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HIV, Vascular Risk Factors, and Cognition in the Combination Antiretroviral Therapy Era: A Systematic Review and Meta-Analysis

Published online by Cambridge University Press:  09 November 2020

Elissa C. McIntosh Open the ORCID record for Elissa C. McIntosh [Opens in a new window] ,
Kayla Tureson ,
Lindsay J. Rotblatt ,
Elyse J. Singer  and
April D. Thames Open the ORCID record for April D. Thames [Opens in a new window]
Elissa C. McIntosh
Affiliation:
Department of Psychology, University of Southern California, Los Angeles, CA, USA
Kayla Tureson
Affiliation:
Department of Psychology, University of Southern California, Los Angeles, CA, USA
Lindsay J. Rotblatt
Affiliation:
Department of Clinical and Health Psychology, University of Florida, Gainesville, FL, USA
Elyse J. Singer
Affiliation:
Department of Neurology, UCLA David Geffen School of Medicine, Los Angeles, CA, USA
April D. Thames*
Affiliation:
Department of Psychology, University of Southern California, Los Angeles, CA, USA
*
*Correspondence and reprint requests to: April D. Thames, Ph.D., Associate Professor of Psychology, University of Southern California, 3620 South McClintock Ave., Building/room: SGM 520, Los Angeles, CA 90089-1061, USA. Tel: +1 213 740 4436. E-mail: thames@usc.edu
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Abstract

Objectives:

Mounting evidence indicates that vascular risk factors (VRFs) are elevated in HIV and play a significant role in the development and persistence of HIV-associated neurocognitive disorder. Given the increased longevity of people living with HIV (PLWH), there is a great need to better elucidate vascular contributions to neurocognitive impairment in HIV. This systematic review and meta-analysis examine relationships between traditional VRFs, cardiovascular disease (CVD), and cognition in PLWH in the combination antiretroviral therapy era.

Methods:

For the systematic review, 44 studies met inclusion criteria and included data from 14,376 PLWH and 6,043 HIV-seronegative controls. To better quantify the contribution of VRFs to cognitive impairment in HIV, a robust variance estimation meta-analysis (N = 11 studies) was performed and included data from 2139 PLWH.

Results:

In the systematic review, cross-sectional and longitudinal studies supported relationships between VRFs, cognitive dysfunction, and decline, particularly in the domains of attention/processing speed, executive functioning, and fine motor skills. The meta-analysis demonstrated VRFs were associated with increased odds of global neurocognitive impairment (odds ratio [OR ]= 2.059, p = .010), which remained significant after adjustment for clinical HIV variables (p = .017). Analyses of individual VRFs demonstrated type 2 diabetes (p = .004), hyperlipidemia (p = .043), current smoking (p = .037), and previous CVD (p = .0005) were significantly associated with global neurocognitive impairment.

Conclusions:

VRFs and CVD are associated with worse cognitive performance and decline, and neurocognitive impairment in PLWH. Future studies are needed to examine these relationships in older adults with HIV, and investigate how race/ethnicity, gender, medical comorbidities, and psychosocial factors contribute to VRF-associated cognitive dysfunction in HIV.

Keywords

Neurocognitive disordersCognitive agingVascular diseasesCardiovascular diseasesHighly active antiretroviral therapyDiabetes mellitus
Type
Critical Review
Information
Journal of the International Neuropsychological Society , Volume 27 , Issue 4 , April 2021 , pp. 365 - 381
Copyright
Copyright © INS. Published by Cambridge University Press, 2020

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References

REFERENCES

Becker, J.T., Kingsley, L., Mullen, J., Cohen, B., Martin, E., Miller, E.N., … Multictr, A.C.S. (2009). Vascular risk factors, HIV serostatus, and cognitive dysfunction in gay and bisexual men. Neurology, 73(16), 1292–1299. doi: 10.1212/WNL.0b013e3181bd10e7 CrossRefGoogle ScholarPubMed
Becker, J.T., Maruca, V., Kingsley, L.A., Sanders, J.M., Alger, J.R., Barker, P.B., … Selnes, O. (2012). Factors affecting brain structure in men with HIV disease in the post-HAART era. Neuroradiology, 54(2), 113–121. doi: 10.1007/s00234-011-0854-2 CrossRefGoogle ScholarPubMed
Begg, C.B. & Mazumdar, M. (1994). Operating characteristics of a rank correlation test for publication bias. Biometrics, 50(4), 1088–1101.CrossRefGoogle Scholar
Borenstein, M., Hedges, L.V., Higgins, J.P., & Rothstein, H.R. (2010). A basic introduction to fixed-effect and random-effects models for meta-analysis. Research Synthesis Methods, 1(2), 97–111. doi: 10.1002/jrsm.12 CrossRefGoogle ScholarPubMed
Calza, L., Manfredi, R., & Chiodo, F. (2004). Dyslipidaemia associated with antiretroviral therapy in HIV-infected patients. The Journal of Antimicrobial Chemotherapy, 53(1), 10–14. doi: 10.1093/jac/dkh013 CrossRefGoogle ScholarPubMed
Centers for Disease Control and Prevention. (2020, May). HIV Surveillance Report 2018 (Updated); vol. 31. Retrieved from http://www.cdc.gov/hiv/library/reports/hiv-surveillance.html Google Scholar
Ciccarelli, N., Baldonero, E., Milanini, B., Fabbiani, M., Cauda, R., Di Giambenedetto, S., & Silveri, M.C. (2019). Cognitive impairment and cardiovascular disease related to alexithymia in a well-controlled HIV-infected population. Le Infezioni in Medicina, 27(3), 274–282.Google Scholar
Ciccarelli, N., Grima, P., Fabbiani, M., Baldonero, E., Borghetti, A., Milanini, B., … Di Giambenedetto, S. (2015). Baseline CD4(+) T-cell count and cardiovascular risk factors predict the evolution of cognitive performance during 2-year follow-up in HIV-infected patients. Antiviral Therapy, 20(4), 433–440. doi: 10.3851/imp2925 CrossRefGoogle ScholarPubMed
Crum-Cianflone, N., Tejidor, R., Medina, S., Barahona, I., & Ganesan, A. (2008). Obesity among HIV Patients: The Latest Epidemic. AIDS Patient Care STDS, 22(12), 925–930. doi: 10.1089/apc.2008.0082 CrossRefGoogle ScholarPubMed
Crystal, H.A., Weedon, J., Holman, S., Manly, J., Valcour, V., Cohen, M., … Kaplan, R.C. (2011). Associations of cardiovascular variables and HAART with cognition in middle-aged HIV-infected and uninfected women. Journal of Neurovirology, 17(5), 469–476. doi: 10.1007/s13365-011-0052-3 CrossRefGoogle ScholarPubMed
Cunningham, W.E., Hays, R.D., Duan, N., Andersen, R., Nakazono, T.T., Bozette, S.A., & Shapiro, M.E. (2005). The effect of socioeconomic status on the survival of people receiving care for HIV infection in the United States. Journal of Health Care for the Poor and Underserved, 16(4), 655–676. doi: 10.1353/hpu.2005.0093 CrossRefGoogle ScholarPubMed
Cysique, L.A. & Brew, B.J. (2019). Vascular cognitive impairment and HIV-associated neurocognitive disorder: A new paradigm. Journal of NeuroVirology. doi: 10.1007/s13365-018-0706-5 CrossRefGoogle ScholarPubMed
Demir, O.M., Candilio, L., Fuster, D., Muga, R., Barbaro, G., Colombo, A., & Azzalini, L. (2018). Cardiovascular disease burden among human immunodeficiency virus-infected individuals. International Journal of Cardiology, 265, 195–203. doi: 10.1016/j.ijcard.2018.03.137 CrossRefGoogle ScholarPubMed
Dimsdale, J.E. (2008). Psychological stress and cardiovascular disease. Journal of the American College of Cardiology, 51(13), 1237–1246. doi: 10.1016/j.jacc.2007.12.024 CrossRefGoogle ScholarPubMed
Ding, Y.Y., Lin, H.J., Liu, X., Zhang, Y.C., Wong, F.Y., Sun, Y.V., … He, N. (2017). Hypertension in HIV-infected adults compared with similar but uninfected adults in China: Body mass index-dependent effects of nadir CD4 count. Aids Research and Human Retroviruses, 33(11), 1117–1125. doi: 10.1089/aid.2017.0008 CrossRefGoogle ScholarPubMed
Ding, Y.Y., Lin, H.J., Shen, W.W., Wu, Q.H., Gao, M.Y., & He, N. (2017). Interaction effects between HIV and aging on selective neurocognitive impairment. Journal of Neuroimmune Pharmacology, 12(4), 661–669. doi: 10.1007/s11481-017-9748-3 CrossRefGoogle ScholarPubMed
Dufouil, C., Richert, L., Thiebaut, R., Bruyand, M., Amieva, H., Dauchy, F.A., … Chêne, G. (2015). Diabetes and cognitive decline in a French cohort of patients infected with HIV-1. Neurology, 85(12), 1065–1073. doi: 10.1212/wnl.0000000000001815 CrossRefGoogle Scholar
Durazzo, T.C., Meyerhoff, D.J., & Nixon, S.J. (2012). A comprehensive assessment of neurocognition in middle-aged chronic cigarette smokers. Drug and Alcohol Dependence, 122(1–2), 105–111. doi: 10.1016/j.drugalcdep.2011.09.019 CrossRefGoogle ScholarPubMed
Duron, E. & Hanon, O. (2010). Antihypertensive treatments, cognitive decline, and dementia. Journal of Alzheimer’s Disease, 20(3), 903–914. doi: 10.3233/jad-2010-091552 CrossRefGoogle ScholarPubMed
Duval, S. & Tweedie, R. (2000a). A nonparametric “trim and fill” method of accounting for publication bias in meta-analysis. Journal of the American Statistical Association, 95(449), 89–98.Google Scholar
Duval, S. & Tweedie, R. (2000b). Trim and fill: A simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics, 56(2), 455–463. doi: 10.1111/j.0006-341x.2000.00455.x CrossRefGoogle ScholarPubMed
Elicer, I.M., Byrd, D., Clark, U.S., Morgello, S., & Robinson-Papp, J. (2018). Motor function declines over time in human immunodeficiency virus and is associated with cerebrovascular disease, while HIV-associated neurocognitive disorder remains stable. Journal of NeuroVirology, 24(4), 514–522. doi: 10.1007/s13365-018-0640-6 CrossRefGoogle Scholar
Fabbiani, M., Ciccarelli, N., Tana, M., Farina, S., Baldonero, E., Di Cristo, V., … Di Giambenedetto, S. (2013). Cardiovascular risk factors and carotid intima-media thickness are associated with lower cognitive performance in HIV-infected patients. HIV Medicine, 14(3), 136–144. doi: 10.1111/j.1468-1293.2012.01044.x CrossRefGoogle ScholarPubMed
Fisher, Z., Tipton, E., & Zhipeng, H. (2017). Robumeta: Robust variance meta-regression (Version 2.0) [R package]. Retrieved from https://CRAN.R-project.org/package=robumeta Google Scholar
Fitzpatrick, A.L., Kuller, L.H., Lopez, O.L., Diehr, P., O’Meara, E.S., Longstreth, W.T., & Luchsinger, J.A. (2009). Midlife and late-life obesity and the risk of dementia: Cardiovascular health study. Archives of Neurology, 66(3), 336–342. doi: 10.1001/archneurol.2008.582 CrossRefGoogle ScholarPubMed
Foley, J., Ettenhofer, M., Wright, M.J., Siddiqi, I., Choi, M., Thames, A.D., … Hinkin, C.H. (2010). Neurocognitive functioning in HIV-1 infection: Effects of cerebrovascular risk factors and age. Clinical Neuropsychologist, 24(2), 265–285. doi: 10.1080/13854040903482830 CrossRefGoogle ScholarPubMed
Gijsberts, C.M., Groenewegen, K.A., Hoefer, I.E., Eijkemans, M.J.C., Asselbergs, F.W., Anderson, T.J., … den Ruijter, H.M. (2015). Race/ethnic differences in the associations of the Framingham risk factors with carotid IMT and cardiovascular events. PLoS One, 10(7). doi: 10.1371/journal.pone.0132321 CrossRefGoogle ScholarPubMed
Gomez, D., Power, C., Gill, M.J., & Fujiwara, E. (2017). Determinants of risk-taking in HIV-associated neurocognitive disorders. Neuropsychology, 31(7), 798–810. doi: 10.1037/neu0000366 CrossRefGoogle ScholarPubMed
Grima, P., Fabbiani, M., Ciccarelli, N., Tana, M., Farina, S., Colafigli, M., … Di Giambenedetto, S. (2012). Increased ophthalmic artery resistance index is associated with cognitive impairment in HIV-infected patients. Journal of Infection, 65(5), 439–446. doi: 10.1016/j.jinf.2012.07.005 CrossRefGoogle ScholarPubMed
Grinspoon, S. & Carr, A. (2005). Cardiovascular risk and body-fat abnormalities in HIV-infected adults. The New England Journal of Medicine, 352(1), 48–62. doi: 10.1056/NEJMra041811 CrossRefGoogle ScholarPubMed
Gustafson, D. (2008). A life course of adiposity and dementia. European Journal of Pharmacology, 585(1), 163–175. doi: 10.1016/j.ejphar.2008.01.052 CrossRefGoogle ScholarPubMed
Gustafson, D., Mielke, M.M., Tien, P.C., Valcour, V., Cohen, M., Anastos, K., … Crystal, H.A. (2013). Anthropometric measures and cognition in middle-aged HIV-infected and uninfected women. The Women’s Interagency HIV Study. Journal of Neurovirology, 19(6), 574–585. doi: 10.1007/s13365-013-0219-1 CrossRefGoogle ScholarPubMed
Hanna, D.B., Post, W.S., Deal, J.A., Hodis, H.N., Jacobson, L.P., Mack, W.J., … Kingsley, L.A. (2015). HIV infection is associated with progression of subclinical carotid atherosclerosis. Clinical Infectious Diseases, 61(4), 640–650. doi: 10.1093/cid/civ325 CrossRefGoogle ScholarPubMed
Hatleberg, C.I., Ryom, L., El-Sadr, W., Mocroft, A., Reiss, P., de Wit, S., … Sabin, C. (2014). Gender differences in HIV-positive persons in use of cardiovascular disease-related interventions: D:A:D study. Journal of the International AIDS Society, 17(4 Suppl 3), 19516. doi: 10.7448/ias.17.4.19516 CrossRefGoogle ScholarPubMed
Heaton, R.K., Clifford, D.B., Franklin, D.R. Jr, Woods, S.P., Ake, C., Vaida, F., … Grant, I. (2010). HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER Study. Neurology, 75(23), 2087–2096. doi: 10.1212/WNL.0b013e318200d727 CrossRefGoogle ScholarPubMed
Heaton, R.K., Marcotte, T.D., Mindt, M.R., Sadek, J., Moore, D.J., Bentley, H., … Grant, I. (2004). The impact of HIV-associated neuropsychological impairment on everyday functioning. Journal of the International Neuropsychological Society, 10(3), 317–331. doi: 10.1017/s1355617704102130 CrossRefGoogle ScholarPubMed
Hedges, L.V., Tipton, E., & Johnson, M.C. (2010). Robust variance estimation in meta-regression with dependent effect size estimates. Research Synthesis Methods, 1(1), 39–65. doi: 10.1002/jrsm.5 CrossRefGoogle ScholarPubMed
Higgins, J.P., Li, T., & Deeks, J.J. (2019). Chapter 6: Choosing effect measures and computing estimates of effect. In Higgins, J.P., Thomas, J., Chandler, J., Cumpston, M., Li, T., Page, M.J., & Welch, V.A. (Eds.), Cochrane Handbook for Systematic Reviews of Interventions Version 6.0 (Updated July 2019). Cochrane, 2019. Available from www.training.cochrane.org/handbook CrossRefGoogle Scholar
Higgins, J.P.T., Thompson, S.G., Deeks, J.J., & Altman, D.G. (2003). Measuring inconsistency in meta-analyses. BMJ, 327(7414), 557–560. doi: 10.1136/bmj.327.7414.557 CrossRefGoogle ScholarPubMed
Hsue, P.Y., Hunt, P.W., Schnell, A., Kalapus, S.C., Hoh, R., Ganz, P., … Deeks, S.G. (2009). Role of viral replication, antiretroviral therapy, and immunodeficiency in HIV-associated atherosclerosis. AIDS, 23(9), 1059–1067. doi: 10.1097/QAD.0b013e32832b514b CrossRefGoogle ScholarPubMed
Huck, D.M., Hanna, D.B., Rubin, L.H., Maki, P., Valcour, V., Springer, G., … Kizer, J.R. (2018). Carotid artery stiffness and cognitive decline among women with or at risk for HIV infection. Journal of Acquired Immune Deficiency Syndromes, 78(3), 338–347. doi: 10.1097/qai.0000000000001685 CrossRefGoogle ScholarPubMed
Husain, N.E.O. & Ahmed, M.H. (2015). Managing dyslipidemia in HIV/AIDS patients: Challenges and solutions. HIV/AIDS (Auckland, NZ), 7, 1–10. doi: 10.2147/hiv.s46028 Google ScholarPubMed
Jefferson, A.L., Hohman, T.J., Liu, D., Haj-Hassan, S., Gifford, K.A., Benson, E.M., … Ruberg, F.L. (2015). Adverse vascular risk is related to cognitive decline in older adults. Journal of Alzheimer’s Disease, 44(4), 1361–1373. doi: 10.3233/jad-141812 CrossRefGoogle ScholarPubMed
Jumare, J., El-Kamary, S.S., Magder, L., Hungerford, L., Umlauf, A., Franklin, D., … McCutchan, J.A. (2019). Body mass index and cognitive function among HIV-1 infected individuals in China, India and Nigeria. JAIDS – Journal of Acquired Immune Deficiency Syndromes, 80(2), e30–e35. doi: 10.1097/qai.0000000000001906 CrossRefGoogle ScholarPubMed
Kaffashian, S., Dugravot, A., Nabi, H., Batty, G.D., Brunner, E., Kivimaki, M., & Singh-Manoux, A. (2011). Predictive utility of the Framingham general cardiovascular disease risk profile for cognitive function: Evidence from the Whitehall II study. European Heart Journal, 32(18), 2326–2332. doi: 10.1093/eurheartj/ehr133 CrossRefGoogle ScholarPubMed
Khuder, S.S., Chen, S., Letendre, S., Marcotte, T., Grant, I., Franklin, D., … Haughey, N.J. (2019). Impaired insulin sensitivity is associated with worsening cognition in HIV-infected patients. Neurology, 92(12), e1344–e1353. doi: 10.1212/wnl.0000000000007125 CrossRefGoogle ScholarPubMed
Kivipelto, M., Helkala, E.L., Laakso, M.P., Hanninen, T., Hallikainen, M., Alhainen, K., … Nissinen, A. (2001). Midlife vascular risk factors and Alzheimer’s disease in later life: Longitudinal, population based study. BMJ, 322(7300), 1447–1451. doi: 10.1136/bmj.322.7300.1447 CrossRefGoogle ScholarPubMed
Lake, J.E., Vo, Q.T., Jacobson, L.P., Sacktor, N., Miller, E.N., Post, W.S., … Brown, T.T. (2015). Adiponectin and interleukin-6, but not adipose tissue, are associated with worse neurocognitive function in HIV-infected men. Antiviral Therapy, 20(2), 235–244. doi: 10.3851/imp2952 CrossRefGoogle Scholar
Lang, S., Mary-Krause, M., Simon, A., Partisani, M., Gilquin, J., Cotte, L., … Costagliola, D. (2012). HIV replication and immune status are independent predictors of the risk of myocardial infarction in HIV-infected individuals. Clinical Infectious Diseases, 55(4), 600–607. doi: 10.1093/cid/cis489 CrossRefGoogle ScholarPubMed
Lo, J., Abbara, S., Shturman, L., Soni, A., Wei, J., Rocha-Filho, J.A., … Grinspoon, S.K. (2010). Increased prevalence of subclinical coronary atherosclerosis detected by coronary computed tomography angiography in HIV-infected men. AIDS, 24(2), 243–253. doi: 10.1097/QAD.0b013e328333ea9e CrossRefGoogle ScholarPubMed
Longenecker, C.T., Sullivan, C., & Baker, J.V. (2016). Immune activation and cardiovascular disease in chronic HIV infection. Current Opinion in HIV and AIDS, 11(2), 216–225. doi: 10.1097/coh.0000000000000227 CrossRefGoogle ScholarPubMed
Marquine, M.J., Heaton, A., Johnson, N., Rivera-Mindt, M., Cherner, M., Bloss, C., … Heaton, R.K. (2018). Differences in neurocognitive impairment among HIV-infected Latinos in the United States. Journal of the International Neuropsychological Society, 24(2), 163–175. doi: 10.1017/s1355617717000832 CrossRefGoogle ScholarPubMed
McCutchan, J.A., Marquie-Beck, J.A., FitzSimons, C.A., Letendre, S.L., Ellis, R.J., Heaton, R.K., … Grp, C. (2012). Role of obesity, metabolic variables, and diabetes in HIV-associated neurocognitive disorder. Neurology, 78(7), 485–492. doi: 10.1212/WNL.0b013e3182478d64 CrossRefGoogle ScholarPubMed
McIntosh, E.C. & Nation, D.A. (2019). Importance of treatment status in links between type 2 diabetes and Alzheimer’s disease. Diabetes Care, 42(5), 972–979. doi: 10.2337/dc18-1399 CrossRefGoogle ScholarPubMed
Montoya, J.L., Iudicello, J., Fazeli, P.L., Hong, S.Z., Potter, M., Ellis, R.J., … the HIV Neurobehavioral Research Program (HNRP) Group (2017). Elevated markers of vascular remodeling and arterial stiffness are associated with neurocognitive function in older HIV plus adults on suppressive antiretroviral therapy. JAIDS – Journal of Acquired Immune Deficiency Syndromes, 74(2), 134–141. doi: 10.1097/qai.0000000000001230 CrossRefGoogle Scholar
Mukerji, S.S., Locascio, J.J., Misra, V., Lorenz, D.R., Holman, A., Dutta, A., … Gabuzda, D. (2016). Lipid profiles and APOE4 allele impact midlife cognitive decline in HIV-infected men on antiretroviral therapy. Clinical Infectious Diseases, 63(8), 1130–1139. doi: 10.1093/cid/ciw495 CrossRefGoogle ScholarPubMed
Nakamoto, B.K., Jahanshad, N., McMurtray, A., Kallianpur, K.J., Chow, D.C., Valcour, V.G., … Shikuma, C.M. (2012). Cerebrovascular risk factors and brain microstructural abnormalities on diffusion tensor images in HIV-infected individuals. Journal of Neurovirology, 18(4), 303–312. doi: 10.1007/s13365-012-0106-1 CrossRefGoogle ScholarPubMed
Nakamoto, B.K., Valcour, V., Kallianpur, K., Liang, C.Y., McMurtray, A., Chow, D., … Shikuma, C.M. (2011). Impact of cerebrovascular disease on cognitive function in HIV-infected patients. JAIDS – Journal of Acquired Immune Deficiency Syndromes, 57(3), e66–e68. doi: 10.1097/QAI.0b013e31821ff8bd CrossRefGoogle ScholarPubMed
Nou, E., Lo, J., & Grinspoon, S.K. (2016). Inflammation, immune activation, and cardiovascular disease in HIV. AIDS, 30(10), 1495–1509. doi: 10.1097/qad.0000000000001109 CrossRefGoogle ScholarPubMed
Okafor, C.N., Kelso, N.E., Bryant, V., Burrell, L.E., Miguez, M.J., Gongvatana, A., … Cohen, R.A. (2017). Body mass index, inflammatory biomarkers and neurocognitive impairment in HIV-infected persons. Psychology Health & Medicine, 22(3), 289–302. doi: 10.1080/13548506.2016.1199887 CrossRefGoogle ScholarPubMed
Onen, N.F., Overton, E.T., Seyfried, W., Stumm, E.R., Snell, M., Mondy, K., & Tebas, P. (2010). Aging and HIV infection: A comparison between older HIV-infected persons and the general population. HIV Clinical Trials, 11(2), 100–109. doi: 10.1310/hct1102-100 CrossRefGoogle ScholarPubMed
Palella, F.J. & Phair, J.P. (2011). Cardiovascular disease in HIV infection. Current Opinion in HIV and AIDS, 6(4), 266–271. doi: 10.1097/COH.0b013e328347876c CrossRefGoogle ScholarPubMed
Pantoni, L. (2010). Cerebral small vessel disease: From pathogenesis and clinical characteristics to therapeutic challenges. The Lancet Neurology, 9(7), 689–701. doi: 10.1016/s1474-4422(10)70104-6 CrossRefGoogle ScholarPubMed
Patel, S.M., Thames, A.D., Arbid, N., Panos, S.E., Castellon, S., & Hinkin, C.H. (2013). The aggregate effects of multiple comorbid risk factors on cognition among HIV-infected individuals. Journal of Clinical and Experimental Neuropsychology, 35(4), 421–434. doi: 10.1080/13803395.2013.783000 CrossRefGoogle ScholarPubMed
Portilla, I., Reus, S., León, R., van-der Hofstadt, C., Sánchez, J., López, N., … Portilla, J. (2019). Neurocognitive impairment in well-controlled HIV-infected patients: A cross-sectional study. AIDS Research and Human Retroviruses, 35(7). doi: 10.1089/AID.2018.0279 CrossRefGoogle ScholarPubMed
Raz, N., Rodrigue, K.M., & Acker, J.D. (2003). Hypertension and the brain: Vulnerability of the prefrontal regions and executive functions. Behavioral Neuroscience, 117(6), 1169–1180. doi: 10.1037/0735-7044.117.6.1169 CrossRefGoogle ScholarPubMed
Rider, O.J., Asaad, M., Ntusi, N., Wainwright, E., Clutton, G., Hancock, G., … Holloway, C.J. (2014). HIV is an independent predictor of aortic stiffness. Journal of Cardiovascular Magnetic Resonance, 16(1), 57. doi: 10.1186/s12968-014-0057-1 CrossRefGoogle ScholarPubMed
Rosenthal, R. (1979). The file drawer problem and tolerance for null results. Psychological Bulletin, 86(3), 638–641. doi: 10.1037/0033-2909.86.3.638 CrossRefGoogle Scholar
Rubin, L.H., Gustafson, D., Hawkins, K.L., Zhang, L., Jacobson, L.P., Becker, J.T., … Erlandson, K.M. (2019). Midlife adiposity predicts cognitive decline in the prospective Multicenter AIDS Cohort Study. Neurology, 93(3). doi: 10.1212/WNL.0000000000007779 CrossRefGoogle ScholarPubMed
Saloner, R., Campbell, L.M., Serrano, V., Montoya, J.L., Pasipanodya, E., Paolillo, E.W., … Moore, D.J. (2019). Neurocognitive SuperAging in older adults living with HIV: Demographic, neuromedical and everyday functioning correlates. Journal of the International Neuropsychological Society, 25(5), 507–519. doi: 10.1017/s1355617719000018 CrossRefGoogle ScholarPubMed
Sanford, R., Strain, J., Dadar, M., Maranzano, J., Bonnet, A., Mayo, N.E., … Collins, D.L. (2019). HIV infection and cerebral small vessel disease are independently associated with brain atrophy and cognitive impairment. AIDS (London, England), 33(7). doi: 10.1097/QAD.0000000000002193 CrossRefGoogle ScholarPubMed
Sattler, F.R., He, J.X., Letendre, S., Wilson, C., Sanders, C., Heaton, R., … the CHARTER Group (2015). Abdominal obesity contributes to neurocognitive impairment in HIV-infected patients with increased inflammation and immune activation. JAIDS – Journal of Acquired Immune Deficiency Syndromes, 68(3), 281–288. doi: 10.1097/qai.0000000000000458 CrossRefGoogle ScholarPubMed
Satz, P., Morgenstern, H., Miller, E.N., Selnes, O.A., McArthur, J.C., Cohen, B.A., … D’Elia, L.F. (1993). Low education as a possible risk factor for cognitive abnormalities in HIV-1: Findings from the multicenter AIDS Cohort Study (MACS). JAIDS – Journal of Acquired Immune Deficiency Syndromes, 6(5), 503–511.CrossRefGoogle Scholar
Schouten, J., Su, T., Wit, F.W., Kootstra, N.A., Caan, M.W.A., Geurtsen, G.J., … AGEhIV Study Group (2016). Determinants of reduced cognitive performance in HIV-1-infected middle-aged men on combination antiretroviral therapy. AIDS, 30(7), 1027–1038. doi: 10.1097/qad.0000000000001017 CrossRefGoogle ScholarPubMed
Seaberg, E.C., Benning, L., Sharrett, A.R., Lazar, J.M., Hodis, H.N., Mack, W.J., … Kaplan, R.C. (2010). Association between human immunodeficiency virus infection and stiffness of the common carotid artery. Stroke, 41(10), 2163–2170. doi: 10.1161/strokeaha.110.583856 CrossRefGoogle ScholarPubMed
Singer, E.J., Valdes-Sueiras, M., Commins, D.L., Yong, W., & Carlson, M. (2013). HIV stroke risk: Evidence and implications. Therapeutic Advances in Chronic Disease, 4(2), 61–70. doi: 10.1177/2040622312471840 CrossRefGoogle ScholarPubMed
Soliman, E.Z., Sharma, S., Arasteh, K., Wohl, D., Achhra, A., Tambussi, G., … Phillips, A. (2015). Baseline cardiovascular risk in the INSIGHT Strategic Timing of AntiRetroviral Treatment (START) trial. HIV Medicine, 16(Suppl 1), 46–54. doi: 10.1111/hiv.12233 CrossRefGoogle ScholarPubMed
Soontornniyomkij, V., Umlauf, A., Chung, S.A., Cochran, M.L., Soontornniyomkij, B., Gouaux, B., … Achim, C.L. (2014). HIV protease inhibitor exposure predicts cerebral small vessel disease. AIDS, 28(9), 1297–1306. doi: 10.1097/qad.0000000000000262 CrossRefGoogle ScholarPubMed
Stein, J.H. & Hsue, P.Y. (2012). Inflammation, immune activation, and CVD risk in individuals with HIV infection. JAMA, 308(4), 405–406. doi: 10.1001/jama.2012.8488 CrossRefGoogle ScholarPubMed
Su, T., Mutsaerts, H., Caan, M.W.A., Wit, F., Schouten, J., Geurtsen, G.J., … AGEhIV Study Group (2017). Cerebral blood flow and cognitive function in HI-infected men with sustained suppressed viremia on combination antiretroviral therapy. AIDS, 31(6), 847–856. doi: 10.1097/qad.0000000000001414 CrossRefGoogle ScholarPubMed
Su, T., Wit, F., Caan, M.W.A., Schouten, J., Prins, M., Geurtsen, G.J., … AGEhIV Study Group (2016). White matter hyperintensities in relation to cognition in HIV-infected men with sustained suppressed viral load on combination antiretroviral therapy. AIDS, 30(15), 2329–2339. doi: 10.1097/qad.0000000000001133 CrossRefGoogle ScholarPubMed
Taki, Y., Goto, R., Evans, A., Zijdenbos, A., Neelin, P., Lerch, J., … Fukuda, H. (2004). Voxel-based morphometry of human brain with age and cerebrovascular risk factors. Neurobiology of Aging, 25(4), 455–463. doi: 10.1016/j.neurobiolaging.2003.09.002 CrossRefGoogle ScholarPubMed
Tanner-Smith, E.E., Tipton, E., & Polanin, J.R. (2016). Handling complex meta-analytic data structures using robust variance estimates: A tutorial in R. Journal of Developmental and Life-Course Criminology, 2(1), 85–112. doi: 10.1007/s40865-016-0026-5 CrossRefGoogle Scholar
R Core Team (2014). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Retrieved from http://www.R-project.org/ Google Scholar
Tedaldi, E.M., Minniti, N.L., & Fischer, T. (2015). HIV-associated neurocognitive disorders: The relationship of HIV infection with physical and social comorbidities. BioMed Research International, 2015, 641913. doi: 10.1155/2015/641913 CrossRefGoogle ScholarPubMed
Thames, A.D., Arentoft, A., Rivera-Mindt, M., & Hinkin, C.H. (2013). Functional disability in medication management and driving among individuals with HIV: A 1-year follow-up study. Journal of Clinical and Experimental Neuropsychology, 35(1), 49–58. doi: 10.1080/13803395.2012.747596 CrossRefGoogle ScholarPubMed
Triant, V.A. (2013). Cardiovascular disease and HIV infection. Current HIV/AIDS Reports, 10(3), 199–206. doi: 10.1007/s11904-013-0168-6 CrossRefGoogle ScholarPubMed
Triant, V.A., Lee, H., Hadigan, C., & Grinspoon, S.K. (2007). Increased acute myocardial infarction rates and cardiovascular risk factors among patients with human immunodeficiency virus disease. The Journal of Clinical Endocrinology and Metabolism, 92(7), 2506–2512. doi: 10.1210/jc.2006-2190 CrossRefGoogle ScholarPubMed
Unverzagt, F.W., McClure, L.A., Wadley, V.G., Jenny, N.S., Go, R.C., Cushman, M., … Howard, G. (2011). Vascular risk factors and cognitive impairment in a stroke-free cohort. Neurology, 77(19), 1729–1736. doi: 10.1212/WNL.0b013e318236ef23 CrossRefGoogle Scholar
Valcour, V., Maki, P., Bacchetti, P., Anastos, K., Crystal, H., Young, M., … Tien, P.C. (2012). Insulin resistance and cognition among HIV-infected and HIV-uninfected adult women: The Women’s Interagency HIV Study. AIDS Research and Human Retroviruses, 28(5), 447–453. doi: 10.1089/aid.2011.0159 CrossRefGoogle ScholarPubMed
Valcour, V., Rubin, L.H., Tien, P., Anastos, K., Young, M., Mack, W., … Maki, P.M. (2015). 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). Journal of Neurovirology, 21(4), 415–421. doi: 10.1007/s13365-015-0330-6 CrossRefGoogle Scholar
Valcour, V., Sacktor, N.C., Paul, R.H., Watters, M.R., Selnes, O.A., Shiramizu, B.T., … Shikuma, C.M. (2006). Insulin resistance is associated with cognition among HIV-1-infected patients – The Hawaii aging with HIV cohort. JAIDS – Journal of Acquired Immune Deficiency Syndromes, 43(4), 405–410. doi: 10.1097/01.qai.0000243119.67529.f5 CrossRefGoogle ScholarPubMed
Valcour, V., Shikuma, C.M., Shiramizu, B.T., Williams, A.E., Watters, M.R., Poff, P.W., … Sacktor, N.C. (2005). Diabetes, insulin resistance, and dementia among HIV-1-infected patients. JAIDS – Journal of Acquired Immune Deficiency Syndromes, 38(1), 31–36. doi: 10.1097/00126334-200501010-00006 CrossRefGoogle ScholarPubMed
Valdez, A.N., Rubin, L.H., & Neigh, G.N. (2016). Untangling the Gordian knot of HIV, stress, and cognitive impairment. Neurobiology of Stress, 4, 44–54. doi: 10.1016/j.ynstr.2016.02.005 CrossRefGoogle ScholarPubMed
van den Berg, E., Kloppenborg, R.P., Kessels, R.P., Kappelle, L.J., & Biessels, G.J. (2009). Type 2 diabetes mellitus, hypertension, dyslipidemia and obesity: A systematic comparison of their impact on cognition. Biochimica et Biophysica Acta, 1792(5), 470–481. doi: 10.1016/j.bbadis.2008.09.004 CrossRefGoogle ScholarPubMed
Viechtbauer, W. (2010). Conducting meta-analyses in R with the metafor package. Journal of Statistical Software, 36, 1–48.CrossRefGoogle Scholar
Watson, C., Busovaca, E., Foley, J.M., Allen, I.E., Schwarz, C.G., Jahanshad, N., … Valcour, V.G. (2017). White matter hyperintensities correlate to cognition and fiber tract integrity in older adults with HIV. Journal of Neurovirology, 23(3), 422–429. doi: 10.1007/s13365-016-0509-5 CrossRefGoogle ScholarPubMed
Wilson, D.B. (n.d.). Practical meta-analysis effect size calculator [Online calculator]. Retrieved from https://campbellcollaboration.org/research-resources/effect-size-calculator.html Google Scholar
Womack, J.A., Chang, C.C., So-Armah, K.A., Alcorn, C., Baker, J.V., Brown, S.T., … Freiberg, M.S. (2014). HIV infection and cardiovascular disease in women. Journal of the American Heart Association, 3(5), e001035. doi: 10.1161/jaha.114.001035 CrossRefGoogle ScholarPubMed
Wright, E.J., Grund, B., Cysique, L.A., Robertson, K.R., Brew, B.J., Collins, G., … Int Network Strategic, I. (2015). Factors associated with neurocognitive test performance at baseline: A substudy of the INSIGHT Strategic Timing of AntiRetroviral Treatment (START) trial. HIV Medicine, 16, 97–108. doi: 10.1111/hiv.12238 CrossRefGoogle ScholarPubMed
Wright, E.J., Grund, B., Robertson, K., Brew, B.J., Roediger, M., Bain, M.P., … Price, R.W. (2010). Cardiovascular risk factors associated with lower baseline cognitive performance in HIV-positive persons. Neurology, 75(10), 864–873. doi: 10.1212/WNL.0b013e3181f11bd8 CrossRefGoogle ScholarPubMed
Yaldizli, O., Kastrup, O., Obermann, M., Esser, S., Wilhelm, H., Ley, C., … Maschke, M. (2006). Carotid intima-media thickness in HIV-Infected individuals: Relationship of premature atherosclerosis to neuropsychological deficits? European Neurology, 55(3), 166–171. doi: 10.1159/000093576 CrossRefGoogle ScholarPubMed
Yang, J., Jacobson, L.P., Becker, J.T., Levine, A., Martin, E.M., Munro, C.A., … Brown, T.T. (2018). Impact of glycemic status on longitudinal cognitive performance in men with and without HIV infection. AIDS, 32(13), 1849–1860. doi: 10.1097/qad.0000000000001842 CrossRefGoogle ScholarPubMed
Yang, Y.K., Yao, W.J., Yeh, T.L., Lee, I.H., Chen, P.S., Lu, R.B., & Chiu, N.T. (2008). Decreased dopamine transporter availability in male smokers – a dual isotope SPECT study. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 32(1). doi: 10.1016/j.pnpbp.2007.08.018 CrossRefGoogle ScholarPubMed
Yu, B., Pasipanodya, E., Montoya, J.L., Moore, R.C., Gianella, S., McCutchan, A., … Marquine, M.J. (2019). Metabolic syndrome and neurocognitive deficits in HIV infection. JAIDS – Journal of Acquired Immune Deficiency Syndromes, 81(1). doi: 10.1097/QAI.0000000000001964 CrossRefGoogle ScholarPubMed
Yuen, T., Brouillette, M.J., Fellows, L.K., Ellis, R.J., Letendre, S., Heaton, R., … CHARTER group (2017). Personalized risk index for neurocognitive decline among people with well-controlled HIV infection. JAIDS – Journal of Acquired Immune Deficiency Syndromes, 76(1), 48–54.CrossRefGoogle ScholarPubMed
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