Korean Journal of Radiology

The Korean Society of Radiology (대한영상의학회)
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Altered White Matter Integrity in Human Immunodeficiency Virus-Associated Neurocognitive Disorder: A Tract-Based Spatial Statistics Study

  • Oh, Se Won (Department of Radiology, Soonchunhyang University Cheonan Hospital) ;
  • Shin, Na-Young (Department of Radiology, College of Medicine, The Catholic University of Korea) ;
  • Choi, Jun Yong (Department of Internal Medicine and AIDS Research Institute, Yonsei University College of Medicine) ;
  • Lee, Seung-Koo (Department of Radiology, Research Institute of Radiological Science, Yonsei University College of Medicine) ;
  • Bang, Mi Rim (Department of Radiology, College of Medicine, The Catholic University of Korea)
  • Received : 2017.04.03
  • Accepted : 2017.09.28
  • Published : 2018.06.01
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Abstract

Objective: Human immunodeficiency virus (HIV) infection has been known to damage the microstructural integrity of white matter (WM). However, only a few studies have assessed the brain regions in HIV-associated neurocognitive disorders (HAND) with diffusion tensor imaging (DTI). Therefore, we sought to compare the DTI data between HIV patients with and without HAND using tract-based spatial statistics (TBSS). Materials and Methods: Twenty-two HIV-infected patients (10 with HAND and 12 without HAND) and 11 healthy controls (HC) were enrolled in this study. A whole-brain analysis of fractional anisotropy (FA), mean diffusivity (MD), radial diffusivity (RD), and axial diffusivity was performed with TBSS and a subsequent 20 tract-specific region-of-interest (ROI)-based analysis to localize and compare altered WM integrity in all group contrasts. Results: Compared with HC, patients with HAND showed decreased FA in the right frontoparietal WM including the upper corticospinal tract (CST) and increased MD and RD in the bilateral frontoparietal WM, corpus callosum, bilateral CSTs and bilateral cerebellar peduncles. The DTI values did not significantly differ between HIV patients with and without HAND or between HIV patients without HAND and HC. In the ROI-based analysis, decreased FA was observed in the right superior longitudinal fasciculus and was significantly correlated with decreased information processing speed, memory, executive function, and fine motor function in HIV patients. Conclusion: These results suggest that altered integrity of the frontoparietal WM contributes to cognitive dysfunction in HIV patients.

Keywords

Acknowledgement

Supported by : National Research Foundation of Korea (NRF), Soonchunhyang University

References

  1. Holt JL, Kraft-Terry SD, Chang L. Neuroimaging studies of the aging HIV-1-infected brain. J Neurovirol 2012;18:291-302 https://doi.org/10.1007/s13365-012-0114-1
  2. 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 https://doi.org/10.1097/QAD.0b013e3283437f9a
  3. Dore GJ, McDonald A, Li Y, Kaldor JM, Brew BJ; National HIV Surveillance Committee. Marked improvement in survival following AIDS dementia complex in the era of highly active antiretroviral therapy. AIDS 2003;17:1539-1545 https://doi.org/10.1097/00002030-200307040-00015
  4. Ku NS, Lee Y, Ahn JY, Song JE, Kim MH, Kim SB, et al. HIVassociated neurocognitive disorder in HIV-infected Koreans: the Korean NeuroAIDS Project. HIV Med 2014;15:470-477 https://doi.org/10.1111/hiv.12137
  5. Chernoff RA, Martin DJ, Schrock DA, Huy MP. Neuropsychological functioning as a predictor of employment activity in a longitudinal study of HIV-infected adults contemplating workforce reentry. J Int Neuropsychol Soc 2010;16:38-48 https://doi.org/10.1017/S1355617709990828
  6. Antinori A, Arendt G, Becker JT, Brew BJ, Byrd DA, Cherner M, et al. Updated research nosology for HIV-associated neurocognitive disorders. Neurology 2007;69:1789-1799 https://doi.org/10.1212/01.WNL.0000287431.88658.8b
  7. Hill-Briggs F, Dial JG, Morere DA, Joyce A. Neuropsychological assessment of persons with physical disability, visual impairment or blindness, and hearing impairment or deafness. Arch Clin Neuropsychol 2007;22:389-404 https://doi.org/10.1016/j.acn.2007.01.013
  8. Ostrosky-Solis F, Ardila A, Rosselli M, Lopez-Arango G, Uriel-Mendoza V. Neuropsychological test performance in illiterate subjects. Arch Clin Neuropsychol 1998;13:645-660 https://doi.org/10.1093/arclin/13.7.645
  9. Masters MC, Ances BM. Role of neuroimaging in HIVassociated neurocognitive disorders. Semin Neurol 2014;34:89-102 https://doi.org/10.1055/s-0034-1372346
  10. Karampekios S, Hesselink J. Cerebral infections. Eur Radiol 2005;15:485-493 https://doi.org/10.1007/s00330-004-2556-1
  11. Sundgren PC, Dong Q, Gomez-Hassan D, Mukherji SK, Maly P, Welsh R. Diffusion tensor imaging of the brain: review of clinical applications. Neuroradiology 2004;46:339-350 https://doi.org/10.1007/s00234-003-1114-x
  12. Dore GJ, Correll PK, Li Y, Kaldor JM, Cooper DA, Brew BJ. Changes to AIDS dementia complex in the era of highly active antiretroviral therapy. AIDS 1999;13:1249-1253 https://doi.org/10.1097/00002030-199907090-00015
  13. Heaton RK, Chelune GJ, Talley JL, Kay GG, Curtiss G. Wisconsin card sorting test manual: revised and expanded. Odessa, FL: Psychological Assessment Resources, 1993:92-193
  14. Kim HK. Handbook of Rey-Kim memory assessment. Daegu: Neuropsychology Press, 1999:130-148
  15. Kim MK, Hyun MH. Relationships between Trail Making Test (A, B, B-A. B/A) scores and ape, education, comparison of performance head injury patient and psychiatric patient. Korean J Clin Psychol 2004;23:353-366
  16. Lee T. Normative values for the Grooved Pegboard Test in adult. Phys Ther Korea 2001;8:87-94
  17. Yeom TH, Park YS, Oh KJ, Kim JK, Lee YH. K-WAIS manual. Seoul: Korea Guidance, 1992:105-119
  18. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, et al. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 2006;31:1487-1505 https://doi.org/10.1016/j.neuroimage.2006.02.024
  19. Purohit V, Rapaka R, Frankenheim J, Avila A, Sorensen R, Rutter J. National Institute on Drug Abuse symposium report: drugs of abuse, dopamine, and HIV-associated neurocognitive disorders/HIV-associated dementia. J Neurovirol 2013;19:119-122 https://doi.org/10.1007/s13365-013-0153-2
  20. Mediouni S, Marcondes MC, Miller C, McLaughlin JP, Valente ST. The cross-talk of HIV-1 Tat and methamphetamine in HIV-associated neurocognitive disorders. Front Microbiol 2015;6:1164
  21. Lentz MR, Kim WK, Kim H, Soulas C, Lee V, Venna N, et al. Alterations in brain metabolism during the first year of HIV infection. J Neurovirol 2011;17:220-229 https://doi.org/10.1007/s13365-011-0030-9
  22. Valcour V, Chalermchai T, Sailasuta N, Marovich M, Lerdlum S, Suttichom D, et al. Central nervous system viral invasion and inflammation during acute HIV infection. J Infect Dis 2012;206:275-282 https://doi.org/10.1093/infdis/jis326
  23. Anthony IC, Bell JE. The neuropathology of HIV/AIDS. Int Rev Psychiatry 2008;20:15-24 https://doi.org/10.1080/09540260701862037
  24. Reiche EMV, Moritmoto HK, de Almeida ERD, Oliveira SR, Kallaur AP, Simao ANC. Oxidative stress and human immunodeficiency virus type 1 (HIV-1) infection. In: Dichi I, Bregano JW, Simao ANC, Cecchini R, eds. Role of oxidative stress in chronic diseases. Boca Raton, FL: CRC Press, 2014:45-89
  25. Barber SC, Shaw PJ. Oxidative stress in ALS: key role in motor neuron injury and therapeutic target. Free Radic Biol Med 2010;48:629-641 https://doi.org/10.1016/j.freeradbiomed.2009.11.018
  26. Wang X, Michaelis EK. Selective neuronal vulnerability to oxidative stress in the brain. Front Aging Neurosci 2010;2:12
  27. Chen Y, An H, Zhu H, Stone T, Smith JK, Hall C, et al. White matter abnormalities revealed by diffusion tensor imaging in non-demented and demented HIV+ patients. Neuroimage 2009;47:1154-1162 https://doi.org/10.1016/j.neuroimage.2009.04.030
  28. Correa DG, Zimmermann N, Doring TM, Wilner NV, Leite SC, Cabral RF, et al. Diffusion tensor MR imaging of white matter integrity in HIV-positive patients with planning deficit. Neuroradiology 2015;57:475-482 https://doi.org/10.1007/s00234-015-1489-5
  29. Feldman HM, Yeatman JD, Lee ES, Barde LH, Gaman-Bean S. Diffusion tensor imaging: a review for pediatric researchers and clinicians. J Dev Behav Pediatr 2010;31:346-356 https://doi.org/10.1097/DBP.0b013e3181dcaa8b
  30. Stebbins GT, Smith CA, Bartt RE, Kessler HA, Adeyemi OM, Martin E, et al. HIV-associated alterations in normalappearing white matter: a voxel-wise diffusion tensor imaging study. J Acquir Immune Defic Syndr 2007;46:564-573 https://doi.org/10.1097/QAI.0b013e318159d807
  31. Wu Y, Storey P, Cohen BA, Epstein LG, Edelman RR, Ragin AB. Diffusion alterations in corpus callosum of patients with HIV. AJNR Am J Neuroradiol 2006;27:656-660
  32. Zhu T, Zhong J, Hu R, Tivarus M, Ekholm S, Harezlak J, et al. Patterns of white matter injury in HIV infection after partial immune reconstitution: a DTI tract-based spatial statistics study. J Neurovirol 2013;19:10-23 https://doi.org/10.1007/s13365-012-0135-9
  33. Budde MD, Xie M, Cross AH, Song SK. Axial diffusivity is the primary correlate of axonal injury in the experimental autoimmune encephalomyelitis spinal cord: a quantitative pixelwise analysis. J Neurosci 2009;29:2805-2813 https://doi.org/10.1523/JNEUROSCI.4605-08.2009
  34. Shin NY, Hong J, Choi JY, Lee SK, Lim SM, Yoon U. Retrosplenial cortical thinning as a possible major contributor for cognitive impairment in HIV patients. Eur Radiol 2017;27:4721-4729 https://doi.org/10.1007/s00330-017-4836-6
  35. Thompson PM, Dutton RA, Hayashi KM, Toga AW, Lopez OL, Aizenstein HJ, et al. Thinning of the cerebral cortex visualized in HIV/AIDS reflects CD4+ T lymphocyte decline. Proc Natl Acad Sci U S A 2005;102:15647-15652 https://doi.org/10.1073/pnas.0502548102
  36. Stubbe-Drger B, Deppe M, Mohammadi S, Keller SS, Kugel H, Gregor N, et al.; German Competence Network HIV/AIDS. Early microstructural white matter changes in patients with HIV: a diffusion tensor imaging study. BMC Neurol 2012;12:23 https://doi.org/10.1186/1471-2377-12-23
  37. Schmahmann JD, Smith EE, Eichler FS, Filley CM. Cerebral white matter: neuroanatomy, clinical neurology, and neurobehavioral correlates. Ann N Y Acad Sci 2008;1142:266-309 https://doi.org/10.1196/annals.1444.017
  38. Turken A, Whitfield-Gabrieli S, Bammer R, Baldo JV, Dronkers NF, Gabrieli JD. Cognitive processing speed and the structure of white matter pathways: convergent evidence from normal variation and lesion studies. Neuroimage 2008;42:1032-1044 https://doi.org/10.1016/j.neuroimage.2008.03.057
  39. Gutierrez R, Boison D, Heinemann U, Stoffel W. Decompaction of CNS myelin leads to a reduction of the conduction velocity of action potentials in optic nerve. Neurosci Lett 1995;195:93-96 https://doi.org/10.1016/0304-3940(94)11789-L
  40. Tolhurst DJ, Lewis PR. Effect of myelination on the conduction velocity of optic nerve fibres. Ophthalmic Physiol Opt 1992;12:241-243
  41. Waxman SG. Determinants of conduction velocity in myelinated nerve fibers. Muscle Nerve 1980;3:141-150 https://doi.org/10.1002/mus.880030207
  42. Wilson TW, Heinrichs-Graham E, Robertson KR, Sandkovsky U, O'Neill J, Knott NL, et al. Functional brain abnormalities during finger-tapping in HIV-infected older adults: a magnetoencephalography study. J Neuroimmune Pharmacol 2013;8:965-974 https://doi.org/10.1007/s11481-013-9477-1
  43. Chung SJ, Shin JH, Cho KH, Lee Y, Sohn YH, Seong JK, et al. Subcortical shape analysis of progressive mild cognitive impairment in Parkinson's disease. Mov Disord 2017;32:1447-1456 https://doi.org/10.1002/mds.27106
  44. Katzen HL, Levin BE, Weiner W. Side and type of motor symptom influence cognition in Parkinson's disease. Mov Disord 2006;21:1947-1953 https://doi.org/10.1002/mds.21105
  45. Tomer R, Levin BE, Weiner WJ. Side of onset of motor symptoms influences cognition in Parkinson's disease. Ann Neurol 1993;34:579-584 https://doi.org/10.1002/ana.410340412

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