Could antiretroviral neurotoxicity play a role in the pathogenesis of cognitive impairment in treated HIV disease?

AIDS

Volumn 29, Issue 3, 2014, Pages 253-261

  Underwood, Jonathan ^a,c   Robertson, Kevin R ^b   Winston, Alan ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c ST MARY S HOSPITAL   (United Kingdom)

Author keywords

Antiretroviral; Cognitive impairment; HIV; Neurotoxicity

Indexed keywords

ABACAVIR; AMPRENAVIR; ANTIRETROVIRUS AGENT; ATAZANAVIR; DARUNAVIR; DIDANOSINE; EFAVIRENZ; EMTRICITABINE; ETRAVIRINE; INDINAVIR; LAMIVUDINE; MARAVIROC; MITOCHONDRIAL DNA; NEVIRAPINE; NONNUCLEOSIDE REVERSE TRANSCRIPTASE INHIBITOR; RALTEGRAVIR; RITONAVIR; RNA DIRECTED DNA POLYMERASE INHIBITOR; SAQUINAVIR; STAVUDINE; TENOFOVIR; ZALCITABINE; ZIDOVUDINE;

ALZHEIMER DISEASE; CLINICAL PRACTICE; CLINICAL RESEARCH; COGNITIVE DEFECT; DRUG EFFICACY; DRUG WITHDRAWAL; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LYMPHOCYTIC INFILTRATION; MITOCHONDRIAL TOXICITY; NEUROTOXICITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; REVIEW; CHEMICALLY INDUCED; COMPLICATION; HIV INFECTIONS; MEDICAL RESEARCH; TRENDS;

ANTI-RETROVIRAL AGENTS; BIOMEDICAL RESEARCH; COGNITION DISORDERS; HIV INFECTIONS; HUMANS;

EID: 84927674275     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0000000000000538     Document Type: Review

References (57)

1. Guaraldi G, Orlando G, Zona S, Menozzi M, Carli F, Garlassi E, et al. Premature aging and premature age-related comorbidities in HIV-infected patients: facts and hypotheses. Clin Infect Dis 2011; 53:1127-1129
2. McArthur JC, Hoover DR, Bacellar H, Miller EN, Cohen BA, Becker JT, et al. Dementia in AIDS patients: incidence and risk factors. Multicenter AIDS Cohort Study. Neurology 1993; 43:2245-2252
3. Heaton RK, Franklin DR, Ellis RJ, McCutchan JA, Letendre SL, Leblanc S, et al. HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: differences in rates, nature, and predictors. J Neurovirol 2011; 17:3-16
4. Robertson KR, Smurzynski M, Parsons TD, Wu K, Bosch RJ, Wu J, et al. The prevalence and incidence of neurocognitive impairment in the HAART era. AIDS 2007; 21:1915-1921
5. Lescure F-X, Omland LH, Engsig FN, Roed C, Gerstoft J, Pialoux G, et al. Incidence and impact on mortality of severe neurocognitive disorders in persons with and without HIV infection: a Danish nationwide cohort study. Clin Infect Dis 2011; 52:235-243
6. Hinkin CH, Castellon SA, Durvasula RS, Hardy DJ, Lam MN, Mason KI, et al. Medication adherence among HIVR adults: effects of cognitive dysfunction and regimen complexity. Neurology 2002; 59:1944-1950
7. Wright EJ, Grund B, Robertson K, Brew BJ, Roediger M, Bain MP, et al. Cardiovascular risk factors associated with lower baseline cognitive performance in HIV-positive persons. Neurology 2010; 75:864-873
8. Soontornniyomkij V, Umlauf A, Soontornniyomkij B, Ben Gouaux, Toperoff W, Moore DJ, et al. Cerebral small vessel disease and HAND in ARV-treated subjects. CROI 2014 [Abstract 35]
9. High KP, Brennan-Ing M, Clifford DB, Cohen MH, Currier J, Deeks SG, et al. HIV and aging: state of knowledge and areas of critical need for research. A report to the NIH Office of AIDS Research by the HIV and Aging Working Group. J Acquir Immune Defic Syndr 2012; 60 (Suppl 1):S1-S18
10. Pathai S, Lawn SD, Gilbert CE, McGuinness D, McGlynn L, Weiss HA, et al. Accelerated biological ageing in HIV-infected individuals in South Africa. AIDS 2013; 27:2375-2384
11. Leeansyah E, Cameron PU, Solomon A, Tennakoon S, Velayudham P, Gouillou M, et al. Inhibition of telomerase activity by human immunodeficiency virus (HIV) nucleos(t)ide reverse transcriptase inhibitors: a potential factor contributing to HIV-associated accelerated aging. J Infect Dis 2013; 207:1157-1165
12. Lin MT, Beal MF. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006; 443:787-795
13. Zhang Y, Wang M, Li H, Zhang H, Shi Y, Wei F, et al. Accumulation of nuclear and mitochondrial DNA damage in the frontal cortex cells of patients with HIV-associated neurocognitive disorders. Brain Res 2012; 1458:1-11
14. Zhang Y, Song F, Gao Z, Ding W, Qiao L, Yang S, et al. Longterm exposure of mice to nucleoside analogues disrupts mitochondrial DNA maintenance in cortical neurons. PLoS One 2014; 9:e85637
15. White AJ. Mitochondrial toxicity and HIV therapy. Sex Transm Infect 2001; 77:158-173
16. Payne BAI, Wilson IJ, Hateley CA, Horvath R, Santibanez-Koref M, Samuels DC, et al. Mitochondrial aging is accelerated by antiretroviral therapy through the clonal expansion of mtDNA mutations. Nat Genet 2011; 43:806-810
17. Smyth K, Affandi JS, McArthur JC, Bowtell-Harris C, Mijch AM, Watson K, et al. Prevalence of and risk factors for HIV-associated neuropathy in Melbourne, Australia 1993-2006. HIV Med 2007; 8:367-373
18. Silva DF, Santana I, Esteves AR, Baldeiras I, Arduino DM, Oliveira CR, et al. Prodromal metabolic phenotype in MCI cybrids: implications for Alzheimer's disease. Curr Alzheimer Res 2013; 10:180-190
19. Robertson K, Liner J, Meeker RB. Antiretroviral neurotoxicity. J Neurovirol 2012; 18:388-399
20. Mehta A, Prabhakar M, Kumar P, Deshmukh R, Sharma PL. Excitotoxicity: bridge to various triggers in neurodegenerative disorders. Eur J Pharmacol 2013; 698:6-18
21. Vázquez-Santiago FJ, Noel RJ, Porter JT, Rivera-Amill V. Glutamate metabolism and HIV-associated neurocognitive disorders. J Neurovirol 2014; 20:315-331
22. Tovar-y-Romo LB, Bumpus NN, Pomerantz D, Avery LB, Sacktor N, McArthur JC, et al. Dendritic spine injury induced by the 8-hydroxy metabolite of efavirenz. J Pharmacol Exp Therapeut 2012; 343:696-703
23. Funes HA, Apostolova N, Alegre F, Blas-Garcia A, Alvarez A, Marti-Cabrera M, et al. Neuronal bioenergetics and acute mitochondrial dysfunction: a clue to understanding the central nervous system side effects of efavirenz. J Infect Dis 2014. 210:1385-1395
24. Streck EL, Scaini G, Rezin GT, Moreira J, Fochesato CM, Romão PRT. Effects of the HIV treatment drugs nevirapine and efavirenz on brain creatine kinase activity. Metab Brain Dis 2008; 23:485-492
25. Akay C, Cooper M, Odeleye A, Jensen BK, White MG, Vassoler F, et al. Antiretroviral drugs induce oxidative stress and neuronal damage in the central nervous system. J Neurovirol 2014; 20:39-53
26. Giunta B, Ehrhart J, Obregon DF, Lam L, Le L, Jin J, et al. Antiretroviral medications disrupt microglial phagocytosis of b-amyloid and increase its production by neurons: Implications for HIV-associated neurocognitive disorders. Molec Brain 2011; 4:23
27. Brown LAM, Jin J, Ferrell D, Sadic E, Obregon D, Smith AJ, et al. Efavirenz promotes (-secretase expression and increased A(1-40,42 via oxidative stress and reduced microglial phagocytosis: implications for HIV associated neurocognitive disorders (HAND). PLoS One 2014; 9:e95500
28. Giometto B, An SF, Groves M, Scaravilli T, Geddes JF, Miller R, et al. Accumulation of beta-amyloid precursor protein in HIV encephalitis: relationship with neuropsychological abnormalities. Ann Neurol 1997; 42:34-40
29. Goedert M, Spillantini MG, Crowther RA. Tau proteins and neurofibrillary degeneration. Brain Pathol 1991; 1:279-286
30. Anthony IC, Ramage SN, Carnie FW, Simmonds P, Bell JE. Accelerated Tau deposition in the brains of individuals infected with human immunodeficiency virus-1 before and after the advent of highly active antiretroviral therapy. Acta Neuropathol 2006; 111:529-538
31. Anthony IC, Ramage SN, Carnie FW, Simmonds P, Bell JE. Influence of HAART on HIV-related CNS disease and neuroinflammation. J Neuropathol Exp Neurol 2005; 64:529-536
32. López-Armada MJ, Riveiro-Naveira RR, Vaamonde-García C, Valcárcel-Ares MN. Mitochondrial dysfunction and the inflammatory response. Mitochondrion 2013; 13:106-118
33. Leuner K, M͡ller WE, Reichert AS. From mitochondrial dysfunction to amyloid beta formation: novel insights into the pathogenesis of Alzheimer's disease. Mol Neurobiol 2012; 46:186-193
34. Xie H, Guan J, Borrelli LA, Xu J, Serrano-Pozo A, Bacskai BJ. Mitochondrial alterations near amyloid plaques in an Alzheimer's disease mouse model. J Neurosci 2013; 33:17042-17051
35. Schouten J, Cinque P, Gisslen M, Reiss P, Portegies P. HIV-1 infection and cognitive impairment in the cART era: a review. AIDS 2011; 25:561-575
36. Jernigan TL, Archibald SL, Fennema-Notestine C, Taylor MJ, Theilmann RJ, Julaton MD, et al. Clinical factors related to brain structure in HIV: the CHARTER study. J Neurovirol 2011; 17:248-257
37. Becker JT, Maruca V, Kingsley LA, Sanders JM, Alger JR, Barker PB, et al. Factors affecting brain structure in men with HIV disease in the post-HAART era. Neuroradiology 2011; 54:113-121
38. Paul R, Cohen R, Navia B, Tashima K. Relationships between cognition and structural neuroimaging findings in adults with human immunodeficiency virus type-1. Neurosci Biobehav Rev 2002; 26:353-359
39. Hua X, Boyle CP, Harezlak J, Tate DF, Yiannoutsos CT, Cohen R, et al. Disrupted cerebral metabolite levels and lower nadir CD4R counts are linked to brain volume deficits in 210 HIVinfected patients on stable treatment. Neuroimage Clin 2013; 3:132-142
40. Schweinsburg BC, Taylor MJ, Alhassoon OM, Gonzalez R, Brown GG, Ellis RJ, et al. Brain mitochondrial injury in human immunodeficiency virus: seropositive (HIVR) individuals taking nucleoside reverse transcriptase inhibitors. J Neurovirol 2005; 11:356-364
41. Winston A, Duncombe C, Li PCK, Gill JM, Kerr SJ, Puls R, et al. Does choice of combination antiretroviral therapy (cART) alter changes in cerebral function testing after 48 weeks in treatment-naive, HIV-1-infected individuals commencing cART? A randomized controlled study. Clin Infect Dis 2010; 50:920-929
42. Winston A, Puls R, Kerr S, Duncombe C, Li P, Gill J, et al. Dynamics of changes in cerebral metabolites over 144 weeks in HIVR individuals commencing ART. CROI 2013[Abstract 462]
43. Gongvatana A, Harezlak J, Buchthal S, Daar E, Schifitto G, Campbell T, et al. Progressive cerebral injury in the setting of chronic HIV infection and antiretroviral therapy. J Neurovirol 2013; 19:209-218
44. Chang L, Yakupov R, Nakama H, Stokes B, Ernst T. Antiretroviral treatment is associated with increased attentional loaddependent brain activation in HIV patients. J Neuroimmune Pharmacol 2007; 19:169-185
45. Ances BM, Roc AC, Korczykowski M, Wolf RL, Kolson DL. Combination antiretroviral therapy modulates the blood oxygen level-dependent amplitude in human immunodeficiency virus-seropositive patients. J Neurovirol 2008; 14:418-424
46. Letendre S, Marquie-Beck J, Capparelli E, Best B, Clifford D, Collier AC, et al. Validation of the CNS penetration-effectiveness rank for quantifying antiretroviral penetration into the central nervous system. Arch Neurol 2008; 65:65-70
47. Ciccarelli N, Fabbiani M, Di Giambenedetto S, Fanti I, Baldonero E, Bracciale L, et al. Efavirenz associated with cognitive disorders in otherwise asymptomatic HIV-infected patients. Neurology 2011; 76:1403-1409
48. Letendre S, Vaida F, Croteau D, Clifford D, Collier A, Gelman B, et al. Long-term efavirenz use is associated with worse neurocognitive functioning. CROI 2013[Abstract 407]
49. Waters L, Fisher M, Winston A, Higgs C, Hadley W, Garvey L, et al. A phase IV, double-blind, multicentre, randomized, placebo-controlled, pilot study to assess the feasibility of switching individuals receiving efavirenz with continuing central nervous system adverse events to etravirine. AIDS 2011; 25:65-71
50. Nguyen A, Calmy A, Delhumeau C, Mercier I, Cavassini M, Mello AF, et al. A randomized cross-over study to compare raltegravir and efavirenz (SWITCH-ER study). AIDS 2011; 25:1481-1487
51. Madeddu G, Menzaghi B, Ricci E, Carenzi L, Martinelli C, di Biagio A, et al. Raltegravir central nervous system tolerability in clinical practice: results from a multicenter observational study. AIDS 2012; 26:2412-2415
52. Robertson KR, Su Z, Margolis DM, Krambrink A, Havlir DV, Evans S, et al. Neurocognitive effects of treatment interruption in stable HIV-positive patients in an observational cohort. Neurology 2010; 74:1260-1266
53. Tozzi V, Balestra P, Salvatori MF, Vlassi C, Liuzzi G, Giancola ML, et al. Changes in cognition during antiretroviral therapy: comparison of 2 different ranking systems to measure antiretroviral drug efficacy on HIV-associated neurocognitive disorders. J Acquir Immune Defic Syndr 2009; 52:56-63
54. Cysique LA, Vaida F, Letendre S, Gibson S, Cherner M, Woods SP, et al. Dynamics of cognitive change in impaired HIVpositive patients initiating antiretroviral therapy. Neurology 2009; 73:342-348
55. Marra CM, Zhao Y, Clifford DB, Letendre S, Evans S, Henry K, et al. Impact of combination antiretroviral therapy on cerebrospinal fluid HIV RNA and neurocognitive performance. AIDS 2009; 23:1359-1366
56. Caniglia EC, Cain LE, Justice A, Tate J, Logan R, Sabin C, et al. Antiretroviral penetration into the CNS and incidence of AIDSdefining neurologic conditions. Neurology 2014; 83:134-141
57. Winston A, Jose S, Gibbons S, Back D, Stohr W, Post F, et al. Effects of age on antiretroviral plasma drug concentration in HIV-infected subjects undergoing routine therapeutic drug monitoring. J Antimicrob Chemother 2013; 68:1354-1359.