Generic placeholder image

Current HIV Research

Editor-in-Chief

ISSN (Print): 1570-162X
ISSN (Online): 1873-4251

Research Article

Association of Lower Adiponectin Plasma Levels, Increased Age and Smoking with Subclinical Atherosclerosis in Patients with HIV-1 Infection

Author(s): Philipe Quagliato Bellinati, Daniela Frizon Alfieri, Tamires Flauzino, Paulo Fernando Gasparetto Junior, Diogo Jorge Rossi, José Wander Breganó, Andrea Name Colado Simão, Elaine Regina Delicato de Almeida, Marcell Alysson Batisti Lozovoy and Edna Maria Vissoci Reiche*

Volume 18, Issue 4, 2020

Page: [292 - 306] Pages: 15

DOI: 10.2174/1570162X18666200609114741

Price: $65

Abstract

Background: The association between subclinical atherosclerosis and traditional cardiovascular disease (CVD) risk factors, inflammatory and metabolic biomarkers has been demonstrated around the world and specifically Brazilian human immunodeficiency virus type 1 (HIV-1)- infected individuals. However, the association between subclinical atherosclerosis and these aforementioned factors combined with anti-inflammatory biomarkers has not been examined in these populations.

Objectives: To evaluate the association of the carotid intima-media thickness (cIMT) with CVD risk factors, inflammatory, metabolic and HIV-1 infection markers combined with adiponectin and interleukin (IL)-10 as anti-inflammatory variables.

Methods: In this case-control study, 49 HIV-1-infected patients on combined antiretroviral therapy (cART) and 85 controls were compared for traditional CVD risk factors, inflammatory, metabolic, and anti-inflammatory variables. Further, we compared HIV-1-infected patients according to their cIMT (as continuous and categorized <0.9 or ≥0.9 mm variable) visualized by carotid ultrasonography doppler (USGD).

Results: Twenty-four (48.9%) HIV-1-infected patients showed cIMT ≥0.9 mm. The patients had higher levels of C reactive protein on high sensitivity assay (hsCRP), tumor necrosis factor α, IL-6, IL-10, triglycerides, and insulin, and lower levels of adiponectin, total cholesterol and low-density lipoprotein cholesterol than controls (all p<0.05). Low levels of adiponectin were negatively associated with cIMT ≥0.9 mm (p=0.019), and explained 18.7% of the cIMT variance. Age (p=0.033) and current smoking (p=0.028) were positively associated with cIMT values, while adiponectin levels (p=0.008) were negatively associated with cIMT values; together, these three variables explained 27.3% of cIMT variance.

Conclusion: Low adiponectin was associated with higher cIMT in HIV-1-infected patients on cART. Low adiponectin levels in combination with age and smoking could explain, in part, the increased subclinical atherosclerosis observed in these patients. Adiponectin may be a good candidate for predicting subclinical atherosclerosis in the management of HIV-1-infected patients in public health care, especially where USGD is not available.

Keywords: HIV-1, adiponectin, subclinical atherosclerosis, carotid intima-media thickness, inflammation, biomarker.

« Previous
Graphical Abstract
[1]
d’Ettorre G, Ceccarelli G, Pavone P, et al. What happens to cardiovascular system behind the undetectable level of HIV viremia? AIDS Res Ther 2016; 13: 21.
[http://dx.doi.org/10.1186/s12981-016-0105-z] [PMID: 27127532]
[2]
Pacheco AG, Tuboi SH, Faulhaber JC, Harrison LH, Schechter M. Increase in non-AIDS related conditions as causes of death among HIV-infected individuals in the HAART era in Brazil. PLoS One 2008; 3(1) e1531
[http://dx.doi.org/10.1371/journal.pone.0001531] [PMID: 18231611]
[3]
Paula AA, Falcão MC, Pacheco AG. Metabolic syndrome in HIV-infected individuals: underlying mechanisms and epidemiological aspects. AIDS Res Ther 2013; 10(1): 32.
[http://dx.doi.org/10.1186/1742-6405-10-32] [PMID: 24330597]
[4]
Hsue PY, Scherzer R, Hunt PW, et al. Carotid Intima-Media Thickness Progression in HIV-Infected Adults Occurs Preferentially at the Carotid Bifurcation and Is Predicted by Inflammation. J Am Heart Assoc 2012; 1(2): jah3-e000422.
[http://dx.doi.org/10.1161/JAHA.111.000422] [PMID: 23130122]
[5]
D'Abramo A, Zingaropoli MA, Oliva A, et al. Immune activation, immunosenescence, and osteoprotegerin as markers of endothelial dysfunction in subclinical HIV-associated atherosclerosis. Mediators Inflamm 2014 2014.192594.
[6]
Hsue PY. Mechanisms of Cardiovascular Disease in the Setting of HIV Infection. Can J Cardiol 2019; 35(3): 238-48.
[http://dx.doi.org/10.1016/j.cjca.2018.12.024] [PMID: 30825947]
[7]
Adeyemi O, Rezai K, Bahk M, Badri S, Thomas-Gossain N. Metabolic syndrome in older HIV-infected patients: data from the CORE50 cohort. AIDS Patient Care STDS 2008; 22(12): 941-5.
[http://dx.doi.org/10.1089/apc.2008.0119] [PMID: 19072100]
[8]
Kotler DP. HIV and antiretroviral therapy: lipid abnormalities and associated cardiovascular risk in HIV-infected patients. J Acquir Immune Defic Syndr 2008; 49(Suppl. 2): S79-85.
[http://dx.doi.org/10.1097/QAI.0b013e318186519c] [PMID: 18725816]
[9]
Vachiat A, McCutcheon K, Tsabedze N, Zachariah D, Manga P. HIV and Ischemic Heart Disease. J Am Coll Cardiol 2017; 69(1): 73-82.
[http://dx.doi.org/10.1016/j.jacc.2016.09.979] [PMID: 28057253]
[10]
Piconi S, Parisotto S, Rizzardini G, et al. Atherosclerosis is associated with multiple pathogenic mechanisms in HIV-infected antiretroviral-naive or treated individuals. AIDS 2013; 27(3): 381-9.
[http://dx.doi.org/10.1097/QAD.0b013e32835abcc9] [PMID: 23079800]
[11]
Appay V, Kelleher AD. Immune activation and immune aging in HIV infection. Curr Opin HIV AIDS 2016; 11(2): 242-9.
[http://dx.doi.org/10.1097/COH.0000000000000240] [PMID: 26845675]
[12]
Hulten E, Mitchell J, Scally J, Gibbs B, Villines TC. HIV positivity, protease inhibitor exposure and subclinical atherosclerosis: a systematic review and meta-analysis of observational studies. Heart 2009; 95(22): 1826-35.
[http://dx.doi.org/10.1136/hrt.2009.177774] [PMID: 19632982]
[13]
Gupta PK, Gupta M, Lal AK, Taneja A, Taneja RS, Rewari BB. Markers of subclinical atherosclerotic disease in HIV-infected individuals. J Virus Erad 2018; 4(1): 21-5.
[PMID: 29568549]
[14]
Pacheco AG, Grinsztejn B, da Fonseca M de J, et al. Traditional risk factors are more relevant than HIV-specific ones for carotid intima-media thickness (cIMT) in a Brazilian cohort of HIV-infected patients. PLoS One 2015; 10(2) e0117461
[http://dx.doi.org/10.1371/journal.pone.0117461] [PMID: 25692764]
[15]
Ross AC, Rizk N, O’Riordan MA, et al. Relationship between inflammatory markers, endothelial activation markers, and carotid intima-media thickness in HIV-infected patients receiving antiretroviral therapy. Clin Infect Dis 2009; 49(7): 1119-27.
[http://dx.doi.org/10.1086/605578] [PMID: 19712036]
[16]
Kaplan RC, Sinclair E, Landay AL, et al. T cell activation and senescence predict subclinical carotid artery disease in HIV-infected women. J Infect Dis 2011; 203(4): 452-63.
[http://dx.doi.org/10.1093/infdis/jiq071] [PMID: 21220772]
[17]
Longenecker CT, Funderburg NT, Jiang Y, et al. Markers of inflammation and CD8 T-cell activation, but not monocyte activation, are associated with subclinical carotid artery disease in HIV-infected individuals. HIV Med 2013; 14(6): 385-90.
[http://dx.doi.org/10.1111/hiv.12013] [PMID: 23332012]
[18]
Hsue PY, Hunt PW, Schnell A, et al. Role of viral replication, antiretroviral therapy, and immunodeficiency in HIV-associated atherosclerosis. AIDS 2009; 23(9): 1059-67.
[http://dx.doi.org/10.1097/QAD.0b013e32832b514b] [PMID: 19390417]
[19]
Falasca K, Ucciferri C, Manzoli L, et al. Metabolic syndrome and cardiovascular risk in HIV-infected patients with lipodystrophy. Int J Immunopathol Pharmacol 2007; 20(3): 519-27.
[http://dx.doi.org/10.1177/039463200702000310] [PMID: 17880765]
[20]
Falasca K, Ucciferri C, Mancino P, et al. Cystatin C, adipokines and cardiovascular risk in HIV infected patients. Curr HIV Res 2010; 8(5): 405-10.
[http://dx.doi.org/10.2174/157016210791330365] [PMID: 20426756]
[21]
Ouchi N, Walsh K. Adiponectin as an anti-inflammatory factor. Clin Chim Acta 2007; 380(1-2): 24-30.
[http://dx.doi.org/10.1016/j.cca.2007.01.026] [PMID: 17343838]
[22]
Villarreal-Molina MT, Antuna-Puente B. Adiponectin: anti-inflammatory and cardioprotective effects. Biochimie 2012; 94(10): 2143-9.
[http://dx.doi.org/10.1016/j.biochi.2012.06.030] [PMID: 22796520]
[23]
Ohashi K, Ouchi N, Matsuzawa Y. Anti-inflammatory and anti-atherogenic properties of adiponectin. Biochimie 2012; 94(10): 2137-42.
[http://dx.doi.org/10.1016/j.biochi.2012.06.008] [PMID: 22713764]
[24]
Wang Y, Lam KS, Xu JY, et al. Adiponectin inhibits cell proliferation by interacting with several growth factors in an oligomerization-dependent manner. J Biol Chem 2005; 280(18): 18341-7.
[http://dx.doi.org/10.1074/jbc.M501149200] [PMID: 15734737]
[25]
Gable DR, Hurel SJ, Humphries SE. Adiponectin and its gene variants as risk factors for insulin resistance, the metabolic syndrome and cardiovascular disease. Atherosclerosis 2006; 188(2): 231-44.
[http://dx.doi.org/10.1016/j.atherosclerosis.2006.02.010] [PMID: 16581078]
[26]
Yanai H, Yoshida H. Beneficial Effects of Adiponectin on Glucose and Lipid Metabolism and Atherosclerotic Progression: Mechanisms and Perspectives. Int J Mol Sci 2019; 20(5): 1190.
[http://dx.doi.org/10.3390/ijms20051190] [PMID: 30857216]
[27]
Chen H, Montagnani M, Funahashi T, Shimomura I, Quon MJ. Adiponectin stimulates production of nitric oxide in vascular endothelial cells. J Biol Chem 2003; 278(45): 45021-6.
[http://dx.doi.org/10.1074/jbc.M307878200] [PMID: 12944390]
[28]
Adamczak M, Chudek J, Wiecek A. Adiponectin in patients with chronic kidney disease. Semin Dial 2009; 22(4): 391-5.
[http://dx.doi.org/10.1111/j.1525-139X.2009.00587.x] [PMID: 19708988]
[29]
Ntaios G, Gatselis NK, Makaritsis K, Dalekos GN. Adipokines as mediators of endothelial function and atherosclerosis. Atherosclerosis 2013; 227(2): 216-21.
[http://dx.doi.org/10.1016/j.atherosclerosis.2012.12.029] [PMID: 23332774]
[30]
Yamamoto Y, Hirose H, Saito I, et al. Correlation of the adipocyte-derived protein adiponectin with insulin resistance index and serum high-density lipoprotein-cholesterol, independent of body mass index, in the Japanese population. Clin Sci (Lond) 2002; 103(2): 137-42.
[http://dx.doi.org/10.1042/cs1030137] [PMID: 12149104]
[31]
Hui E, Xu A, Chow W-S, et al. Hypoadiponectinemia as an independent predictor for the progression of carotid atherosclerosis: a 5-year prospective study. Metab Syndr Relat Disord 2014; 12(10): 517-22.
[http://dx.doi.org/10.1089/met.2014.0024] [PMID: 25211296]
[32]
Ketlogetswe KS, Post WS, Li X, et al. Lower adiponectin is associated with subclinical cardiovascular disease among HIV-infected men. AIDS 2014; 28(6): 901-9.
[http://dx.doi.org/10.1097/QAD.0000000000000186] [PMID: 24401646]
[33]
Tong Q, Sankalé JL, Hadigan CM, et al. Regulation of adiponectin in human immunodeficiency virus-infected patients: relationship to body composition and metabolic indices. J Clin Endocrinol Metab 2003; 88(4): 1559-64.
[http://dx.doi.org/10.1210/jc.2002-021600] [PMID: 12679439]
[34]
Addy CL, Gavrila A, Tsiodras S, Brodovicz K, Karchmer AW, Mantzoros CS. Hypoadiponectinemia is associated with insulin resistance, hypertriglyceridemia, and fat redistribution in human immunodeficiency virus-infected patients treated with highly active antiretroviral therapy. J Clin Endocrinol Metab 2003; 88(2): 627-36.
[http://dx.doi.org/10.1210/jc.2002-020795] [PMID: 12574192]
[35]
Gasbarrino K, Gorgui J, Nauche B, Côté R, Daskalopoulou SS. Circulating adiponectin and carotid intima-media thickness: A systematic review and meta-analysis. Metabolism 2016; 65(7): 968-86.
[http://dx.doi.org/10.1016/j.metabol.2016.03.008] [PMID: 27282868]
[36]
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]
[37]
Falcão Mda C, Zírpoli JC, Albuquerque VM, et al. Association of biomarkers with atherosclerosis and risk for coronary artery disease in patients with HIV. Arq Bras Cardiol 2012; 99(5): 971-8.
[http://dx.doi.org/10.1590/s0066-782x2012005000093] [PMID: 23080223]
[38]
Salmazo PS, Bazan SGZ, Shiraishi FG, Bazan R, Okoshi K, Hueb JC. Frequency of Subclinical Atherosclerosis in Brazilian HIV-Infected Patients. Arq Bras Cardiol 2018; 110(5): 402-10.
[http://dx.doi.org/10.5935/abc.20180058] [PMID: 29641646]
[39]
Leite KME, Santos Júnior GG, Godoi ETAM, et al. Inflammatory Biomarkers and Carotid Thickness in HIV Infected Patients under Antiretroviral Therapy, Undetectable HIV-1 Viral Load, and Low Cardiovascular Risk. Arq Bras Cardiol 2020; 114(1): 90-7.
[http://dx.doi.org/10.5935/abc.20190230] [PMID: 31664319]
[40]
Brazil Clinical Protocol and Therapeutic Guidelines for Managing HIV Infection in Adults. Brasilia: Ministry of Health 2018.
[41]
James PA, Oparil S, Carter BL, et al. 2014 evidence-based guideline for the management of high blood pressure in adults: report from the panel members appointed to the Eighth Joint National Committee (JNC 8). JAMA 2014; 311(5): 507-20.
[http://dx.doi.org/10.1001/jama.2013.284427] [PMID: 24352797]
[42]
American Diabetes Association. Standards of medical care in diabetes – 2014. Diabetes Care 2014; 37(Supplement_1): S14-80.
[43]
Johnson EL, Feldman H, Butts A, et al. American Diabetes Association. Standards of medical care in diabetes—2019. Clin Diabetes 2019; 37(1): 11-34.
[http://dx.doi.org/10.2337/cd18-0105] [PMID: 30705493]
[44]
National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) final report. Circulation 2002; 106(25): 3143-421.
[http://dx.doi.org/10.1161/circ.106.25.3143] [PMID: 12485966]
[45]
Grunfeld C, Kotler DP, Arnett DK, et al. Working Group 1. Contribution of metabolic and anthropometric abnormalities to cardiovascular disease risk factors. Circulation 2008; 118(2): e20-8.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.107.189623] [PMID: 18566314]
[46]
Williams B, Mancia G, Spiering W, et al. 2018 ESC/ESH Guidelines for the management of arterial hypertension. Eur Heart J 2018; 39(33): 3021-104.
[http://dx.doi.org/10.1093/eurheartj/ehy339] [PMID: 30165516]
[47]
Pirš M, Jug B, Eržen B, et al. Relationship between markers of endothelial dysfunction and inflammation and subclinical atherosclerosis in HIV-infected male patients below 55 years of age. Acta Dermatovenerol Alp Panonica Adriat 2014; 23(3): 49-52.
[PMID: 25242160]
[48]
Friis-Møller N, Thiébaut R, Reiss P, et al. DAD study group. Predicting the risk of cardiovascular disease in HIV-infected patients: the data collection on adverse effects of anti-HIV drugs study. Eur J Cardiovasc Prev Rehabil 2010; 17(5): 491-501.
[http://dx.doi.org/10.1097/HJR.0b013e328336a150] [PMID: 20543702]
[49]
Freiberg MS, Chang CCH, Kuller LH, et al. HIV infection and the risk of acute myocardial infarction. JAMA Intern Med 2013; 173(8): 614-22.
[http://dx.doi.org/10.1001/jamainternmed.2013.3728] [PMID: 23459863]
[50]
Hanna DB, Post WS, Deal JA, et al. HIV Infection is associated with progression of subclinical carotid atherosclerosis. Clin Infect Dis 2015; 61(4): 640-50.
[http://dx.doi.org/10.1093/cid/civ325] [PMID: 25904369]
[51]
Sico JJ, Chang CC, So-Armah K, et al. Veterans Aging Cohort Study. HIV status and the risk of ischemic stroke among men. Neurology 2015; 84(19): 1933-40.
[http://dx.doi.org/10.1212/WNL.0000000000001560] [PMID: 25862803]
[52]
Triant VA, Lee H, Hadigan C, Grinspoon SK. Increased acute myocardial infarction rates and cardiovascular risk factors among patients with human immunodeficiency virus disease. J Clin Endocrinol Metab 2007; 92(7): 2506-12.
[53]
Currier JS, Kendall MA, Zackin R, et al. AACTG 5078 Study Team. Carotid artery intima-media thickness and HIV infection: traditional risk factors overshadow impact of protease inhibitor exposure. AIDS 2005; 19(9): 927-33.
[http://dx.doi.org/10.1097/01.aids.0000171406.53737.f9] [PMID: 15905673]
[54]
Maggi P, Bellacosa C, Leone A, et al. Cardiovascular risk in advanced naïve HIV-infected patients starting antiretroviral therapy: Comparison of three different regimens - PREVALEAT II cohort. Atherosclerosis 2017; 263: 398-404.
[http://dx.doi.org/10.1016/j.atherosclerosis.2017.05.004] [PMID: 28522147]
[55]
Currier JS, Lundgren JD, Carr A, et al. Working Group 2. Epidemiological evidence for cardiovascular disease in HIV-infected patients and relationship to highly active antiretroviral therapy. Circulation 2008; 118(2): e29-35.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.107.189624] [PMID: 18566319]
[56]
Fontas E, van Leth F, Sabin CA, et al. D:A:D Study Group. Lipid profiles in HIV-infected patients receiving combination antiretroviral therapy: are different antiretroviral drugs associated with different lipid profiles? J Infect Dis 2004; 189(6): 1056-74.
[http://dx.doi.org/10.1086/381783] [PMID: 14999610]
[57]
Rhew DC, Bernal M, Aguilar D, Iloeje U, Goetz MB. Association between protease inhibitor use and increased cardiovascular risk in patients infected with human immunodeficiency virus: a systematic review. Clin Infect Dis 2003; 37(7): 959-72.
[http://dx.doi.org/10.1086/378064] [PMID: 13130409]
[58]
Hakala SM, Tilvis RS. Determinants and significance of declining blood pressure in old age. A prospective birth cohort study. Eur Heart J 1998; 19(12): 1872-8.
[http://dx.doi.org/10.1053/euhj.1998.1232] [PMID: 9886731]
[59]
Manolio TA, Cushman M, Gottdiener JS, Dobs A, Kuller LH, Kronmal RA. CHS Collaborative Research Group. Predictors of falling cholesterol levels in older adults: the Cardiovascular Health Study. Ann Epidemiol 2004; 14(5): 325-31.
[http://dx.doi.org/10.1016/j.annepidem.2003.09.006] [PMID: 15177271]
[60]
Lorenz MW, Markus HS, Bots ML, Rosvall M, Sitzer M. Prediction of clinical cardiovascular events with carotid intima-media thickness: a systematic review and meta-analysis. Circulation 2007; 115(4): 459-67.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.106.628875] [PMID: 17242284]
[61]
van den Munckhof ICL, Jones H, Hopman MTE, et al. Relation between age and carotid artery intima-medial thickness: a systematic review. Clin Cardiol 2018; 41(5): 698-704.
[http://dx.doi.org/10.1002/clc.22934] [PMID: 29752816]
[62]
Herder M, Johnsen SH, Arntzen KA, Mathiesen EB. Risk factors for progression of carotid intima-media thickness and total plaque area: a 13-year follow-up study: the Tromsø Study. Stroke 2012; 43(7): 1818-23.
[http://dx.doi.org/10.1161/STROKEAHA.111.646596] [PMID: 22550052]
[63]
Dratva J, Probst-Hensch N, Schmidt-Trucksäss A, et al. Atherogenesis in youth--early consequence of adolescent smoking. Atherosclerosis 2013; 230(2): 304-9.
[http://dx.doi.org/10.1016/j.atherosclerosis.2013.08.004] [PMID: 24075761]
[64]
Li S, Yun M, Fernandez C, et al. Cigarette smoking exacerbates the adverse effects of age and metabolic syndrome on subclinical atherosclerosis: the Bogalusa Heart Study. PLoS One 2014; 9(5) e96368
[http://dx.doi.org/10.1371/journal.pone.0096368] [PMID: 24789040]
[65]
Kiriyama H, Kaneko H, Itoh H, et al. Effect of cigarette smoking on carotid artery atherosclerosis: a community-based cohort study. Heart Vessels 2019; 35(1): 22-9.
[http://dx.doi.org/10.1007/s00380-019-01455-5] [PMID: 31222551]
[66]
Fitch KV, Looby SE, Rope A, et al. Effects of aging and smoking on carotid intima-media thickness in HIV-infection. AIDS 2013; 27(1): 49-57.
[http://dx.doi.org/10.1097/QAD.0b013e328358b29c] [PMID: 22874518]
[67]
Barua RS, Ambrose JA. Mechanisms of coronary thrombosis in cigarette smoke exposure. Arterioscler Thromb Vasc Biol 2013; 33(7): 1460-7.
[http://dx.doi.org/10.1161/ATVBAHA.112.300154] [PMID: 23685556]
[68]
Cnop M, Havel PJ, Utzschneider KM, et al. Relationship of adiponectin to body fat distribution, insulin sensitivity and plasma lipoproteins: evidence for independent roles of age and sex. Diabetologia 2003; 46(4): 459-69.
[http://dx.doi.org/10.1007/s00125-003-1074-z] [PMID: 12687327]
[69]
Tschritter O, Fritsche A, Thamer C, et al. Plasma adiponectin concentrations predict insulin sensitivity of both glucose and lipid metabolism. Diabetes 2003; 52(2): 239-43.
[http://dx.doi.org/10.2337/diabetes.52.2.239] [PMID: 12540592]
[70]
Yatagai T, Nagasaka S, Taniguchi A, et al. Hypoadiponectinemia is associated with visceral fat accumulation and insulin resistance in Japanese men with type 2 diabetes mellitus. Metabolism 2003; 52(10): 1274-8.
[http://dx.doi.org/10.1016/S0026-0495(03)00195-1] [PMID: 14564678]
[71]
Gradinaru D, Margina D, Borsa C, et al. Adiponectin: possible link between metabolic stress and oxidative stress in the elderly. Aging Clin Exp Res 2017; 29(4): 621-9.
[http://dx.doi.org/10.1007/s40520-016-0629-z] [PMID: 27688246]
[72]
van Andel M, Heijboer AC, Drent ML. Adiponectin and Its Isoforms in Pathophysiology. Adv Clin Chem 2018; 85: 115-47.
[http://dx.doi.org/10.1016/bs.acc.2018.02.007] [PMID: 29655459]
[73]
Lui G, Ma RCW, Chook P, et al. Brief Report: Progression of Atherosclerosis in HIV-Infected Individuals-Prospective Data From an Asian Cohort. J Acquir Immune Defic Syndr 2017; 75(2): 198-202.
[http://dx.doi.org/10.1097/QAI.0000000000001358] [PMID: 28498145]
[74]
Arita Y, Kihara S, Ouchi N, et al. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun 1999; 257(1): 79-83.
[http://dx.doi.org/10.1006/bbrc.1999.0255] [PMID: 10092513]
[75]
Wolf AM, Wolf D, Rumpold H, Enrich B, Tilg H. Adiponectin induces the anti-inflammatory cytokines IL-10 and IL-1RA in human leukocytes. Biochem Biophys Res Commun 2004; 323(2): 630-5.
[http://dx.doi.org/10.1016/j.bbrc.2004.08.145] [PMID: 15369797]
[76]
Saijo S, Nagata K, Nakano Y, Tobe T, Kobayashi Y. Inhibition by adiponectin of IL-8 production by human macrophages upon coculturing with late apoptotic cells. Biochem Biophys Res Commun 2005; 334(4): 1180-3.
[http://dx.doi.org/10.1016/j.bbrc.2005.07.016] [PMID: 16039610]
[77]
Longenecker CT, Sullivan C, Baker JV. Immune activation and cardiovascular disease in chronic HIV infection. Curr Opin HIV AIDS 2016; 11(2): 216-25.
[http://dx.doi.org/10.1097/COH.0000000000000227] [PMID: 26599166]
[78]
Subramanya V, McKay HS, Brusca RM, et al. Inflammatory biomarkers and subclinical carotid atherosclerosis in HIV-infected and HIV-uninfected men in the Multicenter AIDS Cohort Study. PLoS One 2019; 14(4) e0214735
[http://dx.doi.org/10.1371/journal.pone.0214735] [PMID: 30946765]
[79]
Penzak SR, Chuck SK. Hyperlipidemia associated with HIV protease inhibitor use: pathophysiology, prevalence, risk factors and treatment. Scand J Infect Dis 2000; 32(2): 111-23.
[http://dx.doi.org/10.1080/003655400750045196] [PMID: 10826894]
[80]
Fisher SD, Miller TL, Lipshultz SE. Impact of HIV and highly active antiretroviral therapy on leukocyte adhesion molecules, arterial inflammation, dyslipidemia, and atherosclerosis. Atherosclerosis 2006; 185(1): 1-11.
[http://dx.doi.org/10.1016/j.atherosclerosis.2005.09.025] [PMID: 16297390]
[81]
Sellmeyer DE, Grunfeld C. Endocrine and metabolic disturbances in human immunodeficiency virus infection and the acquired immune deficiency syndrome. Endocr Rev 1996; 17(5): 518-32.
[http://dx.doi.org/10.1210/edrv-17-5-518] [PMID: 8897023]
[82]
Schroecksnadel K, Frick B, Winkler C, Fuchs D. Crucial role of interferon-gamma and stimulated macrophages in cardiovascular disease. Curr Vasc Pharmacol 2006; 4(3): 205-13.
[http://dx.doi.org/10.2174/157016106777698379] [PMID: 16842138]
[83]
Cobos Jiménez V, Booiman T, de Taeye SW, et al. Differential expression of HIV-1 interfering factors in monocyte-derived macrophages stimulated with polarizing cytokines or interferons. Sci Rep 2012; 2: 763.
[http://dx.doi.org/10.1038/srep00763] [PMID: 23094138]
[84]
de Almeida ER, Reiche EM, Kallaur AP, Flauzino T, Watanabe MA. The roles of genetic polymorphisms and human immunodeficiency virus infection in lipid metabolism. BioMed Res Int 2013; 2013 836790
[http://dx.doi.org/10.1155/2013/836790] [PMID: 24319689]
[85]
Stylianou E, Aukrust P, Kvale D, Müller F, Frøland SS. IL-10 in HIV infection: increasing serum IL-10 levels with disease progression--down-regulatory effect of potent anti-retroviral therapy. Clin Exp Immunol 1999; 116(1): 115-20.
[http://dx.doi.org/10.1046/j.1365-2249.1999.00865.x] [PMID: 10209514]
[86]
Gorenec L, Zidovec Lepej S, Grgic I, et al. The comparison of Th1, Th2, Th9, Th17 and Th22 cytokine profiles in acute and chronic HIV-1 infection. Microb Pathog 2016; 97: 125-30.
[http://dx.doi.org/10.1016/j.micpath.2016.06.008] [PMID: 27268396]
[87]
Welsh P, Murray HM, Ford I, et al. PROSPER Study Group. Circulating interleukin-10 and risk of cardiovascular events: a prospective study in the elderly at risk. Arterioscler Thromb Vasc Biol 2011; 31(10): 2338-44.
[http://dx.doi.org/10.1161/ATVBAHA.111.231795] [PMID: 21757655]
[88]
Kwon DS, Kaufmann DE. Protective and detrimental roles of IL-10 in HIV pathogenesis. Eur Cytokine Netw 2010; 21(3): 208-14.
[http://dx.doi.org/10.1684/ecn.2010.0201] [PMID: 20732847]
[89]
Planès R, Ben Haij N, Leghmari K, Serrero M, BenMohamed L, Bahraoui E. HIV-1 Tat protein activates both the MyD88 and TRIF pathways to induce tumor necrosis factor alpha and interleukin-10 in human monocytes. J Virol 2016; 90(13): 5886-98.
[http://dx.doi.org/10.1128/JVI.00262-16] [PMID: 27053552]
[90]
Planès R, Serrero M, Leghmari K, BenMohamed L, Bahraoui E. HIV-1 Envelope Glycoproteins Induce the Production of TNF-α and IL-10 in Human Monocytes by Activating Calcium Pathway. Sci Rep 2018; 8(1): 17215.
[http://dx.doi.org/10.1038/s41598-018-35478-1] [PMID: 30464243]
[91]
Liu J, Zhan W, Kim CJ, et al. IL-10-producing B cells are induced early in HIV-1 infection and suppress HIV-1-specific T cell responses. PLoS One 2014; 9(2) e89236
[http://dx.doi.org/10.1371/journal.pone.0089236] [PMID: 24586620]

Rights & Permissions Print Export Cite as
© 2024 Bentham Science Publishers | Privacy Policy