Advertisement

AIDS and Behavior

, Volume 22, Issue 5, pp 1596–1605 | Cite as

Memory Impairment in HIV-Infected Individuals with Early and Late Initiation of Regular Marijuana Use

  • Linda M. Skalski
  • Sheri L. Towe
  • Kathleen J. Sikkema
  • Christina S. Meade
Original Paper

Abstract

Marijuana use is disproportionately prevalent among HIV-infected individuals. The strongest neurocognitive effect of marijuana use is impairment in the domain of memory. Memory impairment is also high among HIV-infected persons. The present study examined 69 HIV-infected individuals who were stratified by age of regular marijuana initiation to investigate how marijuana use impacts neurocognitive functioning. A comprehensive battery assessed substance use and neurocognitive functioning. Findings indicated early onset marijuana users (regular use prior to age 18), compared to non-marijuana users and late onset marijuana users (regular use at age 18 or later), were over 8 times more likely to have learning impairment and nearly 4 times more likely to have memory impairment. A similar pattern of early onset marijuana users performing worse in learning emerged when examining domain deficit scores. The potential for early onset of regular marijuana use to exacerbate already high levels of memory impairment among HIV-infected persons has important clinical implications, including increased potential for medication non-adherence and difficulty with independent living.

Keywords

Marijuana Cannabis HIV/AIDS Memory Neurocognitive functioning 

Notes

Acknowledgements

This study was supported by grants from the National Institute on Drug Abuse (F31-DA035131, K23-DA028660, & R03-DA035670), the National Institute of Allergy and Infectious Diseases (T32-AI007392), & the Duke Center for AIDS Research (P30-AI064518).

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. 1.
    Mimiaga MJ, Reisner SL, Grasso C, et al. Substance use among HIV-infected patients engaged in primary care in the United States: findings from the Centers for AIDS Research Network of Integrated Clinical Systems cohort. Am J Public Health. 2013;103(8):1457–67.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Substance Abuse and Mental Health Services Administration. Behavioral health trends in the United States: results from the 2014 National Survey on Drug Use and Health. Rockville: SAMHSA; 2015.Google Scholar
  3. 3.
    Bruce D, Harper GW, Fernandez MI. Heavy marijuana use among gay and bisexual male emerging adults living with HIV/AIDS. J HIV AIDS Soc Serv. 2013;12(1):26–48.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Woolridge E, Barton S, Samuel J, Osorio J, Dougherty A, Holdcroft A. Cannabis use in HIV for pain and other medical symptoms. J Pain Symptom Manag. 2005;29(4):358–67.CrossRefGoogle Scholar
  5. 5.
    National Organization for the Reform of Marijuana Laws. State laws: medicinal marijuana. 2017; http://norml.org/legal/medical-marijuana-2. Accessed 19 Jan 2017.
  6. 6.
    Valcour V, Sithinamsuwan P, Letendre S, Ances B. Pathogenesis of HIV in the central nervous system. Curr HIV/AIDS Rep. 2011;8(1):54–61.CrossRefPubMedGoogle Scholar
  7. 7.
    Antinori A, Arendt G, Becker JT, et al. Updated research nosology for HIV-associated neurocognitive disorders. Neurology. 2007;69(18):1789–99.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Heaton RK, Clifford DB, Franklin DR Jr, et al. HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER Study. Neurology. 2010;75(23):2087–96.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Heaton RK, Franklin D, Ellis R, et al. HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: differences in rates, nature, and predictors. J Neurovirol. 2011;17(1):3–16.CrossRefPubMedGoogle Scholar
  10. 10.
    Schiller A, Foley J, Burns W, Sellers AL, Golden C. Subcortical profile of memory compromise among HIV-1-infected individuals. Int J Neurosci. 2009;119(10):1779–803.CrossRefPubMedGoogle Scholar
  11. 11.
    Scott J, Woods S, Carey C, Weber E, Bondi M, Grant I. Neurocognitive consequences of HIV infection in older adults: an evaluation of the “cortical” hypothesis. AIDS Behav. 2011;15(6):1187–96.CrossRefPubMedGoogle Scholar
  12. 12.
    Maki PM, Cohen MH, Weber K, et al. Impairments in memory and hippocampal function in HIV-positive vs HIV-negative women: a preliminary study. Neurology. 2009;72(19):1661–8.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Moore D, Letendre S, Morris S, et al. Neurocognitive functioning in acute or early HIV infection. J Neurovirol. 2011;17(1):50–7.CrossRefPubMedGoogle Scholar
  14. 14.
    Wright MJ, Woo E, Foley J, et al. Antiretroviral adherence and the nature of HIV-associated verbal memory impairment. Am Neuropsych Assoc. 2011;23(3):324–31.Google Scholar
  15. 15.
    Reger M, Welsh R, Razani J, Martin DJ, Boone KB. A meta-analysis of the neuropsychological sequelae of HIV infection. J Int Neuropsychol Soc. 2002;8(3):410–24.CrossRefPubMedGoogle Scholar
  16. 16.
    Maki PM, Rubin LH, Valcour V, et al. Cognitive function in women with HIV: findings from the Women’s Interagency HIV Study. Neurology. 2015;84(3):231–40.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Martin EM, Nixon H, Pitrak DL, et al. Characteristics of prospective memory deficits in HIV-seropositive substance-dependent individuals: preliminary observations. J Clin Exp Neuropsychol. 2007;29(5):496–504.CrossRefPubMedGoogle Scholar
  18. 18.
    Waldrop D, Ownby RL, Kumar M. Serial position effects in HIV-infected injecting drug users. Int J Neurosci. 2004;114(4):493–516.CrossRefPubMedGoogle Scholar
  19. 19.
    Woods SP, Dawson MS, Weber E, Grant I. The semantic relatedness of cue–intention pairings influences event-based prospective memory failures in older adults with HIV infection. J Clin Exp Neuropsychol. 2010;32(4):398–407.CrossRefPubMedGoogle Scholar
  20. 20.
    Ellis RJ, Badiee J, Vaida F, et al. Nadir CD4 is a predictor of HIV neurocognitive impairment in the era of combination antiretroviral therapy. AIDS. 2011;25(14):1747–51.CrossRefPubMedGoogle Scholar
  21. 21.
    Valcour V, Yee P, Williams AE, et al. Lowest ever CD4 lymphocyte count (CD4 nadir) as a predictor of current cognitive and neurological status in human immunodeficiency virus type 1 infection–The Hawaii Aging with HIV Cohort. J Neurovirol. 2006;12(5):387–91.CrossRefPubMedGoogle Scholar
  22. 22.
    D’Amico R, Yang Y, Mildvan D, et al. Lower CD4+ T lymphocyte nadirs may indicate limited immune reconstitution in HIV-1 infected individuals on potent antiretroviral therapy: analysis of immunophenotypic marker results of AACTG 5067. J Clin Immunol. 2005;25(2):106–15.CrossRefPubMedGoogle Scholar
  23. 23.
    Gonzalez R. Acute and non-acute effects of cannabis on brain functioning and neuropsychological performance. Neuropsychol Rev. 2007;17(3):347–61.CrossRefPubMedGoogle Scholar
  24. 24.
    Grant I, Gonzalez R, Carey C, Natara L, Woflson T. Non-acute (residual) neurocognitive effects of cannabis use: a meta-analytic study. J Int Neuropsychol Soc. 2003;9(5):679–89.CrossRefPubMedGoogle Scholar
  25. 25.
    Crane NA, Schuster RM, Fusar-Poli P, Gonzalez R. Effects of cannabis on neurocognitive functioning: recent advances, neurodevelopmental influences, and sex differences. Neuropsychol Rev. 2013;23(2):117–37.CrossRefPubMedGoogle Scholar
  26. 26.
    Schreiner AM, Dunn ME. Residual effects of cannabis use on neurocognitive performance after prolonged abstinence: a meta-analysis. Exp Clin Psychopharmacol. 2012;20(5):420–9.CrossRefPubMedGoogle Scholar
  27. 27.
    Solowij N, Battisti R. The chronic effects of cannabis on memory in humans: a review. Curr Drug Abuse Rev. 2008;1(1):81–98.CrossRefPubMedGoogle Scholar
  28. 28.
    Ranganathan M, D’Souza D. The acute effects of cannabinoids on memory in humans: a review. Psychopharmacology. 2006;188(4):425–44.CrossRefPubMedGoogle Scholar
  29. 29.
    Volkow ND, Swanson JM, Evins A, et al. Effects of cannabis use on human behavior, including cognition, motivation, and psychosis: a review. JAMA Psychiatry. 2016;73(3):292–7.CrossRefPubMedGoogle Scholar
  30. 30.
    Solowij N, Pesa N. Cannabis and cognition: short- and long-term effects. In: Castle D, Murray R, D’Souza D, editors. Marijuana and madness. 2nd ed. Cambridge: Cambridge University Press; 2012.Google Scholar
  31. 31.
    Meier MH, Caspi A, Ambler A, et al. Persistent cannabis users show neuropsychological decline from childhood to midlife. PNAS. 2012;109(40):E2657–64.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Pope HG Jr, Gruber AJ, Hudson JI, Cohane G, Huestis MA, Yurgelun-Todd D. Early-onset cannabis use and cognitive deficits: what is the nature of the association? Drug Alcohol Depend. 2003;69(3):303–10.CrossRefPubMedGoogle Scholar
  33. 33.
    Gruber SA, Sagar KA, Dahlgren MK, Racine M, Lukas SE. Age of onset of marijuana use and executive function. Psychol Addict Behav. 2012;26(3):496–506.CrossRefPubMedGoogle Scholar
  34. 34.
    Tait R, Mackinnon A, Christensen H. Cannabis use and cognitive function: 8-year trajectory in a young adult cohort. Addiction. 2011;106(12):2195–203.CrossRefPubMedGoogle Scholar
  35. 35.
    Becker B, Wagner D, Gouzoulis-Mayfrank E, Spuentrup E, Daumann J. Altered parahippocampal functioning in cannabis users is related to the frequency of use. Psychopharmacology. 2010;209(4):361–74.CrossRefPubMedGoogle Scholar
  36. 36.
    Solowij N, Stephens RS, Roffman RA, et al. Cognitive functioning of long-term heavy cannabis users seeking treatment. JAMA. 2002;287(9):1123–31.CrossRefPubMedGoogle Scholar
  37. 37.
    Messinis L, Kyprianidou A, Malefaki S, Papathanasopoulos P. Neuropsychological deficits in long-term frequent cannabis users. Neurology. 2006;66(5):737–9.CrossRefPubMedGoogle Scholar
  38. 38.
    Wadsworth EJ, Moss SC, Simpson SA, Smith AP. Cannabis use, cognitive performance and mood in a sample of workers. J Psychopharmacol. 2006;20(1):14–23.CrossRefPubMedGoogle Scholar
  39. 39.
    Jager G, Van Hell HH, De Win MM, et al. Effects of frequent cannabis use on hippocampal activity during an associative memory task. Eur Neuropsychopharmacol. 2007;17(4):289–97.CrossRefPubMedGoogle Scholar
  40. 40.
    Indlekofer F, Piechatzek M, Daamen M, et al. Reduced memory and attention performance in a population-based sample of young adults with a moderate lifetime use of cannabis, ecstasy and alcohol. J Psychopharmacol. 2009;23(5):495–509.CrossRefPubMedGoogle Scholar
  41. 41.
    Bolla KI, Brown K, Eldreth D, Tate K, Cadet JL. Dose-related neurocognitive effects of marijuana use. Neurology. 2002;59(9):1337–43.CrossRefPubMedGoogle Scholar
  42. 42.
    Hadjiefthyvoulou F, Fisk JE, Montgomery C, Bridges N. Prospective memory functioning among ecstasy/polydrug users: evidence from the Cambridge Prospective Memory Test (CAMPROMPT). Psychopharmacology. 2011;215(4):761–74.CrossRefPubMedGoogle Scholar
  43. 43.
    Cristiani SA, Pukay-Martin ND, Bornstein RA. Marijuana use and cognitive function in HIV-infected people. J Neuropsychiatry Clin Neurosci. 2004;16(3):330–5.CrossRefPubMedGoogle Scholar
  44. 44.
    Thames AD, Kuhn TP, Williamson TJ, Jones JD, Mahmood Z, Hammond A. Marijuana effects on changes in brain structure and cognitive function among HIV+ and HIV-adults. Drug Alcohol Depend. 2017;2017(170):120–7.CrossRefGoogle Scholar
  45. 45.
    McLellan AT, Kushner H, Metzger D, et al. The fifth edition of the Addiction Severity Index. J Subst Abuse Treat. 1992;9(3):199–213.CrossRefPubMedGoogle Scholar
  46. 46.
    Gruber SA, Dahlgren MK, Sagar KA, Gönenç A, Lukas SE. Worth the wait: effects of age of onset of marijuana use on white matter and impulsivity. Psychopharmacology. 2014;231(8):1455–65.CrossRefPubMedGoogle Scholar
  47. 47.
    APA. Diagnostic and statistical manual of mental disorders, Fourth Edition, text revision. Washington: American Psychiatric Association; 2000.Google Scholar
  48. 48.
    Wechsler D. Wechsler test of adult reading (WTAR) manual. San Antonio: Harcourt Assessment; 2001.Google Scholar
  49. 49.
    Sobell LC, Sobell MB. Timeline Follow-back user’s guide: a calendar method for assessing alcohol and drug use. Toronto: Addiction Research Foundation; 1996.Google Scholar
  50. 50.
    NIAAA. The physician’s guide to helping patients with alcohol problems. Washington, DC: National Institutes of Health; 1995.Google Scholar
  51. 51.
    McGahan PL, Griffith JA, Parente R, McLellan AT. Addiction severity index composite scores manual. Philadelphia: The University of Pennsylvania/Veterans Administration Center for Studies of Addiction; 1986.Google Scholar
  52. 52.
    First MB, Spitzer RL, Gibbon M, Williams JBW. Structured clinical interview for DSM-IV axis I disorders, research version, patient/non-patient edition. New York: Biometrics Research, New York State Psychiatric Institute; 1996.Google Scholar
  53. 53.
    Sheehan DV, Lecrubier Y, Sheehan KH, et al. The Mini International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry. 1998;59(Suppl 30):22–33.PubMedGoogle Scholar
  54. 54.
    Derogatis LR. Brief Symptom Inventory: administration, scoring, and procedures manual. 3rd ed. Minneapolis: National Computer Systems, Inc.; 1993.Google Scholar
  55. 55.
    Brandt J, Benedict RHB. Hopkins verbal learning test—revised professional manual. Lutz: Psychological Assessment Resources, Inc; 2001.Google Scholar
  56. 56.
    Benedict RHB. Brief visuospatial memory test-revised professional manual. Odessa: Psychological Assessment Resources, Inc.; 1997.Google Scholar
  57. 57.
    Lezac MD. Neuropsychological assessment. 3rd ed. New York: Oxford University Press; 1995.Google Scholar
  58. 58.
    Golden CJ. Stroop color and word test. Chicago: Stoelting; 1978.Google Scholar
  59. 59.
    Wechsler D. Wechsler Adult Intelligence Scale-Third Edition: Administration and Scoring Manual. San Antonio: Harcourt Brace; 1997.Google Scholar
  60. 60.
    Heaton RK, Grant I, Matthews CG. Comprehensive norms for an expanded Halstead-Reitan battery: demographic corrections, research findings, and clinical applications. Odessa: Psychological Assessment Resources; 1991.Google Scholar
  61. 61.
    Benton A, Hamsher K, Sivan A. Multilingual aphasia examination. 3rd ed. Iowa City: AJA Associates; 1983.Google Scholar
  62. 62.
    Gronwall DM. Paced auditory serial-addition task: a measure of recovery from concussion. Percept Mot Skills. 1977;44(2):367–73.CrossRefPubMedGoogle Scholar
  63. 63.
    Stern RA, White T. Neuropsychological assessment battery: administration, scoring, and interpretation manual. Lutz: Psychological Assessment Resources, Inc; 2003.Google Scholar
  64. 64.
    Diehr MC, Cherner M, Wolfson TJ, Miller SW, Grant I, Heaton RK. The 50 and 100-item short forms of the Paced Auditory Serial Addition Task (PASAT): demographically corrected norms and comparisons with the full PASAT in normal and clinical samples. J Clin Exp Neuropsychol. 2003;25(4):571–85.CrossRefPubMedGoogle Scholar
  65. 65.
    Heaton RK, Miller SW, Taylor MJ, Grant I. Revised comprehensive norms for an expanded Halstead-Reitan battery: demographically adjusted neuropsychological norms for African American and Caucasian adults. Lutz: Psychological Assessment Resources, Inc; 2004.Google Scholar
  66. 66.
    Norman MA, Moore DJ, Taylor M, et al. Demographically corrected norms for African Americans and Caucasians on the hopkins verbal learning test-revised, brief visuospatial memory test-revised, stroop color and word test, and wisconsin card sorting test 64-card version. J Clin Exp Neuropsychol. 2011;33(7):793–804.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Stern RA, White T. NAB digits forward/digits backward test: professional manual. Lutz: Psychological Assessment Resources, Inc. (PAR); 2009.Google Scholar
  68. 68.
    Heaton RK, Grant I, Butters N, et al. The HNRC 500–neuropsychology of HIV infection at different disease stages. HIV Neurobehavioral Research Center. J Int Neuropsychol Soc. 1995;1(3):231–51.CrossRefPubMedGoogle Scholar
  69. 69.
    Carey CL, Woods SP, Gonzalez R, et al. Predictive validity of global deficit scores in detecting neuropsychological impairment in HIV infection. J Clin Exp Neuropsychol. 2004;26(3):307–19.CrossRefPubMedGoogle Scholar
  70. 70.
    Jacobus J, Tapert SF. Effects of cannabis on the adolescent brain. Curr Pharmaceut Des. 2014;20(13):2186–93.CrossRefGoogle Scholar
  71. 71.
    Tseng A, Seet J, Phillips EJ. The evolution of three decades of antiretroviral therapy: challenges, triumphs and the promise of the future. Br J Clin Pharmacol. 2015;79(2):182–94.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Deeks SG, Lewin SR, Havlir DV. The end of AIDS: HIV infection as a chronic disease. Lancet. 2013;382(9903):1525–33.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Hoffmann DE, Weber E. Medical marijuana and the law. New Engl J Med. 2010;362(16):1453–7.CrossRefPubMedGoogle Scholar
  74. 74.
    Zogg JB, Woods SP, Weber E, et al. HIV-associated prospective memory impairment in the laboratory predicts failures on a semi-naturalistic measure of health care compliance. Clin Neuropsychol. 2010;24(6):945–62.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Hinkin CH, Castellon SA, Durvasula RS, et al. Medication adherence among HIV+ adults: effects of cognitive dysfunction and regimen complexity. Neurology. 2002;59(12):1944–50.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Hinkin CH, Hardy DJ, Mason KI, et al. Medication adherence in HIV-infected adults: effect of patient age, cognitive status, and substance abuse. AIDS. 2004;18(Supp 1):19–25.CrossRefGoogle Scholar
  77. 77.
    Contardo C, Black AC, Beauvais J, Dieckhaus K, Rosen MI. Relationship of prospective memory to neuropsychological function and antiretroviral adherence. Arch Clin Neuropsychol. 2009;24(6):547–54.CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Ettenhofer ML, Foley J, Castellon SA, Hinkin CH. Reciprocal prediction of medication adherence and neurocognition in HIV/AIDS. Neurology. 2010;74(15):1217–22.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Andrade A, McGruder H, Wu A, et al. A programmable prompting device improves adherence to highly active antiretroviral therapy in HIV-Infected subjects with memory impairment. Clin Infect Dis. 2005;41(6):875–82.CrossRefPubMedGoogle Scholar
  80. 80.
    Harrigan PR, Hogg RS, Dong WWY, et al. Predictors of HIV drug-resistance mutations in a large antiretroviral-naive cohort initiating triple antiretroviral therapy. J Infect Dis. 2005;191(3):339–47.CrossRefPubMedGoogle Scholar
  81. 81.
    Cohen MS, Chen YQ, McCauley M, et al. Prevention of HIV-1 infection with early antiretroviral therapy. NEJM. 2011;365(6):493–505.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    van Gorp WG, Rabkin JG, Ferrando SJ, et al. Neuropsychiatric predictors of return to work in HIV/AIDS. J Int Neuropsychol Soc. 2007;13(1):80–9.PubMedGoogle Scholar
  83. 83.
    de Wit H. Impulsivity as a determinant and consequence of drug use: a review of underlying processes. Addict Biol. 2009;14(1):22–31.CrossRefPubMedGoogle Scholar
  84. 84.
    Verdejo-Garcia A, Lawrence AJ, Clark L. Impulsivity as a vulnerability marker for substance-use disorders: review of findings from high-risk research, problem gamblers and genetic association studies. Neurosci Biobehav Rev. 2008;32(4):777–810.CrossRefPubMedGoogle Scholar
  85. 85.
    Squeglia LM, Cservenka A. Adolescence and drug use vulnerability: findings from neuroimaging. Curr Opin Behav Sci. 2017;13:164–70.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Department of Psychology & NeuroscienceDuke UniversityDurhamUSA
  2. 2.Department of Psychiatry& Behavioral SciencesDuke University School of MedicineDurhamUSA
  3. 3.Global Health InstituteDuke UniversityDurhamUSA

Personalised recommendations