Imaging Neuroinflammation? A Perspective from MR Spectroscopy

Brain Pathology

Volumn 24, Issue 6, 2014, Pages 654-664

  Zahr, Natalie M ^a,b   Mayer, Dirk ^b,c   Rohlfing, Torsten ^b   Sullivan, Edith V ^a   Pfefferbaum, Adolf ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SRI INTERNATIONAL   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

choline; in vivo; magnetic resonance spectroscopy; myo inositol

Indexed keywords

BIOLOGICAL MARKER; CHOLINE; EFAVIRENZ; EFAVIRENZ PLUS EMTRICITABINE PLUS TENOFOVIR DISOPROXIL; EMTRICITABINE; INOSITOL; TENOFOVIR; THIAMINE;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ADULT; AGED; ALCOHOL CONSUMPTION; ALCOHOLISM; ARTICLE; CONTROLLED STUDY; FEMALE; HEPATITIS C; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; METABOLITE; NERVOUS SYSTEM INFLAMMATION; NEUROIMAGING; NEUROPATHOLOGY; NUCLEAR MAGNETIC RESONANCE SCANNER; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; ACQUIRED IMMUNODEFICIENCY SYNDROME; BRAIN; COMPARATIVE STUDY; DRUG EFFECTS; FOLLOW UP; HIV INFECTIONS; IMMUNOLOGY; IMMUNOMODULATION; METABOLISM; MIDDLE AGED; PHYSIOLOGY; VERY ELDERLY; YOUNG ADULT;

ACQUIRED IMMUNODEFICIENCY SYNDROME; ADULT; AGED; AGED, 80 AND OVER; ALCOHOLISM; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; BRAIN; CHOLINE; FEMALE; FOLLOW-UP STUDIES; HEPATITIS C; HIV INFECTIONS; HUMANS; INOSITOL; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MIDDLE AGED; NEUROIMMUNOMODULATION; THIAMINE; YOUNG ADULT;

EID: 84911993093     PISSN: 10156305     EISSN: 17503639     Source Type: Journal    
DOI: 10.1111/bpa.12197     Document Type: Article

References (113)

1. Abers MS, Shandera WX, Kass JS, (2014) Neurological and psychiatric adverse effects of antiretroviral drugs. CNS Drugs 28: 131-145.
2. Allison JH, Cicero TJ, (1980) Alcohol acutely depresses myo-inositol 1-phosphate levels in the male rat cerebral cortex. J Pharmacol Exp Ther 213: 24-27.
3. Balasubramanya KS, Kovoor JM, Jayakumar PN, Ravishankar S, Kamble RB, Panicker J, Nagaraja D, (2007) Diffusion-weighted imaging and proton MR spectroscopy in the characterization of acute disseminated encephalomyelitis. Neuroradiology 49: 177-183.
4. Bartels AL, Leenders KL, (2007) Neuroinflammation in the pathophysiology of Parkinson's disease: evidence from animal models to human in vivo studies with [11C]-PK11195 PET. Mov Disord 22: 1852-1856.
5. Biller A, Bartsch AJ, Homola G, Solymosi L, Bendszus M, (2009) The effect of ethanol on human brain metabolites longitudinally characterized by proton MR spectroscopy. J Cereb Blood Flow Metab 29: 891-902.
6. Binesh N, Huda A, Thomas MA, Wyckoff N, Bugbee M, Han S, et al (2006) Hepatic encephalopathy: a neurochemical, neuroanatomical, and neuropsychological study. J Appl Clin Med Phys 7: 86-96.
7. Bizzi A, Ulug AM, Crawford TO, Passe T, Bugiani M, Bryan RN, Barker PB, (2001) Quantitative proton MR spectroscopic imaging in acute disseminated encephalomyelitis. AJNR Am J Neuroradiol 22: 1125-1130.
8. Bladowska J, Zimny A, Knysz B, Malyszczak K, Koltowska A, Szewczyk P, et al (2013) Evaluation of early cerebral metabolic, perfusion and microstructural changes in HCV-positive patients: a pilot study. J Hepatol 59: 651-657.
9. Block ML, Hong JS, (2005) Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog Neurobiol 76: 77-98.
10. Bothwell JH, Rae C, Dixon RM, Styles P, Bhakoo KK, (2001) Hypo-osmotic swelling-activated release of organic osmolytes in brain slices: implications for brain oedema in vivo. J Neurochem 77: 1632-1640.
11. Brand A, Richter-Landsberg C, Leibfritz D, (1993) Multinuclear NMR studies on the energy metabolism of glial and neuronal cells. Dev Neurosci 15: 289-298.
12. Braunova Z, Kasparova S, Mlynarik V, Mierisova S, Liptaj T, Tkac I, Gvozdjakova A, (2000) Metabolic changes in rat brain after prolonged ethanol consumption measured by 1H and 31P MRS experiments. Cell Mol Neurobiol 20: 703-715.
13. Brooks WM, Stidley CA, Petropoulos H, Jung RE, Weers DC, Friedman SD, et al (2000) Metabolic and cognitive response to human traumatic brain injury: a quantitative proton magnetic resonance study. J Neurotrauma 17: 629-640.
14. Brooks WM, Sibbitt WL Jr, Kornfeld M, Jung RE, Bankhurst AD, Roldan CA, (2010) The histopathologic associates of neurometabolite abnormalities in fatal neuropsychiatric systemic lupus erythematosus. Arthritis Rheum 62: 2055-2063.
15. Callot V, Galanaud D, Le Fur Y, Confort-Gouny S, Ranjeva JP, Cozzone PJ, (2008) (1)H MR spectroscopy of human brain tumours: a practical approach. Eur J Radiol 67: 268-274.
16. Campbell JH, Burdo TH, Autissier P, Bombardier JP, Westmoreland SV, Soulas C, et al (2011) Minocycline inhibition of monocyte activation correlates with neuronal protection in SIV neuroAIDS. PLoS ONE 6: e18688.
17. Castro-Fornieles J, Bargallo N, Lazaro L, Andres S, Falcon C, Plana MT, Junque C, (2007) Adolescent anorexia nervosa: cross-sectional and follow-up frontal gray matter disturbances detected with proton magnetic resonance spectroscopy. J Psychiatr Res 41: 952-958.
18. Cecil KM, Lenkinski RE, Meaney DF, McIntosh TK, Smith DH, (1998) High-field proton magnetic resonance spectroscopy of a swine model for axonal injury. J Neurochem 70: 2038-2044.
19. Chang L, Ernst T, Leonido-Yee M, Witt M, Speck O, Walot I, Miller EN, (1999) Highly active antiretroviral therapy reverses brain metabolite abnormalities in mild HIV dementia. Neurology 53: 782-789.
20. Chang L, Ernst T, Witt MD, Ames N, Gaiefsky M, Miller E, (2002) Relationships among brain metabolites, cognitive function, and viral loads in antiretroviral-naive HIV patients. Neuroimage 17: 1638-1648.
21. Chang L, Lee PL, Yiannoutsos CT, Ernst T, Marra CM, Richards T, et al (2004) A multicenter in vivo proton-MRS study of HIV-associated dementia and its relationship to age. Neuroimage 23: 1336-1347.
22. Chang L, Munsaka SM, Kraft-Terry S, Ernst T, (2013) Magnetic resonance spectroscopy to assess neuroinflammation and neuropathic pain. J Neuroimmune Pharmacol 8: 576-593.
23. Ciccarelli N, Fabbiani M, Di Giambenedetto S, Fanti I, Baldonero E, Bracciale L, et al (2011) Efavirenz associated with cognitive disorders in otherwise asymptomatic HIV-infected patients. Neurology 76: 1403-1409.
24. Cosenza MA, Zhao ML, Si Q, Lee SC, (2002) Human brain parenchymal microglia express CD14 and CD45 and are productively infected by HIV-1 in HIV-1 encephalitis. Brain Pathol 12: 442-455.
25. Crovitz HF, Zener KA, (1962) Group test for assessing hand and eye dominance. Am J Psychol 75: 271-276.
26. Cysique LA, Moffat K, Moore DM, Lane TA, Davies NW, Carr A, et al (2013) HIV, vascular and aging injuries in the brain of clinically stable HIV-infected adults: a (1)H MRS study. PLoS ONE 8: e61738.
27. De Stefano N, Matthews PM, Antel JP, Preul M, Francis G, Arnold DL, (1995) Chemical pathology of acute demyelinating lesions and its correlation with disability. Ann Neurol 38: 901-909.
28. De Stefano N, Filippi M, Miller D, Pouwels PJ, Rovira A, Gass A, et al (2007) Guidelines for using proton MR spectroscopy in multicenter clinical MS studies. Neurology 69: 1942-1952.
29. Decloedt EH, Maartens G, (2013) Neuronal toxicity of efavirenz: a systematic review. Expert Opin Drug Saf 12: 841-846.
30. Dreher W, Leibfritz D, (1999) Detection of homonuclear decoupled in vivo proton NMR spectra using constant time chemical shift encoding: CT-PRESS. Magn Reson Imaging 17: 141-150.
31. Filibian M, Frasca A, Maggioni D, Micotti E, Vezzani A, Ravizza T, (2012) In vivo imaging of glia activation using 1H-magnetic resonance spectroscopy to detect putative biomarkers of tissue epileptogenicity. Epilepsia 53: 1907-1916.
32. Fischer-Smith T, Croul S, Adeniyi A, Rybicka K, Morgello S, Khalili K, Rappaport J, (2004) Macrophage/microglial accumulation and proliferating cell nuclear antigen expression in the central nervous system in human immunodeficiency virus encephalopathy. Am J Pathol 164: 2089-2099.
33. Fonnum F, (1984) Glutamate: a neurotransmitter in the mammalian brain. J Neurochem 42: 1-11.
34. Fulham MJ, Bizzi A, Dietz MJ, Shih HH, Raman R, Sobering GS, et al (1992) Mapping of brain tumor metabolites with proton MR spectroscopic imaging: clinical relevance. Radiology 185: 675-686.
35. Fuller RA, Westmoreland SV, Ratai E, Greco JB, Kim JP, Lentz MR, et al (2004) A prospective longitudinal in vivo 1H MR spectroscopy study of the SIV/macaque model of neuroAIDS. BMC Neurosci 5: 10.
36. Gendelman HE, Baldwin T, Baca-Regen L, Swindells S, Loomis L, Skurkovich S, (1994) Regulation of HIV1 replication by interferon alpha: from laboratory bench to bedside. Res Immunol 145: 679-684, discussion 84-85.
37. Gendelman HE, Persidsky Y, Ghorpade A, Limoges J, Stins M, Fiala M, Morrisett R, (1997) The neuropathogenesis of the AIDS dementia complex. AIDS 11 (Suppl. A): S35-S45.
38. Ghafouri M, Amini S, Khalili K, Sawaya BE, (2006) HIV-1 associated dementia: symptoms and causes. Retrovirology 3: 28.
39. Gonzalez RG, Cheng LL, Westmoreland SV, Sakaie KE, Becerra LR, Lee PL, et al (2000) Early brain injury in the SIV-macaque model of AIDS. AIDS 14: 2841-2849.
40. Gonzalez-Scarano F, Martin-Garcia J, (2005) The neuropathogenesis of AIDS. Nat Rev Immunol 5: 69-81.
41. Govindaraju V, Young K, Maudsley AA, (2000) Proton NMR chemical shifts and coupling constants for brain metabolites. NMR Biomed 13: 129-153.
42. Graeber MB, (2010) Changing face of microglia. Science 330: 783-788.
43. Graeber MB, Streit WJ, Kreutzberg GW, (1988) Axotomy of the rat facial nerve leads to increased CR3 complement receptor expression by activated microglial cells. J Neurosci Res 21: 18-24.
44. Gray F, Chretien F, Vallat-Decouvelaere AV, Scaravilli F, (2003) The changing pattern of HIV neuropathology in the HAART era. J Neuropathol Exp Neurol 62: 429-440.
45. Grover VP, Pavese N, Koh SB, Wylezinska M, Saxby BK, Gerhard A, et al (2012) Cerebral microglial activation in patients with hepatitis C: in vivo evidence of neuroinflammation. J Viral Hepat 19: e89-e96.
46. Grovit-Ferbas K, Harris-White ME, (2010) Thinking about HIV: the intersection of virus, neuroinflammation and cognitive dysfunction. Immunol Res 48: 40-58.
47. Haase AT, (1986) The AIDS lentivirus connection. Microb Pathog 1: 1-4.
48. Haris M, Cai K, Singh A, Hariharan H, Reddy R, (2011) In vivo mapping of brain myo-inositol. Neuroimage 54: 2079-2085.
49. Häussinger D, Laubenberger J, Dahl SV, Ernst T, Bayer S, Langer M, et al (1994) Proton magnetic resonance spectroscopy studies on human brain myo-inositol in hypo-osmolarity and hepatic encephalopathy. Gastroenterology 107: 1475-1480.
50. Heindel WC, Jernigan TL, Archibald SL, Achim CL, Masliah E, Wiley CA, (1994) The relationship of quantitative brain magnetic resonance imaging measures to neuropathologic indexes of human immunodeficiency virus infection. Arch Neurol 51: 1129-1135.
51. Hollingshead A, (1975) Four-Factor Index of Social Status. Yale University, Department of Sociology: New Haven, CT.
52. Inglese M, Li BS, Rusinek H, Babb JS, Grossman RI, Gonen O, (2003) Diffusely elevated cerebral choline and creatine in relapsing-remitting multiple sclerosis. Magn Reson Med 50: 190-195.
53. Kaul M, Garden GA, Lipton SA, (2001) Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 410: 988-994.
54. Koopmans RA, Li DK, Zhu G, Allen PS, Penn A, Paty DW, (1993) Magnetic resonance spectroscopy of multiple sclerosis: in-vivo detection of myelin breakdown products. Lancet 341: 631-632.
55. Kramer-Hammerle S, Rothenaigner I, Wolff H, Bell JE, Brack-Werner R, (2005) Cells of the central nervous system as targets and reservoirs of the human immunodeficiency virus. Virus Res 111: 194-213.
56. Langford D, Masliah E, (2001) Crosstalk between components of the blood brain barrier and cells of the CNS in microglial activation in AIDS. Brain Pathol 11: 306-312.
57. Langford TD, Letendre SL, Marcotte TD, Ellis RJ, McCutchan JA, Grant I, et al (2002) Severe, demyelinating leukoencephalopathy in AIDS patients on antiretroviral therapy. AIDS 16: 1019-1029.
58. Langford TD, Letendre SL, Larrea GJ, Masliah E, (2003) Changing patterns in the neuropathogenesis of HIV during the HAART era. Brain Pathol 13: 195-210.
59. Laubenberger J, Haussinger D, Bayer S, Gufler H, Hennig J, Langer M, (1997) Proton magnetic resonance spectroscopy of the brain in symptomatic and asymptomatic patients with liver cirrhosis. Gastroenterology 112: 1610-1616.
60. Lentz MR, Westmoreland SV, Lee V, Ratai EM, Halpern EF, Gonzalez RG, (2008) Metabolic markers of neuronal injury correlate with SIV CNS disease severity and inoculum in the macaque model of neuroAIDS. Magn Reson Med 59: 475-484.
61. Letendre SL, Zheng JC, Kaul M, Yiannoutsos CT, Ellis RJ, Taylor MJ, et al (2011) Chemokines in cerebrospinal fluid correlate with cerebral metabolite patterns in HIV-infected individuals. J Neurovirol 17: 63-69.
62. Mader I, Rauer S, Gall P, Klose U, (2008) (1)H MR spectroscopy of inflammation, infection and ischemia of the brain. Eur J Radiol 67: 250-257.
63. Mascalchi M, Belli G, Guerrini L, Nistri M, Del Seppia I, Villari N, (2002) Proton MR spectroscopy of Wernicke encephalopathy. AJNR Am J Neuroradiol 23: 1803-1806.
64. Masliah E, DeTeresa RM, Mallory ME, Hansen LA, (2000) Changes in pathological findings at autopsy in AIDS cases for the last 15 years. AIDS 14: 69-74.
65. Mattis S, (2004) Dementia Rating Scale (DRS) Professional Manual. Psychological Assessment Resources, Inc.: Odessa, FL.
66. Mayer D, Spielman DM, (2005) Detection of glutamate in the human brain at 3 T using optimized constant time point resolved spectroscopy. Magn Reson Med 54: 439-442.
67. Mayer D, Zahr NM, Sullivan EV, Pfefferbaum A, (2007) In vivo metabolite differences between the basal ganglia and cerebellum of the rat brain detected with proton MRS at 3T. Psychiatry Res 154: 267-273.
68. McAndrews MP, Farcnik K, Carlen P, Damyanovich A, Mrkonjic M, Jones S, Heathcote EJ, (2005) Prevalence and significance of neurocognitive dysfunction in hepatitis C in the absence of correlated risk factors. Hepatology 41: 801-808.
69. McGeer PL, McGeer EG, (1999) Inflammation of the brain in Alzheimer's disease: implications for therapy. J Leukoc Biol 65: 409-415.
70. McGeer PL, McGeer EG, (2001) Inflammation, autotoxicity and Alzheimer disease. Neurobiol Aging 22: 799-809.
71. Meyerhoff DJ, Bloomer C, Cardenas V, Norman D, Weiner MW, Fein G, (1999) Elevated subcortical choline metabolites in cognitively and clinically asymptomatic HIV+ patients. Neurology 52: 995-1003.
72. Meyerhoff DJ, Blumenfeld R, Truran D, Lindgren J, Flenniken D, Cardenas V, et al (2004) Effects of heavy drinking, binge drinking, and family history of alcoholism on regional brain metabolites. Alcohol Clin Exp Res 28: 650-661.
73. Miese F, Kircheis G, Wittsack HJ, Wenserski F, Hemker J, Modder U, et al (2006) 1H-MR spectroscopy, magnetization transfer, and diffusion-weighted imaging in alcoholic and nonalcoholic patients with cirrhosis with hepatic encephalopathy. AJNR Am J Neuroradiol 27: 1019-1026.
74. Miller BL, (1991) A review of chemical issues in 1H NMR spectroscopy: N-acetyl-L-aspartate, creatine and choline. NMR Biomed 4: 47-52.
75. Miller DH, (2014) Magnetic resonance spectroscopy: a possible in vivo marker of disease progression for multiple sclerosis? JAMA Neurol 71: 828-830.
76. 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.
77. Monfort P, Cauli O, Montoliu C, Rodrigo R, Llansola M, Piedrafita B, et al (2009) Mechanisms of cognitive alterations in hyperammonemia and hepatic encephalopathy: therapeutical implications. Neurochem Int 55: 106-112.
78. Moore GJ, Koch S, Chen G, et al (1999) myo-Inositol is not exclusively glial in the human CNS. [Abstract] Proc Intl Soc Mag Reson Med 7: 33.
79. Murata T, Fujito T, Kimura H, Omori M, Itoh H, Wada Y, (2001) Serial MRI and (1)H-MRS of Wernicke's encephalopathy: report of a case with remarkable cerebellar lesions on MRI. Psychiatry Res 108: 49-55.
80. Nelson HE, (1982) The National Adult Reading Test (NART). Nelson Publishing Company: Windsor, Canada.
81. O'Callaghan JP, Sriram K, Miller DB, (2008) Defining "neuroinflammation." Ann N Y Acad Sci 1139: 318-330.
82. Peluso R, Haase A, Stowring L, Edwards M, Ventura P, (1985) A Trojan Horse mechanism for the spread of visna virus in monocytes. Virology 147: 231-236.
83. Peluso MJ, Meyerhoff DJ, Price RW, Peterson J, Lee E, Young AC, et al (2013) Cerebrospinal fluid and neuroimaging biomarker abnormalities suggest early neurological injury in a subset of individuals during primary HIV infection. J Infect Dis 207: 1703-1712.
84. Pfefferbaum A, Adalsteinsson E, Spielman D, Sullivan EV, Lim KO, (1999) In vivo spectroscopic quantification of the N-acetyl moiety, creatine, and choline from large volumes of brain gray and white matter: effects of normal aging. Magn Reson Med 41: 276-284.
85. Pulliam L, Herndier BG, Tang NM, McGrath MS, (1991) Human immunodeficiency virus-infected macrophages produce soluble factors that cause histological and neurochemical alterations in cultured human brains. J Clin Invest 87: 503-512.
86. Qian L, Flood PM, Hong JS, (2010) Neuroinflammation is a key player in Parkinson's disease and a prime target for therapy. J Neural Transm 117: 971-979.
87. Ratai EM, Pilkenton SJ, Greco JB, Lentz MR, Bombardier JP, Turk KW, et al (2009) In vivo proton magnetic resonance spectroscopy reveals region specific metabolic responses to SIV infection in the macaque brain. BMC Neurosci 10: 63.
88. Ratai EM, Annamalai L, Burdo T, Joo CG, Bombardier JP, Fell R, et al (2011) Brain creatine elevation and N-acetylaspartate reduction indicates neuronal dysfunction in the setting of enhanced glial energy metabolism in a macaque model of neuroAIDS. Magn Reson Med 66: 625-634.
89. Rezai-Zadeh K, Gate D, Town T, (2009) CNS infiltration of peripheral immune cells: D-Day for neurodegenerative disease? J Neuroimmune Pharmacol 4: 462-475.
90. Rock KL, Latz E, Ontiveros F, Kono H, (2010) The sterile inflammatory response. Annu Rev Immunol 28: 321-342.
91. Rogers J, Mastroeni D, Leonard B, Joyce J, Grover A, (2007) Neuroinflammation in Alzheimer's disease and Parkinson's disease: are microglia pathogenic in either disorder? Int Rev Neurobiol 82: 235-246.
92. Ross BD, Jacobson S, Villamil F, Korula J, Kreis R, Ernst T, et al (1994) Subclinical hepatic encephalopathy: proton MR spectroscopic abnormalities. Radiology 193: 457-463.
93. Schuhmann MU, Stiller D, Skardelly M, Bernarding J, Klinge PM, Samii A, et al (2003) Metabolic changes in the vicinity of brain contusions: a proton magnetic resonance spectroscopy and histology study. J Neurotrauma 20: 725-743.
94. Schweinsburg B, Taylor M, Videen J, Alhassoon O, Patterson T, Grant I, (2000) Elevated myo-inositol in gray matter of recently detoxified but not long-term abstinent alcoholics: a preliminary MR spectroscopy study. Alcohol Clin Exp Res 24: 699-705.
95. Stuckey DJ, Anthony DC, Lowe JP, Miller J, Palm WM, Styles P, et al (2005) Detection of the inhibitory neurotransmitter GABA in macrophages by magnetic resonance spectroscopy. J Leukoc Biol 78: 393-400.
96. Tarasow E, Wiercinska-Drapalo A, Jaroszewicz J, Orzechowska-Bobkiewicz A, Dzienis W, Prokopowicz D, Walecki J, (2004) Antiretroviral therapy and its influence on the stage of brain damage in patients with HIV-1H MRS evaluation. Med Sci Monit 10 (Suppl. 3): 101-106.
97. Thangnipon W, Taxt T, Brodal P, Storm-Mathisen J, (1983) The corticopontine projection: axotomy-induced loss of high affinity L-glutamate and D-aspartate uptake, but not of gamma-aminobutyrate uptake, glutamate decarboxylase or choline acetyltransferase, in the pontine nuclei. Neuroscience 8: 449-457.
98. Tracey I, Carr CA, Guimaraes AR, Worth JL, Navia BA, Gonzalez RG, (1996) Brain choline-containing compounds are elevated in HIV-positive patients before the onset of AIDS dementia complex: a proton magnetic resonance spectroscopic study. Neurology 46: 783-788.
99. Valcour V, Chalermchai T, Sailasuta N, Marovich M, Lerdlum S, Suttichom D, et al (2012) Central nervous system viral invasion and inflammation during acute HIV infection. J Infect Dis 206: 275-282.
100. Vazeux R, Brousse N, Jarry A, Henin D, Marche C, Vedrenne C, et al (1987) AIDS subacute encephalitis. Identification of HIV-infected cells. Am J Pathol 126: 403-410.
101. Vitaliano PP, Breen AR, Albert MS, Russo J, Prinz PN, (1984) Memory, attention, and functional status in community-residing Alzheimer type dementia patients and optimally healthy aged individuals. J Gerontol 39: 58-64.
102. Weissenborn K, Krause J, Bokemeyer M, Hecker H, Schuler A, Ennen JC, et al (2004) Hepatitis C virus infection affects the brain-evidence from psychometric studies and magnetic resonance spectroscopy. J Hepatol 41: 845-851.
103. Wiley CA, (2003) Detection of HIV-1 DNA in microglia/macrophages, astrocytes and neurons isolated from brain tissue with HIV-1 encephalitis by laser capture microdissection. Brain Pathol 13: 415.
104. Wiley CA, Schrier RD, Nelson JA, Lampert PW, Oldstone MB, (1986) Cellular localization of human immunodeficiency virus infection within the brains of acquired immune deficiency syndrome patients. Proc Natl Acad Sci U S A 83: 7089-7093.
105. Williams K, Westmoreland S, Greco J, Ratai E, Lentz M, Kim WK, et al (2005) Magnetic resonance spectroscopy reveals that activated monocytes contribute to neuronal injury in SIV neuroAIDS. J Clin Invest 115: 2534-2545.
106. Zahr NM, Mayer D, Pfefferbaum A, Sullivan EV, (2008) Low striatal glutamate levels underlie cognitive decline in the elderly: evidence from in vivo molecular spectroscopy. Cereb Cortex 18: 2241-2250.
107. Zahr NM, Mayer D, Vinco S, Orduna J, Luong R, Sullivan EV, Pfefferbaum A, (2009) In vivo evidence for alcohol-induced neurochemical changes in rat brain without protracted withdrawal, pronounced thiamine deficiency, or severe liver damage. Neuropsychopharmacology 34: 1427-1442.
108. Zahr NM, Mayer D, Rohlfing T, Hasak M, Hsu O, Vinco S, et al (2010) Brain injury and recovery following binge ethanol: evidence from in vivo magnetic resonance spectroscopy. Biol Psychiatry 67: 846-854.
109. Zahr NM, Mayer D, Rohlfing T, Chanraud S, Gu M, Sullivan EV, Pfefferbaum A, (2013) In vivo glutamate measured with magnetic resonance spectroscopy: behavioral correlates in aging. Neurobiol Aging 34: 1265-1276.
110. Zahr NM, Mayer D, Rohlfing T, Orduna J, Luong R, Sullivan EV, Pfefferbaum A, (2013) A mechanism of rapidly reversible cerebral ventricular enlargement independent of tissue atrophy. Neuropsychopharmacology 38: 1121-1129.
111. Zahr NM, Alt C, Mayer D, Rohlfing T, Manning-Bog A, Luong R, et al (2014) Associations between in vivo neuroimaging and postmortem brain cytokine markers in a rodent model of Wernicke's encephalopathy. Exp Neurol 25: 109-119.
112. Zahr NM, Mayer D, Rohlfing T, Hsu O, Vinco S, Orduna J, et al (2014) Rat strain differences in brain structure and neurochemistry in response to binge alcohol. Psychopharmacology (Berl) 231: 429-445.
113. Zemtsova I, Gorg B, Keitel V, Bidmon HJ, Schror K, Haussinger D, (2011) Microglia activation in hepatic encephalopathy in rats and humans. Hepatology 54: 204-215.