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Neuroimaging studies of the aging HIV-1-infected brain

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Abstract

Highly active antiretroviral therapy (HAART) has increased life expectancy among HIV-infected individuals, and by 2015, at least half of all HIV-infected individuals will be over 50 years of age. Neurodegenerative processes associated with aging may be facilitated by HIV-1 infection, resulting in premature brain aging. This review will highlight brain abnormalities in HIV patients in the setting of aging, focusing on recent neuroimaging studies of the structural, physiological, functional and neurochemical changes. Magnetic resonance imaging (MRI) and magnetic resonance spectroscopy studies performed during the pre-HAART era or on antiretroviral-naive subjects suggest an accelerated aging process, while those on HAART-treated subjects suggest premature brain atrophy. Diffusion tensor imaging studies yielded conflicting findings on the relationship between HIV and age in neuroasymptomatic individuals. Functional MRI studies found evidence of premature or accelerated aging processes in the brains of HIV subjects. Lastly, many age-related illnesses such as diabetes, stroke, and depression, as well as comorbid substance abuse, may further exacerbate the aging process in the HIV-infected brain, leading to premature or accelerated age-related brain changes. Given the different pathologic or physiologic changes in the brain assessed by the different neuroimaging techniques, using a multimodal approach in longitudinal follow-up studies is recommended for future studies.

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References

  • Ances BM, Vaida F, Yeh MJ, Liang CL, Buxton RB, Letendre S, McCutchan JA, Ellis RJ (2010) HIV infection and aging independently affect brain function as measured by functional magnetic resonance imaging. J Infect Dis 201:336–340

    Article  PubMed  Google Scholar 

  • Ances BM, Vaida F, Cherner M, Yeh MJ, Liang CL, Gardner C, Grant I, Ellis RJ, Buxton RB (2011) HIV and chronic methamphetamine dependence affect cerebral blood flow. J Neuroimmune Pharmacol 6:409–419

    Article  PubMed  Google Scholar 

  • Ances BM, Benzinger TL, Christensen JJ, Thomas J, Venkat R, Teshome M, Aldea P, Fagan AM, Holtzman DM, Morris JC, Clifford DB (2012a) 11C-PiB imaging of human immunodeficiency virus-associated neurocognitive disorder. Arch Neurol 69:72–77

    Article  PubMed  Google Scholar 

  • Ances BM, Ortega M, Vaida F, Heaps J, Paul R (2012b) Independent effects of HIV, aging, and HAART on brain volumetric measures. J Acquir Immune Defic Syndr 59:469–477

    Article  PubMed  Google Scholar 

  • Antinori A, Arendt G, Becker JT, Brew BJ, Byrd DA, Cherner M, Clifford DB, Cinque P, Epstein LG, Goodkin K, Gisslen M, Grant I, Heaton RK, Joseph J, Marder K, Marra CM, McArthur JC, Nunn M, Price RW, Pulliam L, Robertson KR, Sacktor N, Valcour V, Wojna VE (2007) Updated research nosology for HIV-associated neurocognitive disorders. Neurology 69:1789–1799

    Article  PubMed  CAS  Google Scholar 

  • Archibald SL, Masliah E, Fennema-Notestine C, Marcotte TD, Ellis RJ, McCutchan JA, Heaton RK, Grant I, Mallory M, Miller A, Jernigan TL (2004) Correlation of in vivo neuroimaging abnormalities with postmortem human immunodeficiency virus encephalitis and dendritic loss. Arch Neurol 61:369–376

    Article  PubMed  Google Scholar 

  • Arthurs OJ, Boniface S (2002) How well do we understand the neural origins of the fMRI BOLD signal? Trends Neurosci 25:27–31

    Article  PubMed  CAS  Google Scholar 

  • Becker JT, Maruca V, Kingsley LA, Sanders JM, Alger JR, Barker PB, Goodkin K, Martin E, Miller EN, Ragin A, Sacktor N, Selnes O (2011) Factors affecting brain structure in men with HIV disease in the post-HAART era. Neuroradiology 54:113–121

    Article  PubMed  Google Scholar 

  • Bell J (1998) The neuropathology of adult HIV infection. Rev Neurol 154:816–829

    PubMed  CAS  Google Scholar 

  • Bonacini M (2011) Alcohol use among patients with HIV infection. Ann Hepatol 10:502–507

    PubMed  CAS  Google Scholar 

  • Brew BJ, Crowe SM, Landay A, Cysique LA, Guillemin G (2009) Neurodegeneration and ageing in the HAART era. J Neuroimmune Pharmacol 4:163–174

    Article  PubMed  Google Scholar 

  • Brown TT, Cole SR, Li X, Kingsley LA, Palella FJ, Riddler SA, Visscher BR, Margolick JB, Dobs AS (2005) Antiretroviral therapy and the prevalence and incidence of diabetes mellitus in the multicenter AIDS cohort study. Arch Intern Med 165:1179–1184

    Article  PubMed  Google Scholar 

  • Cardenas VA, Meyerhoff DJ, Studholme C, Kornak J, Rothlind J, Lampiris H, Neuhaus J, Grant RM, Chao LL, Truran D, Weiner MW (2009) Evidence for ongoing brain injury in human immunodeficiency virus-positive patients treated with antiretroviral therapy. J Neurovirol 15:324–333

    Article  PubMed  CAS  Google Scholar 

  • Carr A, Samaras K, Thorisdottir A, Kaufmann GR, Chisholm DJ, Cooper DA (1999) Diagnosis, prediction, and natural course of HIV-1 protease-inhibitor-associated lipodystrophy, hyperlipidaemia, and diabetes mellitus: a cohort study. Lancet 353:2093–2099

    Article  PubMed  CAS  Google Scholar 

  • Catani M, Cherubini A, Howard R, Tarducci R, Pelliccioli GP, Piccirilli M, Gobbi G, Senin U, Mecocci P (2001) (1)H-MR spectroscopy differentiates mild cognitive impairment from normal brain aging. Neuroreport 12:2315–2317

    Article  PubMed  CAS  Google Scholar 

  • Chang L, Ernst T, Poland RE, Jenden DJ (1996) In vivo proton magnetic resonance spectroscopy of the normal aging human brain. Life Sci 58:2049–2056

    Article  PubMed  CAS  Google Scholar 

  • Chang L, Speck O, Miller EN, Braun J, Jovicich J, Koch C, Itti L, Ernst T (2001) Neural correlates of attention and working memory deficits in HIV patients. Neurology 57:1001–1007

    Article  PubMed  CAS  Google Scholar 

  • Chang L, Ernst T, Witt MD, Ames N, Gaiefsky M, Miller E (2002) Relationships among brain metabolites, cognitive function, and viral loads in antiretroviral-naive HIV patients. Neuroimage 17:1638–1648

    Article  PubMed  Google Scholar 

  • Chang L, Lee PL, Yiannoutsos CT, Ernst T, Marra CM, Richards T, Kolson D, Schifitto G, Jarvik JG, Miller EN, Lenkinski R, Gonzalez G, Navia BA (2004a) A multicenter in vivo proton-MRS study of HIV-associated dementia and its relationship to age. Neuroimage 23:1336–1347

    Article  PubMed  CAS  Google Scholar 

  • Chang L, Tomasi D, Yakupov R, Lozar C, Arnold S, Caparelli E, Ernst T (2004b) Adaptation of the attention network in human immunodeficiency virus brain injury. Ann Neurol 56:259–272

    Article  PubMed  Google Scholar 

  • Chang L, Cloak C, Patterson K, Grob C, Miller EN, Ernst T (2005a) Enlarged striatum in abstinent methamphetamine abusers: a possible compensatory response. Biol Psychiatry 57:967–974

    Article  PubMed  CAS  Google Scholar 

  • Chang L, Ernst T, Speck O, Grob CS (2005b) Additive effects of HIV and chronic methamphetamine use on brain metabolite abnormalities. Am J Psychiatry 162:361–369

    Article  PubMed  Google Scholar 

  • Chang L, Cloak C, Yakupov R, Ernst T (2006) Combined and independent effects of chronic marijuana use and HIV on brain metabolites. J Neuroimmune Pharmacol 1:65–76

    Article  PubMed  CAS  Google Scholar 

  • Chang L, Wong V, Nakama H, Watters M, Ramones D, Miller EN, Cloak C, Ernst T (2008a) Greater than age-related changes in brain diffusion of HIV patients after 1 year. J Neuroimmune Pharmacol 3:265–274

    Article  PubMed  Google Scholar 

  • Chang L, Yakupov R, Nakama H, Stokes B, Ernst T (2008b) Antiretroviral treatment is associated with increased attentional load-dependent brain activation in HIV patients. J Neuroimmune Pharmacol 3:95–104

    Article  PubMed  CAS  Google Scholar 

  • Chang L, Andres M, Sadino J, Jiang CS, Nakama H, Miller E, Ernst T (2011) Impact of apolipoprotein E epsilon4 and HIV on cognition and brain atrophy: antagonistic pleiotropy and premature brain aging. Neuroimage 58:1017–1027

    Article  PubMed  CAS  Google Scholar 

  • Chang L, Feger U, Ernst T (2012) Bioimaging. In: Gendelman H, Grant I, Everall IP, Fox HS, Gelbard HA, Lipton SA, Swindells S (eds) The neurology of AIDS. Oxford University Press, New York, pp 763–797

    Google Scholar 

  • Chiang MC, Dutton RA, Hayashi KM, Lopez OL, Aizenstein HJ, Toga AW, Becker JT, Thompson PM (2007) 3D pattern of brain atrophy in HIV/AIDS visualized using tensor-based morphometry. Neuroimage 34:44–60

    Article  PubMed  Google Scholar 

  • Cole JW, Pinto AN, Hebel JR, Buchholz DW, Earley CJ, Johnson CJ, Macko RF, Price TR, Sloan MA, Stern BJ, Wityk RJ, Wozniak MA, Kittner SJ (2004) Acquired immunodeficiency syndrome and the risk of stroke. Stroke 35:51–56

    Article  PubMed  Google Scholar 

  • Dagan T, Sable C, Bray J, Gerschenson M (2002) Mitochondrial dysfunction and antiretroviral nucleoside analog toxicities: what is the evidence? Mitochondrion 1:397–412

    Article  PubMed  CAS  Google Scholar 

  • Deeks SG (2011) HIV infection, inflammation, immunosenescence, and aging. Annu Rev Med 62:141–155

    Article  PubMed  CAS  Google Scholar 

  • den Heijer T, Vermeer SE, van Dijk EJ, Prins ND, Koudstaal PJ, Hofman A, Breteler MM (2003) Type 2 diabetes and atrophy of medial temporal lobe structures on brain MRI. Diabetologia 46:1604–1610

    Article  Google Scholar 

  • Dever LL, Oruwari PA, Figueroa WE, O'Donovan CA, Eng RH (2000) Hyperglycemia associated with protease inhibitors in an urban HIV-infected minority patient population. Ann Pharmacother 34:580–584

    Article  PubMed  CAS  Google Scholar 

  • Dewey J, Hana G, Russell T, Price J, McCaffrey D, Harezlak J, Sem E, Anyanwu JC, Guttmann CR, Navia B, Cohen R, Tate DF (2010) Reliability and validity of MRI-based automated volumetry software relative to auto-assisted manual measurement of subcortical structures in HIV-infected patients from a multisite study. Neuroimage 51:1334–1344

    Article  PubMed  Google Scholar 

  • Effros RB, Fletcher CV, Gebo K, Halter JB, Hazzard WR, Horne FM, Huebner RE, Janoff EN, Justice AC, Kuritzkes D, Nayfield SG, Plaeger SF, Schmader KE, Ashworth JR, Campanelli C, Clayton CP, Rada B, Woolard NF, High KP (2008) Aging and infectious diseases: workshop on HIV infection and aging: what is known and future research directions. Clin Infect Dis 47:542–553

    Article  PubMed  Google Scholar 

  • Ernst T, Chang L (2004) Effect of aging on brain metabolism in antiretroviral-naive HIV patients. AIDS 18(Suppl 1):S61–S67

    PubMed  CAS  Google Scholar 

  • Ernst T, Chang L, Jovicich J, Ames N, Arnold S (2002) Abnormal brain activation on functional MRI in cognitively asymptomatic HIV patients. Neurology 59:1343–1349

    Article  PubMed  CAS  Google Scholar 

  • Ernst T, Chang L, Arnold S (2003) Increased glial metabolites predict increased working memory network activation in HIV brain injury. Neuroimage 19:1686–1693

    Article  PubMed  CAS  Google Scholar 

  • Ernst T, Yakupov R, Nakama H, Crocket G, Cole M, Watters M, Ricardo-Dukelow ML, Chang L (2009) Declined neural efficiency in cognitively stable human immunodeficiency virus patients. Ann Neurol 65:316–325

    Article  PubMed  Google Scholar 

  • Ernst T, Jiang CS, 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. J Magn Reson Imaging 32:1045–1053

    Article  PubMed  Google Scholar 

  • Everall I, Luther P, Lantos P (1993) A review of neuronal damage in human immunodeficiency virus infection: its assessment, possible mechanism and relationship to dementia. J Neuropathol 52:561–566

    Article  CAS  Google Scholar 

  • Ghafouri M, Amini S, Khalili K, Sawaya BE (2006) HIV-1 associated dementia: symptoms and causes. Retrovirology 3:28

    Article  PubMed  Google Scholar 

  • Gongvatana A, Cohen RA, Correia S, Devlin KN, Miles J, Kang H, Ombao H, Navia B, Laidlaw DH, Tashima KT (2011) Clinical contributors to cerebral white matter integrity in HIV-infected individuals. J Neurovirol 17:477–486

    Article  PubMed  Google Scholar 

  • Gorelick PB, Scuteri A, Black SE, Decarli C, Greenberg SM, Iadecola C, Launer LJ, Laurent S, Lopez OL, Nyenhuis D, Petersen RC, Schneider JA, Tzourio C, Arnett DK, Bennett DA, Chui HC, Higashida RT, Lindquist R, Nilsson PM, Roman GC, Sellke FW, Seshadri S (2011) Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 42:2672–2713

    Article  PubMed  Google Scholar 

  • Gray F, Scaravilli F, Everall I, Chretien F, An S, Boche D, Adle-Biassette H, Wingertsmann L, Durigon M, Hurtrel B, Chiodi F, Bell J, Lantos P (1996) Neuropathology of early HIV-1 infection. Brain Pathol 6:1–15

    Article  PubMed  CAS  Google Scholar 

  • Haase AT (1986) Pathogenesis of lentivirus infections. Nature 322:130–136

    Article  PubMed  CAS  Google Scholar 

  • Harezlak J, Buchthal S, Taylor M, Schifitto G, Zhong J, Daar E, Alger J, Singer E, Campbell T, Yiannoutsos C, Cohen R, Navia B (2011) Persistence of HIV-associated cognitive impairment, inflammation, and neuronal injury in era of highly active antiretroviral treatment. AIDS 25:625–633

    Article  PubMed  CAS  Google Scholar 

  • Jernigan TL, Gamst AC, Archibald SL, Fennema-Notestine C, Mindt MR, Marcotte TD, Heaton RK, Ellis RJ, Grant I (2005) Effects of methamphetamine dependence and HIV infection on cerebral morphology. Am J Psychiatry 162:1461–1472

    Article  PubMed  Google Scholar 

  • Kaul M, Zheng J, Okamoto S, Gendelman HE, Lipton SA (2005) HIV-1 infection and AIDS: consequences for the central nervous system. Cell Death Differ 12(Suppl 1):878–892

    Article  PubMed  CAS  Google Scholar 

  • Langford D, Adame A, Grigorian A, Grant I, McCutchan JA, Ellis RJ, Marcotte TD, Masliah E (2003) Patterns of selective neuronal damage in methamphetamine-user AIDS patients. J Acquir Immune Defic Syndr 34:467–474

    Article  PubMed  CAS  Google Scholar 

  • Lepore N, Brun C, Chou YY, Chiang MC, Dutton RA, Hayashi KM, Luders E, Lopez OL, Aizenstein HJ, Toga AW, Becker JT, Thompson PM (2008) Generalized tensor-based morphometry of HIV/AIDS using multivariate statistics on deformation tensors. IEEE Trans Med Imaging 27:129–141

    Article  PubMed  CAS  Google Scholar 

  • Lim KO, Helpern JA (2002) Neuropsychiatric applications of DTI—a review. NMR Biomed 15:587–593

    Article  PubMed  CAS  Google Scholar 

  • Madden DJ, Spaniol J, Whiting WL, Bucur B, Provenzale JM, Cabeza R, White LE, Huettel SA (2007) Adult age differences in the functional neuroanatomy of visual attention: a combined fMRI and DTI study. Neurobiol Aging 28:459–476

    Article  PubMed  Google Scholar 

  • McBean AM, Li S, Gilbertson DT, Collins AJ (2004) Differences in diabetes prevalence, incidence, and mortality among the elderly of four racial/ethnic groups: Whites, Blacks, Hispanics, and Asians. Diabetes Care 27:2317–2324

    Article  PubMed  Google Scholar 

  • Nakama H, Chang L, Fein G, Shimotsu R, Jiang CS, Ernst T (2011) Methamphetamine users show greater than normal age-related cortical gray matter loss. Addiction 106:1474–1483

    Article  PubMed  Google Scholar 

  • Navia BA, Cho ES, Petito CK, Price RW (1986) The AIDS dementia complex: II. Neuropathology. Ann Neurol 19:525–535

    Article  PubMed  CAS  Google Scholar 

  • Ostrow DG (1994) Substance abuse and HIV infection. Psychiatr Clin North Am 17:69–89

    PubMed  CAS  Google Scholar 

  • Ovbiagele B, Nath A (2011) Increasing incidence of ischemic stroke in patients with HIV infection. Neurology 76:444–450

    Article  PubMed  Google Scholar 

  • Palacios R, Merchante N, Macias J, Gonzalez M, Castillo J, Ruiz J, Marquez M, Gomez-Mateos J, Pineda JA, Santos J (2006) Incidence of and risk factors for insulin resistance in treatment-naive HIV-infected patients 48 weeks after starting highly active antiretroviral therapy. Antivir Ther 11:529–535

    PubMed  CAS  Google Scholar 

  • Pfefferbaum A, Adalsteinsson E, Sullivan EV (2005) Cortical NAA deficits in HIV infection without dementia: influence of alcoholism comorbidity. Neuropsychopharmacology 30:1392–1399

    Article  PubMed  CAS  Google Scholar 

  • Pfefferbaum A, Rosenbloom MJ, Rohlfing T, Adalsteinsson E, Kemper CA, Deresinski S, Sullivan EV (2006) Contribution of alcoholism to brain dysmorphology in HIV infection: effects on the ventricles and corpus callosum. Neuroimage 33:239–251

    Article  PubMed  Google Scholar 

  • Pfefferbaum A, Rosenbloom MJ, Adalsteinsson E, Sullivan EV (2007) Diffusion tensor imaging with quantitative fibre tracking in HIV infection and alcoholism comorbidity: synergistic white matter damage. Brain 130:48–64

    Article  PubMed  Google Scholar 

  • Pfefferbaum A, Rosenbloom MJ, Sassoon SA, Kemper CA, Deresinski S, Rohlfing T, Sullivan EV (2012) Regional brain structural dysmorphology in human immunodeficiency virus infection: effects of acquired immune deficiency syndrome, alcoholism, and age. Biol Psychiatry. doi:10.1016/j.biopsych.2012.02.018

  • Pomara N, Crandall D, Choi S, Johnson G, Lim K (2001) White matter abnormalities in HIV-1 infection: a diffusion tensor imaging study. Psychiatry Res 106:15–24

    Article  PubMed  CAS  Google Scholar 

  • Prentiss D, Power R, Balmas G, Tzuang G, Israelski DM (2004) Patterns of marijuana use among patients with HIV/AIDS followed in a public health care setting. J Acquir Immune Defic Syndr 35:38–45

    Article  PubMed  Google Scholar 

  • Qureshi AI, Janssen RS, Karon JM, Weissman JP, Akbar MS, Safdar K, Frankel MR (1997) Human immunodeficiency virus infection and stroke in young patients. Arch Neurol 54:1150–1153

    Article  PubMed  CAS  Google Scholar 

  • Raz N, Lindenberger U, Rodrigue KM, Kennedy KM, Head D, Williamson A, Dahle C, Gerstorf D, Acker JD (2005) Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb Cortex 15:1676–1689

    Article  PubMed  Google Scholar 

  • Reynolds NR (2009) Cigarette smoking and HIV: more evidence for action. AIDS Educ Prev 21:106–121

    Article  PubMed  Google Scholar 

  • Schneider JA, Aggarwal NT, Barnes L, Boyle P, Bennett DA (2009) The neuropathology of older persons with and without dementia from community versus clinic cohorts. J Alzheimers Dis 18:691–701

    PubMed  Google Scholar 

  • Schuitemaker A, van der Doef TF, Boellaard R, van der Flier WM, Yaqub M, Windhorst AD, Barkhof F, Jonker C, Kloet RW, Lammertsma AA, Scheltens P, van Berckel BN (2012) Microglial activation in healthy aging. Neurobiol Aging 33:1067–1072

    Article  PubMed  CAS  Google Scholar 

  • Smith GH (2005) Opening statement of Senator Gordon H. Smith. Aging hearing: HIV over fifty, exploring the new threat. Senate Committee on Aging, Washington, DC, U.S. Government Printing Office

    Google Scholar 

  • Sowell ER, Peterson BS, Thompson PM, Welcome SE, Henkenius AL, Toga AW (2003) Mapping cortical change across the human life span. Nat Neurosci 6:309–315

    Article  PubMed  CAS  Google Scholar 

  • Sowell ER, Thompson PM, Toga AW (2004) Mapping changes in the human cortex throughout the span of life. Neuroscientist 10:372–392

    Article  PubMed  Google Scholar 

  • Stout JC, Ellis RJ, Jernigan TL, Archibald SL, Abramson I, Wolfson T, McCutchan JA, Wallace MR, Atkinson JH, Grant I (1998) Progressive cerebral volume loss in human immunodeficiency virus infection: a longitudinal volumetric magnetic resonance imaging study. HIV Neurobehavioral Research Center Group. Arch Neurol 55:161–168

    Article  PubMed  CAS  Google Scholar 

  • Streit WJ, Xue QS (2010) The brain's aging immune system. Aging Dis 1:254–261

    PubMed  Google Scholar 

  • Taylor MJ, Letendre SL, Schweinsburg BC, Alhassoon OM, Brown GG, Gongvatana A, Grant I (2004) Hepatitis C virus infection is associated with reduced white matter N-acetylaspartate in abstinent methamphetamine users. J Int Neuropsychol Soc 10:110–113

    PubMed  CAS  Google Scholar 

  • Thames AD, Foley J, Panos SE, Singer EJ, Patel SM, El-Saden S, Hinkin CH (2011) Past stimulant abuse is associated with reduced basal ganglia and hippocampal integrity in older HIV+ adults: a diffusion tensor imaging study. J AIDS Clinic Res 2:129. doi:10.4172/2155-6113.1000129

  • Tiehuis AM, van der Graaf Y, Visseren FL, Vincken KL, Biessels GJ, Appelman AP, Kappelle LJ, Mali WP (2008) Diabetes increases atrophy and vascular lesions on brain MRI in patients with symptomatic arterial disease. Stroke 39:1600–1603

    Article  PubMed  Google Scholar 

  • Tipping B, de Villiers L, Wainwright H, Candy S, Bryer A (2007) Stroke in patients with human immunodeficiency virus infection. J Neurol Neurosurg Psychiatry 78:1320–1324

    Article  PubMed  Google Scholar 

  • Tomasi D, Ernst T, Caparelli EC, Chang L (2006) Common deactivation patterns during working memory and visual attention tasks: an intra-subject fMRI study at 4 Tesla. Hum Brain Mapp 27:694–705

    Article  PubMed  Google Scholar 

  • Towgood KJ, Pitkanen M, Kulasegaram R, Fradera A, Kumar A, Soni S, Sibtain NA, Reed L, Bradbeer C, Barker GJ, Kopelman MD (2011) 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 48:230–241

    Article  PubMed  Google Scholar 

  • Tyler LK, Wright P, Randall B, Marslen-Wilson WD, Stamatakis EA (2010) Reorganization of syntactic processing following left-hemisphere brain damage: does right-hemisphere activity preserve function? Brain 133:3396–3408

    Article  PubMed  Google Scholar 

  • Vink D, Aartsen MJ, Comijs HC, Heymans MW, Penninx BW, Stek ML, Deeg DJ, Beekman AT (2009) Onset of anxiety and depression in the aging population: comparison of risk factors in a 9-year prospective study. Am J Geriatr Psychiatry 17:642–652

    Article  PubMed  Google Scholar 

  • Walli R, Goebel FD, Demant T (1998) Impaired glucose tolerance and protease inhibitors. Ann Intern Med 129:837–838

    PubMed  CAS  Google Scholar 

  • Woods SP, Moore DJ, Weber E, Grant I (2009) Cognitive neuropsychology of HIV-associated neurocognitive disorders. Neuropsychol Rev 19:152–168

    Article  PubMed  Google Scholar 

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Holt, J.L., Kraft-Terry, S.D. & Chang, L. Neuroimaging studies of the aging HIV-1-infected brain. J. Neurovirol. 18, 291–302 (2012). https://doi.org/10.1007/s13365-012-0114-1

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