Journal of NeuroVirology

, Volume 21, Issue 4, pp 422–432 | Cite as

The association of perceived stress and verbal memory is greater in HIV-infected versus HIV-uninfected women

  • Leah H. Rubin
  • Judith A. Cook
  • Kathleen M. Weber
  • Mardge H. Cohen
  • Eileen Martin
  • Victor Valcour
  • Joel Milam
  • Kathryn Anastos
  • Mary A. Young
  • Christine Alden
  • Deborah R. Gustafson
  • Pauline M. Maki
Article

Abstract

In contrast to findings from cohorts comprised primarily of HIV-infected men, verbal memory deficits are the largest cognitive deficit found in HIV-infected women from the Women’s Interagency HIV Study (WIHS), and this deficit is not explained by depressive symptoms or substance abuse. HIV-infected women may be at greater risk for verbal memory deficits due to a higher prevalence of cognitive risk factors such as high psychosocial stress and lower socioeconomic status. Here, we investigate the association between perceived stress using the Perceived Stress Scale (PSS-10) and verbal memory performance using the Hopkins Verbal Learning Test (HVLT) in 1009 HIV-infected and 496 at-risk HIV-uninfected WIHS participants. Participants completed a comprehensive neuropsychological test battery which yielded seven cognitive domain scores, including a primary outcome of verbal memory. HIV infection was not associated with a higher prevalence of high perceived stress (i.e., PSS-10 score in the top tertile) but was associated with worse performance on verbal learning (p < 0.01) and memory (p < 0.001), as well as attention (p = 0.02). Regardless of HIV status, high stress was associated with poorer performance in those cognitive domains (p’s < 0.05) as well as processing speed (p = 0.01) and executive function (p < 0.01). A significant HIV by stress interaction was found only for the verbal memory domain (p = 0.02); among HIV-infected women only, high stress was associated with lower performance (p’s < 0.001). That association was driven by the delayed verbal memory measure in particular. These findings suggest that high levels of perceived stress contribute to the deficits in verbal memory observed in WIHS women.

Keywords

HIV Verbal memory Stress Women Cognition 

References

  1. Alderson AL, Novack TA (2002) Neurophysiological and clinical aspects of glucocorticoids and memory: a review. J Clin Exp Neuropsychol 24:335–355PubMedCrossRefGoogle Scholar
  2. Anthony IC, Ramage SN, Carnie FW, Simmonds P, Bell JE (2005) Influence of HAART on HIV-related CNS disease and neuroinflammation. J Neuropathol Exp Neurol 64:529–536PubMedGoogle Scholar
  3. Armstrong GL, Wasley A, Simard EP, McQuillan GM, Kuhnert WL, Alter MJ (2006) The prevalence of hepatitis C virus infection in the United States, 1999 through 2002. Ann Intern Med 144:705–714PubMedCrossRefGoogle Scholar
  4. Bacon MC, von Wyl V, Alden C, Sharp G, Robison E, Hessol N, Gange S, Barranday Y, Holman S, Weber K, Young MA (2005) The Women’s Interagency HIV Study: an observational cohort brings clinical sciences to the bench. Clin Diagn Lab Immunol 12:1013–1019PubMedCentralPubMedGoogle Scholar
  5. Bangasser DA, Shors TJ (2004) Acute stress impairs trace eye blink conditioning in females without altering the unconditioned response. Neurobiol Learn Mem 82:57–60PubMedCentralPubMedCrossRefGoogle Scholar
  6. Barkan SE, Melnick SL, Preston-Martin S, Weber K, Kalish LA, Miotti P, Young M, Greenblatt R, Sacks H, Feldman J (1998) The Women’s Interagency HIV Study. WIHS Collaborative Study Group. Epidemiology 9:117–125PubMedCrossRefGoogle Scholar
  7. Benton AL (1968) Differential behavioral effects in frontal lobe disease. Neuropsychologia 6Google Scholar
  8. Brandt J, Benedict RHB (2001) Hopkins verbal learning test revised. PAR, OdessaGoogle Scholar
  9. Bremner JD (2007) Neuroimaging in posttraumatic stress disorder and other stress-related disorders. Neuroimaging Clin N Am 17:523–538, ixPubMedCentralPubMedCrossRefGoogle Scholar
  10. Bremner JD, Vythilingam M, Vermetten E, Afzal N, Nazeer A, Newcomer JW, Charney DS (2004) Effects of dexamethasone on declarative memory function in posttraumatic stress disorder. Psychiatry Res 129:1–10PubMedCrossRefGoogle Scholar
  11. Brief DJ, Bollinger AR, Vielhauer MJ, Berger-Greenstein JA, Morgan EE, Brady SM, Buondonno LM, Keane TM (2004) Understanding the interface of HIV, trauma, post-traumatic stress disorder, and substance use and its implications for health outcomes. AIDS Care 16(Suppl 1):S97–S120PubMedCrossRefGoogle Scholar
  12. Brooke SM, Sapolsky RM (2002) Glucocorticoid exacerbation of gp120 neurotoxicity: role of microglia. Exp Neurol 177:151–158PubMedCrossRefGoogle Scholar
  13. Buwalda B, Kole MH, Veenema AH, Huininga M, de Boer SF, Korte SM, Koolhaas JM (2005) Long-term effects of social stress on brain and behavior: a focus on hippocampal functioning. Neurosci Biobehav Rev 29:83–97PubMedCrossRefGoogle Scholar
  14. Carter CS, Braver TS, Barch DM, Botvinick MM, Noll D, Cohen JD (1998) Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 280:747–749PubMedCrossRefGoogle Scholar
  15. Cohen J (1992) A power primer. Psychol Bull 112:155–159PubMedCrossRefGoogle Scholar
  16. Cohen M, Deamant C, Barkan S, Richardson J, Young M, Holman S, Anastos K, Cohen J, Melnick S (2000) Domestic violence and childhood sexual abuse in HIV-infected women and women at risk for HIV. Am J Public Health 90:560–565PubMedCentralPubMedCrossRefGoogle Scholar
  17. Cohen RA, Grieve S, Hoth KF, Paul RH, Sweet L, Tate D, Gunstad J, Stroud L, McCaffery J, Hitsman B, Niaura R, Clark CR, McFarlane A, Bryant R, Gordon E, Williams LM (2006) Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei. Biol Psychiatry 59:975–982PubMedCrossRefGoogle Scholar
  18. Cohen S, Kamarck T, Mermelstein R (1983) A global measure of perceived stress. J Health Soc Behav 24:385–396PubMedCrossRefGoogle Scholar
  19. Cohen S, Williamson G (1988) Perceived stress in a probability sample of the United States. In: Spacapan S, Oskamp S (eds) The social psychology of health: Claremont Symposium on applied social psychology. Sage, Newbury Park, CAGoogle Scholar
  20. Comalli PE, Wapner S, Werner H (1962) Interference effects of Stroop color-word test in childhood, adulthood, and aging. J Genet Psychol 100:47–53PubMedCrossRefGoogle Scholar
  21. DeVries AC, Craft TK, Glasper ER, Neigh GN, Alexander JK (2007) 2006 Curt P. Richter award winner: social influences on stress responses and health. Psychoneuroendocrinology 32:587–603PubMedCrossRefGoogle Scholar
  22. Diorio D, Viau V, Meaney MJ (1993) The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J Neurosci 13:3839–3847PubMedGoogle Scholar
  23. Gorman AA, Foley JM, Ettenhofer ML, Hinkin CH, van Gorp WG (2009) Functional consequences of HIV-associated neuropsychological impairment. Neuropsychol Rev 19:186–203PubMedCentralPubMedCrossRefGoogle Scholar
  24. Grossman R, Yehuda R, Golier J, McEwen B, Harvey P, Maria NS (2006) Cognitive effects of intravenous hydrocortisone in subjects with PTSD and healthy control subjects. Ann N Y Acad Sci 1071:410–421PubMedCrossRefGoogle Scholar
  25. Heaton RK, Franklin DR, Ellis RJ, McCutchan JA, Letendre SL, Leblanc S, Corkran SH, Duarte NA, Clifford DB, Woods SP, Collier AC, Marra CM, Morgello S, Mindt MR, Taylor MJ, Marcotte TD, Atkinson JH, Wolfson T, Gelman BB, McArthur JC, Simpson DM, Abramson I, Gamst A, Fennema-Notestine C, Jernigan TL, Wong J, Grant I (2011) HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: differences in rates, nature, and predictors. J Neurovirol 17:3–16PubMedCentralPubMedCrossRefGoogle Scholar
  26. Heaton RK, Grant I, Matthews CG (1991) Comprehensive norms for an expanded Halstead-Reitan battery: demographic corrections, research findings, and clinical applications. Psychological Assessment Resources, Odessa, FLGoogle Scholar
  27. Hinkin CH, Castellon SA, Durvasula RS, Hardy DJ, Lam MN, Mason KI, Thrasher D, Goetz MB, Stefaniak M (2002) Medication adherence among HIV+ adults: effects of cognitive dysfunction and regimen complexity. Neurology 59:1944–1950PubMedCentralPubMedCrossRefGoogle Scholar
  28. Hinkin CH, Hardy DJ, Mason KI, Castellon SA, Durvasula RS, Lam MN, Stefaniak M (2004) Medication adherence in HIV-infected adults: effect of patient age, cognitive status, and substance abuse. AIDS 18(Suppl 1):S19–S25PubMedCentralPubMedCrossRefGoogle Scholar
  29. Hochhauser CJ, Gaur S, Marone R, Lewis M (2008) The impact of environmental risk factors on HIV-associated cognitive decline in children. AIDS Care 20:692–699PubMedCrossRefGoogle Scholar
  30. Johansson L, Guo X, Waern M, Ostling S, Gustafson D, Bengtsson C, Skoog I (2010) Midlife psychological stress and risk of dementia: a 35-year longitudinal population study. Brain 133:2217–2224PubMedCrossRefGoogle Scholar
  31. Johansson L, Skoog I, Gustafson DR, Olesen PJ, Waern M, Bengtsson C, Bjorkelund C, Pantoni L, Simoni M, Lissner L, Guo X (2012) Midlife psychological distress associated with late-life brain atrophy and white matter lesions: a 32-year population study of women. Psychosom Med 74:120–125PubMedCrossRefGoogle Scholar
  32. Kajantie E, Phillips DI (2006) The effects of sex and hormonal status on the physiological response to acute psychosocial stress. Psychoneuroendocrinology 31:151–178PubMedCrossRefGoogle Scholar
  33. Kim JJ, Diamond DM (2002) The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci 3:453–462PubMedGoogle Scholar
  34. Kirschbaum C, Wolf OT, May M, Wippich W, Hellhammer DH (1996) Stress- and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. Life Sci 58:1475–1483PubMedCrossRefGoogle Scholar
  35. Kirschbaum C, Wust S, Hellhammer D (1992) Consistent sex differences in cortisol responses to psychological stress. Psychosom Med 54:648–657PubMedCrossRefGoogle Scholar
  36. Kudielka BM, Kirschbaum C (2005) Sex differences in HPA axis responses to stress: a review. Biol Psychol 69:113–132PubMedCrossRefGoogle Scholar
  37. Li H, Li W, Wei D, Chen Q, Jackson T, Zhang Q, Qiu J (2014) Examining brain structures associated with perceived stress in a large sample of young adults via voxel-based morphometry. Neuroimage 92C:1–7CrossRefGoogle Scholar
  38. Luine V, Martinez C, Villegas M, Magarinos AM, McEwen BS (1996) Restraint stress reversibly enhances spatial memory performance. Physiol Behav 59:27–32PubMedCrossRefGoogle Scholar
  39. Lupien SJ, Fiocco A, Wan N, Maheu F, Lord C, Schramek T, Tu MT (2005) Stress hormones and human memory function across the lifespan. Psychoneuroendocrinology 30:225–242PubMedCrossRefGoogle Scholar
  40. Lupien SJ, Lepage M (2001) Stress, memory, and the hippocampus: can’t live with it, can’t live without it. Behav Brain Res 127:137–158PubMedCrossRefGoogle Scholar
  41. Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10:434–445PubMedCrossRefGoogle Scholar
  42. Magarinos AM, Somoza G, De Nicola AF (1987) Glucocorticoid negative feedback and glucocorticoid receptors after hippocampectomy in rats. Horm Metab Res 19:105–109PubMedCrossRefGoogle Scholar
  43. Maki PM, Cohen MH, Weber K, Little DM, Fornelli D, Rubin LH, Perschler P, Gould F, Martin E (2009) Impairments in memory and hippocampal function in HIV-positive vs HIV-negative women: a preliminary study. Neurology 72:1661–1668PubMedCentralPubMedCrossRefGoogle Scholar
  44. Maki PM, Rubin LH, Valcour V, Martin E, Crystal HA, Young M, Weber KM, Manly J, Richardson J, Alden C, Anastos K (2015) Cognitive function in women with HIV: findings from the Women’s Interagency HIV Study. Neurology 84(3):231–240Google Scholar
  45. Manly JJ, Jacobs DM, Touradji P, Small SA, Stern Y (2002) Reading level attenuates differences in neuropsychological test performance between African American and White elders. J Int Neuropsychol Soc 8:341–348PubMedCrossRefGoogle Scholar
  46. Manly JJ, Smith C, Crystal HA, Richardson J, Golub ET, Greenblatt R, Robison E, Martin EM, Young M (2011) Relationship of ethnicity, age, education, and reading level to speed and executive function among HIV+ and HIV− women: the Women’s Interagency HIV Study (WIHS) Neurocognitive Substudy. J Clin Exp Neuropsychol 33:853–863PubMedCentralPubMedCrossRefGoogle Scholar
  47. Massad LS, Agniel D, Minkoff H, Watts DH, D’Souza G, Levine AM, Darragh TM, Young M, Cajigas A, Weber K (2011) Effect of stress and depression on the frequency of squamous intraepithelial lesions. J Low Genit Tract Dis 15:42–47PubMedCentralPubMedCrossRefGoogle Scholar
  48. McCormick CM, Lewis E, Somley B, Kahan TA (2007) Individual differences in cortisol levels and performance on a test of executive function in men and women. Physiol Behav 91:87–94PubMedCrossRefGoogle Scholar
  49. McEwen BS (2000) Effects of adverse experiences for brain structure and function. Biol Psychiatry 48:721–731PubMedCrossRefGoogle Scholar
  50. McEwen BS (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 87:873–904PubMedCrossRefGoogle Scholar
  51. McEwen BS, De Kloet ER, Rostene W (1986) Adrenal steroid receptors and actions in the nervous system. Physiol Rev 66:1121–1188PubMedGoogle Scholar
  52. McEwen BS, Sapolsky RM (1995) Stress and cognitive function. Curr Opin Neurobiol 5:205–216PubMedCrossRefGoogle Scholar
  53. Meaney MJ, Aitken DH (1985) [3H]Dexamethasone binding in rat frontal cortex. Brain Res 328:176–180PubMedCrossRefGoogle Scholar
  54. Moore DJ, Masliah E, Rippeth JD, Gonzalez R, Carey CL, Cherner M, Ellis RJ, Achim CL, Marcotte TD, Heaton RK, Grant I (2006) Cortical and subcortical neurodegeneration is associated with HIV neurocognitive impairment. AIDS 20:879–887PubMedCrossRefGoogle Scholar
  55. Olver JS, Pinney M, Maruff P, Norman TR (2014) Impairments of spatial working memory and attention following acute psychosocial stress. Stress HealthGoogle Scholar
  56. Plessow F, Fischer R, Kirschbaum C, Goschke T (2011) Inflexibly focused under stress: acute psychosocial stress increases shielding of action goals at the expense of reduced cognitive flexibility with increasing time lag to the stressor. J Cogn Neurosci 23:3218–3227PubMedCrossRefGoogle Scholar
  57. Pukay-Martin ND, Cristiani SA, Saveanu R, Bornstein RA (2003) The relationship between stressful life events and cognitive function in HIV-infected men. J Neuropsychiatry Clin Neurosci 15:436–441PubMedCrossRefGoogle Scholar
  58. Pukay-Martin ND, Pontoski KE, Maxwell MA, Calhoun PS, Dutton CE, Clancy CP, Hertzberg MA, Collie CF, Beckham JC (2012) The influence of depressive symptoms on suicidal ideation among U.S. Vietnam-era and Afghanistan/Iraq-era veterans with posttraumatic stress disorder. J Trauma Stress 25:578–582PubMedCentralPubMedCrossRefGoogle Scholar
  59. Reitan R (1978) Manual for administration of neuropsychological test batteries for adults and children. Neuropsychology Laboratories, Inc., Tuscon, AZGoogle Scholar
  60. Reitan R, Wolfson D (eds) (1985) The Halstead-Reitan neuropsychological test battery: theory and clinical interpretation. Neuropsychology Press, Tuscon, AZGoogle Scholar
  61. Rubin LH, Sundermann EE, Cook JA, Martin EM, Golub ET, Weber KM, Cohen MH, Crystal H, Cederbaum JA, Anastos K, Young M, Greenblatt RM, Maki PM (2014) Investigation of menopausal stage and symptoms on cognition in human immunodeficiency virus-infected women. MenopauseGoogle Scholar
  62. Sanchez MM, Young LJ, Plotsky PM, Insel TR (2000) Distribution of corticosteroid receptors in the rhesus brain: relative absence of glucocorticoid receptors in the hippocampal formation. J Neurosci 20:4657–4668PubMedGoogle Scholar
  63. Schoofs D, Pabst S, Brand M, Wolf OT (2013) Working memory is differentially affected by stress in men and women. Behav Brain Res 241:144–153PubMedCrossRefGoogle Scholar
  64. Schoofs D, Preuss D, Wolf OT (2008) Psychosocial stress induces working memory impairments in an n-back paradigm. Psychoneuroendocrinology 33:643–653PubMedCrossRefGoogle Scholar
  65. Seeman TE, McEwen BS, Singer BH, Albert MS, Rowe JW (1997) Increase in urinary cortisol excretion and memory declines: MacArthur studies of successful aging. J Clin Endocrinol Metab 82:2458–2465PubMedGoogle Scholar
  66. Servatius RJ, Shors TJ (1994) Exposure to inescapable stress persistently facilitates associative and nonassociative learning in rats. Behav Neurosci 108:1101–1106PubMedCrossRefGoogle Scholar
  67. Shors TJ, Chua C, Falduto J (2001) Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. J Neurosci 21:6292–6297PubMedGoogle Scholar
  68. Shors TJ, Lewczyk C, Pacynski M, Mathew PR, Pickett J (1998) Stages of estrous mediate the stress-induced impairment of associative learning in the female rat. Neuroreport 9:419–423PubMedCrossRefGoogle Scholar
  69. Shors TJ, Servatius RJ (1997) The contribution of stressor intensity, duration, and context to the stress-induced facilitation of associative learning. Neurobiol Learn Mem 68:92–96PubMedCrossRefGoogle Scholar
  70. Sinha R (2008) Chronic stress, drug use, and vulnerability to addiction. Ann N Y Acad Sci 1141:105–130PubMedCentralPubMedCrossRefGoogle Scholar
  71. Sinha R, Lacadie C, Skudlarski P, Fulbright RK, Rounsaville BJ, Kosten TR, Wexler BE (2005) Neural activity associated with stress-induced cocaine craving: a functional magnetic resonance imaging study. Psychopharmacology (Berl) 183:171–180CrossRefGoogle Scholar
  72. Smith A (1968) The Symbol-Digit Modalities Test: a neuropsychologic test for economic screening of learning and other cerebral disorders. Learn Disord 3:83–91Google Scholar
  73. VonDras DD, Powless MR, Olson AK, Wheeler D, Snudden AL (2005) Differential effects of everyday stress on the episodic memory test performances of young, mid-life, and older adults. Aging Ment Health 9:60–70PubMedCrossRefGoogle Scholar
  74. Wilkinson GS (1993) Wide range achievement test 3—administration manual. Jastak Associates, Inc, Wilimington, DEGoogle Scholar
  75. Wolf OT, Schommer NC, Hellhammer DH, McEwen BS, Kirschbaum C (2001) The relationship between stress induced cortisol levels and memory differs between men and women. Psychoneuroendocrinology 26:711–720PubMedCrossRefGoogle Scholar
  76. Woods SP, Scott JC, Dawson MS, Morgan EE, Carey CL, Heaton RK, Grant I (2005) Construct validity of Hopkins Verbal Learning Test-Revised component process measures in an HIV-1 sample. Arch Clin Neuropsychol 20:1061–1071PubMedCrossRefGoogle Scholar
  77. Woon FL, Sood S, Hedges DW (2010) Hippocampal volume deficits associated with exposure to psychological trauma and posttraumatic stress disorder in adults: a meta-analysis. Prog Neuropsychopharmacol Biol Psychiatry 34:1181–1188PubMedCrossRefGoogle Scholar
  78. Yehuda R, Harvey PD, Buchsbaum M, Tischler L, Schmeidler J (2007) Enhanced effects of cortisol administration on episodic and working memory in aging veterans with PTSD. Neuropsychopharmacology 32:2581–2591PubMedCrossRefGoogle Scholar
  79. Yusim A, Franklin L, Brooke S, Ajilore O, Sapolsky R (2000) Glucocorticoids exacerbate the deleterious effects of gp120 in hippocampal and cortical explants. J Neurochem 74:1000–1007PubMedCrossRefGoogle Scholar

Copyright information

© Journal of NeuroVirology, Inc. 2015

Authors and Affiliations

  • Leah H. Rubin
    • 1
  • Judith A. Cook
    • 1
  • Kathleen M. Weber
    • 2
  • Mardge H. Cohen
    • 3
  • Eileen Martin
    • 4
  • Victor Valcour
    • 5
  • Joel Milam
    • 6
  • Kathryn Anastos
    • 7
  • Mary A. Young
    • 8
  • Christine Alden
    • 9
  • Deborah R. Gustafson
    • 10
  • Pauline M. Maki
    • 1
    • 11
  1. 1.Department of PsychiatryUniversity of Illinois at ChicagoChicagoUSA
  2. 2.Bureau of Health Services of Cook CountyThe Core CenterChicagoUSA
  3. 3.Departments of Medicine Stroger Hospital and Rush UniversityChicagoUSA
  4. 4.Department of PsychiatryRush University Medical CenterChicagoUSA
  5. 5.Department of NeurologyUniversity of CaliforniaSan FranciscoUSA
  6. 6.Institute for Health Promotion & Disease Prevention ResearchUniversity of Southern CaliforniaLos AngelesUSA
  7. 7.Departments of Medicine and Epidemiology & Population HealthAlbert Einstein College of MedicineBronxUSA
  8. 8.Department of MedicineGeorgetown UniversityWashingtonUSA
  9. 9.Department of EpidemiologyJohns Hopkins School of Public HealthBaltimoreUSA
  10. 10.Department of NeurologySUNY-Downstate Medical CenterBrooklynUSA
  11. 11.Department of PsychologyUniversity of Illinois at ChicagoChicagoUSA

Personalised recommendations