Hostname: page-component-745bb68f8f-mzp66 Total loading time: 0 Render date: 2025-01-13T00:22:42.108Z Has data issue: false hasContentIssue false
  • English
  • Français

Daily Cannabis Use is Associated With Lower CNS Inflammation in People With HIV

Published online by Cambridge University Press:  15 July 2021

C. Wei-Ming Watson Open the ORCID record for C. Wei-Ming Watson [Opens in a new window] ,
Laura M. Campbell Open the ORCID record for Laura M. Campbell [Opens in a new window] ,
Ni Sun-Suslow ,
Suzi Hong ,
Anya Umlauf ,
Ronald J. Ellis ,
Jennifer E. Iudicello ,
Scott Letendre ,
Thomas D. Marcotte  and
Robert K. Heaton
...Show all authors
C. Wei-Ming Watson*
Affiliation:
Department of Psychiatry, University of California, San Diego, USA San Diego State University/University of California, San Diego Joint Doctoral Program in Clinical Psychology, San Diego, USA
Laura M. Campbell
Affiliation:
Department of Psychiatry, University of California, San Diego, USA San Diego State University/University of California, San Diego Joint Doctoral Program in Clinical Psychology, San Diego, USA
Ni Sun-Suslow
Affiliation:
Department of Psychiatry, University of California, San Diego, USA
Suzi Hong
Affiliation:
Department of Psychiatry, University of California, San Diego, USA Department of Family Medicine and Public Health, University of California, San Diego, USA
Anya Umlauf
Affiliation:
Department of Psychiatry, University of California, San Diego, USA
Ronald J. Ellis
Affiliation:
Department of Psychiatry, University of California, San Diego, USA Department of Neurosciences, University of California, San Diego, USA
Jennifer E. Iudicello
Affiliation:
Department of Psychiatry, University of California, San Diego, USA
Scott Letendre
Affiliation:
Department of Medicine, University of California, San Diego, USA
Thomas D. Marcotte
Affiliation:
Department of Psychiatry, University of California, San Diego, USA
Robert K. Heaton
Affiliation:
Department of Psychiatry, University of California, San Diego, USA
Erin E. Morgan
Affiliation:
Department of Psychiatry, University of California, San Diego, USA
Igor Grant
Affiliation:
Department of Psychiatry, University of California, San Diego, USA
*
*Correspondence and reprint requests to: Caitlin Wei-Ming Watson, M.S., HIV Neurobehavioral Research Program, 220 Dickinson Street, Suite B (8231), San Diego, CA92103, USA. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective:

Recent cannabis exposure has been associated with lower rates of neurocognitive impairment in people with HIV (PWH). Cannabis’s anti-inflammatory properties may underlie this relationship by reducing chronic neuroinflammation in PWH. This study examined relations between cannabis use and inflammatory biomarkers in cerebrospinal fluid (CSF) and plasma, and cognitive correlates of these biomarkers within a community-based sample of PWH.

Methods:

263 individuals were categorized into four groups: HIV− non-cannabis users (n = 65), HIV+ non-cannabis users (n = 105), HIV+ moderate cannabis users (n = 62), and HIV+ daily cannabis users (n = 31). Differences in pro-inflammatory biomarkers (IL-6, MCP-1/CCL2, IP-10/CXCL10, sCD14, sTNFR-II, TNF-α) by study group were determined by Kruskal–Wallis tests. Multivariable linear regressions examined relationships between biomarkers and seven cognitive domains, adjusting for age, sex/gender, race, education, and current CD4 count.

Results:

HIV+ daily cannabis users showed lower MCP-1 and IP-10 levels in CSF compared to HIV+ non-cannabis users (p = .015; p = .039) and were similar to HIV− non-cannabis users. Plasma biomarkers showed no differences by cannabis use. Among PWH, lower CSF MCP-1 and lower CSF IP-10 were associated with better learning performance (all ps < .05).

Conclusions:

Current daily cannabis use was associated with lower levels of pro-inflammatory chemokines implicated in HIV pathogenesis and these chemokines were linked to the cognitive domain of learning which is commonly impaired in PWH. Cannabinoid-related reductions of MCP-1 and IP-10, if confirmed, suggest a role for medicinal cannabis in the mitigation of persistent inflammation and cognitive impacts of HIV.

Keywords

Neuroinflammationcognitionneurocognitive impairmentmarijuanacannabinoidsNeuroAIDSHIV/AIDScerebrospinal fluid
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 27 , Special Issue 6: Clarifying the Complexities of Cannabis and Cognition , July 2021 , pp. 661 - 672
Copyright
Copyright © INS. Published by Cambridge University Press, 2021

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Asensio, V.C., Maier, J., Milner, R., Boztug, K., Kincaid, C., Moulard, M., … Fox, H.S. (2001). Interferon-independent, human immunodeficiency virus type 1 gp120-mediated induction of CXCL10/IP-10 gene expression by astrocytes invivo and invitro. Journal of Virology, 75(15), 7067–7077.CrossRefGoogle Scholar
Beck, A.T., Steer, R.A., & Brown, G.K. (1996). Beck Depression Inventory-II. San Antonio: The Psychological Corporation.Google Scholar
Bilkei-Gorzo, A., Albayram, O., Draffehn, A., Michel, K., Piyanova, A., Oppenheimer, H., … Imbeault, S. (2017). A chronic low dose of Δ 9-tetrahydrocannabinol (THC) restores cognitive function in old mice. Nature Medicine, 23(6), 782.CrossRefGoogle ScholarPubMed
Bisogno, T. & Di Marzo, V. (2010). Cannabinoid receptors and endocannabinoids: role in neuroinflammatory and neurodegenerative disorders. CNS & Neurological Disorders-Drug Targets (Formerly Current Drug Targets-CNS & Neurological Disorders), 9(5), 564–573.Google ScholarPubMed
Bolla, K.I., Brown, K., Eldreth, D., Tate, K., & Cadet, J. (2002). Dose-related neurocognitive effects of marijuana use. Neurology, 59(9), 1337–1343.CrossRefGoogle ScholarPubMed
Burdo, T.H., Weiffenbach, A., Woods, S.P., Letendre, S., Ellis, R.J., & Williams, K.C. (2013). Elevated sCD163 in plasma but not cerebrospinal fluid is a marker of neurocognitive impairment in HIV infection. AIDS (London, England), 27(9), 1387–1395.CrossRefGoogle Scholar
Burlacu, R., Umlauf, A., Marcotte, T., Soontornniyomkij, B., Diaconu, C., Bulacu-Talnariu, A., … Ene, L. (2020). Plasma CXCL10 correlates with HAND in HIV-infected women. Journal of Neurovirology, 26(1), 23–31.CrossRefGoogle ScholarPubMed
Carey, C. L., Woods, S. P., Gonzalez, R., Conover, E., Marcotte, T. D., Grant, I., & Heaton, R. K. (2004). Predictive validity of global deficit scores in detecting neuropsychological impairment in HIV infection. Journal of Clinical Experimental Neuropsychology, 26(3), 307–319.CrossRefGoogle ScholarPubMed
Casaletto, K.B., Weber, E., Iudicello, J.E., & Woods, S.P. (2017). Real-world impact of HIV-associated neurocognitive impairment. In Nancy D. Chiaravalloti & Yael Goverover (Eds.), Changes in the Brain (pp. 211–245). New York, NY: Springer.CrossRefGoogle Scholar
Castro, F.d.O., Silva, J.M., Dorneles, G.P., Barros, J., Ribeiro, C.B., Noronha, I., … Pereira, A.J.C.S. (2019). Distinct inflammatory profiles in HIV-infected individuals under art using cannabis, cocaine or cannabis plus cocaine. AIDS (London, England), 33, 1831–1842.CrossRefGoogle ScholarPubMed
Chang, L., Cloak, C., Yakupov, R., & Ernst, T. (2006). Combined and independent effects of chronic marijuana use and HIV on brain metabolites. Journal of Neuroimmune Pharmacology, 1(1), 65–76.CrossRefGoogle ScholarPubMed
Chen, D.-J., Gao, M., Gao, F.-F., Su, Q.-X., & Wu, J. (2017). Brain cannabinoid receptor 2: expression, function and modulation. Acta Pharmacologica Sinica, 38(3), 312–316.CrossRefGoogle ScholarPubMed
Cohen, R.A., de la Monte, S., Gongvatana, A., Ombao, H., Gonzalez, B., Devlin, K.N., … Tashima, K.T. (2011). Plasma cytokine concentrations associated with HIV/hepatitis C coinfection are related to attention, executive and psychomotor functioning. Journal of Neuroimmunology, 233(1–2), 204–210.CrossRefGoogle Scholar
Costiniuk, C.T. & Jenabian, M.-A. (2019). Cannabinoids and inflammation: Implications for people living with HIV AIDS, 33(15), 2273–2288.Google ScholarPubMed
Cristiani, S.A., Pukay-Martin, N.D., & Bornstein, R.A. (2004). Marijuana use and cognitive function in HIV-infected people. The Journal of Neuropsychiatry and Clinical Neurosciences, 16(3), 330–335.CrossRefGoogle ScholarPubMed
de Almeida, S.M., Letendre, S., Zimmerman, J., Lazzaretto, D., McCutchan, A., & Ellis, R. (2005). Dynamics of monocyte chemoattractant protein type one (MCP-1) and HIV viral load in human cerebrospinal fluid and plasma. Journal of Neuroimmunology, 169(1–2), 144–152.CrossRefGoogle Scholar
Ellis, R.J., Peterson, S., Cherner, M., Morgan, E., Schrier, R., Tang, B., … Iudicello, J. (2020). Beneficial effects of cannabis on blood–brain barrier function in human immunodeficiency virus. Clinical Infectious Diseases. Epub ahead of print. doi: 10.1093/cid/ciaa437 Google Scholar
Ellis, R.J., Peterson, S.N., Li, Y., Schrier, R., Iudicello, J., Letendre, S., … Cherner, M. (2020). Recent cannabis use in HIV is associated with reduced inflammatory markers in CSF and blood. Neurology Neuroimmunology and Neuroinflammation, 7(5), e809. doi: 10.1212/NXI.0000000000000809 CrossRefGoogle ScholarPubMed
Ellis, R.J., Toperoff, W., Vaida, F., Van Den Brande, G., Gonzales, J., Gouaux, B., … Atkinson, J.H. (2009). Smoked medicinal cannabis for neuropathic pain in HIV: A randomized, crossover clinical trial. Neuropsychopharmacology, 34(3), 672–680.CrossRefGoogle ScholarPubMed
Fogarty, A., Rawstorne, P., Prestage, G., Crawford, J., Grierson, J., & Kippax, S. (2007). Marijuana as therapy for people living with HIV/AIDS: Social and health aspects. AIDS Care, 19(2), 295–301.CrossRefGoogle ScholarPubMed
Gannon, P., Khan, M.Z., & Kolson, D.L. (2011). Current understanding of HIV-associated neurocognitive disorders pathogenesis. Current Opinion in Neurology, 24(3), 275.CrossRefGoogle ScholarPubMed
Gonzalez, R., Pacheco-Colon, I., Duperrouzel, J.C., & Hawes, S.W. (2017). Does cannabis use cause declines in neuropsychological functioning? A review of longitudinal studies. Journal of International Neuropsychology Society, 23(9–10), 893–902. doi: 10.1017/S1355617717000789 CrossRefGoogle ScholarPubMed
Gruber, S.A., Sagar, K.A., Dahlgren, M.K., Gonenc, A., Smith, R.T., Lambros, A.M., … Lukas, S.E. (2018). The grass might be greener: medical marijuana patients exhibit altered brain activity and improved executive function after 3 months of treatment. Frontiers in Pharmacology, 8, 983.CrossRefGoogle ScholarPubMed
Heaton, R.K., Clifford, D.B., Franklin, D.R., Woods, S.P., Ake, C., Vaida, F., … Atkinson, J.H. (2010). HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy CHARTER study. Neurology, 75(23), 2087–2096. doi: 10.1212/WNL.0b013e318200d727 CrossRefGoogle ScholarPubMed
Heaton, R.K., Franklin, D.R., Ellis, R.J., McCutchan, J.A., Letendre, S.L., Leblanc, S., … Group, H. (2011). HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: Differences in rates, nature, and predictors. Journal of Neurovirology, 17(1), 3–16. doi: 10.1007/s13365-010-0006-1 CrossRefGoogle ScholarPubMed
Heaton, R.K., Miller, S.W., Taylor, M.J., & Grant, I. (2004). Revised Comprehensive Norms for an Expanded Halstead-Reitan Battery: Demographically Adjusted Neuropsychological Norms for African American and Caucasian Adults. Lutz, FL: Psychological Assessment Resources.Google Scholar
Hinojosa, A.E., Garcia-Bueno, B., Leza, J.C., & Madrigal, J.L. (2011). CCL2/MCP-1 modulation of microglial activation and proliferation. Journal of Neuroinflammation, 8(1), 77.CrossRefGoogle ScholarPubMed
Hirvonen, J., Goodwin, R., Li, C.-T., Terry, G., Zoghbi, S., Morse, C., … Innis, R. (2012). Reversible and regionally selective downregulation of brain cannabinoid CB1 receptors in chronic daily cannabis smokers. Molecular Psychiatry, 17(6), 642–649.CrossRefGoogle ScholarPubMed
Hložek, T., Uttl, L., Kadeřábek, L., Balíková, M., Lhotková, E., Horsley, R.R., … Tylš, F. (2017). Pharmacokinetic and behavioural profile of THC, CBD, and THC+ CBD combination after pulmonary, oral, and subcutaneous administration in rats and confirmation of conversion invivo of CBD to THC. European Neuropsychopharmacology, 27(12), 1223–1237.CrossRefGoogle Scholar
Hong, S. & Banks, W.A. (2015). Role of the immune system in HIV-associated neuroinflammation and neurocognitive implications. Brain Behavior and Immunity, 45, 1–12. doi: 10.1016/j.bbi.2014.10.008 CrossRefGoogle ScholarPubMed
Huestis, M.A. & Smith, M.L. (2007). Human cannabinoid pharmacokinetics and interpretation of cannabinoid concentrations in biological fluids and tissues. In Mahmoud A. ElSohly (Ed.), Marijuana and the Cannabinoids (pp. 205–235). New York, NY: Springer.CrossRefGoogle Scholar
Imp, B.M., Rubin, L.H., Tien, P.C., Plankey, M.W., Golub, E.T., French, A.L., & Valcour, V.G. (2017). Monocyte activation is associated with worse cognitive performance in HIV-infected women with virologic suppression. The Journal of Infectious Diseases, 215(1), 114.CrossRefGoogle ScholarPubMed
Iudicello, J.E., Hussain, M., Watson, C., Morgan, E., Heaton, R.K., Stern, R., & Alosco, M. (2019). HIV-associated neurocognitive disorders. In Michael L. Alosco & Robert A. Stern (Eds.), Oxford Handbook of Adult Cognitive Disorders (pp. 29–60). Oxford, England: Oxford University Press.Google Scholar
Kamat, A., Lyons, J. L., Misra, V., Uno, H., Morgello, S., Singer, E.J., & Gabuzda, D. (2012). Monocyte activation markers in cerebrospinal fluid associated with impaired neurocognitive testing in advanced HIV infection. Journal of Acquired Immune Deficiency Syndrome, 60(3), 234–243. doi: 10.1097/QAI.0b013e318256f3bc CrossRefGoogle ScholarPubMed
Keen, L. & Turner, A.D. (2015). Differential effects of self-reported lifetime marijuana use on interleukin-1α and tumor necrosis factor in African American adults. Journal of Behavioral Medicine, 38(3), 527–534.CrossRefGoogle ScholarPubMed
Kim, H.J., Shin, A.H., & Thayer, S.A. (2011). Activation of cannabinoid type 2 receptors inhibits HIV-1 envelope glycoprotein gp120-induced synapse loss. Molecular Pharmacology, 80(3), 357–366.CrossRefGoogle ScholarPubMed
Krsak, M., Wada, N.I., Plankey, M.W., Kinney, G.L., Epeldegui, M., Okafor, C.N., … Erlandson, K.M. (2020). Self-reported cannabis use and markers of inflammation in men who have sex with men with and without HIV. Cannabis and Cannabinoid Research. Epub ahead of print. doi: 10.1089/can.2019.0083 Google Scholar
Lee, W.-J., Liao, Y.-C., Wang, Y.-F., Lin, I.-F., Wang, S.-J., & Fuh, J.-L. (2018). Plasma MCP-1 and cognitive decline in patients with Alzheimer’s disease and mild cognitive impairment: a 2-year follow-up study. Scientific Reports, 8(1), 1–8.Google Scholar
Letendre, S. (2011). Central nervous system complications in HIV disease: HIV-associated neurocognitive disorder. Topics in Antiviral Medicine, 19(4), 137.Google ScholarPubMed
Manuzak, J.A., Gott, T.M., Kirkwood, J.S., Coronado, E., Hensley-McBain, T., Miller, C., … Martin, J.N. (2018). Heavy cannabis use associated with reduction in activated and inflammatory immune cell frequencies in antiretroviral therapy–treated Human Immunodeficiency Virus–infected individuals. Clinical Infectious Diseases, 66(12), 1872–1882.CrossRefGoogle ScholarPubMed
Mehla, R., Bivalkar-Mehla, S., Nagarkatti, M., & Chauhan, A. (2012). Programming of neurotoxic cofactor CXCL-10 in HIV-1-associated dementia: abrogation of CXCL-10-induced neuro-glial toxicity invitro by PKC activator. Journal of Neuroinflammation, 9(1), 239.CrossRefGoogle Scholar
Montoya, J.L., Jankowski, C.M., O’Brien, K.K., Webel, A.R., Oursler, K.K., Henry, B.L., … Erlandson, K.M. (2019). Evidence-informed practical recommendations for increasing physical activity among persons living with HIV. AIDS (London, England), 33(6), 931.CrossRefGoogle ScholarPubMed
Nagarkatti, P., Pandey, R., Rieder, S.A., Hegde, V.L., & Nagarkatti, M. (2009). Cannabinoids as novel anti-inflammatory drugs. Future Medicinal Chemistry, 1(7), 1333–1349.CrossRefGoogle ScholarPubMed
National Academies of Sciences & Medicine. (2017). The Health Effects of Cannabis and Cannabinoids: The Current State of Evidence and Recommendations for Research. Washington, DC: National Academies Press.Google Scholar
Neuhaus, J., Jacobs, D.R. Jr, Baker, J.V., Calmy, A., Duprez, D., La Rosa, A., … Neaton, J.D. (2010). Markers of inflammation, coagulation, and renal function are elevated in adults with HIV infection. Journal of Infectious Diseases, 201(12), 1788–1795. doi: 10.1086/652749 CrossRefGoogle Scholar
Norman, M.A., Moore, D.J., Taylor, M., Franklin, D. Jr, Cysique, L., Ake, C., … Group, H. (2011). 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. Journal of Clinical Experimental Neuropsychology, 33(7), 793–804.CrossRefGoogle ScholarPubMed
Pacek, L.R., Towe, S.L., Hobkirk, A.L., Nash, D., & Goodwin, R.D. (2018). Frequency of cannabis use and medical cannabis use among persons living with HIV in the United States: findings from a nationally representative sample. AIDS Education and Prevention, 30(2), 169–181.CrossRefGoogle ScholarPubMed
Persidsky, Y., Fan, S., Dykstra, H., Reichenbach, N.L., Rom, S., & Ramirez, S.H. (2015). Activation of cannabinoid type two receptors (CB2) diminish inflammatory responses in macrophages and brain endothelium. Journal of Neuroimmune Pharmacology, 10(2), 302–308. doi: 10.1007/s11481-015-9591-3 CrossRefGoogle ScholarPubMed
Pulliam, L., Rempel, H., Sun, B., Abadjian, L., Calosing, C., & Meyerhoff, D.J. (2011). A peripheral monocyte interferon phenotype in HIV infection correlates with a decrease in magnetic resonance spectroscopy metabolite concentrations. AIDS (London, England), 25(14), 1721.CrossRefGoogle ScholarPubMed
Ramesh, G., MacLean, A.G., & Philipp, M.T. (2013). Cytokines and chemokines at the crossroads of neuroinflammation, neurodegeneration, and neuropathic pain. Mediators of Inflammation, 2013, 20. doi: 10.1155/2013/480739 CrossRefGoogle Scholar
Ramirez, S.H., Reichenbach, N.L., Fan, S., Rom, S., Merkel, S.F., Wang, X., … Persidsky, Y. (2013). Attenuation of HIV-1 replication in macrophages by cannabinoid receptor 2 agonists. Journal of Leukocyte Biology, 93(5), 801–810.CrossRefGoogle ScholarPubMed
Rizzo, M.D., Crawford, R.B., Bach, A., Sermet, S., Amalfitano, A., & Kaminski, N.E. (2019). Δ9-Tetrahydrocannabinol suppresses monocyte-mediated astrocyte production of monocyte chemoattractant protein 1 and interleukin-6 in a toll-like receptor 7–stimulated human coculture. Journal of Pharmacology and Experimental Therapeutics, 371(1), 191–201.CrossRefGoogle Scholar
Rizzo, M.D., Crawford, R.B., Henriquez, J.E., Aldhamen, Y.A., Gulick, P., Amalfitano, A., & Kaminski, N.E. (2018). HIV-infected cannabis users have lower circulating CD16+ monocytes and IFN-γ-inducible protein 10 levels compared with nonusing HIV patients. AIDS, 32(4), 419–429.CrossRefGoogle ScholarPubMed
Robinson, S.M., Sobell, L.C., Sobell, M.B., & Leo, G.I. (2014). Reliability of the Timeline Followback for cocaine, cannabis, and cigarette use. Psychology of Addictive Behaviors, 28(1), 154.CrossRefGoogle ScholarPubMed
Rom, S. & Persidsky, Y. (2013). Cannabinoid receptor 2: Potential role in immunomodulation and neuroinflammation. Journal of Neuroimmune Pharmacology, 8(3), 608–620.CrossRefGoogle ScholarPubMed
Rotter, A., Bayerlein, K., Hansbauer, M., Weiland, J., Sperling, W., Kornhuber, J., & Biermann, T. (2013). CB1 and CB2 receptor expression and promoter methylation in patients with cannabis dependence. European Addiction Research, 19(1), 13–20.CrossRefGoogle ScholarPubMed
Rubin, L.H., Cook, J.A., Springer, G., Weber, K.M., Cohen, M.H., Martin, E.M., … Milam, J. (2017). Perceived and post-traumatic stress are associated with decreased learning, memory, and fluency in HIV-infected women. AIDS (London, England), 31(17), 2393–1401.CrossRefGoogle ScholarPubMed
Rubin, L.H., Neigh, G.N., Sundermann, E.E., Xu, Y., Scully, E.P., & Maki, P.M. (2019). Sex differences in neurocognitive function in adults with HIV: Patterns, predictors, and mechanisms. Current Psychiatry Reports, 21(10), 94.CrossRefGoogle Scholar
Saloner, R. & Cysique, L.A. (2017). HIV-associated neurocognitive disorders: A global perspective. Journal of the International Neuropsychological Society, 23(9–10), 860–869.CrossRefGoogle ScholarPubMed
Saylor, D., Dickens, A.M., Sacktor, N., Haughey, N., Slusher, B., Pletnikov, M., … McArthur, J.C. (2016). HIV-associated neurocognitive disorder--pathogenesis and prospects for treatment. Nat Rev Neurology, 12(4), 234–248. doi: 10.1038/nrneurol.2016.27 CrossRefGoogle ScholarPubMed
Simmons, R.P., Scully, E.P., Groden, E.E., Benedict, K.F., Chang, J.J., Lane, K., … Altfeld, M. (2013). HIV-1 infection induces strong production of IP-10 through TLR7/9-dependent pathways. AIDS (London, England), 27(16), 2505.CrossRefGoogle ScholarPubMed
Struik, D., Sanna, F., & Fattore, L. (2018). The modulating role of sex and anabolic-androgenic steroid hormones in cannabinoid sensitivity. Frontiers in Behavioral Neuroscience, 12, 249.CrossRefGoogle ScholarPubMed
Thames, A.D., Kuhn, T.P., Mahmood, Z., Bilder, R.M., Williamson, T.J., Singer, E.J., & Arentoft, A. (2017). Effects of social adversity and HIV on subcortical shape and neurocognitive function. Brain Imaging and Behavior, 12, 1–13. doi: 10.1007/s11682-017-9676-0 Google Scholar
Thames, A.D., Kuhn, T.P., Williamson, T.J., Jones, J.D., Mahmood, Z., & Hammond, A. (2017). Marijuana effects on changes in brain structure and cognitive function among HIV+ and HIV- adults. Drug Alcohol Depend, 170, 120–127. doi: 10.1016/j.drugalcdep.2016.11.007 CrossRefGoogle ScholarPubMed
Thames, A.D., Mahmood, Z., Burggren, A. C., Karimian, A., & Kuhn, T.P. (2016). Combined effects of HIV and marijuana use on neurocognitive functioning and immune status. AIDS Care, 28(5), 628–632. doi: 10.1080/09540121.2015.1124983 CrossRefGoogle ScholarPubMed
Van Sickle, M.D., Duncan, M., Kingsley, P.J., Mouihate, A., Urbani, P., Mackie, K., … Sharkey, K.A. (2005). Identification and functional characterization of brainstem cannabinoid CB2 receptors. Science, 310(5746), 329–332. doi: 10.1126/science.1115740 CrossRefGoogle ScholarPubMed
Vera, J.H., Guo, Q., Cole, J.H., Boasso, A., Greathead, L., Kelleher, P., … Gunn, R.N. (2016). Neuroinflammation in treated HIV-positive individuals: A TSPO PET study. Neurology, 86(15), 1425–1432.CrossRefGoogle ScholarPubMed
Wada, N.I., Jacobson, L.P., Margolick, J.B., Breen, E.C., Macatangay, B., Penugonda, S., … Bream, J.H. (2015). The effect of HAART-induced HIV suppression on circulating markers of inflammation and immune activation. AIDS, 29(4), 463–471. doi: 10.1097/QAD.0000000000000545 CrossRefGoogle Scholar
Wang, H., Liang, H., Ernst, T., Oishi, K., & Chang, L. (2020). Microstructural brain abnormalities in HIV+ individuals with or without chronic marijuana use. Journal of Neuroinflammation, 17, 230.CrossRefGoogle ScholarPubMed
Watson, C.W.-M., Paolillo, E.W., Morgan, E.E., Umlauf, A., Sundermann, E.E., Ellis, R.J., … Grant, I. (2020). Cannabis exposure is associated with a lower likelihood of neurocognitive impairment in people living with HIV. JAIDS Journal of Acquired Immune Deficiency Syndromes, 83(1), 56–64.CrossRefGoogle ScholarPubMed
Watson, C.W.-M., Sundermann, E.E., Hussain, M.A., Umlauf, A., Thames, A.D., Moore, R.C., … Moore, D.J. (2019). Effects of trauma, economic hardship, and stress on neurocognition and everyday function in HIV. Health Psychology, 38(1), 33.CrossRefGoogle ScholarPubMed
Weiss, J.M., Downie, S.A., Lyman, W.D., & Berman, J.W. (1998). Astrocyte-derived monocyte-chemoattractant protein-1 directs the transmigration of leukocytes across a model of the human blood-brain barrier. The Journal of Immunology, 161(12), 6896–6903.Google Scholar
Whiting, P.F., Wolff, R.F., Deshpande, S., Di Nisio, M., Duffy, S., Hernandez, A.V., … Ryder, S. (2015). Cannabinoids for medical use: A systematic review and meta-analysis. JAMA, 313(24), 2456–2473.CrossRefGoogle ScholarPubMed
Woolridge, E., Barton, S., Samuel, J., Osorio, J., Dougherty, A., & Holdcroft, A. (2005). Cannabis use in HIV for pain and other medical symptoms. Journal of Pain and Symptom Management, 29(4), 358–367.CrossRefGoogle ScholarPubMed
Yang, G., Meng, Y., Li, W., Yong, Y., Fan, Z., Ding, H., … Ke, Z.J. (2011). Neuronal MCP-1 mediates microglia recruitment and neurodegeneration induced by the mild impairment of oxidative metabolism. Brain Pathology, 21(3), 279–297.CrossRefGoogle ScholarPubMed
Yang, L., Li, F.-F., Han, Y.-C., Jia, B., & Ding, Y. (2015). Cannabinoid receptor CB2 is involved in tetrahydrocannabinol-induced anti-inflammation against lipopolysaccharide in MG-63 cells. Mediators of Inflammation, 2015, 11. doi: 10.1155/2015/362126 CrossRefGoogle ScholarPubMed
Yuan, L., Liu, A., Qiao, L., Sheng, B., Xu, M., Li, W., & Chen, D. (2015). The relationship of CSF and plasma cytokine levels in HIV infected patients with neurocognitive impairment. Biomed Research International, 2015, 6. doi: 10.1155/2015/506872 CrossRefGoogle ScholarPubMed
Yuan, L., Qiao, L., Wei, F., Yin, J., Liu, L., Ji, Y., … Chen, D. (2013). Cytokines in CSF correlate with HIV-associated neurocognitive disorders in the post-HAART era in China. Journal of Neurovirology, 19(2), 144–149. doi: 10.1007/s13365-013-0150-5 CrossRefGoogle ScholarPubMed