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Neurobehavioral effects of HIV-1 infection in China and the United States: A pilot study



The HIV epidemic in China has been increasing exponentially, yet there have been no studies of the neurobehavioral effects of HIV infection in that country. Most neuroAIDS research has been conducted in Western countries using Western neuropsychological (NP) methods, and it is unclear whether these testing methods are appropriate for use in China. Twenty-eight HIV seropositive (HIV+) and twenty-three HIV seronegative (HIV−) individuals with comparable gender, age, and education distributions were recruited in Beijing and the rural Anhui province in China. Thirty-nine HIV+ and thirty-one HIV− individuals were selected from a larger U.S. cohort recruited at the HIV Neurobehavioral Research Center, in San Diego, to be matched to the Chinese sample for age, disease status, and treatment variables. The NP test battery used with the U.S. and China cohorts included instruments widely used to study HIV infection in the United States. It consisted of 14 individual test measures, each assigned to one of seven ability areas thought to be especially vulnerable to effects of HIV on the brain (i.e., verbal fluency, abstraction/executive function, speed of information processing, working memory, learning, delayed recall, and motor function). To explore the cross-cultural equivalence and validity of the NP measures, we compared our Chinese and U.S. samples on the individual tests, as well as mean scaled scores for the total battery and seven ability domains. On each NP test measure, the mean of the Chinese HIV+ group was worse than that of the HIV− group. A series of 2 × 2 analyses of variance involving HIV+ and HIV− groups from both countries revealed highly significant HIV effects on the Global and all Domain mean scaled scores. Country effects appeared on two of the individual ability areas, at least partly due to education differences between the two countries. Importantly, the absence of HIV-by-Country interactions suggests that the NP effects of HIV are similar in the two countries. The NP test battery that was chosen and adapted for use in this study of HIV in China appears to have good cross-cultural equivalence, but appropriate Chinese norms will be needed to identify disease-related impairment in individual Chinese people. To inform the development of such norms, a much larger study of demographic effects will be needed, especially considering the wide range of education in that country. (JINS, 2007, 13, 781–790.)


Corresponding author

Correspondence and reprint requests to: Robert K. Heaton, Department of Psychiatry, University of California, San Diego, 9500 Gilman Drive #0603, La Jolla, California 92093-0603, USA. E-mail:


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Albert, S.M., Marder, K., Dooneief, G., Bell, K., Sano, M., Todak, G., & Stern, Y. (1995). Neuropsychologic impairment in early HIV infection. A risk factor for work disability. Archives of Neurology, 52, 525530.
Beck, A. (1976). Cognitive therapy and the emotional disorders. New York: Hoeber.
Benedict, R.H. (1997). Brief Visuospatial Memory Test-Revised. Odessa, FL: Psychological Assessment Resources, Inc.
Benton, A., Hamsher, K., & Sivan, A. (1994). Multilingual aphasia examination. Iowa City, IA: AJA Associates.
Brandt, J. & Benedict, R.H. (2001). Hopkins Verbal Learning Test-Revised. Professional manual. Lutz, FL: Psychological Assessment Resources, Inc.
Carter, S.L., Rourke, S.B., Murji, S., Shore, D., & Rourke, B.P. (2003). Cognitive complaints, depression, medical symptoms, and their association with neuropsychological functioning in HIV infection: A structural equation model analysis. Neuropsychology, 17, 410419.
Chan, A.S., Shum, D., & Cheung, R.W. (2003). Recent development of cognitive and neuropsychological assessment in Asian countries. Psychological Assessment, 15, 257267.
Chelune, G., Heaton, R., & Lehman, R. (1986). Neuropsychological and personality correlates of patient's complaints of disability. In R. Tarter & G. Goldstein (Eds.), Advances in clinical neuropsychology (pp. 95126). New York: New York Plenum Press.
Cherner, M., Masliah, E., Ellis, R.J., Marcotte, T.D., Moore, D.J., Grant, I., & Heaton, R.K. (2002). Neurocognitive dysfunction predicts postmortem findings of HIV encephalitis. Neurology, 59, 15631567.
China Ministry of Health, & the United Nations Theme Group on HIV/AIDS in China. (2003 December 1st). A joint assessment of HIV/AIDS prevention, treatment, and care in China. Beijing.
Chinese Ministry of Health, UNAIDS, & WHO. (December 2005). Progress on implementing UNGASS declaration of commitment in China 2005. Available at: http://data.Unaids.Org/pub/report/2006/2006_country_progress_report_china_en.Pdf.
Cysique, L.A.J., Deutsch, R., Atkinson, H.J., Young, C., Marcotte, T.D., Dawson, L., Grant, I., & Heaton, R.K. (2007). Incident major depression does not affect neuropsychological functioning in HIV infected men. Journal of the International Neuropsychological Society, 13, 111.
Cysique, L.A.J., Maruff, P., & Brew, B.J. (2006). The neuropsychological profile of symptomatic AIDS and ADC patients in the pre–highly active antiretroviral therapy era: A meta-analysis. Journal of the International Neuropsychological Society, 12, 368382.
d'Arminio Monforte, A., Testa, L., Adorni, F., Chiesa, E., Bini, T., Moscatelli, G.C., Abeli, C., Rusconi, S., Sollima, S., Balotta, C., Musicco, M., Galli, M., & Moroni, M. (1998). Clinical outcome and predictive factors of failure of highly active antiretroviral therapy in antiretroviral-experienced patients in advanced stages of HIV-1 infection. AIDS, 12, 16311637.
Diehr, M.C., Heaton, R.K., & Miller, W. (1998). The paced auditory serial addition task (PASAT): Norms for age, education, and ethnicity. Assessment, 5, 375387.
Ellis, R.J., Deutsch, R., Heaton, R.K., Marcotte, T.D., McCutchan, J.A., Nelson, J.A., Abramson, I., Thal, L.J., Atkinson, J.H., Wallace, M.R., & Grant, I. (1997). Neurocognitive impairment is an independent risk factor for death in HIV infection. San Diego HIV Neurobehavioral Research Center group. Archives of Neurology, 54, 416424.
Everall, I.P., Heaton, R.K., Marcotte, T.D., Ellis, R.J., McCutchan, J.A., Atkinson, J.H., Grant, I., Mallory, M., & Masliah, E. (1999). Cortical synaptic density is reduced in mild to moderate human immunodeficiency virus neurocognitive disorder. HNRC group. HIV Neurobehavioral Research Center. Brain Pathology, 9, 209217.
Gladsjo, J.A., Schuman, C.C., & Evans, J.D. (1999). Norms for letter and category fluency: Demographic corrections for age, education, and ethnicity. Assessment, 6, 147178.
Goggin, K.J., Zisook, S., Heaton, R.K., Atkinson, H.J., Marshall, S., McCuthchan, J.A., Chandler J.L., &Grant I. (1997). Neuropsychological performance of HIV-1 infected men with major depression. Journal of the International Neuropsychological Society, 3, 457464.
Grant, I., Atkinson, H.J., Hesselink, J.R., Kennedy, C.J., Richman, D.D., Spector, S.A., & McCuthchan, J.A. (1987). Evidence for early central nervous system involvement in the acquired immunodefieciency syndrome (AIDS) and other human immunodeficiency virus (HIV) infections. Studies with neuropsychological testing and magnetic resonance imaging. Annals of Internal Medicine, 107, 828836.
Grant, I. & Martin, A. (Eds.). (1994). Neuropsychology of HIV infection. New York: Oxford University Press.
Gronwall, D.M. (1977). Paced auditory serial-addition task: A measure of recovery from concussion. Perceptual and Motor Skills, 44, 367373.
Heaton, R., Grant, I., Butters, N., White, D.A., Kirson, D., Atkinson, H.J., McCuthchan, J.A., Taylor, M., Kelly, M.D., Ellis, R.J., Wolfson, T., Velin, R.A., Marcotte, T.D., Hesselink, J.R., Jernigan, T.L., Chandler, J., Wallace, M., & Abramason, I. (1995). The HNRC 500-neuropsychology of HIV infection at different disease stages. Journal of the International Neuropsychological Society, 1, 231251.
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., Marcotte, T.D., Rivera Mindt, M., Sadek, J., Moore, D., Bentley, H., McCutchan, A.J., Reicks, C., & Grant, I. (2004a). The impact of HIV associated neuropsychological impairment on everyday functioning. Journal of the International Neuropsychological Society, 10, 317331.
Heaton, R., Miller, W., Taylor, M.J., & Grant, I. (2004b). Revised comprehensive norms for an expanded Halstead Reitan Battery: Demographically adjusted neuropsychological norms for African American and Caucasian adults. Lutz, FL: Psychological Assessment Resources.
Heaton, R., Taylor, M., & Manly, J. (2003). Demographic effects and use of demographically corrected norms with the WAI-III and WMS-III. In D. Tulsky, D. Saklofske, & R.K. Heaton (Eds.), Clinical interpretation of the WAI-III and WMS-III. San Diego, CA: Academic Press.
Heaton, R.K., Velin, R.A., McCutchan, J.A., Gulevich, S.J., Atkinson, J.H., Wallace, M.R., Godfrey, H.P., Kirson, D.A., & Grant, I. (1994). Neuropsychological impairment in human immunodeficiency virus-infection: Implications for employment. HNRC group. HIV Neurobehavioral Research Center. Psychosomatic Medicine, 56, 817.
Hinkin, C.H., Hardy, D.J., Mason, K.I., Castellon, S.A., Durvasula, R.S., Lam, M.N., & Stefaniak, M. (2004). Medication adherence in HIV infected adults: Effect of patient age, cognitive status and substance. AIDS, 18(Suppl. 1), S19S25.
Jernigan, T.L., Archibald, S., Hesselink, J.R., Atkinson, J.H., Velin, R.A., McCutchan, J.A., Chandler, J.L., & Grant I. (1993). Magnetic resonance imaging morphometric analysis of cerebral volume loss in human immunodeficiency virus infection. The HNRC group. Archives of Neurology, 50, 250255.
Jin, H., Atkinson, H.J., Yu, X., Heaton, R.K., Shi, C., Marcotte, T.P., Young, C., Sadek, J., Wu, Z., & Grant, I. (2006). Depression and suicidality in HIV/AIDS in China. Journal of Affective Disorders, 94, 269275.
Klove, H. (1963). Clinical neuropsychology. In F.M. Forster (Ed.), The medical clinics of North America. New York: Saunders.
Kongs, S.K., Thompson, L.L., Iverson, G.L., & Heaton, R.K. (2000). WCST-64: Wisconsin Card Sorting Test-64 card version professional manual. Odessa, FL: Psychological Assessment Resources, Inc.
Lezak, M., Howieson, D., Loring, D., Hannay, J., & Fischer, J. (2004). Neuropsychological assessment (4th ed.). Oxford: Oxford University Press.
Maj, M., D'Elia, L., Satz, P., Janssen, R., Zaudig, M., Uchiyama, C., Starace, F., Galderisi, S., & Chervinsky, A. (1993). Evaluation of two new neuropsychological tests designed to minimize cultural bias in the assessment of HIV-1 seropositive persons: A WHO study. Archives of Clinical Neuropsychology, 8, 123135.
Maj, M., Satz, P., Janssen, R., Zaudig, R., Starace, F., D'Elia, L., Sughondhabirom, B., Mussa, M., Naber, D., Ndetei, D., Schulte, G., & Sartorius, N. (1994). WHO neuropsychiatric AIDS study, cross-sectional phase II. Archives of General Psychiatry, 51, 5161.
Masliah, E., Achim, C.L., Ge, N., DeTeresa, R., Terry, R.D., & Wiley, C.A. (1992). Spectrum of human immunodeficiency virus-associated neocortical damage. Annals of Neurology, 32, 321329.
Masliah, E., Heaton, R.K., Marcotte, T.D., Ellis, R.J., Wiley, C.A., Mallory, M., Achim, C.L., McCutchan, A.J., Nelson, J.A., Atkinson, H.J., & Grant, I. (1997). Dendritic injury is a pathological substrate for human immunodeficiency virus-related cognitive disorders. Annals of Neurology, 42, 963972.
Mayeux, R., Stern, Y., Tang, M.X., Todak, G., Marder, K., Sano, M., Richards, M., Stein, Z., Ehrhardt, A., & Gorman, J. (1993). Mortality risks in gay men with human immunodeficiency virus infection and cognitive impairment. Neurology, 43, 176182.
Moore, D.J., Masliah, E., Rippeth, J., Gonzalez, R., Carey, C.L., Cherner, M., Ellis, R.J., Achim, C.L., Marcotte, T.D., Heaton, R.K., & Grant, I. (2006). Cortical and subcortical neurodegeneration is associated with HIV neurocognitive impairment. AIDS, 20, 879887.
Navia, B.A., Cho, E.S., Petito, C.K., & Price, R.W. (1986). The AIDS Dementia Complex: II neuropathology. Annals of Neurology, 19, 525535.
Piatt, A.L., Fields, J.A., Paolo, A.M., Koller, W.C., & Tröster, A.I. (1999). Lexical, semantic, and action verbal fluency in Parkinson's disease with and without dementia. Journal of Clinical and Experimental Neuropsychology, 21, 435443.
Ping, L. (1993). Chinese version of BDI. Supplement issue of Mental Health Rating Scale, 191194.
Psychological Corporation. (1997a). Wechsler Adult Intelligence Scale-Third Edition (WAIS-III). San Antonio, TX: Psychological Corporation.
Psychological Corporation. (1997b). Wechsler Memory Scale-Third Edition Manual (WMS-III). San Antonio: The Psychological Corporation.
Reger, M., Wesh, R., Razani, J., Martin, D.J., & Boone, K.B. (2002). A meta-analysis of the neuropsychological sequelae of HIV infection. Journal of the International Neuropsychological Society, 8, 410424.
Rourke, S.B., Halman, M.H., & Bassel, C. (1999). Neurocognitive complaints in HIV-infection and their relationship to depressive symptoms and neuropsychological functioning. Journal of Clinical and Experimental Neuropsychology, 21, 737756.
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. (1998). Progressive cerebral volume loss in human immunodeficiency virus infection: A longitudinal volumetric magnetic resonance imaging study. Archives of Neurology, 55, 161168.
U.S.War Department. (1944). Army individual test battery-manual of directions and scoring. Washington, DC: War Department, Adjutant General's Office.
White, D.A., Heaton, R., & Monsch, A.U. (1995). Neuropsychological studies of asymptomatic human immunodeficiency virus-type 1 infected individuals. Journal of the International Neuropsychological Society, 1, 304315.
Woods, S.P., Scott, J.C., Sires, D.A., Grant, I., Heaton, R.K., & Tröster, A.I. (2005). Action (verb) fluency: Test-retest reliability, normative standards, and construct validity. Journal of the International Neuropsychological Society, 11, 408415.
Yang, Y., Zhang, G., & Xu, Y. (1999). A sero-epidemiological study of HCV and HVB infection among intravenous drug abusers. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi, 30, 247250.
Yepthomi, T., Paul, R., Vallabhaneni, S., Kumarasamy, N., Tate, D.F., Solomon, S., & Flanigan, T. (2006). Neurocognitive consequences of HIV in southern India: A preliminary study of clade c virus. Journal of the International Neuropsychological Society, 12, 424430.
Zheng, Y.P. (1987). Application of BDI in depressive neurosis. Chinese Journal of Neurology and Psychiatry, 13, 236237.


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Neurobehavioral effects of HIV-1 infection in China and the United States: A pilot study



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