Skip to main content

Advertisement

SpringerLink
Log in

Gender Effects on HIV-Associated White Matter Alterations: A Voxel-Wise DTI Study

  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

Sexual dimorphisms within the human brain are well-documented. Human immunodeficiency virus (HIV) infection is associated with atrophy and microstructural white matter alterations, yet sex-specific dimorphic brain alterations in persons living with HIV have not been systematically examined. To address this issue, we evaluated regional differences in normal-appearing white matter (NAWM) in adults with and without HIV utilizing diffusion tensor imaging. Through a voxel-by-voxel analytic approach, sexual dimorphisms in NAWM anisotropy and diffusivity were identified. In comparison to seronegative men and women, HIV infection contributed to a decline in the distribution of anisotropic differences between the sexes. Alterations in diffusivity were more complex, with seropositive women demonstrating an increase in regional diffusivity, while seropositive men demonstrated a reduction in regional differences. Sex by serostatus interactions within the left frontal lobe and bilateral thalamic region were identified. These results suggest that HIV contributes to sex-specific microstructural NAWM alterations, such that sex and serostatus differentially alter the integrity of the neuronal matrix.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abe, O., Aoki, S., Hayashi, N., Yamada, H., Kunimatsu, A., Mori, H., et al. (2002). Normal aging in the central nervous system: Quantitative MR diffusion-tensor analysis. Neurobiology of Aging, 23, 433–441.

    PubMed  Google Scholar 

  • Abe, O., Yamasue, H., Kasai, K., Yamada, H., Aoki, S., Iwanami, A., et al. (2006). Voxel-based diffusion tensor analysis reveals aberrant anterior cingulum integrity in posttraumatic stress disorder due to terrorism. Psychiatry Research, 146, 231–242.

    PubMed  Google Scholar 

  • Allen, J. S., Damasio, H., Grabowski, T. J., Bruss, J., & Zhang, W. (2003). Sexual dimorphism and asymmetries in the gray-white composition of the human cerebrum. Neuroimage, 18, 880–894.

    PubMed  Google Scholar 

  • Amunts, K., Jancke, L., Mohlberg, H., Steinmetz, H., & Zilles, K. (2000). Interhemispheric asymmetry of the human motor cortex related to handedness and gender. Neuropsychologia, 38, 304–312.

    PubMed  CAS  Google Scholar 

  • Ballmaier, M., O’Brien, J. T., Burton, E. J., Thompson, P. M., Rex, D. E., Narr, K. L., et al. (2004). Comparing gray matter loss profiles between dementia with Lewy bodies and Alzheimer’s disease using cortical pattern matching: Diagnosis and gender effects. Neuroimage, 23, 325–335.

    PubMed  Google Scholar 

  • Beck, A. T. (1996). Beck Depression Inventory—II. San Antonio, TX: The Psychological Corporation.

    Google Scholar 

  • Bishop, K. M., & Wahlsten, D. (1997). Sex differences in the human corpus callosum: Myth or reality? Neuroscience and Biobehavior Review, 21(5), 581–601.

    CAS  Google Scholar 

  • Castelo, J. M., Courtney, M. G., Melrose, R. J., & Stern, C. E. (2007). Putamen hypertrophy in nondemented patients with human immunodeficiency virus infection and cognitive compromise. Archives of Neurology, 64(9), 1275–1280.

    PubMed  Google Scholar 

  • Coffey, C. E., Lucke, J. F., Saxton, J. A., Ratcliff, G., Unitas, L. J., Billig, B., et al. (1998). Sex differences in brain aging: A quantitative magnetic resonance imaging study. Archives of Neurology, 55(2), 169–179.

    PubMed  CAS  Google Scholar 

  • Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1975). ‘Mini-mental State’: A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatry Research, 12, 189–198.

    CAS  Google Scholar 

  • Geschwind, N., & Galaburda, A. M. (1985a). Cerebral lateralization. Biological mechanisms, associations, and pathology: I. A hypothesis and a program for research. Archives of Neurology, 42, 428–459.

    PubMed  CAS  Google Scholar 

  • Geschwind, N., & Galaburda, A. M. (1985b). Cerebral lateralization. Biological mechanisms, associations, and pathology: II. A hypothesis and a program for research. Archives of Neurology, 42, 521–552.

    PubMed  CAS  Google Scholar 

  • Geschwind, N., & Galaburda, A. M. (1985c). Cerebral lateralization. Biological mechanisms, associations, and pathology: III. A hypothesis and a program for research. Archives of Neurology, 42, 634–654.

    PubMed  CAS  Google Scholar 

  • Goldstein, J. M., Seidman, L. J., Horton, N. J., Makris, N., Kennedy, D. N., Caviness, V. S., et al. (2001). Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. Cerebral Cortex, 11, 490–497.

    PubMed  CAS  Google Scholar 

  • Good, C. D., Johnsrude, I. S., Ashburner, J., Henson, R. N., Friston, K. J., & Frackowiak, R. S. J. (2001a). A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage, 14, 21–36.

    PubMed  CAS  Google Scholar 

  • Good, C. D., Johnsrude, I. S., Ashburner, J., Henson, R. N., Friston, K. J., & Frackowiak, R. S. J. (2001b). Cerebral asymmetry and the effects of sex and handedness on brain structure: A voxel-based morphometric analysis of 465 normal adult human brains. Neuroimage, 14, 685–700.

    PubMed  CAS  Google Scholar 

  • Gur, R. C., Mozley, P. D., Resnick, S. M., Gottlieb, G. L., Kohn, M., Zimmerman, R., et al. (1991). Gender differences in age effect on brain atrophy measures by magnetic resonance imaging. Proceedings of the National Academy of Sciences of the United States of America, 88, 2845–2849.

    PubMed  CAS  Google Scholar 

  • Gur, R. C., Turetsky, B. I., Matsui, M., Yan, M., Bilker, W., Hughett, P., et al. (1999). Sex differences in brain gray and white matter in healthy young adults: correlations with cognitive performance. The Journal of Neuroscience, 19(10), 4065–4072.

    PubMed  CAS  Google Scholar 

  • Haselgrove, J. C., & Moore, J. R. (1996). Correction for distortion of echo-planar images used to calculate the apparent diffusion coefficient. Magnetic Resonance in Medicine, 36(6), 960–964.

    PubMed  CAS  Google Scholar 

  • Hoeft, F., Barnea-Goraly, N., Haas, B. W., Golarai, G., Ng, D., Mills, D., et al. (2007). More is not always better: increased fractional anisotropy of superior longitudinal fasciculus associated with poor visuospatial abilities in Williams syndrome. Journal of Neuroscience, 27, 11960–11965.

    PubMed  CAS  Google Scholar 

  • Hsu, J. L., Leemans, A., Bai, C. H., Lee, C. H., Tsai, Y. F., Chiu, H. C., et al. (2008). Gender differences and age-related white matter changes of the human brain: A diffusion tensor imaging study. Neuroimage, 39(2), 566–77.

    PubMed  Google Scholar 

  • Im, K., Lee, J. M., Lee, J., Shin, Y. W., Kim, I. Y., Kwon, J. S., et al. (2006). Gender difference analysis of cortical thickness in healthy young adults with surface-based methods. Neuroimage, 31, 31–38.

    PubMed  Google Scholar 

  • Jones, D. K., Symms, M. R., Cercignani, M., & Howard, R. J. (2005). The effect of filter size on VBM analyses of DT-MRI data. Neuroimage, 26, 546–554.

    PubMed  Google Scholar 

  • Kidron, D., Black, S. E., Stanchev, P., Buck, B., Szalai, J. P., Parker, J., et al. (1997). Quantitative MR volumetry in Alzheimer’s disease: Topographic markers and the effects of sex and education. Neurology, 49(6), 1504–1512.

    PubMed  CAS  Google Scholar 

  • Kingsley, P. B. (2006). Inroduction to diffusion tensor imaging mathematics: Part II. Anisotropy, diffusion weighting factors, and gradient encoding schemes. Concepts in Magnetic Resonance Part A, 28A(2), 123–154.

    Google Scholar 

  • Lacerda, A. L., Keshavan, M. S., Hardan, A. Y., Yorbik, O., Brambilla, P., Sassi, R. B., et al. (2004). Anatomic evaluation of the orbitofrontal cortex in major depressive disorder. Biological Psychiatry, 55(4), 353–358.

    PubMed  Google Scholar 

  • Lavretsky, H., Kurbanyan, K., Ballmaier, M., Mintz, J., Toga, A., & Kumar, A. (2004). Sex differences in brain structure in geriatric depression. American Journal of Geriatric Psychiatry, 12(6), 653–657.

    PubMed  Google Scholar 

  • Lopez, O. L., Wess, J., Sanchez, J., Dew, M. A., & Becker, J. T. (1999). Neurological characteristics of HIV-infected men and women seeking primary medical care. European Journal of Neurology, 6, 205–209.

    PubMed  CAS  Google Scholar 

  • Luders, E., Narr, K. L., Thompson, P. M., Rex, D. E., Jancke, L., Steinmetz, H., et al. (2004). Gender differences in cortical complexity. Nature Neuroscience, 7, 799–800.

    PubMed  CAS  Google Scholar 

  • Luders, E., Narr, K. L., Thompson, P. M., Woods, R. P., Rex, D. E., Jancke, L., et al. (2005). Mapping cortical gray matter in the young adult brain: Effects of gender. Neuroimage, 26, 493–501.

    PubMed  CAS  Google Scholar 

  • Luders, E., Narr, K. L., Zaidel, E., Thompson, P. M., & Toga, A. W. (2006). Gender effects on callosal thickness in scaled and unscaled space. Neuroreport, 17(11), 1103–1106.

    PubMed  Google Scholar 

  • Luders, E., Steinmetz, H., & Jancke, L. (2002). Brain size and grey matter volume in the healthy human brain. Neuroreport, 13, 2371–2374.

    PubMed  Google Scholar 

  • Maldjian, J. A., Laurienti, P. J., Kraft, R. A., & Burdette, J. H. (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage, 19(3), 1233–1239.

    PubMed  Google Scholar 

  • McEwen, B. (2002). Estrogen actions throughout the brain. Recent Progress in Hormone Research, 57, 357–384.

    PubMed  CAS  Google Scholar 

  • Medina, D., DeToledo-Morrell, L., Urresta, F., Gabrieli, J. D., Moseley, M., Fleischman, D., et al. (2006). White matter changes in mild cognitive impairment and AD: A diffusion tensor imaging study. Neurobiology of Aging, 27(5), 663–672.

    PubMed  Google Scholar 

  • Moseley, M. E. (2002). Diffusion tensor imaging and aging—A review. NMR Biomed, 15, 553–560.

    PubMed  Google Scholar 

  • Nicastri, E., Angeletti, C., Palmisano, L., Sarmati, L., Chiesi, A., Geraci, A., et al. (2005). Italian Antiretroviral Treatment Group. Gender differences in clinical progression of HIV-1-infected individuals during long-term highly active antiretroviral therapy. AIDS, 19(6), 577–583.

    PubMed  Google Scholar 

  • Nopoulos, P., Flaum, M., O’Leary, D., & Andreasen, N. C. (2000). Sexual dimorphism in the human brain: Evaluation of tissue volume, tissue composition and surface anatomy using magnetic resonance imaging. Psychiatry Research, 98, 1–13.

    PubMed  CAS  Google Scholar 

  • Oh, J. S., Song, I. C., Lee, J. S., Kang, H., Park, K. S., Kang, E., et al. (2007). Tractography-guided statistics (TGIS) in diffusion tensor imaging for the detection of gender difference of fiber integrity in the midsagittal and parasagittal corpora callosa. Neuroimage, 36(3), 606–616.

    PubMed  Google Scholar 

  • Paus, T., Otaky, N., Caramanos, Z., MacDonald, D., Zijdenbos, A., D’Avirro, D., et al. (1996). In vivo morphometry of the intrasulcal gray matter in the human cingulate, paracingulate, and superior-rostral sulci: Hemispheric asymmetries, gender differences and probability maps. Journal of Comparative Neurology, 376(4), 664–73.

    PubMed  CAS  Google Scholar 

  • Pfefferbaum, A., Rosenbloom, M., Deshmukh, A., & Sullivan, E. (2001). Sex differences in the effects of alcohol on brain structure. American Journal of Psychiatry, 158(2), 188–197.

    PubMed  CAS  Google Scholar 

  • Pierpaoli, C., & Basser, P. J. (1996). Toward a quatitative assessment of diffusion anisotropy. Magnetic Resonance in Medicine, 36(6), 893–906.

    PubMed  CAS  Google Scholar 

  • Power, C., Selnes, O. A., Grim, J. A., & McArthur, J. C. (1995). HIV Dementia Scale: A rapid screening test. Journal of Acquired Immune Deficiency Syndromes and Human Retrovirology, 8(3), 273–278.

    PubMed  CAS  Google Scholar 

  • Raz, N., Gunning-Dixon, F., Head, D., Rodrigue, K. M., Williamson, A., & Acker, J. D. (2004). Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex: Replicability of regional differences in volume. Neurobiology of Aging, 25(3), 377–396.

    PubMed  Google Scholar 

  • Raz, N., Gunning-Dixon, F., Head, D., Williamson, A., & Acker, J. D. (2001). Age and sex differences in the cerebellum and the ventral pons: A prospective MR study of healthy adults. American Journal of Neuroradiology, 22(6), 1161–1167.

    PubMed  CAS  Google Scholar 

  • Robertson, K., Fiscus, S., Wilkins, J., van der Horst, C., Hall, C. (1996). Viral load and nueropsychological functioning in HIV seropositive individuals: a preliminary descriptive study. Journal of Nuero-AIDS, 1(4), 7–15.

    CAS  Google Scholar 

  • Robertson, K. R., Kapoor, C., Robertson, W. T., Fiscus, S., Ford, S., & Hall, C. D. (2004). No gender difference in the progression of nervous system disease in HIV infection. Journal of Acquired Immune Deficiency Syndromes, 3, 817–822.

    Google Scholar 

  • Shin, Y. W., Ha, T. H., Park, H. J., Moon, W. J., Chung, E. C., Lee, J. M., et al. (2005). Sex differences in the human corpus callosum: Diffusion tensor imaging study. NeuroReport, 16, 795–798.

    PubMed  Google Scholar 

  • Smith, C. A., Stebbins, G. T., Bartt, R. E., Kessler, H. A., Adeyemi, O. M., Martin, E., et al. (2008). Increased white matter anisotropy and severity of depression symptoms in patients with HIV. Journal of Neuropsychiatry and Clinical Neurosciences (in press).

  • Stebbins, G. T., Smith, C. A., Bartt, R. E., Kessler, H. A., Adeyemi, O. M., Martin, E., et al. (2007). HIV-associated alterations in normal appearing white matter: A voxel-wise DTI study. Journal of Acquired Immune Deficiency Syndromes, 46, 564–573.

    PubMed  Google Scholar 

  • Stern, Y., McDermott, M. P., Albert, S., Palumbo, D., Selnes, O. A., McArthur, J., et al. (2001). Consortium on the therapy of HIV-dementia and related cognitive disorders. Factors associated with incident human immunodeficiency virus-dementia. Archives of Nuerology, 58(3), 473–479.

    CAS  Google Scholar 

  • Sullivan, E. V., Adalsteinsson, E., Hedehus, M., Ju, C., Moseley, M., Lim, K. O., et al. (2001a). Equivalent disruption of regional white matter microstructure in ageing healthy men and women. Neuroreport, 12(1), 99–104.

    PubMed  CAS  Google Scholar 

  • Sullivan, E. V., Rosenbloom, M. J., Desmond, J. E., & Pfefferbaum, A. (2001b). Sex differences in corpus callosum size: relationship to age and intracranial size. Neurobiology of Aging, 22(4), 603–11.

    PubMed  CAS  Google Scholar 

  • Sullivan, E. V., Rosenbloom, M., Serventi, K. L., & Pfefferbaum, A. (2004). Effects of age and sex on volumes of the thalamus, pons, and cortex. Neurobiology of Aging, 25(2), 185–192.

    PubMed  Google Scholar 

  • Swaab, D. F., Chung, W. C. J., Kruijver, F. P. M., Hofman, M. A., & Hestiantoro, A. (2003). Sex differences n the hypothalamus in the different stages of human life. Neurobiology of Aging, 24, S1–S16.

    PubMed  CAS  Google Scholar 

  • Szeszko, P. R., Vogel, J., Ashtari, M., Malhotra, A. K., Bates, J., Kane, J. M., et al. (2003). Sex differences in frontal lobe white matter microstructure: A DTI study. Neuroreport, 14(18), 2469–2473.

    PubMed  Google Scholar 

  • Wang, C., Stebbins, G. T., Nyenhuis, D. L., de Toledo-Morrell, L., Freels, S., Gencheva, E., et al. (2006). Longitudinalchanges in white matter following ischemic stroke: a three-year follow-up study. Neurobiology of Aging, 27(12), 1827–1833.

    PubMed  Google Scholar 

  • Wechsler Test of Adult Reading (2001). Psychological Assessment Resources. FL: ODESSA.

    Google Scholar 

  • Westerhausen, R., Kreuder, F., Sequeira, S. D. S., Walter, C., Woerner, W., Wittling, R. A., et al. (2004). Effects of handedness and gender on macro- and microstructure of the corpus callosum and its subregions: A combined high-resolution and diffusion-tensor imaging study. Cognitive Brain Research, 21, 418–426.

    PubMed  Google Scholar 

  • Westerhausen, R., Walter, C., Kreuder, F., Wittling, R. A., Schweiger, E., & Wittling, W. (2003). The influence of handedness and gender on the microstructure of the human corpus callosum: A diffusion-tensor magnetic resonance imaging study. Neuroscience Letters, 351, 99–102.

    PubMed  CAS  Google Scholar 

  • Wisniewski, A. B., Apel, S., Selnes, O. A., Nath, A., McArthur, J. C., & Dobs, A. S. (2005). Depressive symptoms, quality of life, and neuropsychological performance in HIV/AIDS: the impact of gender and injection drug use. Journal of Neurovirology, 11(2), 138–143.

    PubMed  Google Scholar 

  • Xu, J., Kobayashi, S., Yamaguchi, S., Iijima, K., Okada, K., & Yamashita, K. (2000). Gender effects on age-related changes in brain structure. American Journal of Neuroradiology, 21, 112–118.

    PubMed  CAS  Google Scholar 

Further Reading

  • Ances, B. M., Roc, A. C., Wang, J., Korczykowski, M., Okawa, J., Stern, J., et al. (2006). Caudate blood flow and volume are reduced in HIV + neurocognitively impaired patients. Neurology, 66, 862–866.

    PubMed  CAS  Google Scholar 

  • Archibald, S. L., Masliah, E., Fennema-Notestine, C., Marcotte, T. D., Ellis, R. J., McCutchan, J. A., et al. (2004). Correlation of in vivo neuroimaging abnormalities with postmortem Human Immunodeficiency Virus encephalitis and dentritic loss. Archives of Neurology, 61, 369–376.

    PubMed  Google Scholar 

  • Aylward, E. H., Brettschneider, P. D., McArthur, J. C., Harris, G. J., Schlaepfer, T. E., Henderer, J. D., et al. (1995). Magnetic resonance imaging measurement of gray matter volume reductions in HIV dementia. American Journal of Psychiatry, 152, 987–994.

    PubMed  CAS  Google Scholar 

  • Aylward, E. H., Henderer, J. D., McArthur, J. C., Brettschneider, P. D., Harris, G. J., Barta, P. E., et al. (1993). Reduced basal ganglia volume in HIV-1-associated dementia: results from quantitative neuroimaging. Neurology, 43, 2099–2104.

    PubMed  CAS  Google Scholar 

  • Bornstein, R. A., Chakeres, D., Brogan, M., Nasrallah, H. A., Fass, R. J., Para, M., et al. (1992). Magnetic resonance imaging of white matter lesions in HIV infection. Journal of Neuropsychiatry and Clinical Neurosciences, 4, 174–178.

    PubMed  CAS  Google Scholar 

  • Broderick, D. F., Wippold, F. J., Clifford, D. B., Kido, D., & Wilson, B. S. (1993). White matter lesions and cerebral atrophy on MR images in patients with and without AIDS dementia complex. American Journal of Roentgenology, 161, 177–181.

    PubMed  CAS  Google Scholar 

  • Chiang, M. C., Dutton, R. A., Hayashi, K. M., Lopez, O. L., Aizenstein, H. J., Toga, A. W., et al. (2007). 3D pattern of brain atrophy in HIV/AIDS visualized using tensor-based morphometry. Neuroimage, 34, 44–60.

    PubMed  Google Scholar 

  • Chong, W. K., Sweeney, B., Wilkinson, I. D., Paley, M., Hall-Craggs, M. A., Kendall, B. E., et al. (1993). Proton spectroscopy of the brain in HIV infection: Correlation with clinical, immunologic, and MR imaging findings. Radiology, 188, 119–1124.

    PubMed  CAS  Google Scholar 

  • Cloak, C. C., Chang, L., & Ernst, T. (2004). Increased frontal white matter diffusion is associated with glial metabolites and psychomotor slowing in HIV. Journal of Neuroimmunology, 157, 147–152.

    PubMed  CAS  Google Scholar 

  • Cohen, W. A., Maravilla, K. R., Gerlach, R., Claypoole, K., Collier, A. C., Marra, C., et al. (1992). Prospective cerebral MR study of HIV seropositive and seronegative men: Correlation of MR findings with neurologic, neuropsychologic, and cerebrospinal fluid analysis. American Journal of Neuroradiology, 13, 1231–1240.

    PubMed  CAS  Google Scholar 

  • Dal Pan, G. J., McArthur, J. H., Aylward, E., Selnes, O. A., Nance-Sproson, T. E., Kumar, A., et al. (1992). Patterns of cerebral atrophy in HIV-1-infected individuals: Results of a quantitative MRI analysis. Neurology, 42, 2125–2130.

    PubMed  CAS  Google Scholar 

  • Di Sclafani, V., Mackay, R. D., Meyerhoff, D. J., Norman, D., Weiner, M. W., & Fein, G. (1997). Brain atrophy in HIV infection is more strongly associated with CDC clinical stage than with cognitive impairment. Journal of the International Neuropsychological Society, 3, 276–287.

    PubMed  CAS  Google Scholar 

  • Dooneief, G., Bello, J., Todak, G., Mun, I. K., Marder, K., Malouf, R., et al. (1992). A prospective controlled study of magnetic resonance imaging of the brain in gay men and parenteral drug users with human immunodeficiency virus infection. Archives of Neurology, 49, 38–43.

    PubMed  CAS  Google Scholar 

  • Elovaara, I., Poutiainen, E., Raininko, R., Valanne, L., Virta, A., Valle, S. L., et al. (1990). Mild brain atrophy in early HIV infection: The lack of association with cognitive deficits and HIV-specific intrathecal immune response. Journal of Neurological Sciences, 99, 121–136.

    CAS  Google Scholar 

  • Filippi, C. G., Sze, G., Farber, S. J., Shahmanesh, M., & Selwyn, P. A. (1998). Regression of HIV encephalopathy and basal ganglia hyperintensity abnormality at MR imaging in patients with AIDS after the initiation of protease inhibitor therapy. Radiology, 206, 491–498.

    PubMed  CAS  Google Scholar 

  • Filippi, C. G., Ulug, A. M., Ryan, E., Ferrando, S. J., & van Gorp, W. (2001). Diffusion tensor imaging of patients with HIV and normal-appearing white matter on MR images of the brain. American Journal of Neuroradiology, 22, 277–283.

    PubMed  CAS  Google Scholar 

  • Flowers, C. H., Mafee, M. F., Crowell, R., Raofi, B., Arnold, P., Dobben, G., et al. (1990). Encephalopathy in AIDS patients: Evaluation with MR imaging. American Journal of Neuroradiology, 11, 1235–1245.

    PubMed  CAS  Google Scholar 

  • Ge, Y., Kolson, D. L., Babb, J. S., Mannon, L. J., & Grossman, R. I. (2003). Whole brain imaging of HIV-infected patients: quantitative analysis of magnetization transfer ratio histogram and fractional brain volume. American Journal of Neuroradiology, 24, 82–87.

    PubMed  Google Scholar 

  • Grant, I., Atkinson, J. H., Hesselink, J. R., Kennedy, C. J., Richman, D. D., Spector, S. A., et al. (1987). Evidence for early central nervous system involvement in the acquired immunodeficiency syndrome (AIDS) and other human immunodeficiency virus (HIV) infections. Studies with neuropsychologic testing and magnetic resonance imaging. Annals of Internal Medicine, 107, 828–836.

    PubMed  CAS  Google Scholar 

  • Hall, M., Whaley, R., Robertson, K., Hamby, S., Wilkins, J., & Hall, C. (1996). The correlation between neuropsychological and neuroanatomic changes over time in asymptomatic and symptomatic HIV-1-infected individuals. Neurology, 46, 1697–1702.

    PubMed  CAS  Google Scholar 

  • Handelsman, L., Song, I. S., Losonczy, M., Park, S., Jacobson, J., Wiener, J., et al. (1993). Magnetic resonance abnormalities in HIV infection: A study in the drug-user risk group. Psychiatry Research, 47, 175–186.

    PubMed  CAS  Google Scholar 

  • Harrison, M. J., Newman, S. P., Hall-Craggs, M. A., Fowler, C. J., Miller, R., Kendall, B. E., et al. (1998). Evidence of CNS impairment in HIV infection: Clinical, neuropsychological, EEG, and MRI/MRS study. Journal of Neurology, Neurosurgery, and Psychiatry, 65, 301–307.

    PubMed  CAS  Google Scholar 

  • Hestad, K., McArthur, J. H., Dal Pan, G. J., Selnes, O. A., Nance-Sproson, T. E., Aylward, E., et al. (1993). Regional brain atrophy in HIV-1 infection: Association with specific neuropsychological test performance. Acta Neurologica Scandinavica, 88, 112–118.

    PubMed  CAS  Google Scholar 

  • Heyes, M. P., Ellis, R. J., Ryan, L., Childers, M. E., Grant, I., Wolfson, T., et al. (2001). Elevated cerebrospinal fluid quinolinic acid levels are associated with region-specific cerebral volume loss in HIV infection. Brain, 124, 1033–1042.

    PubMed  CAS  Google Scholar 

  • Jarvik, J. G., Hesselink, J. R., Kennedy, C., Teschke, R., Wiley, C., Spector, S., et al. (1988). Acquired immunodeficiency syndrome: Magnetic resonance patterns of brain involvement with pathologic correlation. Archives of Neurology, 45, 731–736.

    PubMed  CAS  Google Scholar 

  • Jernigan, T. L., Archibald, S., Hesselink, J. R., Atkinson, J. H., Velin, R. A., McCutchan, J. A., et al. (1993). Magnetic resonance imaging morphometric analysis of cerebral volume loss in Human Immunodeficiency Virus infection. Archives of Neurology, 50, 250–255.

    PubMed  CAS  Google Scholar 

  • Jernigan, T. L., Gamst, A. C., Archibald, S. L., Fennema-Notestine, C., Mindt, M. R., Marcotte, T. D., et al. (2005). Effects of methamphetamine dependence and HIV infection on cerebral morphology. American Journal of Psychiatry, 162, 1461–1472.

    PubMed  Google Scholar 

  • Kieburtz, K., Ketonen, L., Cox, C., Grossman, H., Holloway, R., Booth, H., et al. (1996). Cognitive performance and regional brain volume in human immunodeficiency virus type 1 infection. Archives of Neurology, 53, 155–158.

    PubMed  CAS  Google Scholar 

  • Kieburtz, K. D., Ketonen, L., Zettelmaier, A. E., Kido, D., Caine, E. D., & Simon, J. H. (1990). Magnetic resonance imaging findings in HIV cognitive impairment. Archives of Neurology, 47, 643–645.

    PubMed  CAS  Google Scholar 

  • Koralnik, I. J., Beaumanoir, A., Hausler, R., Kohler, A., Safran, A. B., Delacoux, R., et al. (1990). A controlled study of early neurologic abnormalities in men with asymptomatic human immunodeficiency virus infection. New England Journal of Medicine, 323, 864–870.

    PubMed  CAS  Google Scholar 

  • Lepore, N., Brun, C. A., Chiang, M. C., Chou, Y. Y., Dutton, R. A., Hayashi, K. M., et al. (2007). Multivariate statistics of the Jacobian matrices in tensor based morphometry and their application to HIV/AIDS. Medical Image Computing and Computer-Assisted Intervention International Conference on Medical Image Computing and Computer-Assisted Intervention, 9(Pt 1), 191–198.

    Google Scholar 

  • Levin, H. S., Williams, D. H., Borucki, M. J., Hillman, G. R., Williams, J. B., Guinto, F. C., et al. (1990). Magnetic resonance imaging and neuropsychological findings in human immunodeficiency virus infection. Journal of Acquired Immune Deficiency Syndromes, 3, 757–762.

    PubMed  CAS  Google Scholar 

  • McArthur, J. C., Kumar, A. J., Johnson, D. W., Selnes, O. A., Becker, J. T., Herman, C., et al. (1990). Incidental white matter hyperintensities on magnetic resonance imaging in HIV-1 infection: Multicenter AIDS Cohort Study. Journal of Acquired Immune Deficiency Syndromes, 3, 252–259.

    PubMed  CAS  Google Scholar 

  • Paley, M. N., Chong, W. K., Wilkinson, I. D., Shepherd, J. K., Clews, A. M., Sweeney, B. J., et al. (1994). Cerebrospinal fluid-intracranial volume ratio measurements in patients with HIV infection: CLASS image analysis technique. Radiology, 190, 879–886.

    PubMed  CAS  Google Scholar 

  • Patel, S. H., Kolson, D. L., Glosser, G., Matozzo, I., Ge, Y., Babb, J. S., et al. (2002). Correlation between percentage of brain parenchymal volume and neurocognitive performance in HIV-infected patients. American Journal of Neuroradiolgy, 23, 543–549.

    Google Scholar 

  • Paul, R. H., Brickman, A. M., Navia, B., Hinkin, C., Malloy, P. F., Jefferson, A. L., et al. (2005). Apathy is associated with volume of the nucleus accumbens in patients infected with HIV. Journal of Neuropsychiatry and Clinical Neurosciences, 17, 167–171.

    PubMed  Google Scholar 

  • Pfefferbaum, A., Rosenbloom, M. J., Adalsteinsson, E., & Sullivan, E. V. (2007). Diffusion tensor imaging with quantitative fibre tracking in HIV infection and alcoholism comorbidity: Synergistic white matter damage. Brain, 130, 48–64.

    PubMed  Google Scholar 

  • Pfefferbaum, A., Rosenbloom, M. J., Rohlfing, T., Adalsteinsson, E., Kemper, C. A., Deresinski, S., et al. (2006). Contribution of alcoholism to brain dysmorphology in HIV infection: Effects on the ventricles and corpus callosum. NeuroImage, 33, 239–251.

    PubMed  Google Scholar 

  • Pomara, N., Crandall, D. T., Choi, S. J., Johnson, G., & Lim, K. O. (2001). White matter abnormalities in HIV-1 infection: A diffusion tensor imaging study. Psychiatry Research, 106, 15–24.

    PubMed  CAS  Google Scholar 

  • Post, M. J., Berger, J. R., Duncan, R., Quencer, R. M., Pall, L., & Winfield, D. (1993). Asymptomatic and neurologically symptomatic HIV-seropositive subjects: Results of long-term MR imaging and clinical follow-up. Radiology, 188, 727–733.

    PubMed  CAS  Google Scholar 

  • Post, M. J., Berger, J. R., & Quencer, R. M. (1991). Asymptomatic and neurologically symptomatic HIV-seropositive individuals: Prospective evaluation with cranial MR imaging. Radiology, 178, 131–139.

    PubMed  CAS  Google Scholar 

  • Post, M. J., Tate, L. G., Quencer, R. M., Hensley, G. T., Berger, J. R., Sheremata, W. A., et al. (1988). CT, MR, and pathology in HIV encephalitis and meningitis. American Journal of Roentgenology, 151, 373–380.

    PubMed  CAS  Google Scholar 

  • Post, M. J., Levin, B. E., Berger, J. R., Duncan, R., Quencer, R. M., & Calabro, G. (1992). Sequential cranial MR findings of asymptomatic and neurologically symptomatic HIV + subjects. American Journal of Neuroradiology, 13, 359–370.

    PubMed  CAS  Google Scholar 

  • Poutiainen, E., Elovaara, I., Raininko, R., Hokkanen, L., Valle, S. L., Lahdevirta, J., & Iivanainen, M. (1993). Cognitive performance in HIV-1 infection: Relationship to severity of disease and brain atrophy. Acta Neurologica Scandinavica, 87, 88–94.

    Article  PubMed  CAS  Google Scholar 

  • Ragin, A. B., Storey, P., Cohen, B. A., Edelman, R. R., & Epstein, L. G. (2004a). Disease burden in HIV-associated cognitive impairment: a study of whole-brain imaging measures. Neurology, 63, 2293–2297.

    PubMed  CAS  Google Scholar 

  • Ragin, A. B., Storey, P., Cohen, B. A., Epstein, L. G., & Edelman, R. R. (2004b). Whole brain diffusion tensor imaging in HIV-associated cognitive impairment. American Journal of Neuroradiology, 25, 195–200.

    PubMed  Google Scholar 

  • Ragin, A. B., Wu, Y., Storey, P., Cohen, B. A., Edelman, R. R., & Epstein, L. G. (2005). Diffusion tensor imaging of subcortical brain injury in patients infected with human immunodeficiency virus. Journal of Neurovirology, 11, 292–298.

    PubMed  Google Scholar 

  • Raininko, R., Elovaara, I., Virta, A., Valanne, L., Haltia, M., & Valle, S. L. (1992). Radiological study of the brain at various stages of human immunodeficiency virus infection: early development of brain atrophy. Neuroradiology, 34, 190–196.

    PubMed  CAS  Google Scholar 

  • Samuelsson, K., Pirskanen-Matell, R., Bremmer, S., Hindmarsh, T., Nilsson, B. Y., & Persson, H. E. (2006). The nervous system in early HIV infection: A prospective study through 7 years. European Journal of Neurology, 13, 283–291.

    PubMed  CAS  Google Scholar 

  • Sonnerborg, A., Saaf, J., Alexius, B., Strannegard, O., Wahlund, L. O., & Wetterberg, L. (1990). Quantitative detection of brain aberrations in human immunodeficiency virus type 1-infected individuals by magnetic resonance imaging. Journal of Infectious Diseases, 162, 1245–1251.

    PubMed  CAS  Google Scholar 

  • Stout, J. C., Ellis, R. J., Jernigan, T. L., Archibald, S. L., Abramson, I., Wolfson, T., et al. (1998). Progressive cerebral volume loss in human immunodeficiency virus infection: A longitudinal volumetric magnetic resonance imaging study. Archives of Neruology, 55, 161–168.

    CAS  Google Scholar 

  • Thompson, P. M., Dutton, R. A., Hayashi, K. M., Lu, A., Lee, S. E., Lee, J. Y., et al. (2006). 3D mapping of ventricular and corpus callosum abnormalities in HIV/AIDS. Neuroimage, 31(1), 12–23.

    PubMed  Google Scholar 

  • Thompson, P. M., Dutton, R. A., Hayashi, K. M., Toga, A. W., Lopez, O. L., Aizenstein, H. J., et al. (2005). Thinning of the cerebral cortex visualized in HIV/AIDS reflects CD4 + T lymphocyte decline. Proceedings of the National Academy of Sciences of the United States of America, 102(43), 15647–15652.

    PubMed  CAS  Google Scholar 

  • Thurnher, M. M., Castillo, M., Stadler, A., Rieger, A., Schmid, B., & Sundgren, P. C. (2005). Diffusion-tensor MR imaging of the brain in human immunodeficiency virus-positive patients. American Journal of Neuroradiology, 26(9), 2275–2281.

    PubMed  Google Scholar 

  • Thurnher, M. M., Schindler, E. G., Thurnher, S. A., Pernerstorfer-Schon, H., Kleibl-Popov, C., & Rieger, A. (2000). Highly active antiretroviral therapy for patients with AIDS dementia complex: Effect on MR imaging findings and clinical course. American Journal of Neuroradiology, 21, 670–678.

    PubMed  CAS  Google Scholar 

  • Wenserski, F., von Giesen, H. J., Wittsack, H. J., Aulich, A., & Arendt, G. (2003). Human immunodeficiency virus 1-associated minor motor disorders: Perfusion-weighted MR imaging and H MR spectroscopy. Radiology, 228, 185–192.

    PubMed  Google Scholar 

  • Wilkinson, I. D., Lunn, S., Miszkiel, K. A., Miller, R. F., Paley, M. N., Williams, I., et al. (1997). Proton MRS and quantitative MRI assessment of the short term neurological response to antiretroviral therapy in AIDS. Journal of Neurology, Neruosurgery, and Psychiatry, 63, 477–482.

    Article  CAS  Google Scholar 

  • Wu, Y., Storey, P., Cohen, B. A., Epstein, L. G., Edelman, R. R., & Ragin, A. (2006). Diffusion alterations in corpus callosum of patients with HIV. American Journal of Neuroradiology, 27(3), 656–660.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Data in this manuscript were collected at the Ruth M. Rothstein CORE Center for the Prevention, Care and Research of Infectious Diseases, a joint venture of the Cook County Bureau of Health Services and Rush University Medical Center. The study was supported by: NIA R21 AG23491 and a Rush University Medical Center-Cook County Collaborative Grant.

Author information

Authors and Affiliations

  1. Rush University Medical Center, 1653 West Congress Parkway, Chicago, IL, 60612, USA

    Clifford A. Smith, Glenn T. Stebbins, Russell E. Bartt, Harold A. Kessler & Oluwatoyin M. Adeyemi

  2. John H. Stroger, Jr. Hospital of Cook County, Chicago, IL, USA

    Russell E. Bartt, Harold A. Kessler & Oluwatoyin M. Adeyemi

  3. Ruth M. Rothstein CORE Center, Chicago, IL, USA

    Russell E. Bartt, Harold A. Kessler & Oluwatoyin M. Adeyemi

  4. University of Illinois—Chicago, Chicago, IL, USA

    Eileen Martin

  5. Stanford University, Stanford, CA, USA

    Roland Bammer & Michael E. Moseley

Authors
  1. Clifford A. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Glenn T. Stebbins
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Russell E. Bartt
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Harold A. Kessler
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Oluwatoyin M. Adeyemi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Eileen Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Roland Bammer
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Michael E. Moseley
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Clifford A. Smith.

Additional information

References marked with an asterisk indicate HIV-associated studies reviewed for gender distributions.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Smith, C.A., Stebbins, G.T., Bartt, R.E. et al. Gender Effects on HIV-Associated White Matter Alterations: A Voxel-Wise DTI Study. Brain Imaging and Behavior 2, 177–191 (2008). https://doi.org/10.1007/s11682-008-9024-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-008-9024-5

Keywords

Search

Navigation