Association between Antiretroviral Treatment and Markers of Systemic Inflammation among HIV Patients in Ghana

Author(s): Zelalem T. Haile*, Bismark Sarfo, Evelyn Y. Bonney, Eric A. Mensah, Selase Deletsu

Journal Name: Current HIV Research
HIV and Viral Immune Diseases

Volume 18 , Issue 6 , 2020


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Graphical Abstract:


Abstract:

Background: Studies from high-income countries have reported that even after receiving antiretroviral treatment (ART), HIV-infected adults may not achieve normal levels of certain inflammatory markers that are known to be associated with the onset and development of non-communicable diseases.

Objective: The aim of this study is to examine the relationship between ART and markers of systemic inflammation in HIV/AIDS patients at an urban antiretroviral clinic in Ghana.

Methods: We examined serum levels of high sensitivity CRP (hsCRP), interleukin-6 (IL-6), interleukin- 18(IL-18), and tumor necrosis factor-α (sTNFR1 and sTNFR2) from 40 HIV infected patients. Kruskal-Wallis Test was used to examine the differences in markers of systemic inflammation according to the types of ART medication taken. We then utilized generalized additive models (GAM) with non-linear function to examine the association between ART and markers of systemic inflammation after adjusting for potential confounders.

Results: Overall, 30 (75.0%) of the participants received ART and 35 (85%) were female. Kruskal- Wallis Test revealed no significant differences in the markers of systemic inflammation among the three categories of ART (none, AZT, 3TC, EFV/NVP, and TDF, 3TC/FTC, EFV/NVP). In the multivariable- adjusted GAM model, we found a significant but non-linear association between time since diagnosis and CRP levels (p=0.006).

Conclusion: Although the relatively small sample size limits the scope of the study's findings, these results suggest that individuals on ART need to be screened periodically for the development of chronic conditions. This line of investigation has the potential to influence treatment and clinical guidelines that will improve the quality of care for HIV-infected patients.

Keywords: Human Immunodeficiency virus, antiretroviral therapy, systemic inflammation, chronic diseases, CRP, GAM.

[1]
UNICEF. HIV Statistics - Global and Regional Trends https://data.unicef.org/topic/hivaids/global-regional-trends/
[2]
Kharsany ABM, Karim QA. HIV Infection and AIDS in Sub-Saharan Africa: Current Status, Challenges and Opportunities. Open AIDS J 2016; 10: 34-48.
[http://dx.doi.org/10.2174/1874613601610010034] [PMID: 27347270]
[3]
Ghana Statistical Service (GSS), Ghana Health Service (GHS), and ICF International. 2015.https://dhsprogram.com/what-we-do/survey/survey-display-437.cfm
[4]
Ghana AIDS Commission. Ghana National HIV and AIDS Strategic Plan 2016-2020 Accra: GAC 2016.https://ghanaids.gov.gh/mcadmin/Uploads/nationalHIVandAIDSPolicy.pdf
[5]
Bendavid E, Holmes CB, Bhattacharya J, Miller G. HIV development assistance and adult mortality in Africa. JAMA 2012; 307(19): 2060-7.
[http://dx.doi.org/10.1001/jama.2012.2001] [PMID: 22665105]
[6]
Brinkhof MWG, Boulle A, Weigel R, et al. International Epidemiological Databases to Evaluate AIDS (IeDEA). Mortality of HIV-infected patients starting antiretroviral therapy in sub-Saharan Africa: comparison with HIV-unrelated mortality. PLoS Med 2009; 6(4): e1000066.
[http://dx.doi.org/10.1371/journal.pmed.1000066] [PMID: 19399157]
[7]
Pop-Eleches C, Thirumurthy H, Habyarimana JP, et al. Mobile phone technologies improve adherence to antiretroviral treatment in a resource-limited setting: a randomized controlled trial of text message reminders. AIDS 2011; 25(6): 825-34.
[http://dx.doi.org/10.1097/QAD.0b013e32834380c1] [PMID: 21252632]
[8]
Hattab S, Guihot A, Guiguet M, et al. Comparative impact of antiretroviral drugs on markers of inflammation and immune activation during the first two years of effective therapy for HIV-1 infection: an observational study. BMC Infect Dis 2014; 14: 122.
[http://dx.doi.org/10.1186/1471-2334-14-122] [PMID: 24589015]
[9]
Hunt PW. HIV and inflammation: mechanisms and consequences. Curr HIV/AIDS Rep 2012; 9(2): 139-47.
[http://dx.doi.org/10.1007/s11904-012-0118-8] [PMID: 22528766]
[10]
Saeidi A, Zandi K, Cheok YY, et al. T-cell exhaustion in chronic infections: reversing the state of exhaustion and reinvigorating optimal protective immune responses. Front Immunol 2018; 9: 2569.
[http://dx.doi.org/10.3389/fimmu.2018.02569] [PMID: 30473697]
[11]
Neuhaus J, Jacobs DR Jr, Baker JV, et al. Markers of inflammation, coagulation, and renal function are elevated in adults with HIV infection. J Infect Dis 2010; 201(12): 1788-95.
[http://dx.doi.org/10.1086/652749] [PMID: 20446848]
[12]
Wilson EMP, Sereti I. Immune restoration after antiretroviral therapy: the pitfalls of hasty or incomplete repairs. Immunol Rev 2013; 254(1): 343-54.
[http://dx.doi.org/10.1111/imr.12064] [PMID: 23772630]
[13]
Mavigner M, Delobel P, Cazabat M, et al. HIV-1 residual viremia correlates with persistent T-cell activation in poor immunological responders to combination antiretroviral therapy. PLoS One 2009; 4(10): e7658.
[http://dx.doi.org/10.1371/journal.pone.0007658] [PMID: 19876401]
[14]
Boulougoura A, Sereti I. HIV infection and immune activation: the role of coinfections. Curr Opin HIV AIDS 2016; 11(2): 191-200.
[http://dx.doi.org/10.1097/COH.0000000000000241] [PMID: 26720550]
[15]
Chang CC, Crane M, Zhou J, et al. HIV and co-infections. Immunol Rev 2013; 254(1): 114-42.
[http://dx.doi.org/10.1111/imr.12063] [PMID: 23772618]
[16]
Hunt PW, Martin JN, Sinclair E, et al. Valganciclovir reduces T cell activation in HIV-infected individuals with incomplete CD4+ T cell recovery on antiretroviral therapy. J Infect Dis 2011; 203(10): 1474-83.
[http://dx.doi.org/10.1093/infdis/jir060] [PMID: 21502083]
[17]
Paiardini M, Frank I, Pandrea I, Apetrei C, Silvestri G. Mucosal immune dysfunction in AIDS pathogenesis. AIDS Rev 2008; 10(1): 36-46.
[PMID: 18385779]
[18]
Lane HC. Pathogenesis of HIV infection: total CD4+ T-cell pool, immune activation, and inflammation. Top HIV Med 2010; 18(1): 2-6.
[PMID: 20305309]
[19]
Macatangay BJ, Rinaldo CR. Regulatory T cells in HIV immunotherapy. HIV Ther 2010; 4(6): 639-47.
[http://dx.doi.org/10.2217/hiv.10.51] [PMID: 21461400]
[20]
Sokoya T, Steel HC, Nieuwoudt M, Rossouw TM. HIV as a Cause of Immune Activation and Immunosenescence. Mediators Inflamm 2017; 2017: 6825493.
[http://dx.doi.org/10.1155/2017/6825493] [PMID: 29209103]
[21]
Terzieva V. Regulatory T cells and HIV-1 infection. Viral Immunol 2008; 21(3): 285-91.
[http://dx.doi.org/10.1089/vim.2008.0006] [PMID: 18673076]
[22]
Savès M, Raffi F, Capeau J, et al. Antiprotéases Cohorte (APROCO) Study Group. Factors related to lipodystrophy and metabolic alterations in patients with human immunodeficiency virus infection receiving highly active antiretroviral therapy. Clin Infect Dis 2002; 34(10): 1396-405.
[http://dx.doi.org/10.1086/339866] [PMID: 11981737]
[23]
Brown TT, Qaqish RB. Antiretroviral therapy and the prevalence of osteopenia and osteoporosis: a meta-analytic review. AIDS 2006; 20(17): 2165-74.
[http://dx.doi.org/10.1097/QAD.0b013e32801022eb] [PMID: 17086056]
[24]
Lang S, Mary-Krause M, Cotte L, et al. French Hospital Database on HIV-ANRS CO4. Increased risk of myocardial infarction in HIV-infected patients in France, relative to the general population. AIDS 2010; 24(8): 1228-30.
[http://dx.doi.org/10.1097/QAD.0b013e328339192f] [PMID: 20400883]
[25]
Lanoy E, Spano J-P, Bonnet F, et al. ONCOVIH study group. The spectrum of malignancies in HIV-infected patients in 2006 in France: the ONCOVIH study. Int J Cancer 2011; 129(2): 467-75.
[http://dx.doi.org/10.1002/ijc.25903] [PMID: 21207370]
[26]
Worm SW, Lundgren JD. The metabolic syndrome in HIV. Best Pract Res Clin Endocrinol Metab 2011; 25(3): 479-86.
[http://dx.doi.org/10.1016/j.beem.2010.10.018] [PMID: 21663841]
[27]
Jacobson DL, Tang AM, Spiegelman D, Thomas AM, Skinner S, Gorbach SL, et al. Incidence of metabolic syndrome in a cohort of HIV-infected adults and prevalence relative to the US population (National Health and Nutrition Examination Survey) J Acquir Immune Defic Syndr 1999 1999; 43(4): 458-66.
[28]
Wand H, Calmy A, Carey DL, et al. INITIO Trial International Coordinating Committee. Metabolic syndrome, cardiovascular disease and type 2 diabetes mellitus after initiation of antiretroviral therapy in HIV infection. AIDS 2007; 21(18): 2445-53.
[http://dx.doi.org/10.1097/QAD.0b013e3282efad32] [PMID: 18025881]
[29]
Grund B, Peng G, Gibert CL, et al. INSIGHT SMART Body Composition Substudy Group. Continuous antiretroviral therapy decreases bone mineral density. AIDS 2009; 23(12): 1519-29.
[http://dx.doi.org/10.1097/QAD.0b013e32832c1792] [PMID: 19531929]
[30]
Dolan SE, Kanter JR, Grinspoon S. Longitudinal analysis of bone density in human immunodeficiency virus-infected women. J Clin Endocrinol Metab 2006; 91(8): 2938-45.
[http://dx.doi.org/10.1210/jc.2006-0127] [PMID: 16735489]
[31]
Rivas P, Górgolas M, García-Delgado R, Díaz-Curiel M, Goyenechea A, Fernández-Guerrero ML. Evolution of bone mineral density in AIDS patients on treatment with zidovudine/lamivudine plus abacavir or lopinavir/ritonavir. HIV Med 2008; 9(2): 89-95.
[http://dx.doi.org/10.1111/j.1468-1293.2007.00525.x] [PMID: 18093130]
[32]
Chisati EM, Constantinou D, Lampiao F. Reduced bone mineral density among HIV infected patients on anti-retroviral therapy in Blantyre, Malawi: Prevalence and associated factors. PLoS One 2020; 15(1): e0227893.
[http://dx.doi.org/10.1371/journal.pone.0227893] [PMID: 31935270]
[33]
Jarwani B. Cardiovascular Disease and Antiretroviral Therapy. J Glob Infect Dis 2019; 11(3): 91-2.
[http://dx.doi.org/10.4103/jgid.jgid_4_18] [PMID: 31543649]
[34]
Friis-Møller N, Sabin CA, Weber R, et al. Data Collection on Adverse Events of Anti-HIV Drugs (DAD) Study Group. Combination antiretroviral therapy and the risk of myocardial infarction. N Engl J Med 2003; 349(21): 1993-2003.
[http://dx.doi.org/10.1056/NEJMoa030218] [PMID: 14627784]
[35]
Delaney JAC, Scherzer R, Biggs ML, et al. Associations of antiretroviral drug use and HIV-specific risk factors with carotid intima-media thickness. AIDS 2010; 24(14): 2201-9.
[http://dx.doi.org/10.1097/QAD.0b013e32833d2132] [PMID: 20671544]
[36]
Desai M, Joyce V, Bendavid E, et al. Risk of cardiovascular events associated with current exposure to HIV antiretroviral therapies in a US veteran population. Clin Infect Dis 2015; 61(3): 445-52.
[http://dx.doi.org/10.1093/cid/civ316] [PMID: 25908684]
[37]
Worm SW, Sabin C, Weber R, et al. Risk of myocardial infarction in patients with HIV infection exposed to specific individual antiretroviral drugs from the 3 major drug classes: the data collection on adverse events of anti-HIV drugs (D:A:D) study. J Infect Dis 2010; 201(3): 318-30.
[http://dx.doi.org/10.1086/649897] [PMID: 20039804]
[38]
Chao C, Leyden WA, Xu L, et al. Exposure to antiretroviral therapy and risk of cancer in HIV-infected persons. AIDS 2012; 26(17): 2223-31.
[http://dx.doi.org/10.1097/QAD.0b013e32835935b3] [PMID: 22951631]
[39]
Mbang PA, Kowalkowski MA, Amirian ES, et al. Association between time on protease inhibitors and the incidence of squamous cell carcinoma of the anus among U.S. male veterans. PLoS One 2015; 10(12): e0142966.
[http://dx.doi.org/10.1371/journal.pone.0142966] [PMID: 26629701]
[40]
Kirk GD, Merlo C, O’ Driscoll P, et al. HIV infection is associated with an increased risk for lung cancer, independent of smoking. Clin Infect Dis 2007; 45(1): 103-10.
[http://dx.doi.org/10.1086/518606] [PMID: 17554710]
[41]
Silverberg MJ, Neuhaus J, Bower M, et al. Risk of cancers during interrupted antiretroviral therapy in the SMART study. AIDS 2007; 21(14): 1957-63.
[http://dx.doi.org/10.1097/QAD.0b013e3282ed6338] [PMID: 17721103]
[42]
Samji H, Cescon A, Hogg RS, et al. Closing the gap: increases in life expectancy among treated HIV-positive individuals in the United States and Canada. PLoS One 2013; 8(12): e81355.
[http://dx.doi.org/10.1371/journal.pone.0081355] [PMID: 24367482]
[43]
Lewden C, Bouteloup V, De Wit S, et al. All-cause mortality in treated HIV-infected adults with CD4 ≥500/mm3 compared with the general population: evidence from a large European observational cohort collaboration. Int J Epidemiol 2012; 41(2): 433-45.
[http://dx.doi.org/10.1093/ije/dyr164] [PMID: 22493325]
[44]
Antiretroviral Therapy Cohort Collaboration. Life expectancy of individuals on combination antiretroviral therapy in high-income countries: a collaborative analysis of 14 cohort studies. Lancet 2008; 372(9635): 293-9.
[http://dx.doi.org/10.1016/S0140-6736(08)61113-7] [PMID: 18657708]
[45]
Guaraldi G, Orlando G, Zona S, et al. Premature age-related comorbidities among HIV-infected persons compared with the general population. Clin Infect Dis 2011; 53(11): 1120-6.
[http://dx.doi.org/10.1093/cid/cir627] [PMID: 21998278]
[46]
Lifson AR, Neuhaus J, Arribas JR, van den Berg-Wolf M, Labriola AM, Read TRH. INSIGHT SMART Study Group. Smoking-related health risks among persons with HIV in the Strategies for Management of Antiretroviral Therapy clinical trial. Am J Public Health 2010; 100(10): 1896-903.
[http://dx.doi.org/10.2105/AJPH.2009.188664] [PMID: 20724677]
[47]
Petrosillo N, Cicalini S. Smoking and HIV: time for a change? BMC Med 2013; 11: 16.
[http://dx.doi.org/10.1186/1741-7015-11-16] [PMID: 23339539]
[48]
Kariuki W, Manuel JI, Kariuki N, Tuchman E, O’Neal J, Lalanne GA. HIV and smoking: associated risks and prevention strategies. HIV AIDS (Auckl) 2015; 8: 17-36.
[PMID: 26766919]
[49]
Carr A, Cooper DA. Adverse effects of antiretroviral therapy. Lancet 2000; 356(9239): 1423-30.
[http://dx.doi.org/10.1016/S0140-6736(00)02854-3] [PMID: 11052597]
[50]
Reust CE. Common adverse effects of antiretroviral therapy for HIV disease. Am Fam Physician 2011; 83(12): 1443-51.
[PMID: 21671545]
[51]
Fortuny C, Deyà-Martínez Á, Chiappini E, Galli L, de Martino M, Noguera-Julian A. Metabolic and renal adverse effects of antiretroviral therapy in HIV-infected children and adolescents. Pediatr Infect Dis J 2015; 34(5)(Suppl. 1): S36-43.
[http://dx.doi.org/10.1097/INF.0000000000000663] [PMID: 25629891]
[52]
Hawkins T. Understanding and managing the adverse effects of antiretroviral therapy. Antiviral Res 2010; 85(1): 201-9.
[http://dx.doi.org/10.1016/j.antiviral.2009.10.016] [PMID: 19857521]
[53]
Filardi PP, Paolillo S, Marciano C, et al. Cardiovascular effects of antiretroviral drugs: clinical review. Cardiovasc Hematol Disord Drug Targets 2008; 8(4): 238-44.
[http://dx.doi.org/10.2174/187152908786786232] [PMID: 19075633]
[54]
Redd AD, Eaton KP, Kong X, Laeyendecker O, Lutalo T, Wawer MJ, et al. C-reactive protein levels increase during HIV-1 disease progression in Rakai, Uganda despite the absence of microbial translocation J Acquir Immune Defic Syndr 1999 1999; 54(5): 556-9.
[55]
Lau B, Sharrett AR, Kingsley LA, et al. C-reactive protein is a marker for human immunodeficiency virus disease progression. Arch Intern Med 2006; 166(1): 64-70.
[http://dx.doi.org/10.1001/archinte.166.1.64] [PMID: 16401812]
[56]
Borges ÁH, O’Connor JL, Phillips AN, et al. INSIGHT SMART Study and ESPRIT Groups. Interleukin 6 is a stronger predictor of clinical events than high-sensitivity C-Reactive protein or D-Dimer during HIV infection. J Infect Dis 2016; 214(3): 408-16.
[http://dx.doi.org/10.1093/infdis/jiw173] [PMID: 27132283]
[57]
Neaton JD, Neuhaus J, Emery S. Soluble biomarkers and morbidity and mortality among people infected with HIV: summary of published reports from 1997 to 2010. Curr Opin HIV AIDS 2010; 5(6): 480-90.
[http://dx.doi.org/10.1097/COH.0b013e32833ed75d] [PMID: 20978391]
[58]
Grund B, Baker JV, Deeks SG, et al. INSIGHT SMART/ESPRIT/SILCAAT Study Group. Relevance of interleukin-6 and D-Dimer for serious non-AIDS morbidity and death among HIV- positive adults on suppressive antiretroviral therapy. PLoS One 2016; 11(5): e0155100.
[http://dx.doi.org/10.1371/journal.pone.0155100] [PMID: 27171281]
[59]
Wada NI, Bream JH, Martínez-Maza O, et al. Inflammatory biomarkers and mortality risk among HIV-suppressed men: A multisite prospective cohort study. Clin Infect Dis 2016; 63(7): 984-90.
[http://dx.doi.org/10.1093/cid/ciw409] [PMID: 27343547]
[60]
Ahmad R, Sindhu STA, Toma E, Morisset R, Ahmad A. Elevated levels of circulating interleukin-18 in human immunodeficiency virus-infected individuals: role of peripheral blood mononuclear cells and implications for AIDS pathogenesis. J Virol 2002; 76(24): 12448-56.
[http://dx.doi.org/10.1128/JVI.76.24.12448-12456.2002] [PMID: 12438570]
[61]
Lindegaard B, Hansen A-BE, Gerstoft J, Pedersen BK. High plasma level of interleukin-18 in HIV-infected subjects with lipodystrophy J Acquir Immune Defic Syndr 1999 1999; 36(1): 588-93.
[62]
Wiercinska-Drapalo A, Jaroszewicz J, Flisiak R, Prokopowicz D. Plasma interleukin-18 is associated with viral load and disease progression in HIV-1-infected patients. Microbes Infect 2004; 6(14): 1273-7.
[http://dx.doi.org/10.1016/j.micinf.2004.07.009] [PMID: 15555533]
[63]
McComsey GA, Kitch D, Sax PE, Tierney C, Jahed NC, Melbourne K, et al. Associations of inflammatory markers with AIDS and non-AIDS clinical events after initiation of Antiretroviral Therapy: AIDS clinical trials group A5224s, a substudy of ACTG A5202 J Acquir Immune Defic Syndr 1999 1999; 65(2): 167-74.
[64]
Erlandson KM, Allshouse AA, Jankowski CM, et al. Association of functional impairment with inflammation and immune activation in HIV type 1-infected adults receiving effective antiretroviral therapy. J Infect Dis 2013; 208(2): 249-59.
[http://dx.doi.org/10.1093/infdis/jit147] [PMID: 23559466]
[65]
Tenorio AR, Zheng Y, Bosch RJ, et al. Soluble markers of inflammation and coagulation but not T-cell activation predict non-AIDS-defining morbid events during suppressive antiretroviral treatment. J Infect Dis 2014; 210(8): 1248-59.
[http://dx.doi.org/10.1093/infdis/jiu254] [PMID: 24795473]
[66]
Brown TT, Tassiopoulos K, Bosch RJ, Shikuma C, McComsey GA. Association between systemic inflammation and incident diabetes in HIV-infected patients after initiation of antiretroviral therapy. Diabetes Care 2010; 33(10): 2244-9.
[http://dx.doi.org/10.2337/dc10-0633] [PMID: 20664016]
[67]
Dooko CBA, De Wit S, Neuhaus J, Palfreeman A, Pepe R, Pankow JS, et al. Interleukin-6, high sensitivity C-Reactive protein, and the development of type 2 diabetes among HIV positive patients taking Antiretroviral Therapy J Acquir Immune Defic Syndr 1999 1999; 67(5): 538-46.
[68]
Višković K, Židovec Lepej S, Gorenec A, et al. Cardiovascular markers of inflammation and serum lipid levels in HIV-infected patients with undetectable viremia. Sci Rep 2018; 8(1): 6113.
[http://dx.doi.org/10.1038/s41598-018-24446-4] [PMID: 29666424]
[69]
Nou E, Lo J, Grinspoon SK. Inflammation, immune activation, and cardiovascular disease in HIV AIDS Lond Engl 2016; 30(10): 1495-509.
[http://dx.doi.org/10.1097/QAD.0000000000001109]
[70]
Vos AG, Idris NS, Barth RE, Klipstein-Grobusch K, Grobbee DE. Pro-Inflammatory markers in relation to cardiovascular disease in HIV infection. A systematic review. PLoS One 2016; 11(1): e0147484.
[http://dx.doi.org/10.1371/journal.pone.0147484] [PMID: 26808540]
[71]
Duprez DA, Neuhaus J, Kuller LH, et al. INSIGHT SMART Study Group. Inflammation, coagulation and cardiovascular disease in HIV-infected individuals. PLoS One 2012; 7(9): e44454.
[http://dx.doi.org/10.1371/journal.pone.0044454] [PMID: 22970224]
[72]
Triant VA, Meigs JB, Grinspoon SK. Association of C-reactive protein and HIV infection with acute myocardial infarction J Acquir Immune Defic Syndr 1999 1999; 51(3): 268-73.
[73]
Sarfo B, Vanderpuye NA, Addison A, Nyasulu P. HIV case management support service is associated with improved CD4 counts of patients receiving care at the Antiretroviral Clinic of Pantang hospital, Ghana. Aids Res Treat 2017; 2017: 4697473.
[http://dx.doi.org/10.1155/2017/4697473] [PMID: 29085677]
[74]
Statement STROBE. Strengthening the Reporting of Observational Studies in Epidemiology https://www.strobe-statement.org/index.php?id=strobe-home
[75]
Papakonstantinou VD, Chini M, Mangafas N, et al. In vivo effect of two first-line ART regimens on inflammatory mediators in male HIV patients. Lipids Health Dis 2014; 13: 90.
[http://dx.doi.org/10.1186/1476-511X-13-90] [PMID: 24884881]
[76]
Strategies for Management of Anti-Retroviral Therapy/INSIGHT; DAD Study Groups. Use of nucleoside reverse transcriptase inhibitors and risk of myocardial infarction in HIV-infected patients. AIDS 2008; 22(14): F17-24.
[http://dx.doi.org/10.1097/QAD.0b013e32830fe35e] [PMID: 18753925]
[77]
Padilla S, Masiá M, García N, Jarrin I, Tormo C, Gutiérrez F. Early changes in inflammatory and pro-thrombotic biomarkers in patients initiating antiretroviral therapy with abacavir or tenofovir. BMC Infect Dis 2011; 11: 40.
[http://dx.doi.org/10.1186/1471-2334-11-40] [PMID: 21294867]
[78]
Palella FJ Jr, Gange SJ, Benning L, et al. Inflammatory biomarkers and abacavir use in the Women’s Interagency HIV Study and the Multicenter AIDS Cohort Study. AIDS 2010; 24(11): 1657-65.
[http://dx.doi.org/10.1097/QAD.0b013e3283389dfa] [PMID: 20588104]
[79]
Hileman CO, Kinley B, Scharen-Guivel V, et al. Differential reduction in monocyte activation and vascular inflammation with integrase inhibitor-based initial antiretroviral therapy among HIV-infected individuals. J Infect Dis 2015; 212(3): 345-54.
[http://dx.doi.org/10.1093/infdis/jiv004] [PMID: 25583168]
[80]
Kelesidis T, Tran TTT, Stein JH, et al. Changes in inflammation and immune activation with Atazanavir-, Raltegravir-, Darunavir-based i nitial Antiviral Therapy: ACTG 5260s. Clin Infect Dis 2015; 61(4): 651-60.
[http://dx.doi.org/10.1093/cid/civ327] [PMID: 25904376]
[81]
Kumar P, DeJesus E, Huhn G, et al. SUPPORT Study Team. Evaluation of cardiovascular biomarkers in a randomized trial of fosamprenavir/ritonavir vs. efavirenz with abacavir/lamivudine in underrepresented, antiretroviral-naïve, HIV-infected patients (SUPPORT): 96-week results. BMC Infect Dis 2013; 13: 269.
[http://dx.doi.org/10.1186/1471-2334-13-269] [PMID: 23741991]
[82]
Lorenz MW, Stephan C, Harmjanz A, et al. Both long-term HIV infection and highly active antiretroviral therapy are independent risk factors for early carotid atherosclerosis. Atherosclerosis 2008; 196(2): 720-6.
[http://dx.doi.org/10.1016/j.atherosclerosis.2006.12.022] [PMID: 17275008]
[83]
Gomo ZA, Hakim JG, Walker SA, et al. DART Team. Impact of second-line antiretroviral regimens on lipid profiles in an African setting: the DART trial sub-study. AIDS Res Ther 2014; 11(1): 32.
[http://dx.doi.org/10.1186/1742-6405-11-32] [PMID: 25320632]
[84]
Muhammad S, Sani MU, Okeahialam BN. Cardiovascular disease risk factors among HIV-infected Nigerians receiving highly active antiretroviral therapy. Niger Med J 2013; 54(3): 185-90.
[http://dx.doi.org/10.4103/0300-1652.114591] [PMID: 23901181]
[85]
Zhou DT, Kodogo V, Chokuona KFV, Gomo E, Oektedalen O, Stray-Pedersen B. Dyslipidemia and cardiovascular disease risk profiles of patients attending an HIV treatment clinic in Harare, Zimbabwe. HIV AIDS (Auckl) 2015; 7: 145-55.
[http://dx.doi.org/10.2147/HIV.S78523] [PMID: 25999764]
[86]
Gori E, Mduluza T, Nyagura M, Stray-Pedersen B, Gomo ZA. Inflammation-modulating cytokine profile and lipid interaction in HIV-related risk factors for cardiovascular diseases. Ther Clin Risk Manag 2016; 12: 1659-66.
[http://dx.doi.org/10.2147/TCRM.S117980] [PMID: 27956833]
[87]
Estrada V, Portilla J. Dyslipidemia related to antiretroviral therapy. AIDS Rev 2011; 13(1): 49-56.
[PMID: 21412389]
[88]
Feeney ER, Mallon PWG. HIV and HAART-Associated Dyslipidemia. Open Cardiovasc Med J 2011; 5: 49-63.
[http://dx.doi.org/10.2174/1874192401105010049] [PMID: 21643501]
[89]
Troll JG. Approach to dyslipidemia, lipodystrophy, and cardiovascular risk in patients with HIV infection. Curr Atheroscler Rep 2011; 13(1): 51-6.
[http://dx.doi.org/10.1007/s11883-010-0152-1] [PMID: 21181310]
[90]
El-Sadr WM, Lundgren J, Neaton JD, et al. Strategies for Management of Antiretroviral Therapy (SMART) Study Group. CD4+ count-guided interruption of antiretroviral treatment. N Engl J Med 2006; 355(22): 2283-96.
[http://dx.doi.org/10.1056/NEJMoa062360] [PMID: 17135583]
[91]
Kuller LH, Tracy R, Belloso W, et al. INSIGHT SMART Study Group. Inflammatory and coagulation biomarkers and mortality in patients with HIV infection. PLoS Med 2008; 5(10): e203.
[http://dx.doi.org/10.1371/journal.pmed.0050203] [PMID: 18942885]
[92]
Goswami B, Rajappa M, Mallika V, Shukla DK, Kumar S. TNF-alpha/IL-10 ratio and C-reactive protein as markers of the inflammatory response in CAD-prone North Indian patients with acute myocardial infarction. Clin Chim Acta 2009; 408(1-2): 14-8.
[http://dx.doi.org/10.1016/j.cca.2009.06.029] [PMID: 19576194]
[93]
Noursadeghi M, Miller RF. Clinical value of C-reactive protein measurements in HIV-positive patients. Int J STD AIDS 2005; 16(6): 438-41.
[http://dx.doi.org/10.1258/0956462054094006] [PMID: 15969780]
[94]
Fernández-Real JM, Gutiérrez C, Broch M, Casamitjana R, Vendrell J, Ricart W. Insulin response to intravenous glucose correlates with plasma levels of the tumor necrosis factor receptor-1. Diabetes Care 1999; 22(5): 868-70.
[http://dx.doi.org/10.2337/diacare.22.5.868] [PMID: 10332710]


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VOLUME: 18
ISSUE: 6
Year: 2020
Published on: 17 August, 2020
Page: [466 - 474]
Pages: 9
DOI: 10.2174/1570162X18666200817111152
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