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Aging and Neurocognitive Functioning in HIV-Infected Women: a Review of the Literature Involving the Women’s Interagency HIV Study

  • Behavioral-Bio-Medical Interface (JL Brown and RJ DiClemente, Section Editors)
  • Published:
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An Erratum to this article was published on 01 December 2016

Abstract

HIV-infected women may be particularly vulnerable to certain types of neurocognitive impairments which may be exacerbated by aging and other predictors. Within the context of cognitive reserve, this article examines issues surrounding women as they age with HIV. For this, a review of 12 recent studies (2013–2016) using data from the Women’s Interagency HIV Study (WIHS), the largest cohort study comparing HIV-infected and demographically matched uninfected women, is presented that specifically examines neurocognition. In general, HIV-infected women are more vulnerable to developing neurocognitive impairments than uninfected women; other factors that may contribute to these neurocognitive impairments include recent illicit drug use, reading level (educational quality/cognitive reserve), stress, PTSD, insulin resistance, liver fibrosis, and age. Surprisingly, when examined in some analyses, age × HIV interactions were not observed to impact neurocognitive performance, findings largely consistent in the literature; however, longitudinal analyses of these data have yet to be performed which may yield future insights of how cognitive reserve may be compromised over time. Yet, with insulin resistance, liver fibrosis, stress, and other known predictors of poorer neurocognition also occurring more with advanced age, in time, the synergistic effect of age and HIV may be more robust and observable as this population ages.

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References

  1. Rodger AJ, Lodwick R, Schechter M, et al. Mortality in well controlled HIV in the continuous antiretroviral therapy arms of the SMART and ESPRIT trials compared with the general population. AIDS. 2013;27(6):973–9.

    Article  CAS  PubMed  Google Scholar 

  2. Collaboration of Observational HIVEREiE, Lewden C, Bouteloup V, et al. All-cause mortality in treated HIV-infected adults with CD4 >/=500/mm3 compared with the general population: evidence from a large European observational cohort collaboration. Int J Epidemiol. 2012;41(2):433–45.

    Article  Google Scholar 

  3. Deeks SG, Lewin SR, Havlir DV. The end of AIDS: HIV infection as a chronic disease. Lancet. 2013;382(9903):1525–33.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Heaton RK, Clifford DB, Franklin Jr DR, et al. HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER Study. Neurology. 2010;75(23):2087–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Bonnet F, Amieva H, Marquant F, et al. Cognitive disorders in HIV-infected patients: are they HIV-related? AIDS. 2013;27(3):391–400.

    Article  PubMed  Google Scholar 

  6. Valcour V, Shikuma C, Shiramizu B, et al. Higher frequency of dementia in older HIV-1 individuals: the Hawaii Aging with HIV-1 Cohort. Neurology. 2004;63(5):822–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Pathai S, Bajillan H, Landay AL, High KP. Is HIV a model of accelerated or accentuated aging? J Gerontol A Biol Sci Med Sci. 2014;69(7):833–42.

    Article  PubMed  Google Scholar 

  8. Cody SL, Vance DE. The neurobiology of HIV and its impact on cognitive reserve: a review of cognitive interventions for an aging population. Neurobiol Dis. 2016;92(Pt B):144–56.

    Article  PubMed  Google Scholar 

  9. Vance DE, Cody SL, Yoo-Jeong M, Jones GL, Nicholson WC. The role of employment on neurocognitive reserve in adults with HIV: a review of the literature. J Assoc Nurses AIDS Care. 2015;26(4):316–29.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Fazeli PL, Woods SP, Heaton RK, et al. An active lifestyle is associated with better neurocognitive functioning in adults living with HIV infection. J Neurovirol. 2014;20(3):233–42.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Meyer VJ, Little DM, Fitzgerald DA, et al. Crack cocaine use impairs anterior cingulate and prefrontal cortex function in women with HIV infection. J Neurovirol. 2014;20(4):352–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Meyer VJ, Rubin LH, Martin E, et al. HIV and recent illicit drug use interact to affect verbal memory in women. J Acquir Immune Defic Syndr. 2013;63(1):67–76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Rubin LH, Cook JA, Weber KM, et al. The association of perceived stress and verbal memory is greater in HIV-infected versus HIV-uninfected women. J Neurovirol. 2015;21(4):422–32.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Park DC, Lodi-Smith J, Drew L, et al. The impact of sustained engagement on cognitive function in older adults: the Synapse Project. Psychol Sci. 2014;25(1):103–12.

    Article  PubMed  Google Scholar 

  15. De Cock KM, El-Sadr WM. When to start ART in Africa—an urgent research priority. N Engl J Med. 2013;368(10):886–9.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Martin E, Gonzalez R, Vassileva J, Maki P. HIV+ men and women show different performance patterns on procedural learning tasks. J Clin Exp Neuropsychol. 2011;33(1):112–20.

    Article  PubMed  Google Scholar 

  17. Royal 3rd W, Cherner M, Burdo TH, et al. Associations between cognition, gender and monocyte activation among HIV infected individuals in Nigeria. PLoS One. 2016;11(2):e0147182.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Maki PM, Rubin LH, Springer G, et al. Male/female differences in cognitive function in HIV+ individuals. Conference on Retroviruses and Opportunistic Infections (CROI). Boston: 2016.

  19. Martin E, Gonzalez R, Vassileva J, Maki PM, Bechara A, Brand M. Sex and HIV serostatus differences in decision making under risk among substance-dependent individuals. J Clin Exp Neuropsychol. 2016;38(4):404–15.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Behrman-Lay AM, Paul RH, Heaps-Woodruff J, Baker LM, Usher C, Ances BM. Human immunodeficiency virus has similar effects on brain volumetrics and cognition in males and females. J Neurovirol. 2016;22(1):93–103.

    Article  CAS  PubMed  Google Scholar 

  21. Greendale GA, Wight RG, Huang MH, et al. Menopause-associated symptoms and cognitive performance: results from the study of women’s health across the nation. Am J Epidemiol. 2010;171(11):1214–24.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Ferreira CE, Pinto-Neto AM, Conde DM, Costa-Paiva L, Morais SS, Magalhaes J. Menopause symptoms in women infected with HIV: prevalence and associated factors. Gynecol Endocrinol. 2007;23(4):198–205.

    Article  PubMed  Google Scholar 

  23. Boonyanurak P, Bunupuradah T, Wilawan K, et al. Age at menopause and menopause-related symptoms in human immunodeficiency virus-infected Thai women. Menopause. 2012;19(7):820–4.

    Article  PubMed  Google Scholar 

  24. Schoenbaum EE, Hartel D, Lo Y, et al. HIV infection, drug use, and onset of natural menopause. Clin Infect Dis. 2005;41(10):1517–24.

    Article  PubMed  Google Scholar 

  25. Kanapathipillai R, Hickey M, Giles M. Human immunodeficiency virus and menopause. Menopause. 2013;20(9):983–90.

    Article  PubMed  Google Scholar 

  26. Rubin LH, Sundermann E, Golub ET, et al. The influence of serostatus and menopausal stage on menopausal symptoms in the Women’s Interagency HIV Study: are HIV+ women at increased risk for menopausal symptoms? North America Menopause Society 20th Annual Meeting. San Diego: 2009.

  27. Rubin LH, Pyra M, Cook JA, et al. Post-traumatic stress is associated with verbal learning, memory, and psychomotor speed in HIV-infected and HIV-uninfected women. J Neurovirol. 2016;22(2):159–69.

    Article  PubMed  Google Scholar 

  28. WHO. Women and health: today’s evidence tomorrow’s agenda. Geneva: WHO Press; 2009.

    Google Scholar 

  29. Bacon MC, von Wyl V, Alden C, et al. The Women’s Interagency HIV Study: an observational cohort brings clinical sciences to the bench. Clin Diagn Lab Immunol. 2005;12(9):1013–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Maki PM, Rubin LH, Valcour V, et al. Cognitive function in women with HIV: findings from the Women’s Interagency HIV Study. Neurology. 2015;84(3):231–40.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Antinori A, Arendt G, Becker JT, et al. Updated research nosology for HIV-associated neurocognitive disorders. Neurology. 2007;69(18):1789–99.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Valcour V, Rubin LH, Tien P, et al. Human immunodeficiency virus (HIV) modulates the associations between insulin resistance and cognition in the current combination antiretroviral therapy (cART) era: a study of the Women’s Interagency HIV Study (WIHS). J Neurovirol. 2015;21(4):415–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Valcour VG, Rubin LH, Obasi MU, et al. Liver fibrosis linked to cognitive performance in HIV and hepatitis C. J Acquir Immune Defic Syndr. 2016;72(3):266–73.

    Article  CAS  PubMed  Google Scholar 

  34. Valcour VG, Sacktor NC, Paul RH, et al. Insulin resistance is associated with cognition among HIV-1-infected patients: the Hawaii Aging With HIV cohort. J Acquir Immune Defic Syndr. 2006;43(4):405–10.

    Article  PubMed  Google Scholar 

  35. Cysique LA, Becker JT. Lessons to be learned from the largest study of cognition in American women with HIV disease. Neurology. 2015;84(3):220–1.

    Article  PubMed  Google Scholar 

  36. Pukay-Martin ND, Cristiani SA, Saveanu R, Bornstein RA. The relationship between stressful life events and cognitive function in HIV-infected men. J Neuropsychiatry Clin Neurosci. 2003;15(4):436–41.

    Article  PubMed  Google Scholar 

  37. Cougle JR, Timpano KR, Sachs-Ericsson N, Keough ME, Riccardi CJ. Examining the unique relationships between anxiety disorders and childhood physical and sexual abuse in the National Comorbidity Survey-Replication. Psychiatry Res. 2010;177(1-2):150–5.

    Article  PubMed  Google Scholar 

  38. Machtinger EL, Wilson TC, Haberer JE, Weiss DS. Psychological trauma and PTSD in HIV-positive women: a meta-analysis. AIDS Behav. 2012;16(8):2091–100.

    Article  CAS  PubMed  Google Scholar 

  39. Kessler RC, Petukhova M, Sampson NA, Zaslavsky AM, Wittchen HU. Twelve-month and lifetime prevalence and lifetime morbid risk of anxiety and mood disorders in the United States. Int J Methods Psychiatr Res. 2012;21(3):169–84.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Kessler RC, Sonnega A, Bromet E, Hughes M, Nelson CB. Posttraumatic stress disorder in the National Comorbidity Survey. Arch Gen Psychiatry. 1995;52(12):1048–60.

    Article  CAS  PubMed  Google Scholar 

  41. Breslau N, Kessler RC, Chilcoat HD, Schultz LR, Davis GC, Andreski P. Trauma and posttraumatic stress disorder in the community: the 1996 Detroit Area Survey of Trauma. Arch Gen Psychiatry. 1998;55(7):626–32.

    Article  CAS  PubMed  Google Scholar 

  42. Moradi AR, Miraghaei MA, Parhon H, Jabbari H, Jobson L. Posttraumatic stress disorder, depression, executive functioning, and autobiographical remembering in individuals with HIV and in carers of those with HIV in Iran. AIDS Care. 2013;25(3):281–8.

    PubMed  Google Scholar 

  43. Lejuez CW, Bornovalova MA, Reynolds EK, Daughters SB, Curtin JJ. Risk factors in the relationship between gender and crack/cocaine. Exp Clin Psychopharmacol. 2007;15(2):165–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Baum MK, Rafie C, Lai S, Sales S, Page B, Campa A. Crack-cocaine use accelerates HIV disease progression in a cohort of HIV-positive drug users. J Acquir Immune Defic Syndr. 2009;50(1):93–9.

    Article  PubMed  Google Scholar 

  45. Maki PM, Resnick SM. Effects of estrogen on patterns of brain activity at rest and during cognitive activity: a review of neuroimaging studies. Neuroimage. 2001;14(4):789–801.

    Article  CAS  PubMed  Google Scholar 

  46. Resnick SM, Maki PM. Effects of hormone replacement therapy on cognitive and brain aging. Ann N Y Acad Sci. 2001;949:203–14.

    Article  CAS  PubMed  Google Scholar 

  47. Rubin LH, Sundermann EE, Cook JA, et al. Investigation of menopausal stage and symptoms on cognition in human immunodeficiency virus-infected women. Menopause. 2014;21(9):997–1006.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Gustafson DR, Mielke MM, Tien PC, et al. Anthropometric measures and cognition in middle-aged HIV-infected and uninfected women. The Women’s Interagency HIV Study. J Neurovirol. 2013;19(6):574–85.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Fitzpatrick AL, Kuller LH, Lopez OL, et al. Midlife and late-life obesity and the risk of dementia: cardiovascular health study. Arch Neurol. 2009;66(3):336–42.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Al-Khindi T, Zakzanis KK, van Gorp WG. Does antiretroviral therapy improve HIV-associated cognitive impairment? A quantitative review of the literature. J Int Neuropsychol Soc. 2011;17(6):956–69.

    Article  PubMed  Google Scholar 

  51. McCutchan JA, Marquie-Beck JA, Fitzsimons CA, et al. Role of obesity, metabolic variables, and diabetes in HIV-associated neurocognitive disorder. Neurology. 2012;78(7):485–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Liu C, Wang C, Leclair M, Young M, Jiang X. Reduced neural specificity in middle-aged HIV+ women in the absence of behavioral deficits. Neuroimage Clin. 2015;8:667–75.

    Article  PubMed  Google Scholar 

  53. Rubin LH, Meyer VJ, R JC, et al. Prefrontal cortical volume loss is associated with stress-related deficits in verbal learning and memory in HIV-infected women. Neurobiol Dis. 2015

  54. Rubin LH, Wu M, Sundermann EE, et al. Elevated stress is associated with prefrontal cortex dysfunction during a verbal memory task in women with HIV. J Neurovirol. 2016.

  55. Heaton RK, Franklin DR, Ellis RJ, 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(1):3–16.

    Article  CAS  PubMed  Google Scholar 

  56. Woods SP, Scott JC, Dawson MS, et al. Construct validity of Hopkins Verbal Learning Test-Revised component process measures in an HIV-1 sample. Arch Clin Neuropsychol. 2005;20(8):1061–71.

    Article  PubMed  Google Scholar 

  57. Vance DE, Mugavero M, Willig J, Raper JL, Saag MS. Aging with HIV: a cross-sectional study of comorbidity prevalence and clinical characteristics across decades of life. J Assoc Nurses AIDS Care. 2011;22(1):17–25.

    Article  PubMed  Google Scholar 

  58. Vance DE, Fazeli PL, Dodson JE, Ackerman M, Talley M, Appel SJ. The synergistic effects of HIV, diabetes, and aging on cognition: implications for practice and research. J Neurosci Nurs. 2014;46(5):292–305.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Bale TL, Epperson CN. Sex differences and stress across the lifespan. Nat Neurosci. 2015;18(10):1413–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Lee C, Tsenkova V, Carr D. Childhood trauma and metabolic syndrome in men and women. Soc Sci Med. 2014;105:122–30.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Tsenkova V, Pudrovska T, Karlamangla A. Childhood socioeconomic disadvantage and prediabetes and diabetes in later life: a study of biopsychosocial pathways. Psychosom Med. 2014;76(8):622–8.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Cohen M, Deamant C, Barkan S, et al. Domestic violence and childhood sexual abuse in HIV-infected women and women at risk for HIV. Am J Public Health. 2000;90(4):560–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Aggarwal NT, Wilson RS, Beck TL, et al. Perceived stress and change in cognitive function among adults 65 years and older. Psychosom Med. 2014;76(1):80–5.

    Article  PubMed  Google Scholar 

  64. Osmanovic-Thunstrom A, Mossello E, Akerstedt T, Fratiglioni L, Wang HX. Do levels of perceived stress increase with increasing age after age 65? A population-based study. Age Ageing. 2015;44(5):828–34.

    Article  PubMed  Google Scholar 

  65. Valcour V, Paul R, Neuhaus J, Shikuma C. The effects of age and HIV on neuropsychological performance. J Int Neuropsychol Soc. 2011;17(1):190–5.

    Article  PubMed  Google Scholar 

  66. van Gorp WG, Miller EN, Marcotte TD, et al. The relationship between age and cognitive impairment in HIV-1 infection: findings from the Multicenter AIDS Cohort Study and a clinical cohort. Neurology. 1994;44(5):929–35.

    Article  PubMed  Google Scholar 

  67. Vance DE, Fazeli PL, Gakumo CA. The impact of neuropsychological performance on everyday functioning between older and younger adults with and without HIV. J Assoc Nurses AIDS Care. 2013;24(2):112–25.

    Article  PubMed  Google Scholar 

  68. Sheppard DP, Woods SP, Bondi MW, et al. Does older age confer an increased risk of incident neurocognitive disorders among persons living with HIV disease? Clin Neuropsychol. 2015;29(5):656–77.

    Article  PubMed  PubMed Central  Google Scholar 

  69. Maillet D, Rajah MN. Association between prefrontal activity and volume change in prefrontal and medial temporal lobes in aging and dementia: a review. Ageing Res Rev. 2013;12(2):479–89.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. School of Nursing, University of Alabama at Birmingham (UAB), Room 2M026, 1701 University Boulevard, Birmingham, AL, 35294-1210, USA

    David E. Vance

  2. Department of Psychiatry, University of Illinois at Chicago, Room 324, MC 913, Chicago, IL, 60612, USA

    Leah H. Rubin

  3. Department of Neurology, UCSF School of Medicine, 3333 California Street, San Francisco, CA, 94104, USA

    Victor Valcour

  4. Center for Neurocognitive Studies, Nell Hodgson Woodruff School of Nursing, Emory University, Room 442, 1520 Clifton Road, NE, Atlanta, GA, 30322-4027, USA

    Drenna Waldrop-Valverde

  5. Departments of Psychiatry and Psychology, University of Illinois at Chicago, Room 328, MC 913, Chicago, IL, 60612, USA

    Pauline M. Maki

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  1. David E. Vance
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  2. Leah H. Rubin
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  3. Victor Valcour
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Correspondence to David E. Vance.

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Conflict of Interest

David E. Vance is supported by WIHS as chairperson.

Leah H. Rubin, Victor Valcour, Drenna Waldrop-Valverde, and Pauline M. Maki declare that they have no conflict of interest.

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This article does not contain any studies with human or animal subjects performed by any of the authors.

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This article is part of the Topical Collection on Behavioral-Bio-Medical Interface

An erratum to this article is available at http://dx.doi.org/10.1007/s11904-016-0343-7.

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Vance, D.E., Rubin, L.H., Valcour, V. et al. Aging and Neurocognitive Functioning in HIV-Infected Women: a Review of the Literature Involving the Women’s Interagency HIV Study. Curr HIV/AIDS Rep 13, 399–411 (2016). https://doi.org/10.1007/s11904-016-0340-x

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