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Variability in C-reactive protein is associated with cognitive impairment in women living with and without HIV: a longitudinal study

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Abstract

Despite the availability of effective antiretroviral therapies, cognitive impairment (CI) remains prevalent in HIV-infected (HIV+) individuals. Evidence from primarily cross-sectional studies, in predominantly male samples, implicates monocyte- and macrophage-driven inflammatory processes linked to HIV-associated CI. Thus, peripheral systemic inflammatory markers may be clinically useful biomarkers in tracking HIV-associated CI. Given sex differences in immune function, we focused here on whether mean and intra-individual variability in inflammatory marker-predicted CI in HIV+ and HIV− women. Seventy-two HIV+ (36 with CI) and 58 HIV− (29 with CI) propensity-matched women participating in the Women’s Interagency HIV Study completed a neuropsychological battery once between 2009 and 2011, and performance was used to determine CI status. Analysis of 13 peripheral immune markers was conducted on stored biospecimens at three time points (7 and 3.5 years before neuropsychological data collection and concurrent with data collection). HIV+ women showed alterations in 8 immune markers compared to HIV− women. The strongest predictors of CI across HIV+ and HIV− women were lower mean soluble tumor necrosis factor receptor I (sTNFRI) levels, higher mean interleukin (IL)-6 levels, and greater variability in C-reactive protein (CRP) and matrix metalloproteinase (MMP)-9 (p values < 0.05). Stratified by HIV, the only significant predictor of CI was greater variability in CRP for both HIV+ and HIV− women (p values < 0.05). This variability predicted lower executive function, attention/working memory, and psychomotor speed in HIV+ but only learning in HIV− women (p values < 0.05). Intra-individual variability in CRP levels over time may be a good predictor of CI in predominately minority low-socioeconomic status midlife women.

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Acknowledgements

Data in this manuscript were collected by the Women’s Interagency HIV Study (WIHS). 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).

Funding

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). Dr. Valcour’s work was supported by his K24MH098759. 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, and NCCAM. 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).

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Authors and Affiliations

  1. Department of Psychiatry, University of Illinois at Chicago, Chicago, IL, USA

    Leah H. Rubin, Antonia Savarese & Pauline M. Maki

  2. Department of Neurology, Johns Hopkins University School of Medicine, 600 N. Wolfe Street/Meyer 6-113, Baltimore, MD, 21287-7613, USA

    Leah H. Rubin

  3. Department of Epidemiology, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD, USA

    Lorie Benning & Gayle Springer

  4. Blood Systems Research Institute, San Francisco, CA, USA

    Sheila M. Keating & Philip J. Norris

  5. Cook County Health and Hospitals System/Hektoen Institute of Medicine, Chicago, IL, USA

    Jane Burke-Miller & Kathleen M. Weber

  6. School of Public Health, Division of Epidemiology and Biostatistics, University of Illinois at Chicago, Chicago, IL, USA

    Krithika N. Kumanan & Saria Awadalla

  7. Albert Einstein College of Medicine and Montefiore Medical Center, Bronx, NY, USA

    Kathyrn Anastos

  8. Department of Medicine, Georgetown University, Washington, DC, USA

    Mary Young

  9. Institute for Health Promotion and Disease Prevention Research, Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA

    Joel Milam

  10. Memory and Aging Center, Department of Neurology, University of California, San Francisco, CA, USA

    Victor G. Valcour

  11. Department of Psychology, University of Illinois at Chicago, Chicago, IL, USA

    Pauline M. Maki

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  1. Leah H. Rubin
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Correspondence to Leah H. Rubin.

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Rubin, L.H., Benning, L., Keating, S.M. et al. Variability in C-reactive protein is associated with cognitive impairment in women living with and without HIV: a longitudinal study. J. Neurovirol. 24, 41–51 (2018). https://doi.org/10.1007/s13365-017-0590-4

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