Abstract
HIV-associated neurocognitive impairment remains a challenge even in the era of antiretroviral therapy (ART). Over 90% of people living with HIV are in low- and middle-income countries. Hence, it is not surprising that such countries bear a considerable burden of comorbidities like HIV-associated neurocognitive impairment despite an overall increase in life expectancy. The literature suggests differences in patient characteristics, clinical profile, prevalent HIV subtypes, treatment choices, pharmacogenetics, and socioeconomic factors between low- and middle-income countries compared with high-income countries. Therefore, we aimed to evaluate the effect of ART on neurocognitive outcomes in low- and middle-income countries. A comprehensive search of five databases (PubMed, CINAHL, CENTRAL, PsychInfo, Google scholar) for studies published between 1996 to 2020 was performed to identify studies that reported neurocognitive outcomes in ART-treated and ART naïve HIV positive individuals. Two independent reviewers conducted study screening, data extraction, and evaluation of the risk of bias. Pooled effect size estimates (Hedges' g) and 95% CI were computed using random-effects models. Sensitivity analysis, subgroup analysis, meta-regression, and evaluation of publication bias were also conducted. Forty studies (24 cross-sectional, 13 longitudinal studies, and two randomized controlled trials) contributed to a series of meta-analyses. We found significant small to moderate effects of antiretroviral therapy for global cognition (Hedges’ g observed = 0.30; 95% CI: 0.15, 0.44; k = 25; p = 0.0003; I2 = 92.1%; tau = 0.32; Q = 305.1), executive function (Hedges’ g = 0.24, 95%CI: 0.02,0.46; p-0.04; k = 8; I2 = 37.5%; tau = 0.23; Q = 11.2), and speed of information processing (Hedges’ g = 0.25, 95% CI: 0.05, 0.45; k = 9; p = 0.02; I2 = 86.4%; tau = 0.21; Q = 58.9). We found no significant ART effect on attention-working memory, learning and memory, motor function, and verbal fluency. No significant effect was seen with the duration of therapy, efavirenz use, and Central Penetrating Effectiveness (CPE) of antiretroviral therapy. Subgroup analyses identified study design (between-group and within-group; cross-sectional and longitudinal) and normative scores as significant sources of heterogeneity. Meta-regression analysis indicated that nadir CD4 modified the magnitude of ART's effect on cognitive outcomes. Age, gender, and country income-group were not significant moderators. Our findings provide systematic evidence that antiretroviral therapy improves neurocognitive outcomes in the domains of global cognition, executive function and speed of information processing, of people living with HIV in low- and middle-income countries, especially those with advanced immunosuppression. However, these findings are not definitive as they are limited by the probability of publication bias, high heterogeneity, and exclusion of significant confounders. Prospero registration number: CRD42020203791.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
Most of the data used in this systematic review are publicly available.
References
Achappa, B., Priyadarshni, S., Madi, D., Unnikrishnan, B., Ramapuram, J., Rao, S., Chowta, M., & Mahalingam, S. (2014). Neurocognitive dysfunction among HIV positive patients using International HIV dementia scale. Asian Journal of Medical Sciences, 5, 61–64. https://doi.org/10.3126/ajms.v5i4.8724
Al-Khindi, T., Zakzanis, K. K., & van Gorp, W. G. (2011). Does antiretroviral therapy improve HIV-associated cognitive impairment? A quantitative review of the literature. Journal of the International Neuropsychological Society : JINS, 17(6), 956–969. https://doi.org/10.1017/S1355617711000968
Antinori, A., Arendt, G., Becker, J. T., Brew, B. J., Byrd, D. A., Cherner, M., Clifford, D. B., Cinque, P., Epstein, L. G., Goodkin, K., Gisslen, M., Grant, I., Heaton, R. K., Joseph, J., Marder, K., Marra, C. M., McArthur, J. C., Nunn, M., Price, R. W., & Wojna, V. E. (2007). Updated research nosology for HIV-associated neurocognitive disorders. Neurology, 69(18), 1789–1799. https://doi.org/10.1212/01.WNL.0000287431.88658.8b
Balduzzi, S., Rücker, G., & Schwarzer, G. (2019). How to perform a meta-analysis with R: A practical tutorial. Evidence-Based Mental Health, 22(4), 153–160. https://doi.org/10.1136/ebmental-2019-300117
Becker, B. J. (1988). Synthesizing standardized mean-change measures. British Journal of Mathematical and Statistical Psychology, 41(2), 257–278. https://doi.org/10.1111/j.2044-8317.1988.tb00901.x
Bednasz, C. J., Venuto, C. S., Ma, Q., Daar, E. S., Sax, P. E., Fischl, M. A., Collier, A. C., Smith, K. Y., Tierney, C., Acosta, E. P., Mager, D. E., & Morse, G. D. (2019). Race/Ethnicity and Protease Inhibitor Use Influence Plasma Tenofovir Exposure in Adults Living with HIV-1 in AIDS Clinical Trials Group Study A5202. Antimicrobial Agents and Chemotherapy, 63(4), e01638-e1718. https://doi.org/10.1128/AAC.01638-18
Borenstein, M., Hedges, L. V., Higgins, J., & Rothstein, H. (2009). Introduction to Meta‐Analysis (First Edit). John Wiley & Sons, Ltd.
Bougea, A., Spantideas, N., Galanis, P., Gkekas, G., & Thomaides, T. (2019). Optimal treatment of HIV-associated neurocognitive disorders: Myths and reality. A critical review. Therapeutic Advances in Infectious Disease, 6, 2049936119838228–2049936119838228. https://doi.org/10.1177/2049936119838228
Brouillette, M.-J., Fellows, L. K., & Mayo, N. E. (2020). Efavirenz and cognition that matters. AIDS (london, England), 34(7), 1105–1106. https://doi.org/10.1097/QAD.0000000000002545
Brouillette, M.-J., Yuen, T., Fellows, L. K., Cysique, L. A., Heaton, R., & Mayo, N. E. (2016). Identifying Neurocognitive Decline at 36 Months among HIV-Positive Participants in the CHARTER Cohort Using Group-Based Trajectory Analysis. PLoS One, 11(5), e0155766. https://doi.org/10.1371/journal.pone.0155766
Bunupuradah, T., Chetchotisakd, P., Jirajariyavej, S., Valcour, V., Bowonwattanuwong, C., Munsakul, W., Klinbuayaem, V., Prasithsirikul, W., Sophonphan, J., Mahanontharit, A., Hirschel, B., Bhakeecheep, S., Ruxrungtham, K., & Ananworanich, J. (2012). Neurocognitive impairment in patients randomized to second-line lopinavir/ritonavir-based antiretroviral therapy vs. lopinavir/ritonavir monotherapy. Journal of Neurovirology, 18(6), 479–487. https://doi.org/10.1007/s13365-012-0127-9
Butters, N., Grant, I., Haxby, J., Judd, L. L., Martin, A., McClelland, J., Pequegnat, W., Schacter, D., & Stover, E. (1990). Assessment of AIDS-related cognitive changes: Recommendations of the NIMH Workshop on Neuropsychological Assessment Approaches. Journal of Clinical and Experimental Neuropsychology, 12(6), 963–978. https://doi.org/10.1080/01688639008401035
Carvalhal, A. S., Rourke, S. B., Belmonte-Abreu, P., Correa, J., & Goldani, L. Z. (2006). Evaluation of neuropsychological performance of HIV-infected patients with minor motor cognitive dysfunction treated with highly active antiretroviral therapy. In Infection (Vol. 34, Issue 6, pp. 357–360). https://doi.org/10.1007/s15010-006-6610-6
Chen, J., Ramendra, R., Lu, H., & Routy, J.-P. (2018). The early bird gets the worm: Benefits and future directions with early antiretroviral therapy initiation in primary HIV infection. Future Virology, 13(11), 779–786. https://doi.org/10.2217/fvl-2018-0110
Chiolero, A., Santschi, V., Burnand, B., Platt, R. W., & Paradis, G. (2012). Meta-analyses: With confidence or prediction intervals? European Journal of Epidemiology, 27(10), 823–825. https://doi.org/10.1007/s10654-012-9738-y
Ciccarelli, N., Fabbiani, M., & Baldonero, E. (2011a). Efavirenz associated with cognitive disorders in otherwise asymptomatic HIV- infected patients. Neurology, 76(16), 1403–1409.
Ciccarelli, N., Fabbiani, M., Giambenedetto, S., Fanti, I., Baldonero, E., Bracciale, L., Tamburrini, E., Cauda, R., De Luca, A., & Silveri, M. (2011b). Efavirenz associated with cognitive disorders in otherwise asymptomatic HIV-infected patients. Neurology, 76, 1403–1409. https://doi.org/10.1212/WNL.0b013e31821670fb.
Cochran, W. G. (1950). The comparison of percentages in matched samples. Biometrika, 37(3–4), 256–266.
Cohen, J. (1988). Statistical Power Analysis for the Behavioral Sciences (2nd ed.). Routledge. https://doi.org/10.4324/9780203771587
Collie, A., Maruff, P., Darby, D. G., & McStephen, M. (2003). The effects of practice on the cognitive test performance of neurologically normal individuals assessed at brief test-retest intervals. Journal of the International Neuropsychological Society : JINS, 9(3), 419–428. https://doi.org/10.1017/S1355617703930074
Cross, H. M., Combrinck, M. I., & Joska, J. A. (2013). HIV-associated neurocognitive disorders: antiretroviral regimen, central nervous system penetration effectiveness, and cognitive outcomes. South African Medical Journal = Suid-Afrikaanse Tydskrif Vir Geneeskunde, 103(10), 758–762. https://doi.org/10.7196/samj.6677
Cuijpers, P., Weitz, E., Cristea, I. A., & Twisk, J. (2017). Pre-post effect sizes should be avoided in meta-analyses. Epidemiology and Psychiatric Sciences, 26(4), 364–368. https://doi.org/10.1017/S2045796016000809
Cysique, L. A., Letendre, S. L., Ake, C., Jin, H., Franklin, D. R., Gupta, S., Shi, C., Yu, X., Wu, Z., Abramson, I. S., Grant, I., Heaton, R., & Group H. I. V. N. R. C. (2010). Incidence and nature of cognitive decline over 1 year among HIV-infected former plasma donors in China. AIDS (london, England), 24(7), 983–990. https://doi.org/10.1097/QAD.0b013e32833336c8
Cysique, L. A., Waters, E. K., & Brew, B. J. (2011). Central nervous system antiretroviral efficacy in HIV infection: A qualitative and quantitative review and implications for future research. BMC Neurology, 11, 148. https://doi.org/10.1186/1471-2377-11-148
Cysique, L., & Brew, B. (2009). Neuropsychological Functioning and Antiretroviral Treatment in HIV/AIDS: A Review. Neuropsychology Review, 19, 169–185. https://doi.org/10.1007/s11065-009-9092-3
Dalton, J. E., Bolen, S. D., & Mascha, E. J. (2016). Publication Bias: The Elephant in the Review. Anesthesia and Analgesia, 123(4), 812–813. https://doi.org/10.1213/ANE.0000000000001596
Do, T. C., Kerr, S. J., Avihingsanon, A., Suksawek, S., Klungkang, S., Channgam, T., Odermatt, C. C., Maek-A-Nantawat, W., Ruxtungtham, K., Ananworanich, J., Valcour, V., Reiss, P., & Wit, F. W. (2018). HIV-associated cognitive performance and psychomotor impairment in a Thai cohort on long-term cART. Journal of Virus Eradication, 4(1), 41–47. https://pubmed.ncbi.nlm.nih.gov/29568553
Durlak, J. A. (2009). How to Select, Calculate, and Interpret Effect Sizes. Journal of Pediatric Psychology, 34(9), 917–928. https://doi.org/10.1093/jpepsy/jsp004
Duval, S., & Tweedie, R. (2000). Trim and fill: A simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics, 56(2), 455–463. https://doi.org/10.1111/j.0006-341x.2000.00455.x
Egger, M., Smith, G. D., Schneider, M., & Minder, C. (1997). Bias in meta-analysis detected by a simple, graphical test. BMJ, 315(7109), 629 LP – 634. https://doi.org/10.1136/bmj.315.7109.629
Ene, L., Franklin, D. R., Burlacu, R., Luca, A. E., Blaglosov, A. G., Ellis, R. J., Alexander, T. J., Umlauf, A., Grant, I., Duiculescu, D. C., Achim, C. L., & Marcotte, T. D. (2014). Neurocognitive functioning in a Romanian cohort of young adults with parenterally-acquired HIV-infection during childhood. Journal of Neurovirology, 20(5), 496–504. https://doi.org/10.1007/s13365-014-0275-1
Frasco, M. A., Mack, W. J., Van Den Berg, D., Aouizerat, B. E., Anastos, K., Cohen, M., De Hovitz, J., Golub, E. T., Greenblatt, R. M., Liu, C., Conti, D. V., & Pearce, C. L. (2012). Underlying genetic structure impacts the association between CYP2B6 polymorphisms and response to efavirenz and nevirapine. AIDS (london, England), 26(16), 2097–2106. https://doi.org/10.1097/qad.0b013e3283593602
Freedman, D., & Manly, J. (2015). Use of normative data and measures of performance validity and symptom validity in assessment of cognitive function.
Gannon, P., Khan, M. Z., & Kolson, D. L. (2011). Current understanding of HIV-associated neurocognitive disorders pathogenesis. Current Opinion in Neurology, 24(3), 275–283. https://doi.org/10.1097/WCO.0b013e32834695fb
Gao, C., Meng, J., Xiao, X., Wang, M., Williams, A. B., & Wang, H. (2020). Antiretroviral therapy improves neurocognitive impairment in people living with HIV? A meta-analysis. International Journal of Nursing Sciences, 7(2), 238–247. https://doi.org/10.1016/j.ijnss.2020.03.007
Gascon, M. R. P., Vidal, J. E., Mazzaro, Y. M., Smid, J., Marcusso, R. M. N., Capitao, C. G., Coutinho, E. M., Benute, G. R. G., De Lucia, M. C. S., & de Oliveira, A. C. P. (2018). Neuropsychological Assessment of 412 HIV-Infected Individuals in Sao Paulo, Brazil. AIDS Patient Care and STDs, 32(1), 1–8. https://doi.org/10.1089/apc.2017.0202
Ghate, M., Mehendale, S., Meyer, R., Umlauf, A., Deutsch, R., Kamat, R., Thakar, M., Risbud, A., Kulkarni, S., Sakamoto, M., Alexander, T., Franklin, D., Letendre, S., Heaton, R., Grant, I., & Marcotte, T. D. (2015). The effects of antiretroviral treatment initiation on cognition in HIV-infected individuals with advanced disease in Pune, India. Journal of Neurovirology, 21(4), 391–398. https://doi.org/10.1007/s13365-015-0329-z
Gisslen, M., Price, R. W., & Nilsson, S. (2011). The definition of HIV-associated neurocognitive disorders: Are we overestimating the real prevalence? BMC Infectious Diseases, 11, 356. https://doi.org/10.1186/1471-2334-11-356
Goldberg, T. E., Harvey, P. D., Wesnes, K. A., Snyder, P. J., & Schneider, L. S. (2015). Practice effects due to serial cognitive assessment: Implications for preclinical Alzheimer’s disease randomized controlled trials. Alzheimer’s & Dementia (amsterdam, Netherlands), 1(1), 103–111. https://doi.org/10.1016/j.dadm.2014.11.003
Habib, A. G., Yakasai, A. M., Owolabi, L. F., Ibrahim, A., Habib, Z. G., Gudaji, M., Karaye, K. M., Ibrahim, D. A., & Nashabaru, I. (2013). Neurocognitive impairment in HIV-1-infected adults in Sub-Saharan Africa: A systematic review and meta-analysis. International Journal of Infectious Diseases : IJID : Official Publication of the International Society for Infectious Diseases, 17(10), e820–e831. https://doi.org/10.1016/j.ijid.2013.06.011
Hamers, R., Rinke de Wit, T., & Holmes, C. (2018). HIV drug resistance in low-income and middle-income countries. The Lancet HIV, 5. https://doi.org/10.1016/S2352-3018(18)30173-5
Harrer, M., Cujipers, P., Furukawa, T., & Ebert, D. (2019). Doing Meta-Analysis in R: A Hands-on Guide.
Harris, M., Macinko, J., Jimenez, G., & Mullachery, P. (2017). Measuring the bias against low-income country research: An Implicit Association Test. Globalization and Health, 13(1), 80. https://doi.org/10.1186/s12992-017-0304-y
Harris, T. G., Rabkin, M., & El-Sadr, W. M. (2018). Achieving the fourth 90: Healthy aging for people living with HIV. AIDS (london, England), 32(12), 1563–1569. https://doi.org/10.1097/QAD.0000000000001870
Hartung, J., & Knapp, G. (2001). A refined method for the meta-analysis of controlled clinical trials with binary outcome. Statistics in Medicine, 20(24), 3875–3889. https://doi.org/10.1002/sim.1009
Hasselblad, V., & Hedges, L. V. (1995). Meta-analysis of screening and diagnostic tests. Psychological Bulletin, 117(1), 167–178. https://doi.org/10.1037/0033-2909.117.1.167
Heaton, R., Franklin, D. R., Ellis, R. J., McCutchan, J. A., Letendre, S. L., LeBlanc, S., Corkran, S. H., Duarte, N. A., Clifford, D. B., Woods, S. P., Collier, A. C., Marra, C. M., Morgello, S., Rivera Mindt, M., Taylor, M. J., Marcotte, T. D., Atkinson, J. H., Wolfson, T., Gelman, B. B., & Grant, I. (2011). HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: Differences in rates, nature, and predictors. Journal of NeuroVirology, 17(1), 3–16. https://doi.org/10.1007/s13365-010-0006-1
Heaton, R., Grant, I., Butters, N., White, D. A., Kirson, D., Atkinson, J. H., McCutchan, J. A., Taylor, M. J., Kelly, M. D., & Ellis, R. J. (1995). The HNRC 500--neuropsychology of HIV infection at different disease stages. HIV Neurobehavioral Research Center. Journal of the International Neuropsychological Society : JINS, 1(3), 231–251. https://doi.org/10.1017/s1355617700000230
Hedges, L. V, & Olkin, I. (1985). Statistical Methods for Meta-Analysis (L. V Hedges (ed.)). Academic Press .
Higgins, J. P. T., & Thompson, S. G. (2002). Quantifying heterogeneity in a meta-analysis. Statistics in Medicine, 21(11), 1539–1558. https://doi.org/10.1002/sim.1186
Higgins, J. P. T., & Thompson, S. G. (2004). Controlling the risk of spurious findings from meta-regression. Statistics in Medicine, 23(11), 1663–1682. https://doi.org/10.1002/sim.1752
Higgins, J. P. T., Thompson, S. G., Deeks, J. J., & Altman, D. G. (2003). Measuring inconsistency in meta-analyses. BMJ, 327(7414), 557 LP – 560. https://doi.org/10.1136/bmj.327.7414.557
Hozo, S. P., Djulbegovic, B., & Hozo, I. (2005). Estimating the mean and variance from the median, range, and the size of a sample. BMC Medical Research Methodology, 5(1), 13. https://doi.org/10.1186/1471-2288-5-13
IntHout, J., Ioannidis, J. P. A., & Borm, G. F. (2014). The Hartung-Knapp-Sidik-Jonkman method for random effects meta-analysis is straightforward and considerably outperforms the standard DerSimonian-Laird method. BMC Medical Research Methodology, 14(1), 25. https://doi.org/10.1186/1471-2288-14-25
IntHout, J., Ioannidis, J. P. A., Rovers, M. M., & Goeman, J. J. (2016). Plea for routinely presenting prediction intervals in meta-analysis. British Medical Journal Open, 6(7), e010247. https://doi.org/10.1136/bmjopen-2015-010247
Jackson, D., & Turner, R. (2017). Power analysis for random-effects meta-analysis. Research Synthesis Methods, 8(3), 290–302. https://doi.org/10.1002/jrsm.1240
Joanna Briggs Institute. (2020). Critical appraisal tools. https://joannabriggs.org/critical-appraisal-tools
Joska, J. A., Witten, J., Thomas, K. G., Robertson, C., Casson-Crook, M., Roosa, H., et al. (2016). A comparison of five brief screening tools for HIV-associated neurocognitive disorders in the USA and South Africa. AIDS and Behavior, 20(8), 1621–1631. https://doi.org/10.1007/s10461-016-1316-y.
Joska, J., Westgarth-Taylor, J., Hoare, J., Thomas, K., Paul, R., Myer, L., & Stein, D. (2012). Neuropsychological outcomes in adults commencing highly active anti-retroviral treatment in South Africa: A prospective study. BMC Infectious Diseases, 12(1), 39. https://doi.org/10.1186/1471-2334-12-39
Jumare, J., El-Kamary, S. S., Magder, L., Hungerford, L., Ndembi, N., Aliyu, A., Dakum, P., Umlauf, A., Cherner, M., Abimiku, A., Charurat, M., Blattner, W. A., & Royal, W., 3rd. (2018). Plasma HIV RNA level is associated with neurocognitive function among HIV-1-infected patients in Nigeria. Journal of Neurovirology, 24(6), 712–719. https://doi.org/10.1007/s13365-018-0667-8
Kambugu, A., Thompson, J., Hakim, J., Tumukunde, D., van Oosterhout, J. J., Mwebaze, R., Hoppe, A., Abach, J., Kwobah, C., Arenas-Pinto, A., Walker, S. A., & Paton, N. I. (2016). Neurocognitive Function at the First-Line Failure and on the Second-Line Antiretroviral Therapy in Africa: Analyses From the EARNEST Trial. Journal of Acquired Immune Deficiency Syndromes (1999), 71(5), 506–513. https://doi.org/10.1097/QAI.0000000000000898
Kanmogne, G. D., Fonsah, J. Y., Tang, B., Doh, R. F., Kengne, A. M., Umlauf, A., Tagny, C. T., Nchindap, E., Kenmogne, L., Franklin, D., Njamnshi, D. M., Mbanya, D., Njamnshi, A. K., & Heaton, R. (2018). Effects of HIV on executive function and verbal fluency in Cameroon. Scientific Reports, 8(1), 17794. https://doi.org/10.1038/s41598-018-36193-7
Kanmogne, G. D., Fonsah, J. Y., Umlauf, A., Moul, J., Doh, R. F., Kengne, A. M., Tang, B., Tagny, C. T., Nchindap, E., Kenmogne, L., Franklin, D., Njamnshi, D. M., Kuate, C. T., Mbanya, D., Njamnshi, A. K., & Heaton, R. (2020a). Effects of HIV infection, antiretroviral therapy, and immune status on the speed of information processing and complex motor functions in adult Cameroonians. Scientific Reports, 10(1), 14016. https://doi.org/10.1038/s41598-020-70981-4
Kanmogne, G. D., Fonsah, J. Y., Umlauf, A., Moul, J., Doh, R. F., Kengne, A. M., et al. (2020b). Attention/working memory, learning and memory in adult cameroonians: Normative Data, effects of HIV infection and viral genotype. Journal of the International Neuropsychological Society : JINS, 26(6), 607–623. https://doi.org/10.1017/S1355617720000120.
Kelly, C. M., van Oosterhout, J. J., Ngwalo, C., Stewart, R. C., Benjamin, L., Robertson, K. R., et al. (2014). HIV associated neurocognitive disorders (HAND) in Malawian adults and effect on adherence to combination anti-retroviral therapy: A cross sectional study. PLoS One, 9(6), e98962.
Kore, I., Ananworanich, J., Valcour, V., Fletcher, J. L. K., Chalermchai, T., Paul, R., Reynolds, J., Tipsuk, S., Ubolyam, S., Rattanamanee, S., Jagodzinski, L., Kim, J., Spudich, S., & Group, R. 010 S. (2015). Neuropsychological impairment in acute HIV and the effect of immediate antiretroviral therapy. Journal of Acquired Immune Deficiency Syndromes (1999), 70(4), 393–399. https://doi.org/10.1097/QAI.0000000000000746
Lawler, K., Jeremiah, K., Mosepele, M., Ratcliffe, S. J., Cherry, C., Seloilwe, E., & Steenhoff, A. P. (2011). Neurobehavioral effects in HIV-positive individuals receiving highly active antiretroviral therapy (HAART) in Gaborone, Botswana. PLoS One, 6(2), e17233–e17233. https://doi.org/10.1371/journal.pone.0017233.
Lerner, A. M., Eisinger, R. W., & Fauci, A. S. (2019). Comorbidities in Persons With HIV: The Lingering Challenge. JAMA. https://doi.org/10.1001/jama.2019.19775
Letendre, S., Marquie-Beck, J., Capparelli, E., Best, B., Clifford, D., Collier, A. C., Gelman, B. B., McArthur, J. C., McCutchan, J. A., Morgello, S., Simpson, D., Grant, I., & Ellis, R. J. (2008). Validation of the CNS Penetration-Effectiveness rank for quantifying antiretroviral penetration into the central nervous system. Archives of Neurology, 65(1), 65–70. https://doi.org/10.1001/archneurol.2007.31
Lezak, M. D., Howieson, D. B., Loring, D. W., Hannay, H. J., & Fischer, J. S. (2004). Neuropsychological assessment, 4th ed. In Neuropsychological assessment, 4th ed. Oxford University Press.
Lipsey, M. W., & Wilson, D. B. (2001). Practical meta-analysis. Sage Publications Inc.
Lopardo, G. D., Bissio, E., Iannella, M. del C., Crespo, A. D., Garone, D. B., & Cassetti, L. I. (2009). Good neurocognitive performance measured by the international HIV dementia scale in early HIV-1 infection. Journal of Acquired Immune Deficiency Syndromes (1999), 52(4), 488–492. https://doi.org/10.1097/QAI.0b013e3181b06348
Ma, Q., Vaida, F., Wong, J., Sanders, C. A., Kao, Y., Croteau, D., Clifford, D. B., Collier, A. C., Gelman, B. B., Marra, C. M., McArthur, J. C., Morgello, S., Simpson, D. M., Heaton, R., Grant, I., Letendre, S. L., & Group C. (2016a). Long-term efavirenz use is associated with worse neurocognitive functioning in HIV-infected patients. Journal of Neurovirology, 22(2), 170–178. https://doi.org/10.1007/s13365-015-0382-7
Ma, Q., Vaida, F., Wong, J., Sanders, C. A., Kao, Y. T., Croteau, D., Clifford, D. B., Collier, A. C., Gelman, B. B., Marra, C. M., McArthur, J. C., Morgello, S., Simpson, D. M., Heaton, R. K., Grant, I., & Letendre, S. L. (2016b). Long-term efavirenz use is associated with worse neurocognitive functioning in HIV-infected patients. Journal of NeuroVirology, 22(2), 170–178. https://doi.org/10.1007/s13365-015-0382-7
Malagurski, B., Bugarski Ignjatović, V., Marić, D., Nikolašević, Ž, Mihić, L., & Brkić, S. (2018). Neurocognitive profile of HIV-positive adults on combined antiretroviral therapy: A single-centre study in Serbia. Applied Neuropsychology: Adult, 25(6), 513–522. https://doi.org/10.1080/23279095.2017.1336711
Manly, J. J. (2005). Advantages and Disadvantages of Separate Norms for African Americans. The Clinical Neuropsychologist, 19(2), 270–275. https://doi.org/10.1080/13854040590945346
Marcus, J. L., Leyden, W. A., Alexeeff, S. E., Anderson, A. N., Hechter, R. C., Hu, H., et al. (2020). Comparison of overall and comorbidity-free life expectancy between insured adults with and without HIV infection, 2000-2016. JAMA Network Open, 3(6), e207954–e207954. https://doi.org/10.1001/jamanetworkopen.2020.7954.
Michael, H. U., Naidoo, S., Mensah, K. B., Ramlall, S., & Oosthuizen, F. (2020). The Impact of Antiretroviral Therapy on Neurocognitive Outcomes Among People Living with HIV in Low- and Middle-Income Countries (LMICs): A Systematic Review. AIDS and Behavior. https://doi.org/10.1007/s10461-020-03008-8
Milanini, B., Allen, I., Paul, R., Bahemana, E., Kiweewa, F., Nambuya, A., Maswai, J., Langat, R., Owuoth, J., Martin, S., Possin, K., Esber, A., Polyak, C., Ake, J. A., & Valcour, V. (2020). Frequency and Predictors of HIV-Related Cognitive Impairment in East Africa: The Africa Cohort Study (AFRICOS). Journal of Acquired Immune Deficiency Syndromes (1999), 83(2), 157–164. https://doi.org/10.1097/QAI.0000000000002242
Mills, E. J., Bakanda, C., Birungi, J., Chan, K., Ford, N., Cooper, C. L., Nachega, J. B., Dybul, M., & Hogg, R. S. (2011). Life expectancy of persons receiving combination antiretroviral therapy in low-income countries: A cohort analysis from Uganda. Annals of Internal Medicine, 155(4), 209–216. https://doi.org/10.7326/0003-4819-155-4-201108160-00358
Mohamed, A. A., Oduor, C., & Kinyanjui, D. (2020). HIV-associated neurocognitive disorders at Moi teaching and referral hospital, Eldoret, Kenya. BMC Neurology, 20(1), 280. https://doi.org/10.1186/s12883-020-01857-3
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & Group T. P. (2009). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLOS Medicine, 6(7), e1000097. https://doi.org/10.1371/journal.pmed.1000097.
Mora-Peris, B., Stevens, E., Ferretti, F., Underwood, J., Taylor, S., & Winston, A. (2016). Evolution of changes in cognitive function after the initiation of antiretroviral therapy. AIDS Research and Therapy, 13(1), 20. https://doi.org/10.1186/s12981-016-0104-0
Mpye, K. L., Matimba, A., Dzobo, K., Chirikure, S., Wonkam, A., & Dandara, C. (2017). Disease burden and the role of pharmacogenomics in African populations. Global Health, Epidemiology and Genomics, 2, e1–e1. https://doi.org/10.1017/gheg.2016.21
Mugendi, A. G., Kubo, M. N., Nyamu, D. G., Mwaniki, L. M., Wahome, S. K., & Haberer, J. E. (2019). Prevalence and correlates of neurocognitive disorders among HIV patients on antiretroviral therapy at a Kenyan hospital. Neurology Research International, 2019, 5173289. https://doi.org/10.1155/2019/5173289.
Naicker, P., & Sayed, Y. (2014). Non-B HIV-1 subtypes in sub-Saharan Africa: Impact of subtype on protease inhibitor efficacy. Biological Chemistry, 395(10), 1151–1161. https://doi.org/10.1515/hsz-2014-0162
Nakku, J., Kinyanda, E., & Hoskins, S. (2013). Prevalence and factors associated with probable HIV dementia in an African population: A cross-sectional study of an HIV/AIDS clinic population. BMC Psychiatry, 13(1), 126. https://doi.org/10.1186/1471-244X-13-126
Namagga, J. K., Rukundo, G. Z., & Voss, J. G. (2019). Prevalence and risk factors of HIV-associated neurocognitive disorders in rural Southwestern Uganda. The Journal of the Association of Nurses in AIDS Care : JANAC, 30(5), 531–538. https://doi.org/10.1097/JNC.0000000000000036.
Ndashimye, E., & Arts, E. J. (2019). The urgent need for more potent antiretroviral therapy in low-income countries to achieve UNAIDS 90–90-90 and complete eradication of AIDS by 2030. Infectious Diseases of Poverty, 8(1), 63. https://doi.org/10.1186/s40249-019-0573-1
Nightingale, S., Joska, J., Winston, A., Gisslen, M., & Barber, T. (2020). Reader response: Global prevalence and burden of HIV-associated neurocognitive disorder: a meta-analysis. Neurology. https://n.neurology.org/content/reader-response-global-prevalence-and-burden-hiv-associated-neurocognitive-disorder-meta
Njamnshi, A. K., Bissek, A.C.Z.-K., Ongolo-Zogo, P., Tabah, E. N., Lekoubou, A. Z., Yepnjio, F. N., Fonsah, J. Y., Kuate, C. T., Angwafor, S. A., Dema, F., Njamnshi, D. M., Kouanfack, C., de Djientcheu, V. P., Muna, W. F. T., & Kanmogne, G. D. (2009). Risk factors for HIV-associated neurocognitive disorders (HAND) in sub-Saharan Africa: the case of Yaoundé-Cameroon. Journal of the Neurological Sciences, 285(1–2), 149–153. https://doi.org/10.1016/j.jns.2009.06.043
Novakovic, M., Turkulov, V., Maric, D., Kozic, D., Rajkovic, U., Bjelan, M., Lucic, M., & Brkic, S. (2015). Prediction of brain atrophy using three drug scores in neuroasymptomatic HIV-infected patients with controlled viremia . In Brazilian Journal of Infectious Diseases (Vol. 19, pp. 503–509). scielo .
Ntshangase, S., Mdanda, S., Singh, S. D., Naicker, T., Kruger, H. G., Baijnath, S., & Govender, T. (2019). Mass Spectrometry Imaging Demonstrates the Regional Brain Distribution Patterns of Three First-Line Antiretroviral Drugs. ACS Omega, 4(25), 21169–21177. https://doi.org/10.1021/acsomega.9b02582
Nyamayaro, P., Gouse, H., Hakim, J., Robbins, R. N., & Chibanda, D. (2020). Neurocognitive impairment in treatment-experienced adults living with HIV attending primary care clinics in Zimbabwe. BMC Infectious Diseases, 20(1), 383. https://doi.org/10.1186/s12879-020-05090-8
Nyundo, A., Ndetei, D., Othieno, C., & Mathai, A. (2016). Neurocognitive correlates of the use of combined Antiretroviral Therapy among HIV-infected adults attending care and treatment center at Muhimbili National Hospital, Dar es Salaam, Tanzania: An analytical crosssectional study. Tanzania Medical Journal, 27, 114–132. https://doi.org/10.4314/tmj.v27i1.201
Obiabo, Y. O., Ogunrin, O. A., & Ogun, A. S. (2012). Effects of highly active antiretroviral therapy on cognitive functions in severely immune-compromised HIV-seropositive patients. Journal of the Neurological Sciences, 313(1–2), 115–122. https://doi.org/10.1016/j.jns.2011.09.011
Orwin, R. G. (1983). A Fail-Safe N for Effect Size in Meta-Analysis. Journal of Educational Statistics, 8(2), 157–159. https://doi.org/10.2307/1164923
Patel, V. N., Mungwira, R. G., Tarumbiswa, T. F., Heikinheimo, T., & van Oosterhout, J. J. (2010). High prevalence of suspected HIV-associated dementia in adult Malawian HIV patients. International Journal of STD & AIDS, 21(5), 356–358. https://doi.org/10.1258/ijsa.2010.009554
Peters, J. L., Sutton, A. J., Jones, D. R., Abrams, K. R., & Rushton, L. (2007). Performance of the trim and fill method in the presence of publication bias and between-study heterogeneity. Statistics in Medicine, 26(25), 4544–4562. https://doi.org/10.1002/sim.2889
Porritt, K., Gomersall, J., & Lockwood, C. (2014). JBI’s Systematic Reviews: Study selection and critical appraisal. The American Journal of Nursing, 114(6), 47–52. https://doi.org/10.1097/01.NAJ.0000450430.97383.64
Pumpradit, W., Ananworanich, J., Lolak, S., Shikuma, C., Paul, R., Siangphoe, U., Chaoniti, N., Kaew-On, P., Paris, R., Ruxrungtham, K., & Valcour, V. (2010). Neurocognitive impairment and psychiatric comorbidity in well-controlled human immunodeficiency virus-infected Thais from the 2NN Cohort Study. Journal of Neurovirology, 16(1), 76–82. https://doi.org/10.3109/13550280903493914
Qin, P., He, J., Wang, Z., Chen, X., Li, J., Fung, A. W. T., Jiang, H., Chen, J., Wong, A., & Lau, J. T. F. (2020). Efavirenz use and neurocognitive performance among older people living with HIV who were on antiretroviral therapy. AIDS Care, 32(1), 12–20. https://doi.org/10.1080/09540121.2019.1622645
R Core Team. (2020). R: A language and environment for statistical computing (R version 4.0.3 (2020–10–10)-- "Bunny-Wunnies Freak Out"). R Foundation for Statistical Computing. https://www.r-project.org/
Reger, M., Welsh, R., Razani, J., Martin, D. J., & Boone, K. B. (2002). A meta-analysis of the neuropsychological sequelae of HIV infection. Journal of the International Neuropsychological Society : JINS, 8(3), 410–424. https://doi.org/10.1017/s1355617702813212
Ribaudo, H. J., Smith, K. Y., Robbins, G. K., Flexner, C., Haubrich, R., Chen, Y., Fischl, M. A., Schackman, B. R., Riddler, S. A., & Gulick, R. M. (2013). Racial differences in response to antiretroviral therapy for HIV infection: An AIDS clinical trials group (ACTG) study analysis. Clinical Infectious Diseases : An Official Publication of the Infectious Diseases Society of America, 57(11), 1607–1617. https://doi.org/10.1093/cid/cit595
Richardson, W. S., Wilson, M. C., Nishikawa, J., & Hayward, R. S. A. (1995). The well-built clinical question: A key to evidence-based decisions. ACP Journal Club, 123(3), A12. https://doi.org/10.7326/ACPJC-1995-123-3-A12
Robertson, K., Kumwenda, J., Supparatpinyo, K., Jiang, J. H., Evans, S., Campbell, T. B., Price, R. W., Murphy, R., Hall, C., Marra, C. M., Marcus, C., Berzins, B., Masih, R., Santos, B., Silva, M. T., Kumarasamy, N., Walawander, A., Nair, A., Tripathy, S., & Brouwers, P. (2011). A multinational study of neurological performance in antiretroviral therapy-naive HIV-1-infected persons in diverse resource-constrained settings. Journal of Neurovirology, 17(5), 438–447. https://doi.org/10.1007/s13365-011-0044-3
Robertson, K., Liner, J., Hakim, J., Sankalé, J.-L., Grant, I., Letendre, S., Clifford, D., Diop, A. G., Jaye, A., Kanmogne, G., Njamnshi, A., Langford, T. D., Weyessa, T. G., Wood, C., Banda, M., Hosseinipour, M., Sacktor, N., Nakasuja, N., Bangirana, P., … in A. C. (2010). NeuroAIDS in Africa. Journal of Neurovirology, 16(3), 189–202. https://doi.org/10.3109/13550284.2010.489597
Robertson, K., Liner, J., & Heaton, R. (2009). Neuropsychological assessment of HIV-infected populations in international settings. Neuropsychology Review, 19(2), 232–249. https://doi.org/10.1007/s11065-009-9096-z
Robertson, K., Liner, J., & Meeker, R. B. (2012). Antiretroviral neurotoxicity. Journal of Neurovirology, 18(5), 388–399. https://doi.org/10.1007/s13365-012-0120-3
Robertson, K. R., Jiang, H., Kumwenda, J., Supparatpinyo, K., Marra, C. M., Berzins, B., et al. (2019). Human immunodeficiency virus-associated neurocognitive impairment in diverse resource-limited settings. Clinical Infectious Diseases : An Official Publication of the Infectious Diseases Society of America, 68(10), 1733–1738. https://doi.org/10.1093/cid/ciy767.
Rodrigues, R. A., Oliveira, R. L., Grinsztejn, B., & Silva, M. T. T. (2013). Validity of the International HIV Dementia Scale in Brazil. In Arquivos de Neuro-Psiquiatria (Vol. 71, pp. 376–379). scielo .
Rosenthal, R. (1991). Meta-analytic procedures for social research, Rev. ed. In Meta-analytic procedures for social research, Rev. ed. Sage Publications, Inc. https://doi.org/10.4135/9781412984997
Rossouw, T., Tucker, J. D., van Zyl, G. U., Sikwesi, K., & Godfrey, C. (2017). Barriers to HIV remission research in low- and middle-income countries. Journal of the International AIDS Society, 20(1), 21521. https://doi.org/10.7448/IAS.20.1.21521
Rotger, M., Csajka, C., & Telenti, A. (2006). Genetic, ethnic, and gender differences in the pharmacokinetics of antiretroviral agents. Current HIV/AIDS Reports, 3(3), 118–125. https://doi.org/10.1007/BF02696655
Rücker, G., Schwarzer, G., Carpenter, J. R., Binder, H., & Schumacher, M. (2011). Treatment-effect estimates adjusted for small-study effects via a limit meta-analysis. Biostatistics (oxford, England), 12(1), 122–142. https://doi.org/10.1093/biostatistics/kxq046
Sackett, D. L. (1997). Evidence-based medicine. Seminars in Perinatology, 21(1), 3–5. https://doi.org/10.1016/S0146-0005(97)80013-4
Sacktor, N., Nakasujja, N., Skolasky, R. L., Robertson, K., Musisi, S., Ronald, A., Katabira, E., & Clifford, D. B. (2009). Benefits and risks of stavudine therapy for HIV-associated neurologic complications in Uganda. Neurology, 72(2), 165–170. https://doi.org/10.1212/01.wnl.0000339042.96109.86
Sacktor, N., Nakasujja, N., Skolasky, R., Robertson, K., Wong, M., Musisi, S., Ronald, A., & Katabira, E. (2006). Antiretroviral therapy improves cognitive impairment in HIV+ individuals in sub-Saharan Africa. Neurology, 67(2), 311–314. https://doi.org/10.1212/01.wnl.0000225183.74521.72
Sacktor, N., Nakasujja, N., Okonkwo, O., Skolasky, R. L., Robertson, K., Musisi, S., & Katabira, E. (2013). Longitudinal neuropsychological test performance among HIV seropositive individuals in Uganda. Journal of Neurovirology, 19(1), 48–56. https://doi.org/10.1007/s13365-012-0139-5
Sacktor, Ned, Saylor, D., Nakigozi, G., Nakasujja, N., Robertson, K., Grabowski, M. K., Kisakye, A., Batte, J., Mayanja, R., Anok, A., Gray, R. H., & Wawer, M. J. (2019). Effect of HIV Subtype and Antiretroviral Therapy on HIV-Associated Neurocognitive Disorder Stage in Rakai, Uganda. Journal of Acquired Immune Deficiency Syndromes (1999), 81(2), 216–223. https://doi.org/10.1097/QAI.0000000000001992
Salahuddin, M., Manzar, M. D., Hassen, H. Y., Unissa, A., Abdul Hameed, U., Spence, D. W., & Pandi-Perumal, S. R. (2020). Prevalence and Predictors of Neurocognitive Impairment in Ethiopian Population Living with HIV. HIV/AIDS (Auckland, N.Z.), 12, 559–572. https://doi.org/10.2147/HIV.S260831
Sánchez-Meca, J., Marín-Martínez, F., & Chacón-Moscoso, S. (2003). Effect-size indices for dichotomized outcomes in meta-analysis. Psychological Methods, 8(4), 448–467. https://doi.org/10.1037/1082-989X.8.4.448
Scott, J. C., Woods, S. P., Carey, C. L., Weber, E., Bondi, M. W., Grant, I., & Group T. H. I. V. N. R. C. (HNRC). (2011). Neurocognitive Consequences of HIV Infection in Older Adults: An Evaluation of the “Cortical” Hypothesis. AIDS and Behavior, 15(6), 1187–1196. https://doi.org/10.1007/s10461-010-9815-8
Shao, Y., & Williamson, C. (2012). The HIV-1 epidemic: Low- to middle-income countries. Cold Spring Harbor Perspectives in Medicine, 2(3), a007187. https://doi.org/10.1101/cshperspect.a007187
Sidik, K., & Jonkman, J. N. (2006). Robust variance estimation for random effects meta-analysis. Computational Statistics & Data Analysis, 50(12), 3681–3701. https://doi.org/10.1016/j.csda.2005.07.019
Siika, A., McCabe, L., Bwakura-Dangarembizi, M., Kityo, C., Mallewa, J., Berkley, J., Maitland, K., Griffiths, A., Baleeta, K., Mudzingwa, S., Abach, J., Nathoo, K., Thomason, M. J., Prendergast, A. J., Walker, A. S., & Gibb, D. M. (2018). Late Presentation With HIV in Africa: Phenotypes, Risk, and Risk Stratification in the REALITY Trial. Clinical Infectious Diseases, 66(suppl_2), S140–S146. https://doi.org/10.1093/cid/cix1142
Silverberg, M. J., Chao, C., Leyden, W. A., Xu, L., Horberg, M. A., Klein, D., Towner, W. J., Dubrow, R., Quesenberry, C. P., Jr., Neugebauer, R. S., & Abrams, D. I. (2011). HIV infection, immunodeficiency, viral replication, and the risk of cancer. Cancer Epidemiology, Biomarkers & Prevention : A Publication of the American Association for Cancer Research, Cosponsored by the American Society of Preventive Oncology, 20(12), 2551–2559. https://doi.org/10.1158/1055-9965.EPI-11-0777
Simonsohn, U., Nelson, L. D., & Simmons, J. P. (2014). P-curve: A key to the file-drawer. Journal of Experimental Psychology. General, 143(2), 534–547. https://doi.org/10.1037/a0033242
Simonsohn, U., Simmons, J. P., & Nelson, L. D. (2015). Better P-curves: Making P-curve analysis more robust to errors, fraud, and ambitious P-hacking, a Reply to Ulrich and Miller (2015). Journal of Experimental Psychology. General, 144(6), 1146–1152. https://doi.org/10.1037/xge0000104
Singh, D. (2006). Publication bias - A reason for the decreased research output in developing countries. African Journal of Psychiatry, 9. https://doi.org/10.4314/ajpsy.v9i3.30216
Singh, D., Joska, J. A., Goodkin, K., Lopez, E., Myer, L., Paul, R. H., John, S., & Sunpath, H. (2010). Normative scores for a brief neuropsychological battery for the detection of HIV-associated neurocognitive disorder (HAND) among South Africans. BMC Research Notes, 3(1), 28. https://doi.org/10.1186/1756-0500-3-28
Spies, G., Denckla, C. A., Mall, S., Levin, J., Seedat, S., Nakasujja, N., & Kinyanda, E. (2019). The relationship between cognitive change and physical health and behavioural outcomes in a Ugandan cohort of adults living with HIV - a longitudinal study. AIDS Care, 31(7), 803–808. https://doi.org/10.1080/09540121.2018.1545987
Stanley, T. D. (2017). Limitations of PET-PEESE and Other Meta-Analysis Methods. Social Psychological and Personality Science, 8(5), 581–591. https://doi.org/10.1177/1948550617693062
Strauss, E., Sherman, E. M. S., & Spreen, O. (2006). A compendium of neuropsychological tests: Administration, norms, and commentary, 3rd ed. In A compendium of neuropsychological tests: Administration, norms, and commentary, 3rd ed. Oxford University Press.
Symonds, M., & Moussalli, A. (2011). A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behavioral Ecology and Sociobiology, 65, 13–21. https://doi.org/10.1007/s00265-010-1037-6
Temereanca, A., Ene, L., Rosca, A., Diaconu, C. C., Luca, A., Burlacu, R., et al. (2019). Neurocognitive impairment in the combined antiretroviral therapy era in a Romanian cohort of young adults with chronic HIV infection. AIDS Research and Human Retroviruses, 36(5), 367–372. https://doi.org/10.1089/aid.2019.0132.
The World Bank. (2019). Low & middle income. Data. https://data.worldbank.org/income-level/low-and-middle-income
Torti, C., Focà, E., Cesana, B. M., & Lescure, F. X. (2011). Asymptomatic neurocognitive disorders in patients infected by HIV: Fact or fiction? BMC Medicine, 9(1), 138. https://doi.org/10.1186/1741-7015-9-138
Tsegaw, M., Andargie, G., Alem, G., & Tareke, M. (2017). Screening HIV-associated neurocognitive disorders (HAND) among HIV positive patients attending antiretroviral therapy in South Wollo, Ethiopia. Journal of Psychiatric Research, 85, 37–41. https://doi.org/10.1016/j.jpsychires.2016.10.016
Tufanaru, C., Munn, Z., Aromatari, E., Campbell, J., & Hopp, L. (2020). Systematic reviews of effectiveness. In E. Aromataris & Z. Munn (Eds.), JBI Manual for Evidence Synthesis. JBI.
UNAIDS. (2014). People aged 50 years and older. The Gap Report 2014. https://www.unaids.org/sites/default/files/media_asset/12_Peopleaged50yearsandolder.pdf
UNAIDS. (2020). UNAIDS DATA 2020.
Valcour, V. G, Shiramizu, B. T., Sithinamsuwan, P., Nidhinandana, S., Ratto-Kim, S., Ananworanich, J., Siangphoe, U., Kim, J. H., de Souza, M., Degruttola, V., Paul, R. H., Shikuma, C. M., & team, S. A. R. C. with the U. of H. 001 protocol. (2009). HIV DNA and cognition in a Thai longitudinal HAART initiation cohort: the SEARCH 001 Cohort Study. Neurology, 72(11), 992–998. https://doi.org/10.1212/01.wnl.0000344404.12759.83
Valcour, V. G. (2013). HIV, aging, and cognition: emerging issues. Topics in Antiviral Medicine, 21(3), 119–123. https://pubmed.ncbi.nlm.nih.gov/23981600
Venturi, G., Catucci, M., Romano, L., Corsi, P., Leoncini, F., Valensin, P. E., & Zazzi, M. (2000). Antiretroviral resistance mutations in human immunodeficiency virus type 1 reverse transcriptase and protease from paired cerebrospinal fluid and plasma samples. The Journal of Infectious Diseases, 181(2), 740–745. https://doi.org/10.1086/315249.
Viechtbauer, W. (2020). Metafor: Meta-analysis package for R (Version 2.4–0) [Software]. https://cran.r-project.org/web/packages/metafor/metafor.pdf
Viechtbauer, W., & Cheung, M.W.-L. (2010). Outlier and influence diagnostics for meta-analysis. Research Synthesis Methods, 1(2), 112–125. https://doi.org/10.1002/jrsm.11
Walker, K. A., & Brown, G. G. (2018). HIV-associated executive dysfunction in the era of modern antiretroviral therapy: A systematic review and meta-analysis. Journal of Clinical and Experimental Neuropsychology, 40(4), 357–376. https://doi.org/10.1080/13803395.2017.1349879
Wang, Y., Liu, M., Lu, Q., Farrell, M., Lappin, J. M., Shi, J., Lu, L., & Bao, Y. (2020). Global prevalence and burden of HIV-associated neurocognitive disorder: A meta-analysis. Neurology. https://doi.org/10.1212/WNL.0000000000010752
Wang, Z., Zheng, Y., Liu, L., Shen, Y., Zhang, R., Wang, J., & Lu, H. (2013). High prevalence of HIV-associated neurocognitive disorder in HIV-infected patients with a baseline CD4 count ≤ 350 cells/μL in Shanghai, China. Bioscience Trends, 7(6), 284–289.
Warren, M. (2018). First analysis of ‘pre-registered’ studies shows sharp rise in null findings. Nature. https://doi.org/10.1038/d41586-018-07118-1
Wei, J., Hou, J., Su, B., Jiang, T., Guo, C., Wang, W., Zhang, Y., Chang, B., Wu, H., & Zhang, T. (2020). The Prevalence of Frascati-Criteria-Based HIV-Associated Neurocognitive Disorder (HAND) in HIV-Infected Adults: A Systematic Review and Meta-Analysis. Frontiers in Neurology, 11, 581346. https://doi.org/10.3389/fneur.2020.581346
Wilson, D. (n.d.). Practical Meta-Analysis Effect Size Calculator [Online calculator]. Retrieved August 10, 2020, from https://campbellcollaboration.org/research-resources/effect-size-calculator.html
Wing, E. J. (2016). HIV and aging. International Journal of Infectious Diseases, 53, 61–68. https://doi.org/10.1016/j.ijid.2016.10.004
Wong, M. H., Robertson, K., Nakasujja, N., Skolasky, R., Musisi, S., Katabira, E., McArthur, J. C., Ronald, A., & Sacktor, N. (2007). Frequency of and risk factors for HIV dementia in an HIV clinic in sub-Saharan Africa. Neurology, 68(5), 350–355. https://doi.org/10.1212/01.wnl.0000252811.48891.6d
Wood, J. A. (2007). Methodology for dealing with duplicate study effects in a meta-analysis. Organizational Research Methods, 11(1), 79–95. https://doi.org/10.1177/1094428106296638.
Woods, S. P., Moore, D. J., Weber, E., & Grant, I. (2009). Cognitive neuropsychology of HIV-associated neurocognitive disorders. Neuropsychology Review, 19(2), 152–168. https://doi.org/10.1007/s11065-009-9102-5.
World Health Organization. (2016). Clinical guidelines: antiretroviral therapy. In Consolidated guidelines on the use of antiretroviral drugs for treating and preventing HIV infection Recommendations for a public health approach - Second edition (p. 120).
World Health Organization. (2019). Update of Recommendations on First- and Second-line Antiretroviral regimens. https://apps.who.int/iris/bitstream/handle/10665/325892/WHO-CDS-HIV-19.15-eng.pdf?ua=1
Wright, E. J., Grund, B., Cysique, L. A., Robertson, K. R., Brew, B. J., Collins, G., Shlay, J. C., Winston, A., Read, T. R. H., Price, R. W., & Group I. N. for S. I. in G. H. I. V. T. (INSIGHT) S. S. (2015). Factors associated with neurocognitive test performance at baseline: a substudy of the INSIGHT Strategic Timing of AntiRetroviral Treatment (START) trial. HIV Medicine, 16(S1), 97–108. https://doi.org/10.1111/hiv.12238
Xiao, X., Zeng, H., Feng, C., Tan, H., Wu, L., Zhang, H., Brecht, M.-L., Wang, H., & Koniak-Griffin, D. (2020). Cognitive Impairment Among Aging People Living With HIV on Antiretroviral Therapy: A Cross-Sectional Study in Hunan, China. The Journal of the Association of Nurses in AIDS Care : JANAC, 31(3), 301–311. https://doi.org/10.1097/JNC.0000000000000122
Yuan, L., Qiao, L., Wei, F., Yin, J., Liu, L., Ji, Y., Smith, D., Li, N., & Chen, D. (2013). Cytokines in CSF correlate with HIV-associated neurocognitive disorders in the post-HAART era in China. Journal of Neurovirology, 19(2), 144–149. https://doi.org/10.1007/s13365-013-0150-5
Funding
The authors received no funding to perform this study.
Author information
Authors and Affiliations
Contributions
HM conceived the study. HM and MP designed the study. HM, SCO and EY extracted and analyzed the data. HM drafted the manuscript with critical revisions from MP, EY, SCO, FO, and SR. MP, SR, and FO supervised the study.
Corresponding author
Ethics declarations
Ethics Approval
Not required.
Conflict of Interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Michael, H.U., Youbi, E., Ohadoma, S.C. et al. A Meta-Analytic Review of the Effect of Antiretroviral Therapy on Neurocognitive Outcomes in Adults Living with HIV-1 in Low-and Middle-Income Countries. Neuropsychol Rev 32, 828–854 (2022). https://doi.org/10.1007/s11065-021-09527-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11065-021-09527-y