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Use of Neuroimaging to Inform Optimal Neurocognitive Criteria for Detecting HIV-Associated Brain Abnormalities

  • Laura M. Campbell (a1) (a2), Christine Fennema-Notestine (a2) (a3), Rowan Saloner (a1) (a2), Mariam Hussain (a1) (a2), Anna Chen (a2), Donald Franklin (a2), Anya Umlauf (a2), Ronald J. Ellis (a2), Ann C. Collier (a4), Christina M. Marra (a5), David B. Clifford (a6), Benjamin B. Gelman (a7), Ned Sacktor (a8), Susan Morgello (a9), J. Allen McCutchan (a10), Scott Letendre (a2) (a10), Igor Grant (a2), Robert K. Heaton (a2) and for the CHARTER Group...



Frascati international research criteria for HIV-associated neurocognitive disorders (HAND) are controversial; some investigators have argued that Frascati criteria are too liberal, resulting in a high false positive rate. Meyer et al. recommended more conservative revisions to HAND criteria, including exploring other commonly used methodologies for neurocognitive impairment (NCI) in HIV including the global deficit score (GDS). This study compares NCI classifications by Frascati, Meyer, and GDS methods, in relation to neuroimaging markers of brain integrity in HIV.


Two hundred forty-one people living with HIV (PLWH) without current substance use disorder or severe (confounding) comorbid conditions underwent comprehensive neurocognitive testing and brain structural magnetic resonance imaging and magnetic resonance spectroscopy. Participants were classified using Frascati criteria versus Meyer criteria: concordant unimpaired [Frascati(Un)/Meyer(Un)], concordant impaired [Frascati(Imp)/Meyer(Imp)], or discordant [Frascati(Imp)/Meyer(Un)] which were impaired via Frascati criteria but unimpaired via Meyer criteria. To investigate the GDS versus Meyer criteria, the same groupings were utilized using GDS criteria instead of Frascati criteria.


When examining Frascati versus Meyer criteria, discordant Frascati(Imp)/Meyer(Un) individuals had less cortical gray matter, greater sulcal cerebrospinal fluid volume, and greater evidence of neuroinflammation (i.e., choline) than concordant Frascati(Un)/Meyer(Un) individuals. GDS versus Meyer comparisons indicated that discordant GDS(Imp)/Meyer(Un) individuals had less cortical gray matter and lower levels of energy metabolism (i.e., creatine) than concordant GDS(Un)/Meyer(Un) individuals. In both sets of analyses, the discordant group did not differ from the concordant impaired group on any neuroimaging measure.


The Meyer criteria failed to capture a substantial portion of PLWH with brain abnormalities. These findings support continued use of Frascati or GDS criteria to detect HIV-associated CNS dysfunction.


Corresponding author

Correspondence and reprint requests to: Robert K. Heaton, Ph.D., Distinguished Professor of Psychiatry, University of California, San Diego, HIV Neurobehavioral Research Program, 220 Dickinson St, Suite B, MC8231, San Diego, CA 92103-8231. E-mail:


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Alakkas, A., Ellis, R.J., Watson, C.W., Umlauf, A., Heaton, R.K., Letendre, S., Collier, A., Marra, C., Clifford, D.B., Gelman, B., Sacktor, N., Morgello, S., Simpson, D., McCutchan, J.A., Kallianpur, A., Gianella, S., Marcotte, T., Grant, I., Fennema-Notestine, C., & CHARTER Group (2018). White matter damage, neuroinflammation, and neuronal integrity in HAND. Journal of NeuroVirology, 25, 3241. doi:10.1007/s13365-018-0682-9
Ances, B.M. & Hammoud, D.A. (2014). Neuroimaging of HIV associated neurocognitive disorders (HAND). Current Opinion in HIV and AIDS, 9, 545551. doi:10.1097/coh.0000000000000112
Ances, B.M., Sisti, D., Vaida, F., Liang, C., Leontiev, O., Perthen, J., Buxton, R.B., Benson, D., Smith, D.M., Little, S., Richman, D.D., Moore, D.J., Ellis, R.J., & HNRC group (2009). Resting cerebral blood flow a potential biomarker of the effects of HIV in the brain. Neurology, 73, 702708.
Anderson, A.M., Fennema-Notestine, C., Umlauf, A., Taylor, M.J., Clifford, D.B., Marra, C.M., Collier, A.C., Gelman, B.B., McArthur, J.C., McCutchan, J.A., Simpson, D.M., Morgello, S., Grant, I., Letendre, S.L., & CHARTER Group (2015). CSF biomarkers of monocyte activation and chemotaxis correlate with magnetic resonance spectroscopy metabolites during chronic HIV disease. Journal of NeuroVirology, 21, 559567. doi:10.1007/s13365-015-0359-6
Andrade, A.S., Deutsch, R., Celano, A.S., Duarte, N.A., Marcotte, T.D., Umlauf, A., Atkinson, J.H., McCutchan, J.A., Franklin, D., Alexander, T.J., McArthur, J.C., Marra, C., Grant, I., & Collier, A.C. (2013). Relationships among neurocognitive status, medication adherence measured by pharmacy refill records, and virologic suppression in HIV-infected persons. Journal of Acquired Immune Deficiency Syndromes, 62, 282292. doi:10.1097/QAI.0b013e31827ed678
Antinori, A., Arendt, G., Becker, J.T., Brew, B.J., Byrd, D.A., Cherner, M., Clifford, D.B., Cinque, P., Epstein, L.G., Goodkin, K., Gisslen, M., Grant, I., Heaton, R.K., Joseph, J., Marder, K., Marra, C.M., McArthur, J.C., Nunn, M., Price, R.W., Pulliam, L., Robertson, K.R., Sacktor, N., Valcour, V., & Wojna, V.E. (2007). Updated research nosology for HIV-associated neurocognitive disorders. Neurology, 69, 17891799. doi:10.1212/01.WNL.0000287431.88658.8b
Becker, J.T., Maruca, V., Kingsley, L.A., Sanders, J.M., Alger, J.R., Barker, P.B., Goodkin, K., Martin, E., Miller, E.N., Ragin, A., Sacktor, N. Selnes, O., & Multicenter AIDS Cohort Study (2012). Factors affecting brain structure in men with HIV disease in the post-HAART era. Neuroradiology, 54, 113121. doi:10.1007/s00234-011-0854-2
Blackstone, K., Moore, D.J., Franklin, D.R., Clifford, D.B., Collier, A.C., Marra, C.M., Gelman, B.B., McArthur, J.C., Morgello, S., Simpson, D.M., Ellis, R.J., Atkinson, J.H., Grant, I., & Heaton, R.K. (2012). Defining neurocognitive impairment in HIV: Deficit scores versus clinical ratings. The Clinical Neuropsychologist, 26, 894908. doi:10.1080/13854046.2012.694479
Bonnet, F., Amieva, H., Marquant, F., Bernard, C., Bruyand, M., Dauchy, F.A., Mercié, P., Greib, C., Richert, L., Neau, D., Catheline, G., Dehail, P., Dabis, F., Morlat, P., Dartigues, J.F., Chene, G., & S CO3 Aquitaine Cohort (2013). Cognitive disorders in HIV-infected patients: Are they HIV-related? AIDS, 27, 391400. doi:10.1097/QAD.0b013e32835b1019
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 and Experimental Neuropsychology, 26, 307319.
Casaletto, K.B., Cattie, J., Franklin, D.R., Moore, D.J., Woods, S.P., Grant, I., Heaton, R.K., & Group, H. (2014). The wide range achievement test–4 reading subtest “holds” in HIV-infected individuals. Journal of Clinical and Experimental Neuropsychology, 36, 9921001.
Center for Disease Control and Prevention (2016). HIV in the United States and dependent areas. Retrieved from
Chang, L., Lee, P.L., Yiannoutsos, C.T., Ernst, T., Marra, C.M., Richards, T., Kolson, D., Schifitto, G., Jarvik, J.G., Miller, E.N., Lenkinski, R., Gonzalez, G., Navia, B.A., & HIV MRS Consortium (2004). A multicenter in vivo proton-MRS study of HIV-associated dementia and its relationship to age. Neuroimage, 23, 13361347. doi:10.1016/j.neuroimage.2004.07.067
Chelune, G.J., Heaton, R.K., & Lehman, R.A. (1986). Neuropsychological and personality correlates of patients’ complaints of disability, In Goldstein, G. & Tarter, R.E. (Eds.), Advances in clinical neuropsychology, (pp. 95126). Boston, MA: Springer.
Cohen, R.A., Harezlak, J., Schifitto, G., Hana, G., Clark, U., Gongvatana, A., Paul, R., Taylor, M., Thompson, P., Alger, J., Brown, M., Zhong, J., Campbell, T., Singer, E., Daar, E., McMahon, D., Tso, Y., Yiannoutsos, C.T., & Navia, B. (2010). Effects of nadir CD4 count and duration of HIV infection on brain volumes in the HAART era. Journal of NeuroVirology, 16, 2532. doi:10.3109/13550280903552420
Cohen, R.A., Seider, T.R., & Navia, B. (2015). HIV effects on age-associated neurocognitive dysfunction: Premature cognitive aging or neurodegenerative disease? Alzheimer’s Research & Therapy, 7, 37. doi:10.1186/s13195-015-0123-4
Cysique, L.A., Letendre, S.L., Ake, C., Jin, H., Franklin, D.R., Gupta, S., Shi, C., Yu, X., Wu, Z., Abramson, I.S., Grant, I. Heaton, R.K., & HIV Neurobehavioral Research Center group (2010). Incidence and nature of cognitive decline over 1 year among HIV-infected former plasma donors in China. AIDS, 24, 983990. doi:10.1097/QAD.0b013e32833336c8
Cysique, L.A., Moffat, K., Moore, D.M., Lane, T.A., Davies, N. W., Carr, A., Brew, B. J., & Rae, C. (2013). HIV, vascular and aging injuries in the brain of clinically stable HIV-infected adults: A (1)H MRS study. PLoS One, 8, e61738. doi:10.1371/journal.pone.0061738
Cysique, L.A., Soares, J.R., Geng, G., Scarpetta, M., Moffat, K., Green, M., Brew, B.J., Henry, R.G., & Rae, C. (2017). White matter measures are near normal in controlled HIV infection except in those with cognitive impairment and longer HIV duration. Journal of NeuroVirology, 23, 539547.
du Plessis, L., Paul, R.H., Hoare, J., Stein, D.J., Taylor, P.A., Meintjes, E.M., & Joska, J.A. (2017). Resting-state functional magnetic resonance imaging in clade C HIV: Within-group association with neurocognitive function. Journal of NeuroVirology, 23, 875885.
Ernst, T., Jiang, C.S., Nakama, H., Buchthal, S., & Chang, L. (2010). Lower brain glutamate is associated with cognitive deficits in HIV patients: A new mechanism for HIV-associated neurocognitive disorder. Journal of Magnetic Resonance Imaging, 32, 10451053. doi:10.1002/jmri.22366
Fennema-Notestine, C., Ellis, R.J., Archibald, S.L., Jernigan, T.L., Letendre, S.L., Notestine, R.J., Taylor, M.J., Theilmann, R.J., Julaton, M.D., Croteau, D.J., Wolfson, T., Heaton, R.K., Gamst, A.C., Franklin, D.R. Jr., Clifford, D.B., Collier, A.C., Gelman, B.B., Marra, C., McArthur, J.C., McCutchan, J.A., Morgello, S., Simpson, D.M., Grant, I., & CHARTER Group (2013). Increases in brain white matter abnormalities and subcortical gray matter are linked to CD4 recovery in HIV infection. Journal of NeuroVirology, 19, 393401. doi:10.1007/s13365-013-0185-7
Fennema-Notestine, C., Gamst, A.C., Quinn, B.T., Pacheco, J., Jernigan, T.L., Thal, L., Buckner, R., Killiany, R., Blacker, D., Dale, A.M., Fischl, B., Dickerson, B., & Gollub, R.L. (2007). Feasibility of multi-site clinical structural neuroimaging studies of aging using legacy data. Neuroinformatics, 5, 235245. doi:10.1007/s12021-007-9003-9
Foley, J.M., Ettenhofer, M.L., Kim, M.S., Behdin, N., Castellon, S.A., & Hinkin, C.H. (2012). Cognitive reserve as a protective factor in older HIV-positive patients at risk for cognitive decline. Applied Neuropsychology: Adult, 19, 1625.
Gisslén, M., Price, R.W., & Nilsson, S. (2011). The definition of HIV-associated neurocognitive disorders: Are we overestimating the real prevalence? BMC Infectious Diseases, 11, 356.
Harezlak, J., Buchthal, S., Taylor, M., Schifitto, G., Zhong, J., Daar, E., Alger, J., Singer, E., Campbell, T., Yiannoutsos, C., Cohen, R., Navia, B., & HIV Neuroimaging Consortium (2011). Persistence of HIV-associated cognitive impairment, inflammation and neuronal injury in era of highly active antiretroviral treatment. AIDS, 25, 625633. doi:10.1097/QAD.0b013e3283427da7
Heaton, R.K., Clifford, D.B., Franklin, D.R. , Jr., Woods, S.P., Ake, C., Vaida, F., Ellis, R.J., Letendre, S.L., Marcotte, T.D., Atkinson, J.H., Rivera-Mindt, M., Vigil, O.R., Taylor, M.J., Collier, A.C., Marra, C.M., Gelman, B.B., McArthur, J.C., Morgello, S., Simpson, D.M., McCutchan, J.A., Abramson, I., Gamst, A., Fennema-Notestine, C., Jernigan, T.L., Wong, J., Grant, I., & CHARTER Group (2010). HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER Study. Neurology, 75, 20872096. doi:10.1212/WNL.0b013e318200d727
Heaton, R.K., Franklin, D.R., Ellis, R.J., McCutchan, J.A., Letendre, S.L., LeBlanc, S., Corkran, S.H., Duarte, N.A., Clifford, D.B., Woods, S.P., Collier, A.C., Marra, C.M., Morgello, S., Mindt, M.R., Taylor, M.J., Marcotte, T.D., Atkinson, J.H., Wolfson, T., Gelman, B.B., McArthur, J.C., Simpson, D.M., Abramson, I., Gamst, A., Fennema-Notestine, C., Jernigan, T.L., Wong, J. Grant, I. CHARTER Group, & HNRC Group (2011). HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: Differences in rates, nature, and predictors. Journal of NeuroVirology, 17, 316.
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. (1995). The HNRC 500neuropsychology of HIV infection at different disease stages. Journal of the International Neuropsychological Society, 1, 231251.
Heaton, R.K., Marcotte, T.D., Mindt, M.R., Sadek, J., Moore, D.J., Bentley, H., McCutchan, J.A., Reicks, C., Grant, I., & HNRC Group (2004). The impact of HIV-associated neuropsychological impairment on everyday functioning. Journal of the International Neuropsychological Society, 10, 317331. doi:10.1017/S1355617704102130
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.
Heaton, R.K., Taylor, M., & Manly, J. (2003). Demographic effects and use of demographically corrected norms with the WAIS-III and WMS-III. Clinical interpretation of the WAIS-III and WMS-III, 181.
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 abuse. AIDS, 18 Suppl 1, S19–S25.
Hollingshead, A.B. (1975). Four Factor Index of Social Status. Unpublished manuscript, New Haven, CT: Department of Sociology, Yale University.
Iudicello, J.E., Hussain, M.A., Watson, C.W.M., Morgan, E.E., & Heaton, R.K. (2019). HIV-associated neurocognitive disorders, In Stern, R.A. & Alosco, M.L. (Eds.), Oxford Handbook of Adult Cognitive Disorders (pp. 2960). New York: Oxford University Press. doi:10.1093/oxfordhb/9780190664121.013.3
Jansen, J.F., Backes, W.H., Nicolay, K., & Kooi, M.E. (2006). 1H MR spectroscopy of the brain: Absolute quantification of metabolites. Radiology, 240, 318332. doi:10.1148/radiol.2402050314
Jernigan, T.L., Archibald, S.L., Fennema-Notestine, C., Taylor, M.J., Theilmann, R.J., Julaton, M.D., Notestine, R.J., Wolfson, T., Letendre, S.L., Ellis, R.J., Heaton, R.K., Gamst, A.C., Franklin, D.R. Jr., Clifford, D.B., Collier, A.C., Gelman, B.B., Marra, C., McArthur, J.C., McCutchan, J.A., Morgello, S., Simpson, D.M., Grant, I., & CHARTER Group (2011). Clinical factors related to brain structure in HIV: The CHARTER study. Journal of NeuroVirology, 17, 248257. doi:10.1007/s13365-011-0032-7
Kabuba, N., Anitha Menon, J., Franklin, D.R. Jr., Heaton, R.K., & Hestad, K.A. (2017). Use of western neuropsychological test battery in detecting HIV-associated neurocognitive disorders (HAND) in Zambia. AIDS and Behavior, 21, 17171727. doi:10.1007/s10461-016-1443-5
Kallianpur, K.J., Shikuma, C., Kirk, G.R., Shiramizu, B., Valcour, V., Chow, D., Souza, S., Nakamoto, B., & Sailasuta, N. (2013). Peripheral blood HIV DNA is associated with atrophy of cerebellar and subcortical gray matter. Neurology, 80, 17921799. doi:10.1212/WNL.0b013e318291903f
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 Syndromes, 60, 234243. doi:10.1097/QAI.0b013e318256f3bc
Kanmogne, G.D., Kuate, C.T., Cysique, L.A., Fonsah, J.Y., Eta, S., Doh, R., Njamnshi, D.M., Nchindap, E., Franklin, D.R. Jr., Ellis, R.J., McCutchan, J.A., Binam, F., Mbanya, D., Heaton, R.K., & Njamnshi, A.K. (2010). HIV-associated neurocognitive disorders in sub-Saharan Africa: A pilot study in Cameroon. BMC Neurology, 10, 60. doi:10.1186/1471-2377-10-60
Lake, J.E., Popov, M., Post, W.S., Palella, F.J., Sacktor, N., Miller, E.N., Brown, T.T., & Becker, J.T. (2017). Visceral fat is associated with brain structure independent of human immunodeficiency virus infection status. Journal of Neurovirology, 23, 385393.
Lawton, M.P., & Brody, E.M. (1969). Assessment of older people: Self-maintaining and instrumental activities of daily living. The Gerontologist, 9, 179186.
Lentz, M.R., Kim, W.K., Kim, H., Soulas, C., Lee, V., Venna, N., Halpern, E.F., Rosenberg, E.S., Williams, K., & González, R.G. (2011). Alterations in brain metabolism during the first year of HIV infection. Journal of NeuroVirology, 17, 220229. doi:10.1007/s13365-011-0030-9
Maki, P.M., Rubin, L.H., Valcour, V., Martin, E., Crystal, H., Young, M., Weber, K.M., Manly, J., Richardson, J., Alden, C., & Anastos, K. (2015). Cognitive function in women with HIV findings from the women’s interagency HIV study. Neurology, 84, 231240.
Masters, M.C. & Ances, B.M. (2014). Role of neuroimaging in HIV associated neurocognitive disorders (HAND). Seminars in Neurology, 34, 89102. doi:10.1055/s-0034-1372346
Meyer, A.C., Boscardin, W.J., Kwasa, J.K., & Price, R.W. (2013). Is it time to rethink how neuropsychological tests are used to diagnose mild forms of HIV-associated neurocognitive disorders? Impact of false-positive rates on prevalence and power. Neuroepidemiology, 41, 208216. doi:10.1159/000354629
Mohamed, M., Barker, P.B., Skolasky, R.L., & Sacktor, N. (2018). 7T Brain MRS in HIV infection: Correlation with cognitive impairment and performance on neuropsychological tests. American Journal of Neuroradiology, 39, 704712. doi:10.3174/ajnr.A5547
Mohamed, M., Barker, P.B., Skolasky, R.L., Selnes, O.A., Moxley, R., Pomper, M., & Sacktor, N. (2010). Brain metabolism and cognitive impairment in HIV infection: A 3 Tesla magnetic resonance spectroscopy Study. Magnetic Resonance Imaging, 28, 12511257. doi:10.1016/j.mri.2010.06.007
Mohamed, M.A., Lentz, M.R., Lee, V., Halpern, E.F., Sacktor, N., Selnes, O., Barker, P.B., & Pomper, M.G. (2010). Factor analysis of proton MR spectroscopic imaging data in HIV infection: Metabolite-derived factors help identify infection and dementia. Radiology, 254, 577586. doi:10.1148/radiol.09081867
Morgan, E.E., Woods, S.P., Smith, C., Weber, E., Scott, J.C., & Grant, I. (2012). Lower cognitive reserve among individuals with syndromic HIV-associated neurocognitive disorders (HAND). AIDS and Behavior, 16, 22792285. doi:10.1007/s10461-012-0229-7
Nichols, M.J., Gates, T.M., Soares, J.R., Moffat, K.J., Rae, C.D., Brew, B.J., & Cysique, L.A. (2019). Atrophic brain signatures of mild forms of neurocognitive impairment in virally suppressed HIV infection. AIDS, 33, 5566.
Norman, M.A., Moore, D.J., Taylor, M., Franklin, D. Jr., Cysique, L., Ake, C., Lazarretto, D., Vaida, F., Heaton, R.K., & HNRC Group. (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 and Experimental Neuropsycholgy, 33, 793804. doi:10.1080/13803395.2011.559157
O’Connor, E.E., Zeffiro, T.A., & Zeffiro, T.A. (2018). Brain structural changes following HIV infection: Meta-analysis. American Journal of Neuroradiology, 39, 5462. doi:10.3174/ajnr.A5432
Olsen, J.P., Fellows, R.P., Rivera-Mindt, M., Morgello, S., Byrd, D.A., & Bank, M.H.B. (2015). Reading ability as an estimator of premorbid intelligence: Does it remain stable among ethnically diverse HIV+ adults? The Clinical Neuropsychologist, 29, 10341052.
Patel, S.H., Kolson, D.L., Glosser, G., Matozzo, I., Ge, Y., Babb, J.S., Mannon, L.J., Grossman, R.I. (2002). Correlation between percentage of brain parenchymal volume and neurocognitive performance in HIV-infected patients. American Journal of Neuroradiology, 23, 543549.
Patel, S.M., Thames, A.D., Arbid, N., Panos, S.E., Castellon, S., & Hinkin, C.H. (2013). The aggregate effects of multiple comorbid risk factors on cognition among HIV-infected individuals. Journal of Clinical Experimental Neuropsycholgy, 35, 421434. doi:10.1080/13803395.2013.783000
Paul, R.H., Ernst, T., Brickman, A.M., Yiannoutsos, C.T., Tate, D.F., Cohen, R.A., & Navia, B.A. (2008). Relative sensitivity of magnetic resonance spectroscopy and quantitative magnetic resonance imaging to cognitive function among nondemented individuals infected with HIV. Journal of the International Neuropsychological Society, 14, 725733.
Provencher, S.W. (2001). Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR in Biomedicine, 14, 260264.
Saloner, R., & Cysique, L.A. (2017). HIV-associated neurocognitive disorders: A global perspective. Journal of the International Neuropsychological Society, 23, 860869.
Saloner, R., Heaton, R.K., Campbell, L.M., Chen, A., Franklin, D. Jr., Ellis, R.J., Collier, A.C., Marra, C., Clifford, D.B., Gelman, B., Sacktor, N., Morgello, S., McCutchan, J.A., Letendre, S., Grant, I., & Fennema-Notestine, C. (2019). Effects of comorbidity burden and age on brain integrity in HIV. AIDS, 33, 11751185. doi: 10.1097/QAD.0000000000002192
Stern, R.A., Silva, S.G., Chaisson, N., & Evans, D.L. (1996). Influence of cognitive reserve on neuropsychological functioning in asymptomatic human immunodeficiency virus-1 infection. Archives of Neurology, 53, 148153.
Thames, A.D., Foley, J.M., Wright, M.J., Panos, S.E., Ettenhofer, M., Ramezani, A., Streiff, V., El-Saden, S., Goodwin, S., Bookheimer, S.Y., &Hinkin, C.H. (2012). Basal ganglia structures differentially contribute to verbal fluency: evidence from Human Immunodeficiency Virus (HIV)-infected adults. Neuropsychologia, 50, 390395. doi:10.1016/j.neuropsychologia.2011.12.010
Thompson, P.M., Dutton, R.A., Hayashi, K.M., Toga, A.W., Lopez, O.L., Aizenstein, H.J., & Becker, J.T. (2005). Thinning of the cerebral cortex visualized in HIV/AIDS reflects CD4+ T lymphocyte decline. Proceedings of the National Academy of Sciences of the United States of America, 102, 1564715652. doi:10.1073/pnas.0502548102
Torti, C., Focà, E., Cesana, B.M., & Lescure, F.X. (2011). Asymptomatic neurocognitive disorders in patients infected by HIV: Fact or fiction? BMC Medicine, 9, 138.
Towgood, K.J., Pitkanen, M., Kulasegaram, R., Fradera, A., Kumar, A., Soni, S., Sibtain, N.A., Reed, L., Bradbeer, C., Barker, G.J., & Kopelman, M.D. (2012). Mapping the brain in younger and older asymptomatic HIV-1 men: Frontal volume changes in the absence of other cortical or diffusion tensor abnormalities. Cortex, 48, 230241. doi:10.1016/j.cortex.2011.03.006
Tozzi, V., Balestra, P., Bellagamba, R., Corpolongo, A., Salvatori, M.F., Visco-Comandini, U., Vlassi, C., Giulianelli, M., Galgani, S., Antinori, A., & Narciso, P. (2007). Persistence of neuropsychologic deficits despite long-term highly active antiretroviral therapy in patients with HIV-related neurocognitive impairment: Prevalence and risk factors. Journal of Acquired Immune Deficiency Syndromes, 45, 174182.
Valcour, V., Chalermchai, T., Sailasuta, N., Marovich, M., Lerdlum, S., Suttichom, D., Suwanwela, N.C., Jagodzinski, L., Michael, N., Spudich, S., van Griensven, F., de Souza, M., Kim, J., Ananworanich, J., & RV254/SEARCH 010 Study Group (2012). Central nervous system viral invasion and inflammation during acute HIV infection. Journal of Infectious Diseases, 206, 275282. doi:10.1093/infdis/jis326
Wilkinson, G. (1993). Wide Range Achievement Test 3—Administration Manual. Wilmington, DE: Jastak Associates, Inc.
Woods, S.P., Rippeth, J.D., Frol, A.B., Levy, J.K., Ryan, E., Soukup, V.M., Hinkin, C.H., Lazzaretto, D., Cherner, M., Marcotte, T.D., Gelman, B.B., Morgello, S., Singer, E.J., Grant, I., & Heaton, R.K. (2004). Interrater reliability of clinical ratings and neurocognitive diagnoses in HIV. Journal of Clinical and Experimental Neuropsycholgy, 26, 759778. doi:10.1080/13803390490509565
World Health Organization (1997). Composite International Diagnostic Interview (CIDI, version 2.1). Geneva, Switzerland: World Health Organization.


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Campbell et al. supplementary material
Campbell et al. supplementary material

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Use of Neuroimaging to Inform Optimal Neurocognitive Criteria for Detecting HIV-Associated Brain Abnormalities

  • Laura M. Campbell (a1) (a2), Christine Fennema-Notestine (a2) (a3), Rowan Saloner (a1) (a2), Mariam Hussain (a1) (a2), Anna Chen (a2), Donald Franklin (a2), Anya Umlauf (a2), Ronald J. Ellis (a2), Ann C. Collier (a4), Christina M. Marra (a5), David B. Clifford (a6), Benjamin B. Gelman (a7), Ned Sacktor (a8), Susan Morgello (a9), J. Allen McCutchan (a10), Scott Letendre (a2) (a10), Igor Grant (a2), Robert K. Heaton (a2) and for the CHARTER Group...


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