Skip to main content

Advertisement

SpringerLink
Log in

The current understanding of overlap between characteristics of HIV-associated neurocognitive disorders and Alzheimer’s disease

  • Published:
Journal of NeuroVirology Aims and scope Submit manuscript

Abstract

The advent of effective antiretroviral medications (ARVs) has led to an aging of the HIV population with approximately 50% of people with HIV (PWH) being over the age of 50 years. Neurocognitive complications, typically known as HIV-associated neurocognitive disorders (HAND), persist in the era of ARVs and, in addition to risk of HAND, older PWH are also at risk for age-associated, neurodegenerative disorders including Alzheimer’s disease (AD). It has been postulated that risk for AD may be greater among PWH due to potential compounding effects of HIV and aging on mechanisms of neural insult. We are now faced with the challenge of disentangling AD from HAND, which has important prognostic and treatment implications given the more rapidly debilitating trajectory of AD. Herein, we review the evidence to date demonstrating both parallels and differences in the profiles of HAND and AD. We specifically address similarities and difference of AD and HAND as it relates to (1) neuropsychological profiles (cross-sectional/longitudinal), (2) AD-associated neuropathological features as evidenced from neuropathological, cerebrospinal fluid and neuroimaging assessments, (3) biological mechanisms underlying cortical amyloid deposition, (4) parallels in mechanisms of neural insult, and (5) common risk factors. Our current understanding of the similarities and dissimilarities of AD and HAND should be further delineated and leveraged in the development of differential diagnostic methods that will allow for the early identification of AD and more suitable and effective treatment interventions among graying PWH.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abdulle S, Mellgren A, Brew BJ, Cinque P, Hagberg L, Price RW, Rosengren L, Gisslen M (2007) CSF neurofilament protein (NFL)—a marker of active HIV-related neurodegeneration. J Neurol 254:1026–1032

    Article  CAS  PubMed  Google Scholar 

  • Abu-Rumeileh S, Capellari S, Stanzani-Maserati M, Polischi B, Martinelli P, Caroppo P, Ladogana A, Parchi P (2018) The CSF neurofilament light signature in rapidly progressive neurodegenerative dementias. Alzheimers Res Ther 10:3

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Achim CL, Adame A, Dumaop W, Everall IP, Masliah E, Neurobehavioral Research C (2009) Increased accumulation of intraneuronal amyloid beta in HIV-infected patients. J NeuroImmune Pharmacol 4:190–199

    Article  PubMed  PubMed Central  Google Scholar 

  • Aksenov MY, Aksenova MV, Mactutus CF, Booze RM (2010) HIV-1 protein-mediated amyloidogenesis in rat hippocampal cell cultures. Neurosci Lett 475:174–178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ances BM, Christensen JJ, Teshome M, Taylor J, Xiong C, Aldea P, Fagan AM, Holtzman DM, Morris JC, Mintun MA, Clifford DB (2010) Cognitively unimpaired HIV-positive subjects do not have increased 11C-PiB: a case-control study. Neurology 75:111–115

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Andras IE, Toborek M (2013) Amyloid beta accumulation in HIV-1-infected brain: the role of the blood brain barrier. IUBMB Life 65:43–49

    Article  CAS  PubMed  Google Scholar 

  • Anthony IC, Ramage SN, Carnie FW, Simmonds P, Bell JE (2005) Influence of HAART on HIV-related CNS disease and neuroinflammation. J Neuropathol Exp Neurol 64:529–536

    Article  CAS  PubMed  Google Scholar 

  • Anthony IC, Ramage SN, Carnie FW, Simmonds P, Bell JE (2006) Accelerated Tau deposition in the brains of individuals infected with human immunodeficiency virus-1 before and after the advent of highly active anti-retroviral therapy. Acta Neuropathol 111:529–538

    Article  CAS  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  CAS  PubMed  Google Scholar 

  • Antiretroviral Therapy Cohort C (2017) Survival of HIV-positive patients starting antiretroviral therapy between 1996 and 2013: a collaborative analysis of cohort studies. Lancet HIV 4:e349–e356

    Article  Google Scholar 

  • Aukrust P, Muller F, Lien E, Nordoy I, Liabakk NB, Kvale D, Espevik T, Froland SS (1999) Tumor necrosis factor (TNF) system levels in human immunodeficiency virus-infected patients during highly active antiretroviral therapy: persistent TNF activation is associated with virologic and immunologic treatment failure. J Infect Dis 179:74–82

    Article  CAS  PubMed  Google Scholar 

  • Bacioglu M, Maia LF, Preische O, Schelle J, Apel A, Kaeser SA, Schweighauser M, Eninger T, Lambert M, Pilotto A, Shimshek DR, Neumann U, Kahle PJ, Staufenbiel M, Neumann M, Maetzler W, Kuhle J, Jucker M (2016) Neurofilament light chain in blood and CSF as marker of disease progression in mouse models and in neurodegenerative diseases. Neuron 91:56–66

    Article  CAS  PubMed  Google Scholar 

  • Bakkour A, Morris JC, Wolk DA, Dickerson BC (2013) The effects of aging and Alzheimer’s disease on cerebral cortical anatomy: specificity and differential relationships with cognition. Neuroimage 76:332–344

    Article  PubMed  Google Scholar 

  • Banks WA (1999) Physiology and pathology of the blood-brain barrier: implications for microbial pathogenesis, drug delivery and neurodegenerative disorders. J Neuro-Oncol 5:538–555

    CAS  Google Scholar 

  • Bateman RJ, Xiong C, Benzinger TL, Fagan AM, Goate A, Fox NC, Marcus DS, Cairns NJ, Xie X, Blazey TM, Holtzman DM, Santacruz A, Buckles V, Oliver A, Moulder K, Aisen PS, Ghetti B, Klunk WE, McDade E, Martins RN, Masters CL, Mayeux R, Ringman JM, Rossor MN, Schofield PR, Sperling RA, Salloway S, Morris JC, Dominantly Inherited Alzheimer N (2012) Clinical and biomarker changes in dominantly inherited Alzheimer’s disease. N Engl J Med 367:795–804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Becker JT, Caldararo R, Lopez OL, Dew MA, Dorst SK, Banks G (1995) Qualitative features of the memory deficit associated with HIV infection and AIDS: cross-validation of a discriminant function classification scheme. J Clin Exp Neuropsychol 17:134–142

    Article  CAS  PubMed  Google Scholar 

  • Bolmont T, Haiss F, Eicke D, Radde R, Mathis CA, Klunk WE, Kohsaka S, Jucker M, Calhoun ME (2008) Dynamics of the microglial/amyloid interaction indicate a role in plaque maintenance. J Neurosci 28:4283–4292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonnet F, Amieva H, Marquant F, Bernard C, Bruyand M, Dauchy FA, Mercie P, Greib C, Richert L, Neau D, Catheline G, Dehail P, Dabis F, Morlat P, Dartigues JF, Chene G, Cohort SCA (2013) Cognitive disorders in HIV-infected patients: are they HIV-related? AIDS 27:391–400

    Article  PubMed  Google Scholar 

  • Borjabad A, Volsky DJ (2012) Common transcriptional signatures in brain tissue from patients with HIV-associated neurocognitive disorders, Alzheimer’s disease, and multiple sclerosis. J NeuroImmune Pharmacol 7:914–926

    Article  PubMed  PubMed Central  Google Scholar 

  • Bowman GL, Kaye JA, Moore M, Waichunas D, Carlson NE, Quinn JF (2007) Blood-brain barrier impairment in Alzheimer disease: stability and functional significance. Neurology 68:1809–1814

    Article  CAS  PubMed  Google Scholar 

  • Braak H, Braak E, Bohl J, Bratzke H (1998) Evolution of Alzheimer’s disease related cortical lesions. J Neural Transm Suppl 54:97–106

    Article  CAS  PubMed  Google Scholar 

  • Braskie MN, Toga AW, Thompson PM (2013) Recent advances in imaging Alzheimer’s disease. J Alzheimers Dis 33(Suppl 1):S313–S327

    PubMed  PubMed Central  Google Scholar 

  • Brew BJ (2004) Evidence for a change in AIDS dementia complex in the era of highly active antiretroviral therapy and the possibility of new forms of AIDS dementia complex. AIDS 18(Suppl 1):S75–S78

    Article  CAS  PubMed  Google Scholar 

  • Brew BJ, Letendre SL (2008) Biomarkers of HIV related central nervous system disease. Int Rev Psychiatry 20:73–88

    Article  PubMed  Google Scholar 

  • Brew BJ, Pemberton L, Blennow K, Wallin A, Hagberg L (2005) CSF amyloid beta42 and tau levels correlate with AIDS dementia complex. Neurology 65:1490–1492

    Article  CAS  PubMed  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 

  • Brouillette MJ, Yuen T, Fellows LK, Cysique LA, Heaton RK, Mayo NE (2016) Identifying neurocognitive decline at 36 months among HIV-positive participants in the CHARTER cohort using group-based trajectory analysis. PLoS One 11:e0155766

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bryant VE, Whitehead NE, Burrell LE 2nd, Dotson VM, Cook RL, Malloy P, Devlin K, Cohen RA (2015) Depression and apathy among people living with HIV: implications for treatment of HIV associated neurocognitive disorders. AIDS Behav 19:1430–1437

    Article  PubMed  PubMed Central  Google Scholar 

  • Burdo TH, Weiffenbach A, Woods SP, Letendre S, Ellis RJ, Williams KC (2013) Elevated sCD163 in plasma but not cerebrospinal fluid is a marker of neurocognitive impairment in HIV infection. AIDS 27:1387–1395

    Article  CAS  PubMed  Google Scholar 

  • Cameron B, Landreth GE (2010) Inflammation, microglia, and Alzheimer’s disease. Neurobiol Dis 37:503–509

    Article  CAS  PubMed  Google Scholar 

  • CDC (2017) HIV surveillance report, 2016. Centers for Disease Control and Prevention

  • 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  CAS  PubMed  Google Scholar 

  • Chaponda M, Aldhouse N, Kroes M, Wild L, Robinson C, Smith A (2018) Systematic review of the prevalence of psychiatric illness and sleep disturbance as co-morbidities of HIV infection in the UK. Int J STD AIDS 29:704–713

    Article  PubMed  Google Scholar 

  • Clifford DB, Fagan AM, Holtzman DM, Morris JC, Teshome M, Shah AR, Kauwe JS (2009) CSF biomarkers of Alzheimer disease in HIV-associated neurologic disease. Neurology 73:1982–1987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cohen RA, Harezlak J, Gongvatana A, Buchthal S, Schifitto G, Clark U, Paul R, Taylor M, Thompson P, Tate D, Alger J, Brown M, Zhong J, Campbell T, Singer E, Daar E, McMahon D, Tso Y, Yiannoutsos CT, Navia B, Consortium HIVN (2010) Cerebral metabolite abnormalities in human immunodeficiency virus are associated with cortical and subcortical volumes. J Neuro-Oncol 16:435–444

    CAS  Google Scholar 

  • Cohen RA, Seider TR, Navia B (2015) HIV effects on age-associated neurocognitive dysfunction: premature cognitive aging or neurodegenerative disease? Alzheimers Res Ther 7:37

    Article  PubMed  PubMed Central  Google Scholar 

  • Cortes N, Andrade V, Maccioni RB (2018) Behavioral and neuropsychiatric disorders in Alzheimer’s disease. J Alzheimers Dis 63:899–910

    Article  PubMed  Google Scholar 

  • Cysique LA, Maruff P, Bain MP, Wright E, Brew BJ (2011) HIV and age do not substantially interact in HIV-associated neurocognitive impairment. J Neuropsychiatry Clin Neurosci 23:83–89

    Article  PubMed  Google Scholar 

  • de Bruijn RF, Ikram MA (2014) Cardiovascular risk factors and future risk of Alzheimer’s disease. BMC Med 12:130

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deeks SG, Phillips AN (2009) HIV infection, antiretroviral treatment, ageing, and non-AIDS related morbidity. BMJ 338:a3172

    Article  PubMed  Google Scholar 

  • Durand M, Chartrand-Lefebvre C, Baril JG, Trottier S, Trottier B, Harris M, Walmsley S, Conway B, Wong A, Routy JP, Kovacs C, MacPherson PA, Monteith KM, Mansour S, Thanassoulis G, Abrahamowicz M, Zhu Z, Tsoukas C, Ancuta P, Bernard N, Tremblay CL, investigators of the Canadian HIV, Aging Cohort S (2017) The Canadian HIV and aging cohort study—determinants of increased risk of cardio-vascular diseases in HIV-infected individuals: rationale and study protocol. BMC Infect Dis 17:611

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Duskova K, Nagilla P, Le HS, Iyer P, Thalamuthu A, Martinson J, Bar-Joseph Z, Buchanan W, Rinaldo C, Ayyavoo V (2013) MicroRNA regulation and its effects on cellular transcriptome in human immunodeficiency virus-1 (HIV-1) infected individuals with distinct viral load and CD4 cell counts. BMC Infect Dis 13:250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eden A, Price RW, Spudich S, Fuchs D, Hagberg L, Gisslen M (2007) Immune activation of the central nervous system is still present after >4 years of effective highly active antiretroviral therapy. J Infect Dis 196:1779–1783

    Article  CAS  PubMed  Google Scholar 

  • Esiri MM, Biddolph SC, Morris CS (1998) Prevalence of Alzheimer plaques in AIDS. J Neurol Neurosurg Psychiatry 65:29–33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Everall I, Vaida F, Khanlou N, Lazzaretto D, Achim C, Letendre S, Moore D, Ellis R, Cherner M, Gelman B, Morgello S, Singer E, Grant I, Masliah E, National Neuro ATC (2009) Cliniconeuropathologic correlates of human immunodeficiency virus in the era of antiretroviral therapy. J Neuro-Oncol 15:360–370

    CAS  Google Scholar 

  • Fabbiani M, Ciccarelli N, Tana M, Farina S, Baldonero E, Di Cristo V, Colafigli M, Tamburrini E, Cauda R, Silveri MC, Grima P, Di Giambenedetto S (2013) Cardiovascular risk factors and carotid intima-media thickness are associated with lower cognitive performance in HIV-infected patients. HIV Med 14:136–144

    Article  CAS  PubMed  Google Scholar 

  • Fagan AM, Mintun MA, Mach RH, Lee SY, Dence CS, Shah AR, LaRossa GN, Spinner ML, Klunk WE, Mathis CA, DeKosky ST, Morris JC, Holtzman DM (2006) Inverse relation between in vivo amyloid imaging load and cerebrospinal fluid Abeta42 in humans. Ann Neurol 59:512–519

    Article  CAS  PubMed  Google Scholar 

  • Fields JA, Spencer B, Swinton M, Qvale EM, Marquine MJ, Alexeeva A, Gough S, Soontornniyomkij B, Valera E, Masliah E, Achim CL, Desplats P (2018) Alterations in brain TREM2 and amyloid-beta levels are associated with neurocognitive impairment in HIV-infected persons on antiretroviral therapy. J Neurochem

  • Galimberti D, Fenoglio C, Lovati C, Venturelli E, Guidi I, Corra B, Scalabrini D, Clerici F, Mariani C, Bresolin N, Scarpini E (2006) Serum MCP-1 levels are increased in mild cognitive impairment and mild Alzheimer's disease. Neurobiol Aging 27:1763–1768

    Article  CAS  PubMed  Google Scholar 

  • Gelman BB, Schuenke K (2004) Brain aging in acquired immunodeficiency syndrome: increased ubiquitin-protein conjugate is correlated with decreased synaptic protein but not amyloid plaque accumulation. J Neuro-Oncol 10:98–108

    CAS  Google Scholar 

  • Gisslen M, Krut J, Andreasson U, Blennow K, Cinque P, Brew BJ, Spudich S, Hagberg L, Rosengren L, Price RW, Zetterberg H (2009) Amyloid and tau cerebrospinal fluid biomarkers in HIV infection. BMC Neurol 9:63

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gisslen M, Price RW, Andreasson U, Norgren N, Nilsson S, Hagberg L, Fuchs D, Spudich S, Blennow K, Zetterberg H (2016) Plasma concentration of the neurofilament light protein (NFL) is a biomarker of CNS injury in HIV infection: a cross-sectional study. EBioMedicine 3:135–140

    Article  PubMed  Google Scholar 

  • Giunta B, Fernandez F, Nikolic WV, Obregon D, Rrapo E, Town T, Tan J (2008) Inflammaging as a prodrome to Alzheimer’s disease. J Neuroinflammation 5:51

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gray F, Bazille C, Adle-Biassette H, Mikol J, Moulignier A, Scaravilli F (2005) Central nervous system immune reconstitution disease in acquired immunodeficiency syndrome patients receiving highly active antiretroviral treatment. J Neuro-Oncol 11(Suppl 3):16–22

    Google Scholar 

  • Green DA, Masliah E, Vinters HV, Beizai P, Moore DJ, Achim CL (2005) Brain deposition of beta-amyloid is a common pathologic feature in HIV positive patients. AIDS 19:407–411

    Article  CAS  PubMed  Google Scholar 

  • Grober E, Hall CB, Lipton RB, Zonderman AB, Resnick SM, Kawas C (2008) Memory impairment, executive dysfunction, and intellectual decline in preclinical Alzheimer’s disease. J Int Neuropsychol Soc 14:266–278

    PubMed  PubMed Central  Google Scholar 

  • Guillemin GJ, Kerr SJ, Brew BJ (2005) Involvement of quinolinic acid in AIDS dementia complex. Neurotox Res 7:103–123

    Article  CAS  PubMed  Google Scholar 

  • Hardy DJ, Vance DE (2009) The neuropsychology of HIV/AIDS in older adults. Neuropsychol Rev 19:263–272

    Article  PubMed  Google Scholar 

  • Heaton RK, Clifford DB, Franklin DR Jr, Woods SP, Ake C, Vaida F, Ellis RJ, Letendre SL, Marcotte TD, Atkinson JH, Rivera-Mindt M, Vigil OR, Taylor MJ, Collier AC, Marra CM, Gelman BB, McArthur JC, Morgello S, Simpson DM, McCutchan JA, Abramson I, Gamst A, Fennema-Notestine C, Jernigan TL, Wong J, Grant I (2010) HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER study. Neurology 75:2087–2096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heaton RK, Franklin DR, Ellis RJ, McCutchan JA, Letendre SL, Leblanc S, Corkran SH, Duarte NA, Clifford DB, Woods SP, Collier AC, Marra CM, Morgello S, Mindt MR, Taylor MJ, Marcotte TD, Atkinson JH, Wolfson T, Gelman BB, McArthur JC, Simpson DM, Abramson I, Gamst A, Fennema-Notestine C, Jernigan TL, Wong J, Grant I, Group C, Group H (2011) HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: differences in rates, nature, and predictors. J Neuro-Oncol 17:3–16

    CAS  Google Scholar 

  • Helzner EP, Luchsinger JA, Scarmeas N, Cosentino S, Brickman AM, Glymour MM, Stern Y (2009) Contribution of vascular risk factors to the progression in Alzheimer disease. Arch Neurol 66:343–348

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoare J, Westgarth-Taylor J, Fouche JP, Combrinck M, Spottiswoode B, Stein DJ, Joska JA (2013) Relationship between apolipoprotein E4 genotype and white matter integrity in HIV-positive young adults in South Africa. Eur Arch Psychiatry Clin Neurosci 263:189–195

    Article  PubMed  Google Scholar 

  • Hodes RJ, Sierra F, Austad SN, Epel E, Neigh GN, Erlandson KM, Schafer MJ, LeBrasseur NK, Wiley C, Campisi J, Sehl ME, Scalia R, Eguchi S, Kasinath BS, Halter JB, Cohen HJ, Demark-Wahnefried W, Ahles TA, Barzilai N, Hurria A, Hunt PW (2016) Disease drivers of aging. Ann N Y Acad Sci 1386:45–68

    Article  PubMed  PubMed Central  Google Scholar 

  • Holler CJ, Webb RL, Laux AL, Beckett TL, Niedowicz DM, Ahmed RR, Liu Y, Simmons CR, Dowling AL, Spinelli A, Khurgel M, Estus S, Head E, Hersh LB, Murphy MP (2012) BACE2 expression increases in human neurodegenerative disease. Am J Pathol 180:337–350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horvath S, Levine AJ (2015) HIV-1 infection accelerates age according to the epigenetic clock. J Infect Dis 212:1563–1573

    Article  PubMed  PubMed Central  Google Scholar 

  • Imp BM, Rubin LH, Tien PC, Plankey MW, Golub ET, French AL, Valcour VG (2017) Monocyte activation is associated with worse cognitive performance in HIV-infected women with virologic suppression. J Infect Dis 215:114–121

    Article  CAS  PubMed  Google Scholar 

  • Janelidze S, Hertze J, Zetterberg H, Landqvist Waldo M, Santillo A, Blennow K, Hansson O (2016) Cerebrospinal fluid neurogranin and YKL-40 as biomarkers of Alzheimer's disease. Ann Clin Transl Neurol 3:12–20

    Article  CAS  PubMed  Google Scholar 

  • Jessen H, Allen TM, Streeck H (2014) How a single patient influenced HIV research—15-year follow-up. N Engl J Med 370:682–683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnston JA, Liu WW, Todd SA, Coulson DT, Murphy S, Irvine GB, Passmore AP (2005) Expression and activity of beta-site amyloid precursor protein cleaving enzyme in Alzheimer’s disease. Biochem Soc Trans 33:1096–1100

    Article  CAS  PubMed  Google Scholar 

  • Joska JA, Combrinck M, Valcour VG, Hoare J, Leisegang F, Mahne AC, Myer L, Stein DJ (2010) Association between apolipoprotein E4 genotype and human immunodeficiency virus-associated dementia in younger adults starting antiretroviral therapy in South Africa. J Neuro-Oncol 16:377–383

    CAS  Google Scholar 

  • Joubert S, Gour N, Guedj E, Didic M, Gueriot C, Koric L, Ranjeva JP, Felician O, Guye M, Ceccaldi M (2016) Early-onset and late-onset Alzheimer’s disease are associated with distinct patterns of memory impairment. Cortex 74:217–232

    Article  PubMed  Google Scholar 

  • Jucker M, Walker LC (2011) Pathogenic protein seeding in Alzheimer disease and other neurodegenerative disorders. Ann Neurol 70:532–540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kadiu I, Glanzer JG, Kipnis J, Gendelman HE, Thomas MP (2005) Mononuclear phagocytes in the pathogenesis of neurodegenerative diseases. Neurotox Res 8:25–50

    Article  CAS  PubMed  Google Scholar 

  • Kamat R, Doyle KL, Iudicello JE, Morgan EE, Morris S, Smith DM, Little SJ, Grant I, Woods SP, Translational Methamphetamine ARCG (2016) Neurobehavioral disturbances during acute and early HIV infection. Cogn Behav Neurol 29:1–10

    Article  PubMed  PubMed Central  Google Scholar 

  • Karr JE, Graham RB, Hofer SM, Muniz-Terrera G (2018) When does cognitive decline begin? A systematic review of change point studies on accelerated decline in cognitive and neurological outcomes preceding mild cognitive impairment, dementia, and death. Psychol Aging 33:195–218

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim J, Yoon JH, Kim YS (2013) HIV-1 Tat interacts with and regulates the localization and processing of amyloid precursor protein. PLoS One 8:e77972

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kivipelto M, Helkala EL, Laakso MP, Hanninen T, Hallikainen M, Alhainen K, Soininen H, Tuomilehto J, Nissinen A (2001) Midlife vascular risk factors and Alzheimer’s disease in later life: longitudinal, population based study. BMJ 322:1447–1451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kovalevich J, Langford D (2012) Neuronal toxicity in HIV CNS disease. Future Virol 7:687–698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krut JJ, Zetterberg H, Blennow K, Cinque P, Hagberg L, Price RW, Studahl M, Gisslen M (2013) Cerebrospinal fluid Alzheimer’s biomarker profiles in CNS infections. J Neurol 260:620–626

    Article  CAS  PubMed  Google Scholar 

  • Lam FC, Liu R, Lu P, Shapiro AB, Renoir JM, Sharom FJ, Reiner PB (2001) Beta-amyloid efflux mediated by p-glycoprotein. J Neurochem 76:1121–1128

    Article  CAS  PubMed  Google Scholar 

  • Li L, Zhang X, Yang D, Luo G, Chen S, Le W (2009) Hypoxia increases Abeta generation by altering beta- and gamma-cleavage of APP. Neurobiol Aging 30:1091–1098

    Article  CAS  PubMed  Google Scholar 

  • Liao Y, Qi XL, Cao Y, Yu WF, Ravid R, Winblad B, Pei JJ, Guan ZZ (2016) Elevations in the levels of NF-kappaB and inflammatory chemotactic factors in the brains with Alzheimer’s disease—one mechanism may involve alpha3 nicotinic acetylcholine receptor. Curr Alzheimer Res 13:1290–1301

    Article  CAS  PubMed  Google Scholar 

  • Liu D, Cao B, Zhao Y, Huang H, McIntyre RS, Rosenblat JD, Zhou H (2018) Soluble TREM2 changes during the clinical course of Alzheimer’s disease: a meta-analysis. Neurosci Lett 686:10–16

    Article  CAS  PubMed  Google Scholar 

  • Lohse N, Hansen AB, Gerstoft J, Obel N (2007) Improved survival in HIV-infected persons: consequences and perspectives. J Antimicrob Chemother 60:461–463

    Article  CAS  PubMed  Google Scholar 

  • Lovell MA, Markesbery WR (2007) Oxidative damage in mild cognitive impairment and early Alzheimer’s disease. J Neurosci Res 85:3036–3040

    Article  CAS  PubMed  Google Scholar 

  • Lowther K, Selman L, Harding R, Higginson IJ (2014) Experience of persistent psychological symptoms and perceived stigma among people with HIV on antiretroviral therapy (ART): a systematic review. Int J Nurs Stud 51:1171–1189

    Article  PubMed  Google Scholar 

  • Luchsinger JA, Reitz C, Honig LS, Tang MX, Shea S, Mayeux R (2005) Aggregation of vascular risk factors and risk of incident Alzheimer disease. Neurology 65:545–551

    Article  CAS  PubMed  Google Scholar 

  • Maccioni RB, Munoz JP, Barbeito L (2001) The molecular bases of Alzheimer’s disease and other neurodegenerative disorders. Arch Med Res 32:367–381

    Article  CAS  PubMed  Google Scholar 

  • Maezawa I, Zimin PI, Wulff H, Jin LW (2011) Amyloid-beta protein oligomer at low nanomolar concentrations activates microglia and induces microglial neurotoxicity. J Biol Chem 286:3693–3706

    Article  CAS  PubMed  Google Scholar 

  • Maki PM, Rubin LH, Valcour V, Martin E, Crystal H, Young M, Weber KM, Manly J, Richardson J, Alden C, Anastos K (2015) Cognitive function in women with HIV: findings from the Women’s Interagency HIV Study. Neurology 84:231–240

    Article  PubMed  PubMed Central  Google Scholar 

  • Masters MC, Ances BM (2014) Role of neuroimaging in HIV-associated neurocognitive disorders. Semin Neurol 34:89–102

    Article  PubMed  PubMed Central  Google Scholar 

  • May MT, Ingle SM (2011) Life expectancy of HIV-positive adults: a review. Sex Health 8:526–533

    Article  PubMed  Google Scholar 

  • Mega MS, Cummings JL, Fiorello T, Gornbein J (1996) The spectrum of behavioral changes in Alzheimer’s disease. Neurology 46:130–135

    Article  CAS  PubMed  Google Scholar 

  • Mellgren A, Price RW, Hagberg L, Rosengren L, Brew BJ, Gisslen M (2007) Antiretroviral treatment reduces increased CSF neurofilament protein (NFL) in HIV-1 infection. Neurology 69:1536–1541

    Article  CAS  PubMed  Google Scholar 

  • Meng XF, Yu JT, Wang HF, Tan MS, Wang C, Tan CC, Tan L (2014) Midlife vascular risk factors and the risk of Alzheimer’s disease: a systematic review and meta-analysis. J Alzheimers Dis 42:1295–1310

    Article  PubMed  Google Scholar 

  • Milanini B, Valcour V (2017) Differentiating HIV-associated neurocognitive disorders from Alzheimer’s disease: an emerging issue in geriatric NeuroHIV. Curr HIV/AIDS Rep 14:123–132

    Article  PubMed  PubMed Central  Google Scholar 

  • Milanini B AI, Javandel S, Joanna H, Paul R, Valcour V (2016). Discriminant analysis of neuropsychological testing differentiates HIV-associated neurocogntive disorder from mild cognitive impairment due to Alzheimer’s disease. In: International Society of NeuroVirology: Toronto, Canada

  • Milanini B, Catella S, Perkovich B, Esmaeili-Firidouni P, Wendelken L, Paul R, Greene M, Ketelle R, Valcour V (2017) Psychiatric symptom burden in older people living with HIV with and without cognitive impairment: the UCSF HIV over 60 cohort study. AIDS Care 29:1178–1185

    Article  PubMed  PubMed Central  Google Scholar 

  • Minagar A, Shapshak P, Fujimura R, Ownby R, Heyes M, Eisdorfer C (2002) The role of macrophage/microglia and astrocytes in the pathogenesis of three neurologic disorders: HIV-associated dementia, Alzheimer disease, and multiple sclerosis. J Neurol Sci 202:13–23

    Article  CAS  PubMed  Google Scholar 

  • Mocchetti I, Bachis A, Esposito G, Turner SR, Taraballi F, Tasciotti E, Paige M, Avdoshina V (2014) Human immunodeficiency virus-associated dementia: a link between accumulation of viral proteins and neuronal degeneration. Curr Trends Neurol 8:71–85

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moore DJ, Arce M, Moseley S, McCutchan JA, Marquie-Beck J, Franklin DR, Vaida F, Achim CL, McArthur J, Morgello S, Simpson DM, Gelman BB, Collier AC, Marra CM, Clifford DB, Heaton RK, Grant I, Charter G, Group H (2011) Family history of dementia predicts worse neuropsychological functioning among HIV-infected persons. J Neuropsychiatry Clin Neurosci 23:316–323

    Article  PubMed  PubMed Central  Google Scholar 

  • Morgan EE, Woods SP, Letendre SL, Franklin DR, Bloss C, Goate A, Heaton RK, Collier AC, Marra CM, Gelman BB, McArthur JC, Morgello S, Simpson DM, McCutchan JA, Ellis RJ, Abramson I, Gamst A, Fennema-Notestine C, Smith DM, Grant I, Vaida F, Clifford DB, Group CHATER (2013) Apolipoprotein E4 genotype does not increase risk of HIV-associated neurocognitive disorders. J Neuro-Oncol 19:150–156

    CAS  Google Scholar 

  • Morgello S, Jacobs M, Murray J, Byrd D, Neibart E, Mintz L, Meloni G, Chon C, Crary J (2018) Alzheimer’s disease neuropathology may not predict functional impairment in HIV: a report of two individuals. J Neuro-Oncol

  • Morris JC, Price JL (2001) Pathologic correlates of nondemented aging, mild cognitive impairment, and early-stage Alzheimer’s disease. J Mol Neurosci 17:101–118

    Article  CAS  PubMed  Google Scholar 

  • Morris JC, Roe CM, Xiong C, Fagan AM, Goate AM, Holtzman DM, Mintun MA (2010) APOE predicts amyloid-beta but not tau Alzheimer pathology in cognitively normal aging. Ann Neurol 67:122–131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mourao RJ, Mansur G, Malloy-Diniz LF, Castro Costa E, Diniz BS (2016) Depressive symptoms increase the risk of progression to dementia in subjects with mild cognitive impairment: systematic review and meta-analysis. Int J Geriatr Psychiatry 31:905–911

    Article  PubMed  Google Scholar 

  • Nath A, Schiess N, Venkatesan A, Rumbaugh J, Sacktor N, McArthur J (2008) Evolution of HIV dementia with HIV infection. Int Rev Psychiatry 20:25–31

    Article  PubMed  Google Scholar 

  • Ortega M, Ances BM (2014) Role of HIV in amyloid metabolism. J NeuroImmune Pharmacol 9:483–491

    Article  PubMed  PubMed Central  Google Scholar 

  • Panos SE, Hinkin CH, Singer EJ, Thames AD, Patel SM, Sinsheimer JS, Del Re AC, Gelman BB, Morgello S, Moore DJ, Levine AJ (2013) Apolipoprotein-E genotype and human immunodeficiency virus-associated neurocognitive disorder: the modulating effects of older age and disease severity. Neurobehav HIV Med 5:11–22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patrick C, Crews L, Desplats P, Dumaop W, Rockenstein E, Achim CL, Everall IP, Masliah E (2011) Increased CDK5 expression in HIV encephalitis contributes to neurodegeneration via tau phosphorylation and is reversed with Roscovitine. Am J Pathol 178:1646–1661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peavy G, Jacobs D, Salmon DP, Butters N, Delis DC, Taylor M, Massman P, Stout JC, Heindel WC, Kirson D et al (1994) Verbal memory performance of patients with human immunodeficiency virus infection: evidence of subcortical dysfunction. The HNRC Group J Clin Exp Neuropsychol 16:508–523

    Article  CAS  Google Scholar 

  • Perry VH, Nicoll JA, Holmes C (2010) Microglia in neurodegenerative disease. Nat Rev Neurol 6:193–201

    Article  PubMed  Google Scholar 

  • Petersen RC (2004) Mild cognitive impairment as a diagnostic entity. J Intern Med 256:183–194

    Article  CAS  PubMed  Google Scholar 

  • Petersen RC, Smith GE, Waring SC, Ivnik RJ, Tangalos EG, Kokmen E (1999) Mild cognitive impairment: clinical characterization and outcome. Arch Neurol 56:303–308

    Article  CAS  PubMed  Google Scholar 

  • Peterson J, Gisslen M, Zetterberg H, Fuchs D, Shacklett BL, Hagberg L, Yiannoutsos CT, Spudich SS, Price RW (2014) Cerebrospinal fluid (CSF) neuronal biomarkers across the spectrum of HIV infection: hierarchy of injury and detection. PLoS One 9:e116081

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Polvikoski T, Sulkava R, Haltia M, Kainulainen K, Vuorio A, Verkkoniemi A, Niinisto L, Halonen P, Kontula K (1995) Apolipoprotein E, dementia, and cortical deposition of beta-amyloid protein. N Engl J Med 333:1242–1247

    Article  CAS  PubMed  Google Scholar 

  • Qiu C, Fratiglioni L (2015) A major role for cardiovascular burden in age-related cognitive decline. Nat Rev Cardiol 12:267–277

    Article  PubMed  Google Scholar 

  • Rahimian P, He JJ (2017) HIV/neuroAIDS biomarkers. Prog Neurobiol 157:117–132

    Article  CAS  PubMed  Google Scholar 

  • Rempel HC, Pulliam L (2005) HIV-1 Tat inhibits neprilysin and elevates amyloid beta. AIDS 19:127–135

    Article  CAS  PubMed  Google Scholar 

  • Roe CM, Fagan AM, Grant EA, Hassenstab J, Moulder KL, Maue Dreyfus D, Sutphen CL, Benzinger TL, Mintun MA, Holtzman DM, Morris JC (2013) Amyloid imaging and CSF biomarkers in predicting cognitive impairment up to 7.5 years later. Neurology 80:1784–1791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosenmann H (2012) CSF biomarkers for amyloid and tau pathology in Alzheimer’s disease. J Mol Neurosci 47:1–14

    Article  CAS  PubMed  Google Scholar 

  • Royal W 3rd, Cherner M, Burdo TH, Umlauf A, Letendre SL, Jumare J, Abimiku A, Alabi P, Alkali N, Bwala S, Okwuasaba K, Eyzaguirre LM, Akolo C, Guo M, Williams KC, Blattner WA (2016) Associations between cognition, gender and monocyte activation among HIV infected individuals in Nigeria. PLoS One 11:e0147182

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rubin LH, Maki PM, Springer G, Benning L, Anastos K, Gustafson D, Villacres MC, Jiang X, Adimora AA, Waldrop-Valverde D, Vance DE, Bolivar H, Alden C, Martin EM, Valcour VG, Women's Interagency HIVS (2017) Cognitive trajectories over 4 years among HIV-infected women with optimal viral suppression. Neurology 89:1594–1603

    Article  PubMed  PubMed Central  Google Scholar 

  • Sacktor N, Skolasky RL, Cox C, Selnes O, Becker JT, Cohen B, Martin E, Miller EN, Multicenter ACS (2010) Longitudinal psychomotor speed performance in human immunodeficiency virus-seropositive individuals: impact of age and serostatus. J Neuro-Oncol 16:335–341

    Google Scholar 

  • Sacktor N, Skolasky RL, Seaberg E, Munro C, Becker JT, Martin E, Ragin A, Levine A, Miller E (2016) Prevalence of HIV-associated neurocognitive disorders in the multicenter AIDS cohort study. Neurology 86:334–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salmon DP (2012) Neuropsychological features of mild cognitive impairment and preclinical Alzheimer’s disease. Curr Top Behav Neurosci 10:187–212

    Article  PubMed  Google Scholar 

  • Sattler FR, He J, Letendre S, Wilson C, Sanders C, Heaton R, Ellis R, Franklin D, Aldrovandi G, Marra CM, Clifford D, Morgello S, Grant I, McCutchan JA, Group C (2015) Abdominal obesity contributes to neurocognitive impairment in HIV-infected patients with increased inflammation and immune activation. J Acquir Immune Defic Syndr 68:281–288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schouten J, Su T, Wit FW, Kootstra NA, Caan MW, Geurtsen GJ, Schmand BA, Stolte IG, Prins M, Majoie CB, Portegies P, Reiss P, Group AGS (2016) Determinants of reduced cognitive performance in HIV-1-infected middle-aged men on combination antiretroviral therapy. AIDS 30:1027–1038

    Article  CAS  PubMed  Google Scholar 

  • Scott JC, Woods SP, Carey CL, Weber E, Bondi MW, Grant I, Group HIVNRC (2011) Neurocognitive consequences of HIV infection in older adults: an evaluation of the “cortical” hypothesis. AIDS Behav 15:1187–1196

    Article  PubMed  Google Scholar 

  • Sheppard DP, Woods SP, Bondi MW, Gilbert PE, Massman PJ, Doyle KL, Group HIVNRP (2015) Does older age confer an increased risk of incident neurocognitive disorders among persons living with HIV disease? Clin Neuropsychol 29:656–677

    Article  PubMed  PubMed Central  Google Scholar 

  • Sheppard DP, Iudicello JE, Morgan EE et al (2017) Accelerated and accentuated neurocognitive aging in HIV infection. J Neurovirol 23(3):492–500

    Article  PubMed  PubMed Central  Google Scholar 

  • Sjogren M, Vanderstichele H, Agren H, Zachrisson O, Edsbagge M, Wikkelso C, Skoog I, Wallin A, Wahlund LO, Marcusson J, Nagga K, Andreasen N, Davidsson P, Vanmechelen E, Blennow K (2001) Tau and Abeta42 in cerebrospinal fluid from healthy adults 21-93 years of age: establishment of reference values. Clin Chem 47:1776–1781

    CAS  PubMed  Google Scholar 

  • Skoog I, Lernfelt B, Landahl S, Palmertz B, Andreasson LA, Nilsson L, Persson G, Oden A, Svanborg A (1996) 15-year longitudinal study of blood pressure and dementia. Lancet 347:1141–1145

    Article  CAS  PubMed  Google Scholar 

  • Sokolova A, Hill MD, Rahimi F, Warden LA, Halliday GM, Shepherd CE (2009) Monocyte chemoattractant protein-1 plays a dominant role in the chronic inflammation observed in Alzheimer’s disease. Brain Pathol 19:392–398

    Article  CAS  PubMed  Google Scholar 

  • Soontornniyomkij V, Moore DJ, Gouaux B, Soontornniyomkij B, Tatro ET, Umlauf A, Masliah E, Levine AJ, Singer EJ, Vinters HV, Gelman BB, Morgello S, Cherner M, Grant I, Achim CL (2012) Cerebral beta-amyloid deposition predicts HIV-associated neurocognitive disorders in APOE epsilon4 carriers. AIDS 26:2327–2335

    Article  CAS  PubMed  Google Scholar 

  • Steinbrink F, Evers S, Buerke B, Young P, Arendt G, Koutsilieri E, Reichelt D, Lohmann H, Husstedt IW, German Competence Network HA (2013) Cognitive impairment in HIV infection is associated with MRI and CSF pattern of neurodegeneration. Eur J Neurol 20:420–428

    Article  CAS  PubMed  Google Scholar 

  • Stern AL, Ghura S, Gannon PJ, Akay-Espinoza C, Phan JM, Yee AC, Vassar R, Gelman BB, Kolson DL, Jordan-Sciutto KL (2018) BACE1 mediates HIV-associated and excitotoxic neuronal damage through an APP-dependent mechanism. J Neurosci 38:4288–4300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stoff DM, Goodkin K, Jeste D, Marquine M (2017) Redefining aging in HIV infection using phenotypes. Curr HIV/AIDS Rep 14:184–199

    Article  PubMed  PubMed Central  Google Scholar 

  • Stoll M, Schmidt RE (2003) Immune restoration inflammatory syndromes: the dark side of successful antiretroviral treatment. Curr Infect Dis Rep 5:266–276

    Article  PubMed  Google Scholar 

  • Stoll M, Schmidt RE (2004) Immune restoration inflammatory syndromes: apparently paradoxical clinical events after the initiation of HAART. Curr HIV/AIDS Rep 1:122–127

    Article  PubMed  Google Scholar 

  • Streit WJ, Mrak RE, Griffin WS (2004) Microglia and neuroinflammation: a pathological perspective. J Neuroinflammation 1:14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tan IL, Smith BR, Hammond E, Vornbrock-Roosa H, Creighton J, Selnes O, McArthur JC, Sacktor N (2013) Older individuals with HIV infection have greater memory deficits than younger individuals. J Neuro-Oncol 19:531–536

    Google Scholar 

  • Tarawneh R, D'Angelo G, Crimmins D, Herries E, Griest T, Fagan AM, Zipfel GJ, Ladenson JH, Morris JC, Holtzman DM (2016) Diagnostic and prognostic utility of the synaptic marker neurogranin in Alzheimer disease. JAMA Neurol 73:561–571

    Article  PubMed  PubMed Central  Google Scholar 

  • Tarkowski E, Andreasen N, Tarkowski A, Blennow K (2003) Intrathecal inflammation precedes development of Alzheimer’s disease. J Neurol Neurosurg Psychiatry 74:1200–1205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terracciano A, Sutin AR, An Y, O'Brien RJ, Ferrucci L, Zonderman AB, Resnick SM (2014) Personality and risk of Alzheimer’s disease: new data and meta-analysis. Alzheimers Dement 10:179–186

    Article  PubMed  Google Scholar 

  • Thal DR, Attems J, Ewers M (2014) Spreading of amyloid, tau, and microvascular pathology in Alzheimer’s disease: findings from neuropathological and neuroimaging studies. J Alzheimers Dis 42(Suppl 4):S421–S429

    Article  PubMed  CAS  Google Scholar 

  • Tierney S, Woods SP, Verduzco M, Beltran J, Massman PJ, Hasbun R (2018) Semantic memory in HIV-associated neurocognitive disorders: an evaluation of the “cortical” versus “subcortical” hypothesis. Arch Clin Neuropsychol 33:406–416

    Article  PubMed  Google Scholar 

  • Ting KK, Brew B, Guillemin G (2007) The involvement of astrocytes and kynurenine pathway in Alzheimer’s disease. Neurotox Res 12:247–262

    Article  CAS  PubMed  Google Scholar 

  • Town T, Laouar Y, Pittenger C, Mori T, Szekely CA, Tan J, Duman RS, Flavell RA (2008) Blocking TGF-beta-Smad2/3 innate immune signaling mitigates Alzheimer-like pathology. Nat Med 14:681–687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tripathi M, Yadav S, Kumar V, Kumar R, Tripathi M, Gaikwad S, Kumar P, Bal C (2016) HIV encephalitis with subcortical tau deposition: imaging pathology in vivo using F-18 THK 5117. Eur J Nucl Med Mol Imaging 43:2456–2457

    Article  PubMed  Google Scholar 

  • Turner RS, Chadwick M, Horton WA, Simon GL, Jiang X, Esposito G (2016) An individual with human immunodeficiency virus, dementia, and central nervous system amyloid deposition. Alzheimers Dement (Amst) 4:1–5

    Google Scholar 

  • Valcour VG (2013) HIV, aging, and cognition: emerging issues. Top Antivir Med 21:119–123

    PubMed  Google Scholar 

  • Valcour V, Shikuma C, Shiramizu B, Watters M, Poff P, Selnes O, Holck P, Grove J, Sacktor N (2004) Higher frequency of dementia in older HIV-1 individuals: the Hawaii aging with HIV-1 cohort. Neurology 63:822–827

    Article  CAS  PubMed  Google Scholar 

  • Valotassiou V, Malamitsi J, Papatriantafyllou J, Dardiotis E, Tsougos I, Psimadas D, Alexiou S, Hadjigeorgiou G, Georgoulias P (2018) SPECT and PET imaging in Alzheimer’s disease. Ann Nucl Med 32:583–593

    Article  CAS  PubMed  Google Scholar 

  • Van Epps P, Kalayjian RC (2017) Human immunodeficiency virus and aging in the era of effective antiretroviral therapy. Infect Dis Clin N Am 31:791–810

    Article  Google Scholar 

  • van Gorp WG, Miller EN, Marcotte TD, Dixon W, Paz D, Selnes O, Wesch J, Becker JT, Hinkin CH, Mitrushina M et al (1994) The relationship between age and cognitive impairment in HIV-1 infection: findings from the multicenter AIDS cohort study and a clinical cohort. Neurology 44:929–935

    Article  PubMed  Google Scholar 

  • Vance DE, Wadley VG, Crowe MG, Raper JL, Ball KK (2011) Cognitive and everyday functioning in older and younger adults with and without HIV. Clin Gerontol 34:413–426

    Article  PubMed  PubMed Central  Google Scholar 

  • Vassar R, Bennett BD, Babu-Khan S, Kahn S, Mendiaz EA, Denis P, Teplow DB, Ross S, Amarante P, Loeloff R, Luo Y, Fisher S, Fuller J, Edenson S, Lile J, Jarosinski MA, Biere AL, Curran E, Burgess T, Louis JC, Collins F, Treanor J, Rogers G, Citron M (1999) Beta-secretase cleavage of Alzheimer’s amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286:735–741

    Article  CAS  PubMed  Google Scholar 

  • Vernooij MW, Smits M (2012) Structural neuroimaging in aging and Alzheimer’s disease. Neuroimaging Clin N Am 22:33–55 vii-viii

    Article  PubMed  Google Scholar 

  • Wellington H, Paterson RW, Portelius E, Tornqvist U, Magdalinou N, Fox NC, Blennow K, Schott JM, Zetterberg H (2016) Increased CSF neurogranin concentration is specific to Alzheimer disease. Neurology 86:829–835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wendelken LA, Jahanshad N, Rosen HJ, Busovaca E, Allen I, Coppola G, Adams C, Rankin KP, Milanini B, Clifford K, Wojta K, Nir TM, Gutman BA, Thompson PM, Valcour V (2016) ApoE epsilon4 is associated with cognition, brain integrity, and atrophy in HIV over age 60. J Acquir Immune Defic Syndr 73:426–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White DA, Taylor MJ, Butters N, Mack C, Salmon DP, Peavy G, Ryan L, Heaton RK, Atkinson JH, Chandler JL, Grant I (1997) Memory for verbal information in individuals with HIV-associated dementia complex. HNRC Group. J Clin Exp Neuropsychol 19:357–366

    Article  CAS  PubMed  Google Scholar 

  • Wilson RS, Leurgans SE, Boyle PA, Bennett DA (2011) Cognitive decline in prodromal Alzheimer disease and mild cognitive impairment. Arch Neurol 68:351–356

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu J, Ikezu T (2009) The comorbidity of HIV-associated neurocognitive disorders and Alzheimer’s disease: a foreseeable medical challenge in post-HAART era. J NeuroImmune Pharmacol 4:200–212

    Article  CAS  PubMed  Google Scholar 

  • Yang LB, Lindholm K, Yan R, Citron M, Xia W, Yang XL, Beach T, Sue L, Wong P, Price D, Li R, Shen Y (2003) Elevated beta-secretase expression and enzymatic activity detected in sporadic Alzheimer disease. Nat Med 9:3–4

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Kwon D, Esmaeili-Firidouni P, Pfefferbaum A, Sullivan EV, Javitz H, Valcour V, Pohl KM (2016) Extracting patterns of morphometry distinguishing HIV associated neurodegeneration from mild cognitive impairment via group cardinality constrained classification. Hum Brain Mapp 37:4523–4538

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao QF, Tan L, Wang HF, Jiang T, Tan MS, Tan L, Xu W, Li JQ, Wang J, Lai TJ, Yu JT (2016) The prevalence of neuropsychiatric symptoms in Alzheimer's disease: systematic review and meta-analysis. J Affect Disord 190:264–271

    Article  PubMed  Google Scholar 

  • Zhou L, Diefenbach E, Crossett B, Tran SL, Ng T, Rizos H, Rua R, Wang B, Kapur A, Gandhi K, Brew BJ, Saksena NK (2010) First evidence of overlaps between HIV-associated dementia (HAD) and non-viral neurodegenerative diseases: proteomic analysis of the frontal cortex from HIV+ patients with and without dementia. Mol Neurodegener 5:27

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Funding

This work was supported by salary support for Dr. E.E. Sundermann from the Interdisciplinary Research Fellowship in NeuroAIDS [R25MH081482].

Author information

Author notes

  1. Leah H. Rubin and Erin E. Sundermann equally contributed to this work.

Authors and Affiliations

  1. Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, MD, USA

    Leah H. Rubin

  2. Department of Epidemiology, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD, USA

    Leah H. Rubin

  3. Department of Psychiatry, University of California, San Diego (UCSD) School of Medicine, La Jolla, CA, USA

    Erin E. Sundermann & David J. Moore

Authors
  1. Leah H. Rubin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Erin E. Sundermann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David J. Moore
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Erin E. Sundermann.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rubin, L.H., Sundermann, E.E. & Moore, D.J. The current understanding of overlap between characteristics of HIV-associated neurocognitive disorders and Alzheimer’s disease. J. Neurovirol. 25, 661–672 (2019). https://doi.org/10.1007/s13365-018-0702-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13365-018-0702-9

Keywords

Search

Navigation