The association of perceived stress and verbal memory is greater in HIV-infected versus HIV-uninfected women
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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.
KeywordsHIV Verbal memory Stress Women Cognition
Dr. Rubin’s effort was supported by Grant Number 1K01MH098798-01 from the National Institute of Mental Health (NIMH) and by Grant Number K12HD055892 from the Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD) and the National Institutes of Health Office of Research on Women’s Health (ORWH). This grant is also supported in part by the Chicago Developmental Center for AIDS Research (D-CFAR), an NIH-funded program (P30 AI 082151), which is supported by the following NIH Institutes and Centers (NIAID, NCI, NIMH, NIDA, NICHD, NHLBI, NCCAM). Data in this manuscript were collected by the Women’s Interagency HIV Study (WIHS). The contents of this publication are solely the responsibility of the authors and do not represent the official views of the National Institutes of Health (NIH). WIHS (Principal Investigators): UAB-MS WIHS (Michael Saag, Mirjam-Colette Kempf, and Deborah Konkle-Parker), U01-AI-103401; Atlanta WIHS (Ighovwerha Ofotokun and Gina Wingood), U01-AI-103408; Bronx WIHS (Kathryn Anastos), U01-AI-035004; Brooklyn WIHS (Howard Minkoff and Deborah Gustafson), U01-AI-031834; Chicago WIHS (Mardge Cohen), U01-AI-034993; Metropolitan Washington WIHS (Mary Young), U01-AI-034994; Miami WIHS (Margaret Fischl and Lisa Metsch), U01-AI-103397; UNC WIHS (Adaora Adimora), U01-AI-103390; Connie Wofsy Women’s HIV Study, Northern California (Ruth Greenblatt, Bradley Aouizerat, and Phyllis Tien), U01-AI-034989; WIHS Data Management and Analysis Center (Stephen Gange and Elizabeth Golub), U01-AI-042590; Southern California WIHS (Alexandra Levine and Marek Nowicki), U01-HD-032632 (WIHS I – WIHS IV). The WIHS is funded primarily by the National Institute of Allergy and Infectious Diseases (NIAID), with additional co-funding from the Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD), the National Cancer Institute (NCI), the National Institute on Drug Abuse (NIDA), and the National Institute on Mental Health (NIMH). Targeted supplemental funding for specific projects is also provided by the National Institute of Dental and Craniofacial Research (NIDCR), the National Institute on Alcohol Abuse and Alcoholism (NIAAA), the National Institute on Deafness and other Communication Disorders (NIDCD), and the NIH Office of Research on Women’s Health. WIHS data collection is also supported by UL1-TR000004 (UCSF CTSA) and UL1-TR000454 (Atlanta CTSA).
Conflict of interest
The authors declare that they have no conflict of interest.
- Benton AL (1968) Differential behavioral effects in frontal lobe disease. Neuropsychologia 6Google Scholar
- Brandt J, Benedict RHB (2001) Hopkins verbal learning test revised. PAR, OdessaGoogle Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Olver JS, Pinney M, Maruff P, Norman TR (2014) Impairments of spatial working memory and attention following acute psychosocial stress. Stress HealthGoogle Scholar
- 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
- Reitan R (1978) Manual for administration of neuropsychological test batteries for adults and children. Neuropsychology Laboratories, Inc., Tuscon, AZGoogle Scholar
- Reitan R, Wolfson D (eds) (1985) The Halstead-Reitan neuropsychological test battery: theory and clinical interpretation. Neuropsychology Press, Tuscon, AZGoogle Scholar
- 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
- 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
- Wilkinson GS (1993) Wide range achievement test 3—administration manual. Jastak Associates, Inc, Wilimington, DEGoogle Scholar