; Garcia-Ovejero, D.; Molina-Holgado, E.; Molina-Holgado, F. Spicing up pharmacology: A review of synthetic cannabinoids from structure to adverse events. Adv. Pharmacol., 2017, 80, 135-168.
[http://dx.doi.org/10.1016/bs.apha.2017.05.001] [PMID: 28826533]
[22]
Radaelli, D.; Manfredi, A.; Zanon, M.; Fattorini, P.; Scopetti, M.; Neri, M.; Frisoni, P.; D’Errico, S. Synthetic cannabinoids and cathinones cardiotoxicity: Facts and perspectives. Curr. Neuropharmacol., 2021, 19(11), 2038-2048.
[http://dx.doi.org/10.2174/1570159X19666210412101929] [PMID: 33845747]
[23]
Seely, K.A.; Lapoint, J.; Moran, J.H.; Fattore, L. Spice drugs are more than harmless herbal blends: A review of the pharmacology and toxicology of synthetic cannabinoids. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2012, 39(2), 234-243.
[http://dx.doi.org/10.1016/j.pnpbp.2012.04.017] [PMID: 22561602]
[24]
Huffman, J.W.; Padgett, L.W. Recent developments in the medicinal chemistry of cannabimimetic indoles, pyrroles and indenes. Curr. Med. Chem., 2005, 12(12), 1395-1411.
[http://dx.doi.org/10.2174/0929867054020864] [PMID: 15974991]
[25]
Castaneto, M.S.; Gorelick, D.A.; Desrosiers, N.A.; Hartman, R.L.; Pirard, S.; Huestis, M.A. Synthetic cannabinoids: Epidemiology, pharmacodynamics, and clinical implications. Drug Alcohol Depend., 2014, 144, 12-41.
[http://dx.doi.org/10.1016/j.drugalcdep.2014.08.005] [PMID: 25220897]
[26]
Hu, S.S.J.; Mackie, K. Distribution of the endocannabinoid system in the central nervous system. Handb. Exp. Pharmacol., 2015, 231, 59-93.
[http://dx.doi.org/10.1007/978-3-319-20825-1_3] [PMID: 26408158]
[27]
Bodor, Á.L.; Katona, I.; Nyíri, G.; Mackie, K.; Ledent, C.; Hájos, N.; Freund, T.F. Endocannabinoid signaling in rat somatosensory cortex: Laminar differences and involvement of specific interneuron types. J. Neurosci., 2005, 25(29), 6845-6856.
[http://dx.doi.org/10.1523/JNEUROSCI.0442-05.2005] [PMID: 16033894]
[28]
Nyíri, G.; Cserép, C.; Szabadits, E.; Mackie, K.; Freund, T.F. CB1 cannabinoid receptors are enriched in the perisynaptic annulus and on preterminal segments of hippocampal GABAergic axons. Neuroscience, 2005, 136(3), 811-822.
[http://dx.doi.org/10.1016/j.neuroscience.2005.01.026] [PMID: 16344153]
[29]
Bacci, A.; Huguenard, J.R.; Prince, D.A. Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids. Nature, 2004, 431(7006), 312-316.
[http://dx.doi.org/10.1038/nature02913] [PMID: 15372034]
[30]
Kreitzer, A.C.; Carter, A.G.; Regehr, W.G. Inhibition of interneuron firing extends the spread of endocannabinoid signaling in the cerebellum. Neuron, 2002, 34(5), 787-796.
[http://dx.doi.org/10.1016/S0896-6273(02)00695-5] [PMID: 12062024]
[31]
Maroso, M.; Szabo, G.G.; Kim, H.K.; Alexander, A.; Bui, A.D.; Lee, S.H.; Lutz, B.; Soltesz, I. Cannabinoid control of learning and memory through HCN channels. Neuron, 2016, 89(5), 1059-1073.
[http://dx.doi.org/10.1016/j.neuron.2016.01.023] [PMID: 26898775]
[32]
Bénard, G.; Massa, F.; Puente, N.; Lourenço, J.; Bellocchio, L.; Soria-Gómez, E.; Matias, I.; Delamarre, A.; Metna-Laurent, M.; Cannich, A.; Hebert-Chatelain, E.; Mulle, C.; Ortega-Gutiérrez, S.; Martín-Fontecha, M.; Klugmann, M.; Guggenhuber, S.; Lutz, B.; Gertsch, J.; Chaouloff, F.; López-Rodríguez, M.L.; Grandes, P.; Rossignol, R.; Marsicano, G. Mitochondrial CB₁ receptors regulate neuronal energy metabolism. Nat. Neurosci., 2012, 15(4), 558-564.
[http://dx.doi.org/10.1038/nn.3053] [PMID: 22388959]
[33]
Navarrete, M.; Araque, A. Endocannabinoids mediate neuron-astrocyte communication. Neuron, 2008, 57(6), 883-893.
[http://dx.doi.org/10.1016/j.neuron.2008.01.029] [PMID: 18367089]
[34]
Sadhir, M. Pharmacology of cannabis. J. Pain Manag., 2016, 9(4), 375.
[35]
Herkenham, M.; Lynn, A.B.; Little, M.D.; Johnson, M.R.; Melvin, L.S.; de Costa, B.R.; Rice, K.C. Cannabinoid receptor localization in brain. Proc. Natl. Acad. Sci. USA, 1990, 87(5), 1932-1936.
[http://dx.doi.org/10.1073/pnas.87.5.1932] [PMID: 2308954]
[36]
Galiègue, S.; Mary, S.; Marchand, J.; Dussossoy, D.; Carrière, D.; Carayon, P.; Bouaboula, M.; Shire, D.; Le Fur, G.; Casellas, P. Expression of central and peripheral cannabinoid receptors in human immune tissues and leukocyte subpopulations. Eur. J. Biochem., 1995, 232(1), 54-61.
[http://dx.doi.org/10.1111/j.1432-1033.1995.tb20780.x] [PMID: 7556170]
[37]
Cabral, G.A.; Ferreira, G.A.; Jamerson, M.J. Endocannabinoids and the immune system in health and disease. Handb. Exp. Pharmacol., 2015, 231, 185-211.
[http://dx.doi.org/10.1007/978-3-319-20825-1_6] [PMID: 26408161]
[38]
Stella, N. Cannabinoid and cannabinoid-like receptors in microglia, astrocytes, and astrocytomas. Glia, 2010, 58(9), 1017-1030.
[http://dx.doi.org/10.1002/glia.20983] [PMID: 20468046]
[39]
Spiller, K.J.; Bi, G.H.; He, Y.; Galaj, E.; Gardner, E.L.; Xi, Z.X. Cannabinoid CB1 and CB2 receptor mechanisms underlie cannabis reward and aversion in rats. Br. J. Pharmacol., 2019, 176(9), 1268-1281.
[http://dx.doi.org/10.1111/bph.14625] [PMID: 30767215]
[40]
Kendall, D.; Alexander, S. Cannabinoid Pharmacology, 1st ed; Academic Press: Massachusetts, 2017.
[41]
Moher, D.; Liberati, A.; Tetzlaff, J.; Altman, D.G. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med., 2009, 6(7)e1000097
[http://dx.doi.org/10.1371/journal.pmed.1000097] [PMID: 19621072]
[42]
Liberati, A.; Altman, D.G.; Tetzlaff, J.; Mulrow, C.; Gøtzsche, P.C.; Ioannidis, J.P.; Clarke, M.; Devereaux, P.J.; Kleijnen, J.; Moher, D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: Explanation and elaboration. J. Clin. Epidemiol., 2009, 62(10), e1-e34.
[http://dx.doi.org/10.1016/j.jclinepi.2009.06.006] [PMID: 19631507]
[43]
Parrott, A.C.; Hayley, A.C.; Downey, L.A. Recreational stimulants, herbal, and spice cannabis: The core psychobiological processes that underlie their damaging effects. Hum. Psychopharmacol., 2017, 32(3)e2594
[http://dx.doi.org/10.1002/hup.2594] [PMID: 28557129]
[44]
Allsop, D.J.; Copeland, J.; Norberg, M.M.; Fu, S.; Molnar, A.; Lewis, J.; Budney, A.J. Quantifying the clinical significance of cannabis withdrawal. PLoS One, 2012, 7(9)e44864
[http://dx.doi.org/10.1371/journal.pone.0044864] [PMID: 23049760]
[45]
Budney, A.J.; Hughes, J.R.; Moore, B.A.; Novy, P.L. Marijuana abstinence effects in marijuana smokers maintained in their home environment. Arch. Gen. Psychiatry, 2001, 58(10), 917-924.
[http://dx.doi.org/10.1001/archpsyc.58.10.917] [PMID: 11576029]
[46]
Vandrey, R.G.; Budney, A.J.; Moore, B.A.; Hughes, J.R.; Budney, A.J.; Moore, B.A.; Hughes, J.R. A cross-study comparison of cannabis and tobacco withdrawal. Am. J. Addict., 2005, 14(1), 54-63.
[http://dx.doi.org/10.1080/10550490590899853] [PMID: 15804877]
[47]
Ashton, C.H. Pharmacology and effects of cannabis: A brief review. Br. J. Psychiatry, 2001, 178(2), 101-106.
[http://dx.doi.org/10.1192/bjp.178.2.101] [PMID: 11157422]
[48]
D’Souza, D.C.; Perry, E.; MacDougall, L.; Ammerman, Y.; Cooper, T.; Wu, Y.T.; Braley, G.; Gueorguieva, R.; Krystal, J.H. The psychotomimetic effects of intravenous delta-9-tetrahydrocannabinol in healthy individuals: Implications for psychosis. Neuropsychopharmacology, 2004, 29(8), 1558-1572.
[http://dx.doi.org/10.1038/sj.npp.1300496] [PMID: 15173844]
[49]
Paparelli, A.; Di Forti, M.; Morrison, P.D.; Murray, R.M. Drug-induced psychosis: How to avoid star gazing in schizophrenia research by looking at more obvious sources of light. Front. Behav. Neurosci., 2011, 5, 1.
[http://dx.doi.org/10.3389/fnbeh.2011.00001] [PMID: 21267359]
[50]
Di Forti, M.; Morgan, C.; Dazzan, P.; Pariante, C.; Mondelli, V.; Marques, T.R.; Handley, R.; Luzi, S.; Russo, M.; Paparelli, A.; Butt, A.; Stilo, S.A.; Wiffen, B.; Powell, J.; Murray, R.M. High-potency cannabis and the risk of psychosis. Br. J. Psychiatry, 2009, 195(6), 488-491.
[http://dx.doi.org/10.1192/bjp.bp.109.064220] [PMID: 19949195]
[51]
Sami, M.B.; Rabiner, E.A.; Bhattacharyya, S. Does cannabis affect dopaminergic signaling in the human brain? A systematic review of evidence to date. Eur. Neuropsychopharmacol., 2015, 25(8), 1201-1224.
[http://dx.doi.org/10.1016/j.euroneuro.2015.03.011] [PMID: 26068702]
[52]
Mechoulam, R.; Parker, L.A. The endocannabinoid system and the brain. Annu. Rev. Psychol., 2013, 64, 21-47.
[http://dx.doi.org/10.1146/annurev-psych-113011-143739] [PMID: 22804774]
[53]
Colizzi, M.; McGuire, P.; Pertwee, R.G.; Bhattacharyya, S. Effect of cannabis on glutamate signalling in the brain: A systematic review of human and animal evidence. Neurosci. Biobehav. Rev., 2016, 64, 359-381.
[http://dx.doi.org/10.1016/j.neubiorev.2016.03.010] [PMID: 26987641]
[54]
Sarne, Y.; Keren, O. Are cannabinoid drugs neurotoxic or neuroprotective? Med. Hypotheses, 2004, 63(2), 187-192.
[http://dx.doi.org/10.1016/j.mehy.2004.02.043] [PMID: 15236773]
[55]
Fried, P.A.; Watkinson, B.; Gray, R. Neurocognitive consequences of marihuana--a comparison with pre-drug performance. Neurotoxicol. Teratol., 2005, 27(2), 231-239.
[http://dx.doi.org/10.1016/j.ntt.2004.11.003] [PMID: 15734274]
[56]
Fernández-Serrano, M.J.; Pérez-García, M.; Verdejo-García, A. What are the specific vs. generalized effects of drugs of abuse on neuropsychological performance? Neurosci. Biobehav. Rev., 2011, 35(3), 377-406.
[http://dx.doi.org/10.1016/j.neubiorev.2010.04.008] [PMID: 20451551]
[57]
Meier, M.H.; Caspi, A.; Ambler, A.; Harrington, H.; Houts, R.; Keefe, R.S.; McDonald, K.; Ward, A.; Poulton, R.; Moffitt, T.E. Persistent cannabis users show neuropsychological decline from childhood to midlife. Proc. Natl. Acad. Sci. USA, 2012, 109(40), E2657-E2664.
[http://dx.doi.org/10.1073/pnas.1206820109] [PMID: 22927402]
[58]
Yücel, M.; Solowij, N.; Respondek, C.; Whittle, S.; Fornito, A.; Pantelis, C.; Lubman, D.I. Regional brain abnormalities associated with long-term heavy cannabis use. Arch. Gen. Psychiatry, 2008, 65(6), 694-701.
[http://dx.doi.org/10.1001/archpsyc.65.6.694] [PMID: 18519827]
[59]
Volkow, N.D.; Swanson, J.M.; Evins, A.E.; DeLisi, L.E.; Meier, M.H.; Gonzalez, R.; Bloomfield, M.A.P.; Curran, H.V.; Baler, R. Effects of cannabis use on human behavior, including cognition, motivation, and psychosis: A review. JAMA Psychiatry, 2016, 73(3), 292-297.
[http://dx.doi.org/10.1001/jamapsychiatry.2015.3278] [PMID: 26842658]
[60]
Mandelbaum, D.E.; de la Monte, S.M. Adverse structural and functional effects of marijuana on the brain: Evidence reviewed. Pediatr. Neurol., 2017, 66, 12-20.
[http://dx.doi.org/10.1016/j.pediatrneurol.2016.09.004] [PMID: 27789118]
[61]
Nakamura, E.M.M.; da Silva, E.A.; Concilio, G.V.; Wilkinson, D.A.; Masur, J. Reversible effects of acute and long-term administration of delta-9-tetrahydrocannabinol (THC) on memory in the rat. Drug Alcohol Depend., 1991, 28(2), 167-175.
[http://dx.doi.org/10.1016/0376-8716(91)90072-7] [PMID: 1657563]
[62]
Rubino, T.; Realini, N.; Braida, D.; Guidi, S.; Capurro, V.; Viganò, D.; Guidali, C.; Pinter, M.; Sala, M.; Bartesaghi, R.; Parolaro, D. Changes in hippocampal morphology and neuroplasticity induced by adolescent THC treatment are associated with cognitive impairment in adulthood. Hippocampus, 2009, 19(8), 763-772.
[http://dx.doi.org/10.1002/hipo.20554] [PMID: 19156848]
[63]
Pavisian, B.; MacIntosh, B.J.; Szilagyi, G.; Staines, R.W.; O’Connor, P.; Feinstein, A. Effects of cannabis on cognition in patients with MS: A psychometric and MRI study. Neurology, 2014, 82(21), 1879-1887.
[http://dx.doi.org/10.1212/WNL.0000000000000446] [PMID: 24789863]
[64]
Gouzoulis-Mayfrank, E.; Daumann, J. The confounding problem of polydrug use in recreational ecstasy/MDMA users: A brief overview. J. Psychopharmacol., 2006, 20(2), 188-193.
[http://dx.doi.org/10.1177/0269881106059939] [PMID: 16510477]
[65]
Battistella, G.; Fornari, E.; Annoni, J.M.; Chtioui, H.; Dao, K.; Fabritius, M.; Favrat, B.; Mall, J.F.; Maeder, P.; Giroud, C. Long-term effects of cannabis on brain structure. Neuropsychopharmacology, 2014, 39(9), 2041-2048.
[http://dx.doi.org/10.1038/npp.2014.67] [PMID: 24633558]
[66]
Morris, R.G.; Garrud, P.; Rawlins, J.N.; O’Keefe, J. Place navigation impaired in rats with hippocampal lesions. Nature, 1982, 297(5868), 681-683.
[http://dx.doi.org/10.1038/297681a0] [PMID: 7088155]
[67]
Lawston, J.; Borella, A.; Robinson, J.K.; Whitaker-Azmitia, P.M. Changes in hippocampal morphology following chronic treatment with the synthetic cannabinoid WIN 55,212-2. Brain Res., 2000, 877(2), 407-410.
[http://dx.doi.org/10.1016/S0006-8993(00)02739-6] [PMID: 10986361]
[68]
Scallet, A.C.; Uemura, E.; Andrews, A.; Ali, S.F.; McMillan, D.E.; Paule, M.G.; Brown, R.M.; Slikker, W. Jr Morphometric studies of the rat hippocampus following chronic delta-9-tetrahydrocannabinol (THC). Brain Res., 1987, 436(1), 193-198.
[http://dx.doi.org/10.1016/0006-8993(87)91576-9] [PMID: 2825925]
[69]
Scallet, A.C. Neurotoxicology of cannabis and THC: A review of chronic exposure studies in animals. Pharmacol. Biochem. Behav., 1991, 40(3), 671-676.
[http://dx.doi.org/10.1016/0091-3057(91)90380-K] [PMID: 1666926]
[70]
Landfield, P.W.; Cadwallader, L.B.; Vinsant, S. Quantitative changes in hippocampal structure following long-term exposure to delta 9-tetrahydrocannabinol: Possible mediation by glucocorticoid systems. Brain Res., 1988, 443(1-2), 47-62.
[http://dx.doi.org/10.1016/0006-8993(88)91597-1] [PMID: 2834017]
[71]
Guzmán, M.; Sánchez, C.; Galve-Roperh, I. Cannabinoids and cell fate. Pharmacol. Ther., 2002, 95(2), 175-184.
[http://dx.doi.org/10.1016/S0163-7258(02)00256-5] [PMID: 12182964]
[72]
Chan, G.C.K.; Hinds, T.R.; Impey, S.; Storm, D.R. Hippocampal neurotoxicity of Δ9-tetrahydrocannabinol. J. Neurosci., 1998, 18(14), 5322-5332.
[http://dx.doi.org/10.1523/JNEUROSCI.18-14-05322.1998] [PMID: 9651215]
[73]
Gilman, J.M.; Kuster, J.K.; Lee, S.; Lee, M.J.; Kim, B.W.; Makris, N.; van der Kouwe, A.; Blood, A.J.; Breiter, H.C. Cannabis use is quantitatively associated with nucleus accumbens and amygdala abnormalities in young adult recreational users. J. Neurosci., 2014, 34(16), 5529-5538.
[http://dx.doi.org/10.1523/JNEUROSCI.4745-13.2014] [PMID: 24741043]
[74]
Gilman, J.M.; Calderon, V.; Curran, M.T.; Evins, A.E. Young adult cannabis users report greater propensity for risk-taking only in non-monetary domains. Drug Alcohol Depend., 2015, 147, 26-31.
[http://dx.doi.org/10.1016/j.drugalcdep.2014.12.020] [PMID: 25577478]
[75]
Cousijn, J.; Wiers, R.W.; Ridderinkhof, K.R.; van den Brink, W.; Veltman, D.J.; Goudriaan, A.E. Grey matter alterations associated with cannabis use: Results of a VBM study in heavy cannabis users and healthy controls. Neuroimage, 2012, 59(4), 3845-3851.
[http://dx.doi.org/10.1016/j.neuroimage.2011.09.046] [PMID: 21982932]
[76]
Vaidya, J.G.; Block, R.I.; O’Leary, D.S.; Ponto, L.B.; Ghoneim, M.M.; Bechara, A. Effects of chronic marijuana use on brain activity during monetary decision-making. Neuropsychopharmacology, 2012, 37(3), 618-629.
[http://dx.doi.org/10.1038/npp.2011.227] [PMID: 21956445]
[77]
Jacobsen, L.K.; Mencl, W.E.; Westerveld, M.; Pugh, K.R. Impact of cannabis use on brain function in adolescents. Ann. N. Y. Acad. Sci., 2004, 1021(1), 384-390.
[http://dx.doi.org/10.1196/annals.1308.053] [PMID: 15251914]
[78]
Kanayama, G.; Rogowska, J.; Pope, H.G.; Gruber, S.A.; Yurgelun-Todd, D.A. Spatial working memory in heavy cannabis users: A functional magnetic resonance imaging study. Psychopharmacology, 2004, 176(3-4), 239-247.
[http://dx.doi.org/10.1007/s00213-004-1885-8] [PMID: 15205869]
[79]
Zalesky, A.; Solowij, N.; Yücel, M.; Lubman, D.I.; Takagi, M.; Harding, I.H.; Lorenzetti, V.; Wang, R.; Searle, K.; Pantelis, C.; Seal, M. Effect of long-term cannabis use on axonal fibre connectivity. Brain, 2012, 135(Pt 7), 2245-2255.
[http://dx.doi.org/10.1093/brain/aws136] [PMID: 22669080]
[80]
Solowij, N.; Yücel, M.; Respondek, C.; Whittle, S.; Lindsay, E.; Pantelis, C.; Lubman, D.I. Cerebellar white-matter changes in cannabis users with and without schizophrenia. Psychol. Med., 2011, 41(11), 2349-2359.
[http://dx.doi.org/10.1017/S003329171100050X] [PMID: 21466751]
[81]
Chung, T.; Pajtek, S.; Clark, D.B. White matter integrity as a link in the association between motivation to abstain and treatment outcome in adolescent substance users. Psychol. Addict. Behav., 2013, 27(2), 533-542.
[http://dx.doi.org/10.1037/a0026716] [PMID: 22369222]
[82]
Gruber, S.A.; Silveri, M.M.; Dahlgren, M.K.; Yurgelun-Todd, D. Why so impulsive? White matter alterations are associated with impulsivity in chronic marijuana smokers. Exp. Clin. Psychopharmacol., 2011, 19(3), 231-242.
[http://dx.doi.org/10.1037/a0023034] [PMID: 21480730]
[83]
Wolff, V.; Jouanjus, E. Strokes are possible complications of cannabinoids use Epilepsy Behav., 2017, 70(Pt B), 355-363.
[http://dx.doi.org/10.1016/j.yebeh.2017.01.031] [PMID: 28237318]
[84]
Wolff, V.; Schlagowski, A.I.; Rouyer, O.; Charles, A.L.; Singh, F.; Auger, C.; Schini-Kerth, V.; Marescaux, C.; Raul, J.S.; Zoll, J.; Geny, B. Tetrahydrocannabinol induces brain mitochondrial respiratory chain dysfunction and increases oxidative stress: A potential mechanism involved in cannabis-related stroke. BioMed Res. Int., 2015, 2015323706
[http://dx.doi.org/10.1155/2015/323706] [PMID: 25654095]
[85]
Chen, H.; Yoshioka, H.; Kim, G.S.; Jung, J.E.; Okami, N.; Sakata, H.; Maier, C.M.; Narasimhan, P.; Goeders, C.E.; Chan, P.H. Oxidative stress in ischemic brain damage: Mechanisms of cell death and potential molecular targets for neuroprotection. Antioxid. Redox Signal., 2011, 14(8), 1505-1517.
[http://dx.doi.org/10.1089/ars.2010.3576] [PMID: 20812869]
[86]
Wolff, V.; Rouyer, O.; Geny, B. Stroke related to marijuana: An underestimated risk. N. Engl. J. Med., 2014, 371(9), 878.
[PMID: 25162900]
[87]
Pellegrini-Giampietro, D.E.; Mannaioni, G.; Bagetta, G. Post-ischemic brain damage: The endocannabinoid system in the mechanisms of neuronal death. FEBS J., 2009, 276(1), 2-12.
[http://dx.doi.org/10.1111/j.1742-4658.2008.06765.x] [PMID: 19087195]
[88]
Mackie, K.; Hille, B. Cannabinoids inhibit N-type calcium channels in neuroblastoma-glioma cells. Proc. Natl. Acad. Sci. USA, 1992, 89(9), 3825-3829.
[http://dx.doi.org/10.1073/pnas.89.9.3825] [PMID: 1315042]
[89]
Shen, M.; Piser, T.M.; Seybold, V.S.; Thayer, S.A. Cannabinoid receptor agonists inhibit glutamatergic synaptic transmission in rat hippocampal cultures. J. Neurosci., 1996, 16(14), 4322-4334.
[http://dx.doi.org/10.1523/JNEUROSCI.16-14-04322.1996] [PMID: 8699243]
[90]
Muthian, S.; Rademacher, D.J.; Roelke, C.T.; Gross, G.J.; Hillard, C.J. Anandamide content is increased and CB1 cannabinoid receptor blockade is protective during transient, focal cerebral ischemia. Neuroscience, 2004, 129(3), 743-750.
[http://dx.doi.org/10.1016/j.neuroscience.2004.08.044] [PMID: 15541895]
[91]
Amantea, D.; Spagnuolo, P.; Bari, M.; Fezza, F.; Mazzei, C.; Tassorelli, C.; Morrone, L.A.; Corasaniti, M.T.; Maccarrone, M.; Bagetta, G. Modulation of the endocannabinoid system by focal brain ischemia in the rat is involved in neuroprotection afforded by 17β-estradiol. FEBS J., 2007, 274(17), 4464-4775.
[http://dx.doi.org/10.1111/j.1742-4658.2007.05975.x] [PMID: 17666109]
[92]
Berger, C.; Schmid, P.C.; Schabitz, W.R.; Wolf, M.; Schwab, S.; Schmid, H.H. Massive accumulation of N-acylethanolamines after stroke. Cell signalling in acute cerebral ischemia? J. Neurochem., 2004, 88(5), 1159-1167.
[http://dx.doi.org/10.1046/j.1471-4159.2003.02244.x] [PMID: 15009671]
[93]
Melis, M.; Pillolla, G.; Bisogno, T.; Minassi, A.; Petrosino, S.; Perra, S.; Muntoni, A.L.; Lutz, B.; Gessa, G.L.; Marsicano, G.; Di Marzo, V.; Pistis, M. Protective activation of the endocannabinoid system during ischemia in dopamine neurons. Neurobiol. Dis., 2006, 24(1), 15-27.
[http://dx.doi.org/10.1016/j.nbd.2006.04.010] [PMID: 16762556]
[94]
Degn, M.; Lambertsen, K.L.; Petersen, G.; Meldgaard, M.; Artmann, A.; Clausen, B.H.; Hansen, S.H.; Finsen, B.; Hansen, H.S.; Lund, T.M. Changes in brain levels of N-acylethanolamines and 2-arachidonoylglycerol in focal cerebral ischemia in mice. J. Neurochem., 2007, 103(5), 1907-1916.
[http://dx.doi.org/10.1111/j.1471-4159.2007.04892.x] [PMID: 17868306]
[95]
Maccarrone, M.; Finazzi-Agró, A. The endocannabinoid system, anandamide and the regulation of mammalian cell apoptosis. Cell Death Differ., 2003, 10(9), 946-955.
[http://dx.doi.org/10.1038/sj.cdd.4401284] [PMID: 12934069]
[96]
Cernak, I.; Vink, R.; Natale, J.; Stoica, B.; Lea, P.M., IV; Movsesyan, V.; Ahmed, F.; Knoblach, S.M.; Fricke, S.T.; Faden, A.I. The “dark side” of endocannabinoids: A neurotoxic role for anandamide. J. Cereb. Blood Flow Metab., 2004, 24(5), 564-578.
[http://dx.doi.org/10.1097/00004647-200405000-00011] [PMID: 15129189]
[97]
Bari, M.; Battista, N.; Fezza, F.; Finazzi-Agrò, A.; Maccarrone, M. Lipid rafts control signaling of type-1 cannabinoid receptors in neuronal cells. Implications for anandamide-induced apoptosis. J. Biol. Chem., 2005, 280(13), 12212-12220.
[http://dx.doi.org/10.1074/jbc.M411642200] [PMID: 15657045]
[98]
Galve-Roperh, I.; Aguado, T.; Palazuelos, J.; Guzmán, M. Mechanisms of control of neuron survival by the endocannabinoid system. Curr. Pharm. Des., 2008, 14(23), 2279-2288.
[http://dx.doi.org/10.2174/138161208785740117] [PMID: 18781978]
[99]
Downer, E.J.; Fogarty, M.P.; Campbell, V.A. Tetrahydrocannabinol-induced neurotoxicity depends on CB1 receptor-mediated c-Jun N-terminal kinase activation in cultured cortical neurons. Br. J. Pharmacol., 2003, 140(3), 547-557.
[http://dx.doi.org/10.1038/sj.bjp.0705464] [PMID: 14522843]
[100]
Derkinderen, P.; Ledent, C.; Parmentier, M.; Girault, J.A. Cannabinoids activate p38 mitogen-activated protein kinases through CB1 receptors in hippocampus. J. Neurochem., 2001, 77(3), 957-960.
[http://dx.doi.org/10.1046/j.1471-4159.2001.00333.x] [PMID: 11331425]
[101]
Movsesyan, V.A.; Stoica, B.A.; Yakovlev, A.G.; Knoblach, S.M.; Lea, P.M., IV; Cernak, I.; Vink, R.; Faden, A.I. Anandamide-induced cell death in primary neuronal cultures: Role of calpain and caspase pathways. Cell Death Differ., 2004, 11(10), 1121-1132.
[http://dx.doi.org/10.1038/sj.cdd.4401442] [PMID: 15375383]
[102]
Gowran, A.; Campbell, V.A. A role for p53 in the regulation of lysosomal permeability by delta 9-tetrahydrocannabinol in rat cortical neurones: Implications for neurodegeneration. J. Neurochem., 2008, 105(4), 1513-1524.
[http://dx.doi.org/10.1111/j.1471-4159.2008.05278.x] [PMID: 18248609]
[103]
Mestre, L.; Correa, F.; Docagne, F.; Clemente, D.; Guaza, C. The synthetic cannabinoid WIN 55,212-2 increases COX-2 expression and PGE2 release in murine brain-derived endothelial cells following Theiler’s virus infection. Biochem. Pharmacol., 2006, 72(7), 869-880.
[http://dx.doi.org/10.1016/j.bcp.2006.06.037] [PMID: 16914119]
[104]
Ramer, R.; Weinzierl, U.; Schwind, B.; Brune, K.; Hinz, B. Ceramide is involved in r(+)-methanandamide-induced cyclooxygenase-2 expression in human neuroglioma cells. Mol. Pharmacol., 2003, 64(5), 1189-1198.
[http://dx.doi.org/10.1124/mol.64.5.1189] [PMID: 14573769]
[105]
Klegeris, A.; Bissonnette, C.J.; McGeer, P.L. Reduction of human monocytic cell neurotoxicity and cytokine secretion by ligands of the cannabinoid-type CB2 receptor. Br. J. Pharmacol., 2003, 139(4), 775-786.
[http://dx.doi.org/10.1038/sj.bjp.0705304] [PMID: 12813001]
[106]
Bladen, C.; Mirlohi, S.; Santiago, M.; Longworth, M.; Kassiou, M.; Banister, S.; Connor, M. Modulation of human T-type calcium channels by synthetic cannabinoid receptor agonists in vitro. Neuropharmacology, 2021, 187108478
[http://dx.doi.org/10.1016/j.neuropharm.2021.108478] [PMID: 33600843]
[107]
Coccini, T.; De Simone, U.; Lonati, D.; Scaravaggi, G.; Marti, M.; Locatelli, C.A. MAM-2201, one of the most potent-naphthoyl indole derivative-synthetic cannabinoids, exerts toxic effects on human cell-based models of neurons and astrocytes. Neurotox. Res., 2021, 39(4), 1251-1273.
[http://dx.doi.org/10.1007/s12640-021-00369-3] [PMID: 33945101]
[108]
Sarne, Y.; Asaf, F.; Fishbein, M.; Gafni, M.; Keren, O. The dual neuroprotective-neurotoxic profile of cannabinoid drugs. Br. J. Pharmacol., 2011, 163(7), 1391-1401.
[http://dx.doi.org/10.1111/j.1476-5381.2011.01280.x] [PMID: 21323910]
[109]
Nagayama, T.; Sinor, A.D.; Simon, R.P.; Chen, J.; Graham, S.H.; Jin, K.; Greenberg, D.A. Cannabinoids and neuroprotection in global and focal cerebral ischemia and in neuronal cultures. J. Neurosci., 1999, 19(8), 2987-2995.
[http://dx.doi.org/10.1523/JNEUROSCI.19-08-02987.1999] [PMID: 10191316]
[110]
Rubovitch, V.; Gafni, M.; Sarne, Y. The cannabinoid agonist DALN positively modulates L-type voltage-dependent calcium-channels in N18TG2 neuroblastoma cells. Brain Res. Mol. Brain Res., 2002, 101(1-2), 93-102.
[http://dx.doi.org/10.1016/S0169-328X(02)00174-2] [PMID: 12007836]
[111]
Bash, R.; Rubovitch, V.; Gafni, M.; Sarne, Y. The stimulatory effect of cannabinoids on calcium uptake is mediated by Gs GTP-binding proteins and cAMP formation. Neurosignals, 2003, 12(1), 39-44.
[http://dx.doi.org/10.1159/000068915] [PMID: 12624527]
[112]
Stiglick, A.; Llewellyn, M.E.; Kalant, H. Residual effects of prolonged cannabis treatment on shuttle-box avoidance in the rat. Psychopharmacology, 1984, 84(4), 476-479.
[http://dx.doi.org/10.1007/BF00431452] [PMID: 6441947]
[113]
Solowij, N.; Stephens, R.S.; Roffman, R.A.; Babor, T.; Kadden, R.; Miller, M.; Christiansen, K.; McRee, B.; Vendetti, J. Cognitive functioning of long-term heavy cannabis users seeking treatment. JAMA, 2002, 287(9), 1123-1131.
[http://dx.doi.org/10.1001/jama.287.9.1123] [PMID: 11879109]
[114]
van der Stelt, M.; Veldhuis, W.B.; Bär, P.R.; Veldink, G.A.; Vliegenthart, J.F.G.; Nicolay, K. Neuroprotection by Δ9-tetrahydrocannabinol, the main active compound in marijuana, against ouabain-induced in vivo excitotoxicity. J. Neurosci., 2001, 21(17), 6475-6479.
[http://dx.doi.org/10.1523/JNEUROSCI.21-17-06475.2001] [PMID: 11517236]
[115]
Panikashvili, D.; Simeonidou, C.; Ben-Shabat, S.; Hanuš, L.; Breuer, A.; Mechoulam, R.; Shohami, E. An endogenous cannabinoid (2-AG) is neuroprotective after brain injury. Nature, 2001, 413(6855), 527-531.
[http://dx.doi.org/10.1038/35097089] [PMID: 11586361]
[116]
European Monitoring Centre for Drugs and Drug Addiction. Report on the risk assessment of methyl 2-[[1-(cyclohexylmethyl)- 1H-indole-3-carbonyl]amino]-3,3-dimethylbutanoate (MDMBCHMICA) in the framework of the Council Decision on new psychoactive substances, Risk Assessments, Publications Office of the European Union, Luxembourg. 2016. Available from:https://www.emcdda.europa.eu/publications/risk-assessments/mdmb-chmica_en (Accessed on May 26, 2022).
[117]
Hill, S.L.; Najafi, J.; Dunn, M.; Acheampong, P.; Kamour, A.; Grundlingh, J.; Blain, P.G.; Thomas, S.H. Clinical toxicity following analytically confirmed use of the synthetic cannabinoid receptor agonist MDMB-CHMICA. A report from the Identification Of Novel psychoActive substances (IONA) study. Clin. Toxicol. (Phila.), 2016, 54(8), 638-643.
[http://dx.doi.org/10.1080/15563650.2016.1190980] [PMID: 27251903]
[118]
Hermanns-Clausen, M.; Kneisel, S.; Hutter, M.; Szabo, B.; Auwärter, V. Acute intoxication by synthetic cannabinoids--four case reports. Drug Test. Anal., 2013, 5(9-10), 790-794.
[http://dx.doi.org/10.1002/dta.1483] [PMID: 23696237]
[119]
Pant, S.; Deshmukh, A.; Dholaria, B.; Kaur, V.; Ramavaram, S.; Ukor, M.; Teran, G.A. Spicy seizure. Am. J. Med. Sci., 2012, 344(1), 67-68.
[http://dx.doi.org/10.1097/MAJ.0b013e31824cf5c2] [PMID: 22627260]
[120]
Trecki, J.; Gerona, R.R.; Schwartz, M.D. Synthetic cannabinoid-related illnesses and deaths. N. Engl. J. Med., 2015, 373(2), 103-107.
[http://dx.doi.org/10.1056/NEJMp1505328] [PMID: 26154784]
[121]
Katz, K.D.; Leonetti, A.L.; Bailey, B.C.; Surmaitis, R.M.; Eustice, E.R.; Kacinko, S.; Wheatley, S.M. Case series of synthetic cannabinoid intoxication from one toxicology center. West. J. Emerg. Med., 2016, 17(3), 290-294.
[http://dx.doi.org/10.5811/westjem.2016.2.29519] [PMID: 27330661]
[122]
Lapoint, J.; James, L.P.; Moran, C.L.; Nelson, L.S.; Hoffman, R.S.; Moran, J.H. Severe toxicity following synthetic cannabinoid ingestion. Clin. Toxicol., 2011, 49(8), 760-764.
[http://dx.doi.org/10.3109/15563650.2011.609822] [PMID: 21970775]
[123]
Fattore, L.; Fratta, W. Beyond THC: The new generation of cannabinoid designer drugs. Front. Behav. Neurosci., 2011, 5, 60.
[http://dx.doi.org/10.3389/fnbeh.2011.00060] [PMID: 22007163]
[124]
Dines, A.M.; Wood, D.M.; Galicia, M.; Yates, C.M.; Heyerdahl, F.; Hovda, K.E.; Giraudon, I.; Sedefov, R.; Dargan, P.I. Presentations to the emergency department following cannabis use—a multi-centre case series from ten European countries. J. Med. Toxicol., 2015, 11(4), 415-421.
[http://dx.doi.org/10.1007/s13181-014-0460-x] [PMID: 25652342]
[125]
Pélissier, F.; Claudet, I.; Pélissier-Alicot, A.L.; Franchitto, N. Parental cannabis abuse and accidental intoxications in children: Prevention by detecting neglectful situations and at-risk families. Pediatr. Emerg. Care, 2014, 30(12), 862-866.
[http://dx.doi.org/10.1097/PEC.0000000000000288] [PMID: 25407034]
[126]
Appelboam, A.; Oades, P.J. Coma due to cannabis toxicity in an infant. Eur. J. Emerg. Med., 2006, 13(3), 177-179.
[http://dx.doi.org/10.1097/01.mej.0000194405.38206.f2] [PMID: 16679885]
[127]
Claudet, I.; Le Breton, M.; Bréhin, C.; Franchitto, N. A 10-year review of cannabis exposure in children under 3-years of age: Do we need a more global approach? Eur. J. Pediatr., 2017, 176(4), 553-556.
[http://dx.doi.org/10.1007/s00431-017-2872-5] [PMID: 28210835]
[128]
Wang, T.; Collet, J.P.; Shapiro, S.; Ware, M.A. Adverse effects of medical cannabinoids: A systematic review. CMAJ, 2008, 178(13), 1669-1678.
[http://dx.doi.org/10.1503/cmaj.071178] [PMID: 18559804]
[129]
Kaczor, E.E.; Mathews, B.; LaBarge, K.; Chapman, B.P.; Carreiro, S. Cannabis product ingestions in pediatric patients: Ranges of exposure, effects, and outcomes. J. Med. Toxicol., 2021, 17(4), 386-396.
[http://dx.doi.org/10.1007/s13181-021-00849-0] [PMID: 34117620]
[130]
Černe, K. Toxicological properties of Δ9-tetrahydrocannabinol and cannabidiol. Arh. Hig. Rada Toksikol., 2020, 71(1), 1-11.
[http://dx.doi.org/10.2478/aiht-2020-71-3301] [PMID: 32597140]
[131]
Tzadok, M.; Uliel-Siboni, S.; Linder, I.; Kramer, U.; Epstein, O.; Menascu, S.; Nissenkorn, A.; Yosef, O.B.; Hyman, E.; Granot, D.; Dor, M.; Lerman-Sagie, T.; Ben-Zeev, B. CBD-enriched medical cannabis for intractable pediatric epilepsy: The current Israeli experience. Seizure, 2016, 35, 41-44.
[http://dx.doi.org/10.1016/j.seizure.2016.01.004] [PMID: 26800377]
[132]
Novotna, A.; Mares, J.; Ratcliffe, S.; Novakova, I.; Vachova, M.; Zapletalova, O.; Gasperini, C.; Pozzilli, C.; Cefaro, L.; Comi, G.; Rossi, P.; Ambler, Z.; Stelmasiak, Z.; Erdmann, A.; Montalban, X.; Klimek, A.; Davies, P. A randomized, double-blind, placebo-controlled, parallel-group, enriched-design study of nabiximols* (Sativex(®)), as add-on therapy, in subjects with refractory spasticity caused by multiple sclerosis. Eur. J. Neurol., 2011, 18(9), 1122-1131.
[http://dx.doi.org/10.1111/j.1468-1331.2010.03328.x] [PMID: 21362108]
[133]
Langford, R.M.; Mares, J.; Novotna, A.; Vachova, M.; Novakova, I.; Notcutt, W.; Ratcliffe, S. A double-blind, randomized, placebo-controlled, parallel-group study of THC/CBD oromucosal spray in combination with the existing treatment regimen, in the relief of central neuropathic pain in patients with multiple sclerosis. J. Neurol., 2013, 260(4), 984-997.
[http://dx.doi.org/10.1007/s00415-012-6739-4] [PMID: 23180178]
[134]
García-Merino, A. Endocannabinoid system modulator use in everyday clinical practice in the UK and Spain. Expert Rev. Neurother., 2013, 13(3)(Suppl. 1), 9-13.
[http://dx.doi.org/10.1586/ern.13.4] [PMID: 23369054]
[135]
Rekand, T. THC: CBD spray and MS spasticity symptoms: Data from latest studies. Eur. Neurol., 2014, 71(Suppl. 1), 4-9.
[http://dx.doi.org/10.1159/000357742] [PMID: 24457846]
[136]
Schloss, J.; Lacey, J.; Sinclair, J.; Steel, A.; Sughrue, M.; Sibbritt, D.; Teo, C. A phase 2 randomised clinical trial assessing the tolerability of two different ratios of medicinal cannabis in patients with high grade gliomas. Front. Oncol., 2021, 11649555
[http://dx.doi.org/10.3389/fonc.2021.649555] [PMID: 34094937]
[137]
Moore, T.H.; Zammit, S.; Lingford-Hughes, A.; Barnes, T.R.; Jones, P.B.; Burke, M.; Lewis, G. Cannabis use and risk of psychotic or affective mental health outcomes: A systematic review. Lancet, 2007, 370(9584), 319-328.
[http://dx.doi.org/10.1016/S0140-6736(07)61162-3] [PMID: 17662880]
[138]
Pantelis, C.; Yücel, M.; Wood, S.J.; Velakoulis, D.; Sun, D.; Berger, G.; Stuart, G.W.; Yung, A.; Phillips, L.; McGorry, P.D. Structural brain imaging evidence for multiple pathological processes at different stages of brain development in schizophrenia. Schizophr. Bull., 2005, 31(3), 672-696.
[http://dx.doi.org/10.1093/schbul/sbi034] [PMID: 16020551]
[139]
González-Pinto, A.; Alberich, S.; Barbeito, S.; Gutierrez, M.; Vega, P.; Ibáñez, B.; Haidar, M.K.; Vieta, E.; Arango, C. Cannabis and first-episode psychosis: Different long-term outcomes depending on continued or discontinued use. Schizophr. Bull., 2011, 37(3), 631-639.
[http://dx.doi.org/10.1093/schbul/sbp126] [PMID: 19915168]
[140]
Di Forti, M.; Sallis, H.; Allegri, F.; Trotta, A.; Ferraro, L.; Stilo, S.A.; Marconi, A.; La Cascia, C.; Reis Marques, T.; Pariante, C.; Dazzan, P.; Mondelli, V.; Paparelli, A.; Kolliakou, A.; Prata, D.; Gaughran, F.; David, A.S.; Morgan, C.; Stahl, D.; Khondoker, M.; MacCabe, J.H.; Murray, R.M. Daily use, especially of high-potency cannabis, drives the earlier onset of psychosis in cannabis users. Schizophr. Bull., 2014, 40(6), 1509-1517.
[http://dx.doi.org/10.1093/schbul/sbt181] [PMID: 24345517]
[141]
Schoeler, T.; Petros, N.; Di Forti, M.; Klamerus, E.; Foglia, E.; Murray, R.; Bhattacharyya, S. Poor medication adherence and risk of relapse associated with continued cannabis use in patients with first-episode psychosis: A prospective analysis. Lancet Psychiatry, 2017, 4(8), 627-633.
[http://dx.doi.org/10.1016/S2215-0366(17)30233-X] [PMID: 28705600]
[142]
Sideli, L.; Quigley, H.; La Cascia, C.; Murray, R.M. Cannabis use and the risk for psychosis and affective disorders. J. Dual Diagn., 2020, 16(1), 22-42.
[http://dx.doi.org/10.1080/15504263.2019.1674991] [PMID: 31647377]
[143]
D’Errico, S.; Russa, R.; Maiese, A.; Santurro, A.; Scopetti, M.; Romano, S.; Zanon, M.; Frati, P.; Fineschi, V. Atypical antipsychotics and oxidative cardiotoxicity: Review of literature and future perspectives to prevent sudden cardiac death. J. Geriatr. Cardiol., 2021, 18(8), 663-685.
[PMID: 34527032]
[144]
Walterfang, M.; Velakoulis, D.; Whitford, T.J.; Pantelis, C. Understanding aberrant white matter development in schizophrenia: An avenue for therapy? Expert Rev. Neurother., 2011, 11(7), 971-987.
[http://dx.doi.org/10.1586/ern.11.76] [PMID: 21721915]
[145]
Becker, M.P.; Collins, P.F.; Lim, K.O.; Muetzel, R.L.; Luciana, M. Longitudinal changes in white matter microstructure after heavy cannabis use. Dev. Cogn. Neurosci., 2015, 16, 23-35.
[http://dx.doi.org/10.1016/j.dcn.2015.10.004] [PMID: 26602958]
[146]
Walterfang, M.; Wood, S.J.; Velakoulis, D.; Copolov, D.; Pantelis, C. Diseases of white matter and schizophrenia-like psychosis. Aust. N. Z. J. Psychiatry, 2005, 39(9), 746-756.
[http://dx.doi.org/10.1080/j.1440-1614.2005.01678.x] [PMID: 16168032]
[147]
Murray, R.M.; Englund, A.; Abi-Dargham, A.; Lewis, D.A.; Di Forti, M.; Davies, C.; Sherif, M.; McGuire, P.; D’Souza, D.C. Cannabis-associated psychosis: Neural substrate and clinical impact. Neuropharmacology, 2017, 124, 89-104.
[http://dx.doi.org/10.1016/j.neuropharm.2017.06.018] [PMID: 28634109]
[148]
Pearson, N.T.; Berry, J.H. Cannabis and psychosis through the lens of DSM-5. Int. J. Environ. Res. Public Health, 2019, 16(21), 4149.
[http://dx.doi.org/10.3390/ijerph16214149] [PMID: 31661851]
[149]
National Academies of Sciences, Engineering, and Medicine; Health and Medicine Division; Board on Population Health and Public Health Practice; Committee on the Health Effects of Marijuana: An Evidence Review and Research Agenda. The health effects of cannabis and cannabinoids: The current state of evidence and recommendations for research, 1st ed; National Academies Press: Washington, DC, 2017.
[150]
Chesney, E.; Oliver, D.; Green, A.; Sovi, S.; Wilson, J.; Englund, A.; Freeman, T.P.; McGuire, P. Adverse effects of cannabidiol: A systematic review and meta-analysis of randomized clinical trials. Neuropsychopharmacology, 2020, 45(11), 1799-1806.
[http://dx.doi.org/10.1038/s41386-020-0667-2] [PMID: 32268347]
[151]
Hasin, D.S. US epidemiology of cannabis use and associated problems. Neuropsychopharmacology, 2018, 43(1), 195-212.
[http://dx.doi.org/10.1038/npp.2017.198] [PMID: 28853439]
[152]
Robinson, T.E.; Kolb, B. Alterations in the morphology of dendrites and dendritic spines in the nucleus accumbens and prefrontal cortex following repeated treatment with amphetamine or cocaine. Eur. J. Neurosci., 1999, 11(5), 1598-1604.
[http://dx.doi.org/10.1046/j.1460-9568.1999.00576.x] [PMID: 10215912]
[153]
Koob, G.F.; Volkow, N.D. Neurocircuitry of addiction. Neuropsychopharmacology, 2010, 35(1), 217-238.
[http://dx.doi.org/10.1038/npp.2009.110] [PMID: 19710631]
[154]
Wiers, R.W.; Bartholow, B.D.; van den Wildenberg, E.; Thush, C.; Engels, R.C.; Sher, K.J.; Grenard, J.; Ames, S.L.; Stacy, A.W. Automatic and controlled processes and the development of addictive behaviors in adolescents: A review and a model. Pharmacol. Biochem. Behav., 2007, 86(2), 263-283.
[http://dx.doi.org/10.1016/j.pbb.2006.09.021] [PMID: 17116324]
[155]
Hoch, E.; Bonnet, U.; Thomasius, R.; Ganzer, F.; Havemann-Reinecke, U.; Preuss, U.W. Risks associated with the non-medicinal use of cannabis. Dtsch. Arztebl. Int., 2015, 112(16), 271-278.
[http://dx.doi.org/10.3238/arztebl.2015.0271] [PMID: 25939318]