HIV clades B and C are associated with reduced brain volumetrics

Journal of NeuroVirology

Volumn 19, Issue 5, 2013, Pages 479-487

  Ortega, Mario ^a   Heaps, Jodi M ^b   Joska, John ^c   Vaida, Florin ^d   Seedat, Soraya ^e   Stein, Dan J ^c   Paul, Robert ^b   Ances, Beau M ^a,f  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MISSOURI ST LOUIS   (United States)

^c UNIVERSITY OF CAPE TOWN   (South Africa)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e STELLENBOSCH UNIVERSITY   (South Africa)

^f WASHINGTON UNIVERSITY   (United States)

Author keywords

Brain volumetrics; HIV clade; Magnetic resonance imaging; Neuropsychological performance

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; BRAIN CORTEX; BRAIN DISEASE; BRAIN SIZE; CAUDATE NUCLEUS; CD4 LYMPHOCYTE COUNT; COGNITIVE DEFECT; COHORT ANALYSIS; CONTROLLED STUDY; CORPUS CALLOSUM; FEMALE; GRAY MATTER; HIPPOCAMPUS; HIV ASSOCIATED DEMENTIA; HIV CLADE; HIV CLADE B; HIV CLADE C; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS PREVALENCE; MAJOR CLINICAL STUDY; MALE; MEMORY; NEUROPSYCHOLOGICAL TEST; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; PUTAMEN; SEX DIFFERENCE; SOUTH AFRICA; TASK PERFORMANCE; THALAMUS; UNITED STATES; VIRUS LOAD; VIRUS TYPING; WHITE MATTER;

ADULT; BRAIN; BRAIN MAPPING; CASE-CONTROL STUDIES; CD4 LYMPHOCYTE COUNT; COGNITION DISORDERS; EDUCATIONAL STATUS; FEMALE; HIV; HIV INFECTIONS; HUMANS; LINEAR MODELS; LONGITUDINAL STUDIES; MALE; MEMORY, SHORT-TERM; NEUROPSYCHOLOGICAL TESTS; ORGAN SIZE; TASK PERFORMANCE AND ANALYSIS;

EID: 84885621472     PISSN: 13550284     EISSN: 15382443     Source Type: Journal    
DOI: 10.1007/s13365-013-0202-x     Document Type: Article

References (51)

1. Ances BM, Sisti D, Vaida F, Liang CL, Leontiev O, Perthen JE, Buxton RB et al (2009) Resting cerebral blood flow: a potential biomarker of the effects of HIV in the brain. Neurology 73(9):702-708. doi: 10.1212/WNL.0b013e3181b59a97. Available at http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid= 2734291&tool=pmcentrez&rendertype=abstract
2. Ances BM, Ortega M, Vaida F, Heaps J, Paul R (2012) Independent effects of HIV, aging, and HAART on brain volumetric measures. Journal of Acquired Immune Deficiency Syndromes 59(5):469-477. doi: 10.1097/QAI.0b013e318249db17. Available at http://www.ncbi.nlm.nih.gov/pubmed/22269799
3. 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. The Journal of Infectious Diseases 201(3):336-340. doi: 10.1086/649899. Available at http://www. pubmedcentral.nih.gov/articlerender.fcgi?artid=2804778&tool= pmcentrez&rendertype=abstract
4. Anthony IC, Bell JE (2008) The neuropathology of HIV/AIDS. International Review of Psychiatry (Abingdon, England) 20(1): 15-24. doi: 10.1080/ 09540260701862037. Available at http://www.ncbi.nlm.nih.gov/pubmed/18240059
5. Antinori A, Arendt G, Becker JT, Brew BJ, Byrd DA, Cherner M, Clifford DB et al (2007) Updated research nosology for HIV-associated neurocognitive disorders. Neurology 69(18):1789-1799. doi: 10.1212/01.WNL.0000287431.88658.8b. Available at http://www.ncbi.nlm.nih.gov/pubmed/17914061
6. Archibald SL, Masliah E, Fennema-Notestine C, Marcotte TD, Ellis RJ, McCutchan JA, Heaton RK et al (2004) Correlation of in vivo neuroimaging abnormalities with postmortem human immunodeficiency virus encephalitis and dendritic loss. Archives of Neurology 61(3):369-376. doi: 10.1001/archneur.61.3. 369. Available at http://www.ncbi.nlm.nih.gov/pubmed/15023814
7. Arendt G, Hefter H, Elsing C, Strohmeyer G, Freund HJ (1990) Motor dysfunction in HIV-infected patients without clinically detectable central-nervous deficit. J Neurol 237(6):362-368. Available at http://www.springerlink.com/index/K76465858137QW16.pdf
8. Avison MJ, Nath A, Greene-Avison R, Schmitt FA, Greenberg RN, Berger JR (2004) Neuroimaging correlates of HIV-associated BBB compromise. Journal of Neuroimmunology 157(1-2):140-146. doi: 10.1016/j.jneuroim.2004.08.025. Available at http://www.ncbi.nlm.nih.gov/pubmed/15579291
9. Becker JT, Sanders J, Madsen SK, Ragin A, Kingsley L, Maruca V, Cohen B et al (2011) Subcortical brain atrophy persists even in HAART-regulated HIV disease. Brain Imaging Behav 5(2):77-85. doi: 10.1007/s11682-011-9113-8
10. Campbell GR, Watkins JD, Loret EP, Spector SA (2011) Differential induction of rat neuronal excitotoxic cell death by human immunodeficiency virus. AIDS Res Hum Retroviruses 27(6):647-654. doi: 10.1089/aid.2010.0192
11. Cardenas VA, Meyerhoff DJ, Studholme C, Kornak J, Rothlind J, Lampiris H, Neuhaus J et al (2009) Evidence for ongoing brain injury in human immunodeficiency virus-positive patients treated with antiretroviral therapy. Journal of Neurovirology 15(4):324-333. doi: 10.1080/13550280902973960. Available at http://informahealthcare.com/doi/abs/10.1080/13550280902973960
12. Carey CL, Woods SP, Gonzalez R, Conover E, Marcotte TD, Grant I, Heaton RK (2004) Predictive validity of global deficit scores in detecting neuropsychological impairment in HIV infection. Journal of Clinical and Experimental Neuropsychology 26(3):307-319. doi: 10.1080/13803390490510031. Available at http://www.ncbi.nlm.nih.gov/pubmed/15512922
13. 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 pleiotropy and premature brain aging. NeuroImage 58(4):1017-1027. doi: 10.1016/j.neuroimage.2011.07.010. Available at http://www.pubmedcentral. nih.gov/articlerender.fcgi?artid=3171637&tool=pmcentrez&rendertype= abstract
14. Clark US, Cohen RA, Sweet LH, Gongvatana A, Devlin KN, Hana GN, Westbrook ML et al (2012) Effects of HIV and early life stress on amygdala morphometry and neurocognitive function. Journal of the International Neuropsychological Society: JINS 18(4):657-668. doi: 10.1017/S1355617712000434. Available at http://www.ncbi.nlm.nih.gov/pubmed/22621973
15. Cohen RA, Harezlak J, Gongvatana A, Buchthal S, Schifitto G, Clark U, Paul R et al (2010) Cerebral metabolite abnormalities in human immunodeficiency virus are associated with cortical and subcortical volumes. Journal of Neurovirology 16(6): 435-444. doi: 10.3109/13550284.2010.520817
16. Constantino AA, Huang Y, Zhang H, Wood C, Zheng JC (2011) HIV-1 clade B and C isolates exhibit differential replication: relevance to macrophage-mediated neurotoxicity. Neurotoxicity Research 20(3):277-288. doi: 10.1007/s12640-011-9241-3. Available at http://www.pubmedcentral.nih.gov/ articlerender.fcgi?artid=3407549&tool=pmcentrez&rendertype=abstract
17. Crum-Cianflone NF, Roediger MP, Moore DJ, Hale B, Weintrob A, Ganesan A, Eberly LE, Johnson E, Agan BK, Letendre S (2012) Prevalence and factors associated with sleep disturbances among early-treated HIV-infected persons. Clinical Infectious Diseases: an Official Publication of the Infectious Diseases Society of America 54(10):1485-1494. doi: 10.1093/cid/cis192. Available at http://www.ncbi.nlm.nih.gov/pubmed/22431801
18. Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL et al (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. doi: 10.1016/j.neuroimage.2006.01.021. Available at http://www.ncbi.nlm.nih.gov/pubmed/16530430
19. Ellis RJ, Badiee J, Vaida F, Letendre S, Heaton RK, Clifford D, Collier AC et al (2011) CD4 nadir is a predictor of HIV neurocognitive impairment in the era of combination antiretroviral therapy. AIDS (London, England) 25(14):1747-1751. doi: 10.1097/QAD.0b013e32834a40cd. Available at http://www.ncbi.nlm.nih.gov/pubmed/21750419
20. Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences of the United States of America 97(20):11050-11055. doi: 10.1073/pnas.200033797. Available at http://www.pubmedcentral.nih.gov/ articlerender.fcgi?artid=27146&tool=pmcentrez&rendertype=abstract
21. Fischl B, David H, Salat EB, Albert M, Dieterich M, Haselgrove C, Van Der Kouwe A et al (2002) Whole brain segmentation: neurotechnique automated labeling of neuroanatomical structures in the human brain. Analysis 33:341-355
22. Gandhi N, Saiyed Z, Thangavel S, Rodriguez J, Rao KV, Nair MP (2009) Differential effects of HIV type 1 clade B and clade C Tat protein on expression of proinflammatory and antiinflammatory cytokines by primary monocytes. AIDS Research and Human Retroviruses 25(7):691-699. doi: 10.1089/aid.2008.0299. Available at http://online.liebertpub.com/doi/abs/10.1089/aid.2008.0299
23. 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. Journal of Neurovirology 17(5):477-486. doi: 10.1007/s13365-011-0055-0. Available at http://www.ncbi.nlm. nih.gov/pubmed/21965122
24. Gougeon ML, Piacentini M (2009) New insights on the role of apoptosis and autophagy in HIV pathogenesis. Apoptosis: an International Journal on Programmed Cell Death 14(4):501-508. doi: 10.1007/s10495-009-0314-1. Available at http://www.ncbi.nlm.nih.gov/pubmed/19199038
25. 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. Journal of Neurovirology 18(3):151-156. doi: 10.1007/s13365-012-0090-5. Available at http://www.ncbi.nlm.nih.gov/pubmed/ 22528474
26. Heaton RK, Clifford DB, Franklin DR, Woods SP, Ake C, Vaida F, Ellis RJ et al (2010) HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER study. Neurology 75(23):2087-2096. doi: 10.1212/WNL.0b013e318200d727. Available at http://www.pubmedcentral.nih.gov/ articlerender.fcgi?artid=2995535&tool=pmcentrez&rendertype=abstract
27. 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. European Archives of Psychiatry and Clinical Neuroscience 263(3):189-195. doi: 10.1007/s00406-012-0341-8. Available at http://www.ncbi.nlm.nih.gov/pubmed/ 22825739
28. Holt JL, Kraft-Terry SD, Chang L (2012) Neuroimaging studies of the aging HIV-1-infected brain. Journal of Neurovirology 18(4):291-302. doi: 10.1007/s13365-012-0114-1. Available at http://www.ncbi.nlm.nih.gov/pubmed/ 22653528
29. Jayadev S, Garden GA (2009) Host and viral factors influencing the pathogenesis of HIV-associated neurocognitive disorders. Journal of Neuroimmune Pharmacology 4(2):175-189. doi: 10.1007/s11481-009-9154-6.Host. Available at http://www.springerlink.com/index/3067M66N70454864.pdf
30. Joska JA, Westgarth-Taylor J, Myer L, Hoare J, Thomas KGF, Combrinck M, Paul RH, Stein DJ, Flisher AJ (2011) Characterization of HIV-associated neurocognitive disorders among individuals starting antiretroviral therapy in South Africa. AIDS and Behavior 15(6):1197-1203. doi: 10.1007/s10461-010-9744-6. Available at http://www.ncbi.nlm.nih.gov/pubmed/20614176
31. Kallianpur KJ, Kirk GR, Sailasuta N, Valcour V, Shiramizu B, Nakamoto BK, Shikuma C (2012) Regional cortical thinning associated with detectable levels of HIV DNA. Cerebral Cortex 22(9):2065-2075. doi: 10.1093/cercor/bhr285. Available at http://www.ncbi.nlm.nih.gov/pubmed/22016479
32. Kaul M, Garden GA, Lipton SA (2001) Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 410:988-994
33. Kumar AM, Fernandez JB, Singer EJ, Commins D, Waldrop-Valverde D, Ownby RL, Kumar M (2009) Human immunodeficiency virus type 1 in the central nervous system leads to decreased dopamine in different regions of postmortem human brains. Journal of Neurovirology 15(3):257-274. doi: 10.1080/13550280902973952. Available at http://www.ncbi.nlm.nih.gov/pubmed/19499455
34. Mattson MP, Haughey NJ, Nath A (2005) Cell death in HIV dementia. Cell Death and Differentiation 12(Suppl 1): 893-904. doi: 10.1038/sj.cdd.4401577. Available at http://www.ncbi.nlm.nih.gov/pubmed/15761472
35. Mishra M, Vetrivel S, Siddappa NB, Ranga U, Seth P (2008) Clade-specific differences in neurotoxicity of human immunodeficiency virus-1 B and C Tat of human neurons: significance of dicysteine C30C31 motif. Annals of Neurology 63(3):366-376. doi: 10.1002/ana.21292. Available at http://www.ncbi.nlm.nih.gov/ pubmed/18074388
36. Modi G, Hari K, Modi M, Mochan A (2007) The frequency and profile of neurology in Black South African HIV infected (clade C) patients - a hospital-based prospective audit. Journal of the Neurological Sciences 254(1-2):60-64. doi: 10.1016/j.jns.2007.01.001. Available at http://www.ncbi.nlm.nih.gov/pubmed/17291536
37. Pfefferbaum A, Rosenbloom MJ, Rohlfing T, Kemper CA, Deresinski S, Sullivan EV (2009) Frontostriatal fiber bundle compromise in HIV infection without dementia. AIDS (London, England) 23(15):1977-1985. doi: 10.1097/QAD.0b013e32832e77fe. Available at http://www.pubmedcentral.nih.gov/ articlerender.fcgi?artid=2864007&tool=pmcentrez&rendertype=abstract
38. 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. Biological Psychiatry 72(5):361-370. doi: 10.1016/j.biopsych.2012.02.018. Available at http://www.ncbi.nlm.nih.gov/pubmed/ 22458948
39. Rambaut A, Posada D, Crandall KA, Holmes EC (2004) The causes and consequences of HIV evolution. Nature Reviews. Genetics 5(1):52-61. doi: 10.1038/nrg1246. Available at http://www.ncbi.nlm.nih.gov/pubmed/14708016
40. Rao VR, Neogi U, Talboom JS, Padilla L, Rahman M, Fritz-French C, Gonzalez-Ramirez S et al (2013) Clade C HIV-1 isolates circulating in Southern Africa exhibit a greater frequency of dicysteine motif-containing Tat variants than those in Southeast Asia and cause increased neurovirulence. Retrovirology 10(1):61. doi: 10.1186/1742-4690-10-61. Available at http://www.ncbi.nlm.nih. gov/pubmed/23758766
41. Rao VR, Sas AR, Eugenin EA, Siddappa NB, Bimonte-Nelson H, Berman JW, Ranga U, Tyor WR, Prasad VR (2008) HIV-1 clade-specific differences in the induction of neuropathogenesis. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience 28(40):10010-10016. doi: 10.1523/JNEUROSCI.2955-08.2008. Available at http://www.jneurosci.org/content/ 28/40/10010.short
42. Samikkannu T, Agudelo M, Gandhi N, Reddy P, Saiyed Z, Nwankwo D, Nair M (2011) Human immunodeficiency virus type 1 clade B and C Gp120 differentially induce neurotoxin arachidonic acid in human astrocytes: implications for neuroAIDS. Journal of NeuroVirology 17(3):230-238. doi: 10.1007/s13365-011-0026- 5. Available at http://dx.doi.org/10.1007/s13365-011-0026-5
43. Shapshak P, Kangueane P, Fujimura RK, Commins D, Chiappelli F, Singer E, Levine AJ et al (2011) Editorial neuroAIDS review. AIDS (London, England) 25(2):123-141. doi: 10.1097/QAD.0b013e328340fd42. Available at http://www.ncbi.nlm.nih.gov/pubmed/21076277
44. 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. Archives of Neurology 55(2):161-168. Available at http://www.ncbi.nlm.nih.gov/ pubmed/9482357
45. + T lymphocyte decline. Proc Natl Acad Sci U S A 102:15647-15652
46. Towgood KJ, Pitkanen M, Kulasegaram R, Fradera A, Kumar A, Soni S, Sibtain NA et al (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; a Journal Devoted to the Study of the Nervous System and Behavior 48(2):230-241. doi: 10.1016/j.cortex.2011.03.006. Available at http://www.ncbi.nlm.nih.gov/pubmed/21481856
47. Wadia RS, Pujari SN, Kothari S et al (2001) Neurological manifestations of HIV disease. J Assoc Phys India 49:343-348. Available at http://ukpmc.ac.uk/ abstract/MED/11291974
48. Wainberg MA (2004) HIV-1 subtype distribution and the problem of drug resistance. AIDS 18(Suppl 3):S63-S68. doi: 10.1097/01.aids.0000131319.67773.8e. Available at http://journals.lww.com/aidsonline/Abstract/2004/06003/HIV-1- subtype-distribution-and-the-problem-of-drug.12.aspx
49. Wang X, Foryt P, Ochs R, Chung JH, Wu Y, Parrish T, Ragin AB (2011) Abnormalities in resting-state functional connectivity in early human immunodeficiency virus infection. Brain Connectivity 1(3):207-217. doi: 10.1089/brain.2011.0016. Available at http://www.ncbi.nlm.nih.gov/pubmed/ 22433049
50. Wiley CA, Soontornniyomkij V, Radhakrishnan L, Masliah E, Mellors J, Hermann SA, Dailey P, Achim CL (1998) Distribution of brain HIV load in AIDS. Brain Pathology (Zurich, Switzerland) 8(2):277-284. Available at http://www.ncbi.nlm.nih.gov/pubmed/9804386
51. Yepthomi T, Paul R, Vallabhaneni S, Kumarasamy N, Tate DF, Solomon S, Flanigan T (2006) Neurocognitive consequences of HIV in Southern India: a preliminary study of clade C virus. Journal of the International Neuropsychological Society: JINS 12(3):424-430. Available at http://www.ncbi.nlm.nih.gov/pubmed/16903135