Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-23T17:17:08.512Z Has data issue: false hasContentIssue false

Methamphetamine dependence increases risk of neuropsychological impairment in HIV infected persons

Published online by Cambridge University Press:  06 February 2004

JULIE D. RIPPETH
Affiliation:
Department of Psychiatry, University of California, San Diego School of Medicine, San Diego, California
ROBERT K. HEATON
Affiliation:
Department of Psychiatry, University of California, San Diego School of Medicine, San Diego, California San Diego State University and University of California, San Diego Joint Doctoral Program in Clinical Psychology, San Diego, California
CATHERINE L. CAREY
Affiliation:
San Diego State University and University of California, San Diego Joint Doctoral Program in Clinical Psychology, San Diego, California
THOMAS D. MARCOTTE
Affiliation:
Department of Psychiatry, University of California, San Diego School of Medicine, San Diego, California San Diego State University and University of California, San Diego Joint Doctoral Program in Clinical Psychology, San Diego, California
DAVID J. MOORE
Affiliation:
San Diego State University and University of California, San Diego Joint Doctoral Program in Clinical Psychology, San Diego, California
RAUL GONZALEZ
Affiliation:
San Diego State University and University of California, San Diego Joint Doctoral Program in Clinical Psychology, San Diego, California
TANYA WOLFSON
Affiliation:
Department of Psychiatry, University of California, San Diego School of Medicine, San Diego, California
IGOR GRANT
Affiliation:
Department of Psychiatry, University of California, San Diego School of Medicine, San Diego, California San Diego State University and University of California, San Diego Joint Doctoral Program in Clinical Psychology, San Diego, California Veterans Affairs San Diego Healthcare System
THE HNRC GROUP
Affiliation:
Department of Psychiatry, University of California, San Diego School of Medicine, San Diego, California

Abstract

Both HIV infection and methamphetamine dependence can be associated with brain dysfunction. Little is known, however, about the cognitive effects of concurrent HIV infection and methamphetamine dependence. The present study included 200 participants in 4 groups: HIV infected/methamphetamine dependent (HIV+/METH+), HIV negative/methamphetamine dependent (HIV−/METH+), HIV infected/methamphetamine nondependent (HIV+/METH−), and HIV negative/methamphetamine nondependent (HIV−/METH−). Study groups were comparable for age, education, and ethnicity, although the HIV−/METH− group had significantly more females. A comprehensive, demographically corrected neuropsychological battery was administered yielding a global performance score and scores for seven neurobehavioral domains. Rates of neuropsychological impairment were determined by cutoff scores derived from performances of a separate control group and validated with larger samples of HIV+ and HIV− participants from an independent cohort. Rates of global neuropsychological impairment were higher in the HIV+/METH+ (58%), HIV−/METH+ (40%) and HIV+/METH− (38%) groups compared to the HIV−/METH− (18%) group. Nonparametric analyses revealed a significant monotonic trend for global cognitive status across groups, with least impairment in the control group and highest prevalence of impairment in the group with concurrent HIV infection and methamphetamine dependence. The results indicate that HIV infection and methamphetamine dependence are each associated with neuropsychological deficits, and suggest that these factors in combination are associated with additive deleterious cognitive effects. This additivity may reflect common pathways to neural injury involving both cytotoxic and apoptotic mechanisms. (JINS, 2004, 10, 1–14.)Note: Dr. Erin D. Bigler served as action editor during the course of this review.

Type
Research Article
Copyright
© 2004 The International Neuropsychological Society

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

Adams, K.M., Brown, G.G., & Grant, I. (1985). Analysis of covariance as a remedy for demographic mismatch of research subject groups: Some sobering simulations. Journal of Clinical and Experimental Neuropsychology, 7, 445462.Google Scholar
Alhassoon, O.M., Dupont, R.M., Schweinsburg, B.C., Taylor, M.J., Patterson, T.L., & Grant, I. (2001). Regional cerebral blood flow in cocaine- versus methamphetamine-dependent patients with a history of alcoholism. International Journal of Neuropsychopharmacology, 4, 105112.Google Scholar
Atkinson, J.H., Grant, I., Kennedy, C.J., Richman, D.D., Spector, S.A., & McCutchan, J.A. (1988). Prevalence of psychiatric disorders among men infected with human immunodeficiency virus: A controlled study. Archives of General Psychiatry, 45, 859864.Google Scholar
Beck, A.T. & Steer, R.A. (1987). The Beck Depression Inventory. San Antonio, TX: Psychological Corporation.
Benedict, R.H. (1997). Brief Visuospatial Memory Test–Revised. Odessa, FL: Psychological Assessment Resources, Inc.
Benedict, R.H., Schretlen, D., Groninger, L., & Brandt, J. (1998). Hopkins Verbal Learning Test–Revised: Normative data and analysis of inter-form and test–retest reliability. Clinical Neuropsychologist, 12, 4355.CrossRefGoogle Scholar
Bing, E.G., Burnam, A., Longshore, D., Fleishman, J.A., Sherbourne, C.D., London, A.S., Turner, B.J., Eggan, F., Beckman, R., Vitiello, B., Morton, S.C., Orlando, M., Bozzette, S.A., Ortiz-Barron, L., & Shapiro, M. (2001). Psychiatric disorders and drug use among human immunodeficiency virus-infected adults in the United States. Archives of General Psychiatry, 58, 721728.Google Scholar
Bloom, F.E. & Rausch, D.M. (1997). HIV in the brain: Pathology and neurobehavioral consequences (meeting report). Journal of Neurovirology, 3, 102109.Google Scholar
Borkowski, J.G., Benton, A.L., & Spreen, O. (1967). Word fluency and brain damage. Neuropsychologia, 5, 135140.CrossRefGoogle Scholar
Czub, S., Koutsilieri, E., Sopper, S., Czub, M., Stahl-Hennig, C., Muller, J.G., Pedersen, V., Gsell, W., Heeney, J.L., Gerlach, M., Gosztonyi, G., Riederer, P., & ter Meulen, V. (2001). Enhancement of central nervous system pathology in early simian immunodeficiency virus infection by dopaminergic drugs. Acta Neuropathologica (Berl), 101, 8591.Google Scholar
Davidson, C., Gow, A.J., Lee, T.H., & Ellinwood, E.H. (2001). Methamphetamine neurotoxicity: Necrotic and apoptotic mechanisms and relevance to human abuse and treatment. Brain Research Reviews, 36, 122.Google Scholar
Deutsch, R., Ellis, R.J., McCutchan, A., Marcotte, T.D., Letendre, S., Grant, I., & the HNRC Group. (2001). AIDS-associated mild neurocognitive impairment is delayed in the era of highly active antiretroviral therapy (HAART). AIDS, 15, 18981899.Google Scholar
Diehr, M.C., Heaton, R.K., Miller, W., & Grant, I. (1998). The Paced Auditory Serial Addition Task (PASAT): Norms for age, education, and ethnicity. Assessment, 5, 375387.Google Scholar
Dore, G.J., Correll, P.K., Li, Y., Kaldor, J.M., Cooper, D.A., & Brew, B.J. (1999). Changes to AIDS dementia complex in the era of highly active antiretroviral therapy. AIDS, 13, 12491253.Google Scholar
Durvasula, R.S., Myers, H.F., Satz, P., Miller, E.N., Morgenstern, H., Richardson, M.A., Evans, G., & Forney, D. (2000). HIV-1, cocaine, and neuropsychological performance in African American men. Journal of the International Neuropsychological Society, 6, 322335.Google Scholar
Durvasula, R.S., Miller, E.N., Myers, H.F., & Wyatt, G.E. (2001). Predictors of neuropsychological performance in HIV positive women. Journal of Clinical and Experimental Neuropsychology, 23, 149163.Google Scholar
Eisch, A., O'Dell, S., & Marshall, J. (1996). Striatal and cortical NMDA receptors are altered by a neurotoxic regimen of methamphetamine. Synapse, 22, 217225.Google Scholar
Ernst, T., Chang, L., Leonido-Yee, M., & Speck, O. (2000). Evidence for long-term neurotoxicity associated with methamphetamine abuse. Neurology, 54, 13441349.Google Scholar
Ferrando, S., Goggin, K., Sewell, M., Evans, S., Fishman, B., & Rabkin, J. (1998). Substance use disorders in gay/bisexual men with HIV and AIDS. American Journal on Addictions, 7, 5160.Google Scholar
First, M.B., Spitzer, R.L., Gibbon, M., & Williams, J.B. (1996). Structured Clinical Interview for DSM–IV Axis I Disorders. New York: Biometrics Research Department.
Gladsjo, J.A., Schuman, C.C., Evans, J.D., Peavy, G.M., Miller, S.W., & Heaton, R.K. (1999). Norms for letter and category fluency: Demographic corrections for age, education, and ethnicity. Assessment, 6, 147178.Google Scholar
Golden, C. (1974). Stroop Color and Word Test. Chicago: Stoelting.
Gouzoulis-Mayfrank, E., Schreckenberger, M., Sabri, O., Arning, C., Thelen, B., Spitzer, M., Kovar, K.A., Hermle, L., Bull, U., & Sass, H. (1999). Neurometabolic effects of psilocybin, 3,4-methylenedioxyethylamphetamine (MDE) and d-methamphetamine in healthy volunteers. Neuropsychopharmacology, 20, 565581.Google Scholar
Grant, I., Adams, K.M., Carlin, A.S., Rennick, P., Judd, L.L., & Schooff, K. (1978). The collaborative neuropsychological study of polydrug abusers. Archives of General Psychiatry, 35, 10631074.Google Scholar
Grant, I., Atkinson, J.H., Hesselink, J.R., Kennedy, C.J., Richman, D.D., Spector, S.A., & McCutchan, J.A. (1987). Evidence for early central nervous system involvement in the acquired deficiency syndrome (AIDS) and other human immunodeficiency virus (HIV) infections. Studies with neuropsychologic testing and magnetic resonance imaging. Annals of Internal Medicine, 107, 828836.Google Scholar
Grassi, M.P., Clerici, F., Perin, C., Zocchetti, C., Cargnel, A., & Mangoni, A. (1995). HIV infection and drug use: Influence on cognitive function. AIDS, 9, 165170.Google Scholar
Grassi, M.P., Perin, C., Clerici, F., Zocchetti, C., Cargnel, A., & Mangoni, A. (1993). Neuropsychological performance in HIV-1-infected drug abusers. Acta Neurologica Scandinavica, 88, 119122.Google Scholar
Gronwall, D.M.A. (1977). Paced auditory serial-addition task: A measure of recovery from concussion. Perceptual and Motor Skills, 44, 367375.Google Scholar
Halstead, W.C. (1947). Brain and intelligence: A quantitative study of the frontal lobes. Chicago, University of Chicago Press.
Haughey, N.J., Nath, A., Mattson, M.P., Slevin, J.T., & Geiger, J.D. (2001). HIV-1 Tat through phosphorylation of NMDA receptors potentiates glutamate excitotoxicity. Journal of Neurochemistry, 78, 457467.Google Scholar
Heaton, R.K., Grant, I., Butters, N., White, D.A., Kirson, D., Atkinson, J.H., McCutchan, J.A., Taylor, M.J., Kelly, M.D., Ellis, R.J., Wolfson, T., Velin, R., Marcotte, T.D., Hesselink, J.R., Jernigan, T.L., Chandler, J., Wallace, M., Abramson, I., & the HNRC Group. (1995). The HNRC 500–Neuropsychology of HIV infection at different disease stages. Journal of the International Neuropsychological Society, 1, 231251.Google Scholar
Heaton, R.K., Grant, I., & Matthews, C.G. (1991). Comprehensive norms for an expanded Halstead-Reitan Battery: Demographic corrections, research findings, and clinical applications. Odessa, FL: Psychological Assessment Resources.
Heaton, R.K., Paulsen, J., McAdams, L.A., Kuck, J., Zisook, S., Braff, D., Harris, M.J., & Jeste, D.V. (1994). Neuropsychological deficits in schizophrenics: Relationship to age, chronicity, and dementia. Archives of General Psychiatry, 51, 469476.Google Scholar
Heaton, R.K., Taylor, M.J., & Manly, J.J. (2002). Demographic effects and use of demographically corrected norms with the WAIS–III and WMS–III. In D. Tulsky, D. Saklofske, R.K. Heaton, G. Chelune, R. Ivnik, R.A. Bornstein, A. Prifitera, & M. Ledbetter (Eds.), Clinical interpretation of the WAIS–III and WMS–III (pp. 183210). San Diego, CA: Academic Press.
Hesselgesser, J., Taub, D., Baskar, P., Greenberg, M., Hoxie, J., Kolson, D.L., & Horuk, R. (1998). Neuronal apoptosis induced by HIV-1 gp120 and the chemokine SDF-1alpha is mediated by the chemokine receptor CXCR4. Current Biology, 8, 595598.Google Scholar
Hollander, M. & Wolfe, D.A. (1973). Nonparametric statistical methods. New York: John Wiley & Sons, Inc.
Itoh, K., Mehraein, P., & Weis, S. (2000). Neuronal damage of the substantia nigra in HIV-1 infected brains. Acta Neuropathologica (Berl), 99, 376384.Google Scholar
Iyo, M., Namba, H., Yanagisawa, M., Hirai, S., Yui, N., & Fukui, S. (1997). Abnormal cerebral perfusion in chronic methamphetamine abusers: A study using 99MTc-HMPAO and SPECT. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 21, 789796.Google Scholar
Jernigan, T.L., Archibald, S., Hesselink, J.R., Atkinson, J.H., Velin, R.A., McCutchan, J.A., Chandler, J., Grant, I., & the HNRC Group. (1993). Magnetic resonance imaging morphometric analysis of cerebral volume loss in human immunodeficiency virus infection. Archives of Neurology, 50, 250255.Google Scholar
Jonckheere, A.R. (1954). A distribution-free k-sample test against ordered alternatives. Biometricka, 41, 133145.CrossRefGoogle Scholar
Kløve, H. (1963). Grooved Pegboard. Lafayette, IN: Lafayette Instruments.
Kongs, S.K., Thompson, L.L., Iverson, G.L., & Heaton, R.K. (2000). Wisconsin Card Sorting Test–64 Card Computerized Version. Odessa, FL: Psychological Assessment Resources.
Ladenheim, B., Krasnova, I.N., Deng, X., Oyler, J.M., Polettini, A., Moran, T.H., Huestis, M.A., & Cadet, J.L. (2000). Methamphetamine-induced neurotoxicity is attenuated in transgenic mice with a null mutation for interleukin-6. Molecular Pharmacology, 58, 12471256.Google Scholar
Langford, D., Trinh, T., Everson, A., Adame, A., Grant, I., McCutchan, A., Ellis, R., Marcotte, T., Masliah, E., & the HNRC group. (2002). Selective damage of calbindin immunoreactive neurons in methamphetamine-user HIVE patients. Manuscript submitted for publication.
Lipton, S.A. & Gendelman, H.E. (1995). Dementia associated with the acquired immuno-deficiency syndrome. New England Journal of Medicine, 332, 934940.Google Scholar
Marshall, J., O'Dell, S., & Weihmuller, F. (1993). Dopamine–glutamate interactions in methamphetamine-induced neurotoxicity. Journal of Neural Transmission-General Section, 91, 241254.Google Scholar
Martin, E.M., Sullivan, T.S., Reed, R.A., Fletcher, T.A., Pitrak, D.L., Weddington, W., & Harrow, M. (2001). Auditory working memory in HIV-1 infection. Journal of the International Neuropsychological Society, 7, 2026.Google Scholar
Maschke, M., Kastrup, O., Esser, S., Ross, B., Hengge, U., & Hufnagel, A. (2000). Incidence and prevalence of neurological disorders associated with HIV since the introduction of highly active antiretroviral therapy (HAART). Journal of Neurology, Neurosurgery, and Psychiatry, 69, 376380.Google Scholar
McCann, U.D., Wong, D.F., Yokol, F., Villemagne, V., Dannals, R.F., & Ricaurte, G.A. (1998). Reduced striatal dopamine transporter density in abstinent methamphetamine and methcathinone users: Evidence from positron emission tomography studies with [11C]WIN-35,428. Journal of Neuroscience, 18, 84178422.Google Scholar
McKetin, R. & Mattick, R.P. (1997). Attention and memory in illicit amphetamine users. Drug and Alcohol Dependence, 48, 235242.Google Scholar
McKetin, R. & Mattick, R.P. (1998). Attention and memory in illicit amphetamine users: Comparison with non-drug-using controls. Drug and Alcohol Dependence, 50, 181184.Google Scholar
Nath, A., Maragos, W.F., Avison, M.J., Schmitt, F.A., & Berger, J.R. (2001). Acceleration of HIV dementia with methamphetamine and cocaine. Journal of Neurovirology, 7, 6671.Google Scholar
Ohmori, T., Abekawa, T., & Koyama, T. (1996). The role of glutamate in behavioral and neurotoxic effects of methamphetamine. Neurochemistry International, 29, 301307.Google Scholar
Peavy, G., Jacobs, D., Salmon, D.P., Butters, N., Delis, D.C., Taylor, M., Massman, P., Stout, J.C., Heindel, W.C., Kirson, D., Atkinson, J.H., Chandler, J.L., Grant, I., & the HNRC Group. (1994). Verbal memory performance of patients with human immunodeficiency virus infection: Evidence of subcortical dysfunction. Journal of Clinical and Experimental Neuropsychology, 16, 508523.Google Scholar
Pirie, W. (1983). Jonckheere Tests for Ordered Alternatives. In S. Kotz & N.L. Johnson (Eds.), Encyclopedia of statistical sciences, Vol. 4 (pp. 315318). New York: John Wiley & Sons, Inc.
Psychological Corporation. (1997). Wechsler Adult Intelligence Scale–Third Edition. San Antonio, TX: Author.
Rabkin, J.G. (1996). Prevalence of psychiatric disorders in HIV illness. International Review of Psychiatry, 8, 157166.Google Scholar
Rausch, D.M. & Stover, E.S. (2001). Neuroscience research in AIDS. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 25, 231257.Google Scholar
Reitan, R.M. & Davison, L.A. (Eds.). (1974). Clinical Neuropsychology: Current status and applications. Washington, DC: V.H. Winston & Sons.
Reyes, M.G., Faraldi, F., Senseng, C.S., Flowers, C., & Fariello, R. (1991). Nigral degeneration in acquired immune deficiency syndrome (AIDS). Acta Neuropathologica (Berl), 82, 3944.Google Scholar
Robins, L., Cottler, L., Bucholz, K., Compton, W., North, C.S., & Rourke, K.M. (1995). Diagnostic Interview Schedule for DSM–IV. St. Louis, MO: Washington University School of Medicine.
Rothrock, J.F., Rubenstein, R., & Lyden, P.D. (1988). Ischemic stroke associated with methamphetamine inhalation. Neurology, 38, 589592.Google Scholar
Rumbaugh, C.L., Bergeron, R.T., Scanlan, R.L., Teal, J.S., Segall, H.D., Fang, H.C., & McCormick, R. (1971). Cerebral vascular changes secondary to amphetamine abuse in the experimental animal. Radiology, 101, 345351.Google Scholar
Rylander, G. (1969). Clinical and medicocriminological aspects of addiction to central stimulating drugs. In F. Sjoqvist & M. Tottie (Eds.), Abuse of central stimulants (pp. 251274). Stockholm: Almqvist & Wiskell.
Sacktor, N., Lyles, R.H., Skolasky, R., Kleeberger, C., Selnes, O.A., Miller, E.N., Becker, J.T., Cohen, B., McArthur, J.C., & the Multicenter AIDS Cohort Study. (2001). HIV-associated neurologic disease incidence changes: Multicenter AIDS Cohort Study, 1990–1998. Neurology, 56, 257260.Google Scholar
Sekine, Y., Iyo, M., Ouchi, Y., Matsunaga, T., Tsukada, H., Okada, H., Yoshikawa, E., Futatsubashi, M., Takei, N., & Mori, N. (2001). Methamphetamine-related psychiatric symptoms and reduced brain dopamine transporters studied with PET. American Journal of Psychiatry, 158, 12061214.Google Scholar
Simon, S.L., Domier, C., Carnell, J., Brethen, P., Rawson, R., & Ling, W. (2000). Cognitive impairment in individuals currently using methamphetamine. American Journal on Addictions, 9, 222231.Google Scholar
Simon, S.L., Domier, C.P., Sim, T., Richardson, K., Rawson, R.A., & Ling, W. (2002). Cognitive performance of current methamphetamine and cocaine abusers. Journal of Addictive Diseases, 21, 6174.Google Scholar
Stephans, S. & Yamamoto, B. (1994). Methamphetamine-induced neurotoxicity: Roles for glutamate and dopamine efflux. Synapse, 17, 203209.Google Scholar
Stout, J.C., Ellis, R.J., Jernigan, T.L., Archibald, S.L., Abramson, I., Wolfson, T., McCutchan, J.A., Wallace, M.R., Atkinson, J.H., Grant, I., & the HNRC Group. (1998). Progressive cerebral volume loss in human immunodeficiency virus infection: A longitudinal volumetric magnetic resonance imaging study. Archives of Neurology, 55, 161168.Google Scholar
Substance Abuse and Mental Health Administration. (2000). Treatment Episode Data Set: 1993–1998. Rockville, MD: Substance Abuse and Mental Health Administration.
Taylor, M.J., Alhassoon, O.M., Schweinsburg, B.C., Videen, J.S., Grant, I., & the HNRC Group. (2000). MR spectroscopy in HIV and stimulant dependence. Journal of the International Neuropsychological Society, 6, 8385.Google Scholar
Terpstra, T.J. (1952). The asymptotic normality and consistency of Kendall's test against trend, when ties are present in one ranking. Indigationes Mathematicae, 14, 327333.Google Scholar
Tracey, I., Hamberg, L.M., Guirnaraes, A.R., Hunter, G., Chang, I., Navia, B.A., & Gonzalez, R.G. (1998). Increased cerebral blood volume in HIV-positive patients detected by functional MRI. Neurology, 50, 18211826.Google Scholar
Trites, R.L., Suh, M., Offord, D., Nieman, G., & Preston, D. (1974). Neuropsychological and psychosocial antecedents and chronic effects of prolonged use of solvents and methamphetamines. Paper presented at the International Psychiatric Research Society, Ottawa, Canada.
Volkow, N.D., Chang, L., Wang, G.J., Fowler, J.S., Franceschi, D., Sedler, M.J., Gatley, S.J., Hitzemann, R., Ding, Y.S., Wong, C., & Logan, J. (2001a). Higher cortical and lower subcortical metabolism in detoxified methamphetamine abusers. American Journal of Psychiatry, 158, 383389.Google Scholar
Volkow, N.D., Chang, L., Wang, G.J., Fowler, J.S., Leonido-Yee, M., Franceschi, D., Sedler, M.J., Gatley, S.J., Hitzemann, R., Ding, Y.S., Logan, J., Wong, C., & . Miller, E.N. (2001b). Association of dopamine transporter reduction with psychomotor impairment in methamphetamine abusers. American Journal of Psychiatry, 158, 377382.Google Scholar
von Giesen, H.J., Antke, C., Hefter, H., Wenserski, F., Seitz, R.J., & Arendt, G. (2000). Potential time course of human immunodeficiency virus type-1 associated minor motor deficits. Archives of Neurology, 57, 16011607.Google Scholar
White, D.A., Heaton, R.K., & Monsch, A.U. (1995). Neuropsychological studies of asymptomatic human immunodeficiency virus-type 1-infected individuals. Journal of the International Neuropsychological Society, 1, 304315.Google Scholar
Wilkinson, G.S. (1993). The Wide Range Achievement Test–Third Edition. Wilmington, DE: Wide Range, Inc.
Wilson, J.M., Kalasinsky, K.S., Levey, A.I., Bergeron, C., Reiber, G., Anthony, R.M., Schmunk, G.A., Shannak, K., Haycock, J.W., & Kish, S.J. (1996). Striatal and dopamine nerve terminal markers in human, chronic methamphetamine users. Natural Medicine, 2, 699703.Google Scholar
Woody, G.E., Donnell, D., Seage, G.R., Metzger, D., Marmor, M., Koblin, B.A., Buchbinder, S., Gross, M., Stone, B., & Judson, F.N. (1999). Non-injection substance use correlates with risky sex among men having sex with men. Data from HIVNET. Drug and Alcohol Dependence, 53, 197205.Google Scholar