Human immunodeficiency virus has similar effects on brain volumetrics and cognition in males and females

Journal of NeuroVirology

Volumn 22, Issue 1, 2016, Pages 93-103

  Behrman Lay, Ashley M ^a   Paul, Robert H ^a,b   Heaps Woodruff, Jodi ^a,b   Baker, Laurie M ^a   Usher, Christina ^a   Ances, Beau M ^c,d,e  

^a UNIVERSITY OF MISSOURI ST LOUIS   (United States)

^b MISSOURI INSTITUTE OF MENTAL HEALTH   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

Author keywords

Cognition; Gender; HIV; Neuroimaging; Neuropsychology; Volumetrics

Indexed keywords

ANTIRETROVIRUS AGENT; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; VIRUS RNA;

ADULT; ARTICLE; BECK DEPRESSION INVENTORY; BRAIN REGION; COGNITION; CONTROLLED STUDY; EXECUTIVE FUNCTION; FEMALE; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LEARNING; MAJOR CLINICAL STUDY; MALE; MEMORY; NEUROIMAGING; NEUROPSYCHOLOGY; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PSYCHOMOTOR PERFORMANCE; RISK FACTOR; SEX DIFFERENCE; VIRUS LOAD; VOLUMETRY; AGED; ANTAGONISTS AND INHIBITORS; BLOOD; BRAIN; CASE CONTROL STUDY; CD4 LYMPHOCYTE COUNT; CD4+ T LYMPHOCYTE; COGNITION DISORDERS; COMPLICATION; DRUG EFFECTS; FUNCTIONAL NEUROIMAGING; HIV INFECTIONS; MIDDLE AGED; NEUROPSYCHOLOGICAL TEST; PATHOLOGY; PATHOPHYSIOLOGY; VIROLOGY;

AGED; ANTI-HIV AGENTS; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; BRAIN; CASE-CONTROL STUDIES; CD4 LYMPHOCYTE COUNT; CD4-POSITIVE T-LYMPHOCYTES; COGNITION DISORDERS; FEMALE; FUNCTIONAL NEUROIMAGING; HIV INFECTIONS; HUMANS; MALE; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; RNA, VIRAL; VIRAL LOAD;

EID: 84957839703     PISSN: 13550284     EISSN: 15382443     Source Type: Journal    
DOI: 10.1007/s13365-015-0373-8     Document Type: Article

References (81)

1. Ances BM, Ortega M, Vaida F, Heaps J, Paul R (2012) Independent effects of HIV, aging, and HAART on brain volumetric measures. J Acquir Immune Defic Syndr 59(5):469–477
2. Ances BM, Roc AC, Wang J, Korczykowski M, Okawa J, Stern J, Kim J, Wolf R, Lawler K, Kolson DL, Detre JA (2006) Caudate blood flow and volume are reduced in HIV+ neurocognitively impaired patients. Neurology 66(6):862–866
3. Antinori A, Arendt G, Becker JT, Brew BJ, Byrd DA, Cherner M, Clifford DB, Clinque 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(18):1789–1799
4. 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(3):369–376
5. Baker LM, Paul RH, Heaps JM, Westerhaus E, Chang JY, Williams S, Brier MR, Plax K, Ances BM (2014) Impact of human immunodeficiency virus on neurocognition and risky behaviors in young adults. Journal of neurovirology 20(5):466–473
6. Beck AT, Steer RA. Beck (1996). Beck Depression Inventory (2nd ed.). The Psychological Corporation, San Antonio
7. Becker JT, Kingsley L, Mullen J, Cohen B, Martin E, Miller EN, Ragin A, Sacktor N, Selnes OA, Visscher BR, Multicenter AIDS Cohort Study (2009) Vascular risk factors, HIV serostatus, and cognitive dysfunction in gay and bisexual men. Neurology 73(16):1292–1299
8. Becker JT, Sanders J, Madsen SK, Ragin A, Kingsley L, Maruca V, Cohen B, Goodkin K, Martin E, Miller EN, Sacktor N, Alger JR, Barker PB, Saharan P, Carmichael OT, Thompson PM, Multicenter AIDS Cohort Study (2011) Subcortical brain atrophy persists even in HAART-regulated HIV disease. Brain Imaging Behav 5(2):77–85
9. Benedict RHB, Schretlen D, Groninger L, Brandt J (1998) The Hopkins Verbal Learning Test-Revised: normative data and analysis of interform and test-retest reliability. Clin Neuropsychol 12:43–55
10. Borkowski JG, Benton AL, Spreen O (1967) Word fluency and brain damage. Neuropsychologia 5(2):135–140
11. Bouwman FH, Skolasky RL, Hes D, Selnes OA, Glass JD, Nance-Sproson TE, Royal W, Dal Pan GJ, McArthur JC (1998) Variable progression of HIV-associated dementia. Neurology 50(6):1814–1820
12. Boyle PA, Cohen RA, Paul R, Moser D, Gordon N (2002) Cognitive and motor impairments predict functional declines in patients with vascular dementia. Int J Geriatr Psychiatry 17(2):164–169
13. Boyle PA, Paul R, Moser D, Zawacki T, Gordon N, Cohen R (2003) Cognitive and neurological predictors of functional impairment in vascular dementia. Am J Geriatr Psychiatry 11(1):103–106
14. Brandt J, Benedict RHB (2001) Hopkins Verbal Learning Test—Revised. Professional manual. Psychological Assessment Resources, Inc., Lutz
15. Caniglia EC, Cain LE, Justice A, Tate J, Logan R, Sabin C, Winston A, van Sighem A, Miro JM, Podzamczer D, Olson A, Arribas JR, Moreno S, Meyer L, del Romero J, Dabis F, Bucher HC, Wandeler G, Vourli G, Skoutelis A, Lanoy E, Gasnault J, Costagliola D, Hernán MA, HIV-CAUSAL Collaboration (2014) Antiretroviral penetration into the CNS and incidence of AIDS-defining neurologic conditions. Neurology 83(2):134–141
16. Cattie JE, Doyle K, Weber E, Grant I, Woods SP, HIV Neurobehavioral Research Program (HNRP) Group (2012) Planning deficits in HIV-associated neurocognitive disorders: component processes, cognitive correlates, and implications for everyday functioning. J Clin Exp Neuropsychol 34(9):906–918
17. Centers for Disease Control and Prevention (2011) Diagnoses of HIV infection in the United States and dependent areas HIV/AIDS Surveillance Report 23:1–84
18. Chang L, Andres M, Sadino J, Jiang CS, Nakama H, Miller E, Ernst T (2011) Impact of apolipoprotein E ε4 and HIV on cognition and brain atrophy: antagonistic pleiotrophy and premature brain aging. Neuroimag 58(4):1017–1027
19. Chang L, Holt JL, Yahupov R, Jiang CS, Ernst T (2013) Lower cognitive reserve in the aging human immunodeficiency virus-infected brain. Neurobiol Aging 34(4):1240–1253
20. Chang L, Wong V, Nakama H, Watters M, Ramones D, Miller EN, Cloak C, Ernst T (2008) Greater than age-related changes in brain diffusion of HIV patients after 1 year. J Neuroimmune Pharmacol 3(4):265–274
21. Chiesi A, Seeber AC, Dally LG, Floridia M, Rezza G, Vella S (1996a) AIDS dementia complex in the Italian National AIDS Registry: temporal trends (1987–93) and differential incidence according to mode of transmission of HIV-1 infection. J Neurol Sci 144(1–2):107–113
22. Chiesi A, Vella S, Dally LG, Pendersen C, Danner S, Johnson AM, Schwander S, Goebel FD, Glauser M, Antunes F (1996b) Epidemiology of AIDS dementia complex in Europe. AIDS in Europe Study Group. J Acquir Immune Defic Syndr Hum Retrovirol 11(1):39–44
23. Clark US, Cohen RA, Sweet LH, Gongvatana A, Devlin KN, Hana GN, Westbrook ML, Mulligan RC, Jerskey BA, White TL, Navia B, Tashima KT (2012) Effects of HIV and early life stress on amygdala morphometry and neurocognitive function. J Int Neuropsychol Soc 18(4):657–658
24. Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maquire RP, Hyman BT, Albert MS, Killany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 31(3):968–980
25. Fama R, Rosenbloom MJ, Sassoon SA, Rohlfing T, Pfefferbaum A, Sullivan EV (2014) Thalamic volume deficit contributes to procedural and explicit memory impairment in HIV infection with primary alcoholism comorbidity. Brain Imaging Behav 8(4):611–620
26. Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci U S A 97(20):11050–11055
27. Fischl B, David H, Salat EB, Albert M, Dieterich M, Haselgrove C, Van Der Kouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33(3):341–355
28. Ge Y, Kolson DL, Babb JS, Mannon LJ, Grossman RI (2003) Whole brain imaging of HIV-infected patients: quantitative analysis of magnetization transfer ratio histogram and fractional brain volume. AJNR Am J Neuroradiol 24(1):82–87
29. Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS (2001) A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 14(1 Pt 1):21–36
30. Goodkin K, Wilkie FL, Concha M, Asthana D, Shapshak P, Douyon R, Fujimura RK, LoPiccolo C (1997) Subtle neuropsychological impairment and minor cognitive-motor disorder in HIV-1 infection. Neuroimaging Clin N Am 7(3):561−579
31. Grant I, Franklin DR Jr, Deutsch R, Woods SP, Vaida F, Ellis RJ, Letendre SL, Marcotte TD, Atkinson JH, Collier AC, Marra CM, Clifford DB, Gelman BB, McArthur JC, Morgello S, Simpson DM, McCutchan JA, Abramson I, Gamst A, Fennema-Notestine C, Smith DM, Heaton RK, CHARTER Group (2014) Asymptomatic HIV-associated neurocognitive impairment increases risk for symptomatic decline. Neurology 82(23):2055–2062
32. Grant I, Marcotte TD, Heaton RK, HNRC Group (1999) Neurocognitive complications of HIV disease. Psychol Sci 10(3):191–195
33. Heaps JM, Joska J, Hoare J, Ortega M, Agrawal A, Seedat S, Ances BM, Stein DJ, Paul R (2012) Neuroimaging markers of human immunodeficiency virus infection in South Africa. J Neurovirol 18(3):151–156
34. 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, CHARTER Group (2010) HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy CHARTER STUDY. Neurology 75(23):2087–2096
35. Heaton RK, Marcotte TD, Mindt MR, Sadek J, Moore DJ, Bentley H, McCutchan JA, Reichs C, Grant I, HNRC Group (2004) The impact of HIV-associated neuropsychological impairment on everyday functioning. J Int Neuropsychol Soc 10(3):317–331
36. Hestad K, Aukrist P, Tønseth S, Reitan SK (2009) Depression has a strong relationship with alterations in the immune, endocrine and neural system. Curr Psychiatry Rev 5:287–297
37. Hestad KA, Menon JA, Silalukey-Ngoma M, Franklin DR Jr, Imasiku ML, Kalima K, Heaton RK (2012) Sex differences in neuropsychological performance as an effect of immunodeficiency virus infection: a pilot study in Zambia, Africa. J Nerv Ment Dis 200(4):336–342
38. Jernigan TL, Archibald S, Hesselink JR, Atkinson JH, Velin RA, McCutchan JA, Chandler J, Grant I (1993) Magnetic resonance imaging morphometric analysis of cerebral volume loss in human immunodeficiency virus infection. The HNRC Group. Arch Neurol 50(3):250–255
39. 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(8):1461–1472
40. Joint United Nations Programme on HIV/AIDS. Global Report UNAIDS report on the global AIDS epidemic 2013. Available at: http://www.unaids.org/en/media/unaids/contentassets/documents/epidemiology/2013/gr2013/UNAIDS_Global_Report_2013_en.pdf. Accessed April 16, 2014.
41. Kauf TL, Roskell N, Shearer A, Gazzard B, Mauskopf J, Davis EA, Nimsch C (2008) A predictive model of health state utilities for HIV patients in the modern era of highly active antiretroviral therapy. Value Health 11(7):1144–1153
42. Klove H (1963) Grooved pegboard. Lafayette Instruments, Indiana
43. Kumar AM, Ownby RL, Waldrop-Valverde D, Fernandez B, Kumar M (2011) Human immunodeficiency virus infection in the CNS and decreased dopamine availability: relationship with neuropsychological performance. J Neurovirol 17(1):26–40
44. Lüders E, Steinmetz H, Jäncke L (2002) Brain size and grey matter volume in the healthy human brain. Neuroreport 13(17):2371–2374
45. Maki PM, Martin-Thormeyer E (2009) HIV, cognition and women. Neuropsychol Rev 19:204–214
46. 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(3):231–240
47. Martin E, Gonzalez R, Vassileva J, Maki P (2011) HIV+ men and women show different performance patterns on procedural learning tasks. J Clin Exp Neuropsychol 33(1):112–120
48. Mason KI, Campbell A, Hawkins P, Madhere S, Johnson K, Takushi-Chinen R (1998) Neuropsychological functioning in HIV-positive African-American women with a history of drug use. J Natl Med Assoc 90(11):665–674
49. Miller EN, Selnes OA, McArthur JC, Satz P, Becker JT, Cohen BA, Sheridan K, Machado AM, Van Gorp WG, Visscher B (1990) Neuropsychological performance in HIV-1-infected homosexual men: the Multicenter AIDS Cohort Study (MACS). Neurology 40(2):197–203
50. Molsberry SA, Lecci F, Kingsley L, Junker B, Reynolds S, Goodkin K, Levine AJ, Martin E, Miller EN, Munro CA, Ragin A, Sacktor N, Becker JT (2015) Mixed membership trajectory models of cognitive impairment in the multicenter AIDS cohort study. AIDS 29(6):713−721
51. Morlat P, Parneix P, Douard D, Lacoste D, Dupon M, Chėne G, Pellegrin JL, Ragnaud JM, Dabis F (1992) Women and HIV infection: a cohort study of 483 HIV-infected women in Bordeaux, France, 1985–1991. The Group d’Epidémiologi Clinique du SIDA en Aquitaine. AIDS 6(10):1187–1193
52. Ortega M, Heaps JM, Joska J, Vaida F, Seedat S, Stein DJ, Paul R, Ances BM (2013) HIV clades B and C are associated with reduced brain volumetrics. J Neuroviol 19(5):479–487
53. Paul R, Cohen R, Navia B, Tashima K (2002) Relationships between cognition and structural neuroimaging findings in adults with human immunodeficiency virus type-1. Neurosci Biobehav Rev 26(3):353–359
54. Pereira M, Canavarro MC (2011) Gender and age differences in quality of life and the impact of psychopathological symptoms among HIV-infected patients. AIDS Behav 15(8):1857–1869
55. 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(Pt 1):48–64
56. 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(1):239–251
57. 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 72(5):361–370
58. Piatt AL, Fiels JA, Paolo AM, Troster AI (1999) Action (verb naming) fluency as an executive function measure: convergent and divergent evidence of validity. Neuropsychologica 37(13):1499–1503
59. Ragin AB, Wu Y, Storey P, Cohen BA, Edelman RR, Epstein LG (2005) Diffusion tensor imaging of subcortical brain injury in patients infected with human immunodeficiency virus. J Neurovirol 11(3):292–298
60. Raz N, Gunning-Dixon F, Head D, Williamson A, Acker JD (2001) Age and sex differences in the cerebellum and the ventral pons: a prospective MR study of healthy adults. AJNR Am J Neuroradiol 22(6):1161–1167
61. Reger M, Welsh R, Razani J, Martin DJ, Boone KB (2002) A meta-analysis of the neuropsychological sequelae of HIV infection. J Int Neuropsychol Soc 8(3):410–424
62. Reitan RM, Davison LA (1974) Clinical neuropsychology: current status and applications. Hemisphere, New York
63. Robertson K, Liner J, Meeker RB (2012) Antiretroviral neurotoxicity. J Neurovirol 18(5):388–399
64. Robertson K, Wilkins J, Messenheimer J, Robertson W, Hall C (1996) Gender differences in HIV neurological progression: a preliminary study. J NeuroAIDS 1:166
65. Robertson KR, Kapoor C, Robertson WT, Fiscus S, Ford S, Hall CD (2004) No gender difference in the progression of nervous system disease in HIV infection. J Acquir Immune Defic Syndr 36(3):817
66. Rog LA, Park LQ, Harvey DJ, Huang C-J, Mackin S, Farias ST (2014) The independent contributions of cognitive impairment and neuropsychiatric symptoms to everyday function in older adults. Clinical Neuropsychol 28(2):215–236
67. Scott JC, Woods SP, Vigil O, Heaton RK, Schweinsburg BC, Ellis RJ, Grant I, Marcotte TD, San Diego HIV Neurobehavioral Research Center (HNRC) Group (2011) A neuropsychological investigation of multitasking in HIV infection: implications for everyday functioning. Neuropsychology 25(4):511–519
68. Spies G, Fennema-Notestine C, Archibald SL, Cherner M, Seedat S (2012) Neurocognitive deficits in HIV-infected women and victims of childhood trauma. AIDS Care 24(9):1126–1135
69. 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 Neurovirol 55(2):161–168
70. Tate DF, Conley J, Paul RH, Coop K, Zhang S, Zhou W, Laidlaw DH, Taylor LE, Flanigan T, Navia B, Cohen R, Tashima K (2010) Quantitative diffusion tensor imaging tractography metrics are associated with cognitive performance among HIV-infected patients. Brain Imaging Behav 4(1):68–79
71. Teoh SK, Mendelson JH, Woods BT, Mello NK, Hallgring E, Anfinsen P, Douglas A, Mercer G (1993) Pituitary volume in men with concurrent heroin and cocaine dependence. J Clin Endocrinol Metab 76(6):1529–1532
72. Thames AD, Arentoft A, Rivera-Mindt M, Hinkin CH (2013) Functional disability in medication management and driving among individuals with HIV: a 1-year follow up study. J Clin Exp Neuropsychol 35(1):49–58
73. Thompson PM, Dutton RA, Hayashi KM, Toga AW, Lopez OL, Alzenstein HJ, Becker JT (2005) Thinning of the cerebral cortex visualized in HIV/AIDS reflects CD4+ T lymphocyte decline. Proc Natl Acad Sci U S A 102(43):15647–15652
74. Thurnher MM, Castillo M, Stadler A, Rieger A, Schmid B, Sundgren PC (2005) Diffusion-tensor MR imaging od the brain in human immunodeficiency virus-positive patients. AJNR Am J Neuroradiol 26(9):2275–2281
75. Tomaszewski FS, Cahn-Weiner DA, Harvey DJ, Reed BR, Mungas D, Kramer JH, Chui H (2009) Longitudinal changes in memory and executive functioning are associated with longitudinal changes in instrumental activities of daily living in older adults. Clin Neuropsychol 23(3):446–461
76. van Gorp WG, Miller EN, Marcotte TD, Dixon W, Paz D, Selnes O, Wesch J, Becker JT, Hinkin CH, Mitrushina M, Satz P, Weisman JD, Buckingham SL, Stenquist PK (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(5):929–935
77. Vellozzi C, Brooks JT, Bush TJ, Conley LJ, Henry K, Carpenter CC, Overton ET, Hammer J, Wood K, Holmberg SD, SUN Study Investigators (2009) The study to understand the natural history of HIV and AIDS in the era of effective therapy (SUN Study). Am J Epidemiol 69(5):642–652
78. Wechsler D (1997) WAIS-III: Weschsler Adult Intelligence Scale. Psychological Corporation, San Antonio
79. Willig JH, Abroms S, Westfall AO, Routman J, Adusumilli S, Varshney M, Allison J, Chatham A, Raper JL, Kaslow RA, Saag MS, Mugavero MJ (2008) Increased regimen durability in the era of once-daily fixed-dose combination antiretroviral therapy. AIDS 22(15):1951–1960
80. Wojna V, Skolasky RL, Hechavarría R, Mayo R, Seines O, McArthur JC, Meiēndez LM, Maldonado E, Zorrilla CD, García H, Kraiselburd E, Nath A (2006) Prevalence of human immunodeficiency virus-associated cognitive impairment in a group of Hispanic women at risk for neurological impairment. J Neurovirol 12(5):356–364
81. Woods SP, Moore DJ, Weber E, Grant I (2009) Cognitive neuropsychology of HIV-associated neurocognitive disorders. Neuropsychol Rev 19:152–168