Cannabinoids in Late-Onset Alzheimer's Disease

Clinical Pharmacology and Therapeutics

Volumn 97, Issue 6, 2015, Pages 597-606

  Ahmed, A I A ^a,b   Van Der Marck, M A ^b   Van Den Elsen, G A H ^b,c   Olde Rikkert, M G M ^b,c  

^a VINCENT VAN GOGH INSTITUTE FOR PSYCHIATRY   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c RADBOUD UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CANNABINOID; ENDOCANNABINOID;

AGING; ALZHEIMER DISEASE; ARTICLE; DRUG EFFICACY; DRUG SAFETY; HUMAN; MENTAL DISEASE; NEUROLOGIC DISEASE; NONHUMAN; PATHOPHYSIOLOGY; PREVALENCE; PRIORITY JOURNAL; PHYSIOLOGY; PSYCHOLOGY;

AGING; ALZHEIMER DISEASE; CANNABINOIDS; ENDOCANNABINOIDS; HUMANS;

EID: 84938914358     PISSN: 00099236     EISSN: 15326535     Source Type: Journal    
DOI: 10.1002/cpt.117     Document Type: Article

References (75)

1. World Health Organization and Alzheimer's Disease International. Dementia: A public health priority. (World Health Organization, 2012). http://apps.who.int/iris/bitstream/10665/75263/1/9789241564458-eng.pdf?ua51 Accessed 20 December 2014.
2. Andersen, F., Viitanen, M., Halvorsen, D.S., Straume, B. & Engstad, T.A. Co-morbidity and drug treatment in Alzheimer's disease. A cross sectional study of participants in the dementia study in northern Norway. BMC Geriatr. 11, 58 (2011).
3. Ahmed, A.I., Van Den Elsen, G.A., Van Der Marck, M.A. & Olde Rikkert, M.G. Medicinal use of cannabis and cannabinoids in older adults: Where is the evidence? J. Am. Geriatr. Soc. 62, 410-411 (2014).
4. Ahmed, A.I., Van Den Elsen, G.A., Van Der Marck, M.A. & Olde Rikkert, M.G. Cannabinoids for pain in dementia: The good, the bad, and the ugly. J. Am. Geriatr. Soc. 62, 1001-1002 (2014).
5. Van Den Elsen, G.A. et al. Efficacy and safety of medical cannabinoids in older subjects: A systematic review. Ageing Res. Rev. 14, 56-64 (2014).
6. Corsonello, A., Pedone, C. & Incalzi, R.A. Age-related pharmacokinetic and pharmacodynamic changes and related risk of adverse drug reactions. Curr. Med. Chem. 17, 571-584 (2010).
7. Hebert, L.E., Weuve, J., Scherr, P.A. & Evans, D.A. Alzheimer disease in the United States (2010-2050) estimated using the 2010 census. Neurology 80, 1778-1783 (2013).
8. Deckers, K. et al. Target risk factors for dementia prevention: A systematic review and Delphi consensus study on the evidence from observational studies. Int. J. Geriatr. Psychiatry 30, 234-246 (2015).
9. Hardy, J. The amyloid hypothesis for Alzheimer's disease: A critical reappraisal. J. Neurochem. 110, 1129-1134 (2009).
10. Eikelenboom, P., Veerhuis, R., Scheper, W., Rozemuller, A.J., Van Gool, W.A. & Hoozemans, J.J. The significance of neuroinflammation in understanding Alzheimer's disease. J. Neural Transm. 113, 1685-1695 (2006).
11. Chen, J.X. & Yan, S.S. Role of mitochondrial amyloid-beta in Alzheimer's disease. J. Alzheimers Dis. 20 Suppl 2, S569-S578 (2010).
12. Smith, I.F., Green, K.N. & LaFerla, F.M. Calcium dysregulation in Alzheimer's disease: Recent advances gained from genetically modified animals. Cell Calcium 38, 427-437 (2005).
13. Birks, J. Cholinesterase inhibitors for Alzheimer's disease. Cochrane Database Syst. Rev. 1, CD005593 (2006).
14. L-opez-Pousa, S. & Arranz, F.J. Characteristics of patients with Alzheimer's disease who switch to rivastigmine transdermal patches in routine clinical practice. Patient Prefer. Adherence 7, 47-54 (2013).
15. Schenk, D. et al. Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 8, 173-177 (1999).
16. Orgogozo, J.M. et al. Subacute meningoencephalitis in a subset of patients with AD after Abeta42 immunization. Neurology 8, 46-54 (2003).
17. Gilman, S. et al. Clinical effects of Abeta immunization (AN1792) in patients with AD in an interrupted trial. Neurology 10, 1553-1562 (2005).
18. Holmes, C. et al. Long-term effects of Abeta42 immunisation in Alzheimer's disease: Follow-up of a randomised, placebo-controlled phase I trial. Lancet 19, 216-223 (2008).
19. Salomone, S., Caraci, F., Leggio, G.M., Fedotova, J. & Drago, F. New pharmacological strategies for treatment of Alzheimer's disease: Focus on disease modifying drugs. Br. J. Clin. Pharmacol. 73, 504-517 (2012).
20. Mangialasche, F., Solomon, A., Winblad, B., Mecocci, P. & Kivipelto, M. Alzheimer's disease: Clinical trials and drug development. Lancet Neurol. 9, 702-716 (2010).
21. Lyketsos, C.G. et al. Neuropsychiatric symptoms in Alzheimer's disease. Alzheimers Dement. 7, 532-539 (2011).
22. Yaffe, K. et al. Patient and caregiver characteristics and nursing home placement in patients with dementia. JAMA 287, 2090-2097 (2002).
23. Tschanz, J.T., Norton, M.C., Zandi, P.P. & Lyketsos, C.G. The Cache County Study on Memory in Aging: Factors affecting risk of Alzheimer's disease and its progression after onset. Int. Rev. Psychiatry 25, 673-685 (2013).
24. Beeri, M.S., Werner, P., Davidson, M. & Noy, S. The cost of behavioral and psychological symptoms of dementia (BPSD) in community dwelling Alzheimer's disease patients. Int. J. Geriatr. Psychiatry 17, 403-408 (2002).
25. Rodda, J., Morgan, S. & Walker, Z. Are cholinesterase inhibitors effective in the management of the behavioral and psychological symptoms of dementia in Alzheimer's disease? A systematic review of randomized, placebo-controlled trials of donepezil, rivastigmine and galantamine. Int. Psychogeriatr. 21, 813-824 (2009).
26. Fox, C. et al. Efficacy of memantine for agitation in Alzheimer's dementia: A randomised double-blind placebo controlled trial. PLoS One 7, e35185 (2012).
27. Sink, K.M., Holden, K.F. & Yaffe, K. Pharmacological treatment of neuropsychiatric symptoms of dementia: A review of the evidence. JAMA 293, 596-608 (2005).
28. Ham, A.C. et al. Medication-related fall incidents in an older, ambulant population: The B-PROOF study. Drugs Aging 31, 917-927 (2014).
29. Vasilyeva, I., Biscontri, R.G., Enns, M.W., Metge, C.J. & Alessi-Severini, S. Adverse events in elderly users of antipsychotic pharmacotherapy in the province of Manitoba: A retrospective cohort study. J. Clin. Psychopharmacol. 33, 24-30 (2013).
30. Kales, H.C. et al. Mortality risk in patients with dementia treated with antipsychotics versus other psychiatric medications. Am. J. Psychiatry 164, 1568-1576 (2007).
31. Touw, M. The religious and medicinal uses of cannabis in China, India and Tibet. J. Psychoactive Drugs 13, 23-34 (1981).
32. Ashton, C.H. Pharmacology and effects of cannabis: A brief review. Br. J. Psychiatry 178, 101-106 (2001).
33. McPartland, J.M. Phylogenomic and chemotaxonomic analysis of the endocannabinoid system. Brain Res. Brain Res. Rev. 45, 18-29 (2004).
34. Devane, W.A., Dysarz, F.A. 3rd., Johnson, M.R., Melvin, L.S. & Howlett, A.C. Determination and characterization of a cannabinoid receptor in rat brain. Mol. Pharmacol. 34, 605-613 (1988).
35. Matsuda, L.A., Lolait, S.J., Brownstein, M.J., Young, A.C. & Bonner, T.I. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346, 561-564 (1990).
36. Munro, S., Thomas, K.L. & Abu-Shaar, M. Molecular characterization of a peripheral receptor for cannabinoids. Nature 365, 61-65 (1993).
37. Pertwee, R.G. et al. International Union of Basic and Clinical Pharmacology. LXXIX. Cannabinoid receptors and their ligands: Beyond CB1 and CB2. Pharmacol. Rev. 62, 588-631 (2010).
38. Pertwee, RG. The therapeutic potential of drugs that target cannabinoid receptors or modulate the tissue levels or actions of endocannabinoids. AAPS J. 7, E625-E654 (2005).
39. Berrendero, F. et al. Changes in cannabinoid receptor binding and mRNA levels in several brain regions of aged rats. Biochim. Biophys. Acta 1407, 205-214 (1998).
40. Romero, J., Berrendero, F., Garcia-Gil, L., De La Cruz, P., Ramos, J.A. & Fernández-Ruiz, J.J. Loss of cannabinoid receptor binding and messenger RNA levels and cannabinoid agonist-stimulated [35S]guanylyl-50O-(thio)-triphosphate binding in the basal ganglia of aged rats. Neuroscience 84, 1075-1083 (1998).
41. Canas, P.M., Duarte, J.M., Rodrigues, R.J., Kofalvi, A. & Cunha, R.A. Modification upon aging of the density of presynaptic modulation systems in the hippocampus. Neurobiol. Aging 30, 1877-1884 (2009).
42. Benito, C. et al. Cannabinoid CB2 receptors and fatty acid amide hydrolase are selectively overexpressed in neuritic plaque-associated glia in Alzheimer's disease brains. J. Neurosci. 23, 11136-11141 (2003).
43. Mulder, J. et al. Molecular reorganization of endocannabinoid signalling in Alzheimer's disease. Brain 134(Pt 4), 1041-1060 (2011).
44. Ahmad, R. et al. In vivo type 1 cannabinoid receptor availability in Alzheimer's disease. Eur. Neuropsychopharmacol. 24, 242-250 (2014).
45. Lee, J.H. et al. Intact cannabinoid CB1 receptors in the Alzheimer's disease cortex. Neurochem. Int. 57, 985-989 (2010).
46. Ramírez, B.G., Blázquez, C., Gómez del Pulgar, T., Guzmán, M. & De Ceballos, M.L. Prevention of Alzheimer's disease pathology by cannabinoids: Neuroprotection mediated by blockade of microglial activation. J. Neurosci. 25, 1904-1913 (2005).
47. Solas, M., Francis, P.T., Franco, R. & Ramirez, M.J. CB2 receptor and amyloid pathology in frontal cortex of Alzheimer's disease patients. Neurobiol. Aging 34, 805-808 (2013).
48. Westlake, T.M., Howlett, A.C., Bonner, T.I., Matsuda, L.A. & Herkenham, M. Cannabinoid receptor binding and messenger RNA expression in human brain: An in vitro receptor autoradiography and in situ hybridization histochemistry study of normal aged and Alzheimer's brains. Neuroscience 63, 637-652 (1994).
49. Iuvone, T., Esposito, G., Esposito, R., Santamaria, R., Di Rosa, M. & Izzo, A.A. Neuroprotective effect of cannabidiol, a non-psychoactive component from Cannabis sativa, on beta-amyloid-induced toxicity in PC12 cells. J. Neurochem. 89, 134-141 (2004).
50. Pacher, P., Bátkai, S. & Kunos, G. The endocannabinoid system as an emerging target of pharmacotherapy. Pharmacol. Rev. 58, 389-462 (2006).
51. Ruiz-Valdepe~nas, L., Benito, C., Tolón, R.M., Martínez Orgado, J.A., & Romero, J. The endocannabinoid system and amyloid-related diseases. Exp. Neurol. 224, 66-73 (2010).
52. Milton, N.G. Anandamide and noladin ether prevent neurotoxicity of the human amyloid-beta peptide. Neurosci. Lett. 332, 127-130 (2002).
53. Van Der Stelt, M. et al. Endocannabinoids and beta-amyloid-induced neurotoxicity in vivo: Effect of pharmacological elevation of endocannabinoid levels. Cell. Mol. Life Sci. 63, 1410-1424 (2006).
54. Esposito, G., De Filippis, D., Maiuri, M.C., De Stefano, D., Carnuccio, R. & Iuvone, T. Cannabidiol inhibits inducible nitric oxide synthase protein expression and nitric oxide production in beta-amyloid stimulated PC12 neurons through p38 MAP kinase and NF-kappaB involvement. Neurosci. Lett. 399, 91-95 (2006).
55. Esposito, G., De Filippis, D., Carnuccio, R., Izzo, A.A. & Iuvone, T. The marijuana component cannabidiol inhibits beta-amyloid-induced tau protein hyperphosphorylation through Wnt/beta-catenin pathway rescue in PC12 cells. J. Mol. Med. (Berl). 84, 253-258 (2006).
56. Cai, Z., Zhao, Y. & Zhao, B. Roles of glycogen synthase kinase 3 in Alzheimer's disease. Curr. Alzheimer Res. 9, 864-879 (2012).
57. Martín-Moreno, A.M. et al. Cannabidiol and other cannabinoids reduce microglial activation in vitro and in vivo: Relevance to Alzheimer's disease. Mol. Pharmacol. 79, 964-973 (2011).
58. Scuderi, C., Steardo, L. & Esposito, G. Cannabidiol promotes amyloid precursor protein ubiquitination and reduction of beta amyloid expression in SHSY5YAPP1 cells through PPARg involvement. Phytother. Res. 28, 1007-1013 (2014).
59. Eubanks, L.M. et al. A molecular link between the active component of marijuana and Alzheimer's disease pathology. Mol. Pharm. 3, 773-777 (2006).
60. Aso, E., Sánchez-Pla, A., Vegas-Lozano, E., Maldonado, R. & Ferrer, I. Cannabis-based medicine reduces multiple pathological processes in AbPP/PS1 mice. J. Alzheimers Dis. 43, 977-991 (2015).
61. Rubino, T., Zamberletti, E. & Parolaro, D. Adolescent exposure to cannabis as a risk factor for psychiatric disorders. J. Psychopharmacol. 26, 177-188 (2012).
62. Krishnan, S., Cairns, R. & Howard, R. Cannabinoids for the treatment of dementia. Cochrane Database Syst. Rev. 15, CD007204 (2009).
63. Passmore, M.J. The cannabinoid receptor agonist nabilone for the treatment of dementia-related agitation. Int. J. Geriatr. Psychiatry 23, 116-117 (2008).
64. Volicer, L., Stelly, M., Morris, J., McLaughlin, J. & Volicer, B.J. Effects of dronabinol on anorexia and disturbed behavior in patients with Alzheimer's disease. Int. J. Geriatr. Psychiatry 12, 913-919 (1997).
65. Walther, S., Mahlberg, R., Eichmann, U. & Kunz, D. Delta-9-tetrahydrocannabinol for nighttime agitation in severe dementia. Psychopharmacology (Berl). 185, 524-528 (2006).
66. Walther, S., Schupbach, B., Seifritz, E., Homan, P. & Strik, W. Randomized, controlled crossover trial of dronabinol, 2.5 mg, for agitation in 2 patients with dementia. J. Clin. Psychopharmacol. 31, 256-258 (2011).
67. Woodward, M.R., Harper, D.G., Stolyar, A., Forester, B.P. & Ellison, J.M. Dronabinol for the treatment of agitation and aggressive behavior in acutely hospitalized severely demented patients with noncognitive behavioral symptoms. Am. J. Geriatr. Psychiatry 22, 415-419 (2014).
68. Ware, M.A., Adams, H. & Guy, G.W. The medicinal use of cannabis in the UK: Results of a nationwide survey. Int. J. Clin. Pract. 59, 291-295 (2005).
69. Hazekamp, A. & Heerdink, E.R. The prevalence and incidence of medicinal cannabis on prescription in The Netherlands. Eur. J. Clin. Pharmacol. 69, 1575-1580 (2013).
70. Hazekamp, A., Ware, M.A., Muller-Vahl, K.R., Abrams, D. & Grotenhermen, F. The medicinal use of cannabis and cannabinoids- an international cross-sectional survey on administration forms. J. Psychoactive Drugs 45, 199-210 (2013).
71. Ahmed, A.I. et al. Safety and pharmacokinetics of oral delta-9-tetrahydrocannabinol in healthy older subjects: A randomized controlled trial. Eur. Neuropsychopharmacol. 24, 1475-1482 (2014).
72. GW Pharmaceuticals announces physician reports of epidiolex treatment effect in children and young adults with treatment-resistant epilepsy from physician-led expanded access treatment program. http://www.gwpharm.com/GW%20Pharmaceuticals%20Announces%20Physician%20Reports%20of%20Epidiolex-20Treatment%20Effect%20in%20Children%20and%20Young%20-Adults%20with%20Treatment-Resistant%20Epilepsy%20from%20-Physician-Led%20Expanded%20Access%20Treatment%20Program.aspx (2014). Accessed 28 December 2014.
73. Sunderland, T. Neurotransmission in the aging central nervous system. In: Clinical Geriatric Psychopharmacology (ed. Salzman, C.) 77-78. (Lippincott Williams & Wilkins, New York, NY, 2006).
74. Carroll, C.B. et al. Cannabis for dyskinesia in Parkinson disease: A randomized double-blind crossover study. Neurology 63, 1245-1250 (2004).
75. Ahmed, A.I. et al. Safety, pharmacodynamics, and pharmacokinetics of multiple oral doses of delta-9-tetrahydrocannabinol in older persons with dementia. Psychopharmacology (Berl); e-pub ahead of print 11 March 2015.