Skip to main content
Top
Published in: Diabetology & Metabolic Syndrome 1/2018

Open Access 01-12-2018 | Research

Plasma levels of lipopolysaccharide correlate with insulin resistance in HIV patients

Authors: Marcelo Nardi Pedro, Daniela Oliveira Magro, Elizabete Urbano Pinaço Pinto da Silva, Dioze Guadagnini, Andrey Santos, Rogerio de Jesus Pedro, Mario José Abdalla Saad

Published in: Diabetology & Metabolic Syndrome | Issue 1/2018

Login to get access

Abstract

Background

In HIV patients using HAART insulin resistance is a central pathophysiological condition that can contribute to the development of diabetes and cardiovascular complications. To examine the role of adipocyte hormones and LPS in insulin resistance in HIV patients, we investigated the role of adiponectin, leptin, visfatin and LPS levels in the insulin resistance of HIV-infected patients treated with HAART.

Methods

This study included 67 HIV positive individuals on HAART and ten healthy controls. All participants performed plasma or serum levels of glucose; insulin; lipids, visfatin, leptin, adiponectin, and LPS. The homeostasis model assessment (HOMA-IR), was used to estimate insulin resistance.

Results

The levels of visfatin, leptin and adiponectin were similar between controls and HIV patients. However, circulating levels of LPS were higher in HIV patients on HAART than in controls. There was a positive correlation between LPS and TG (r = 0.49, p = 0.0001), between LPS and TG/HDL (r = 0.50, p = 0.0001), between LPS and insulin (r = 0.52, p = 0.0003), and between LPS and HOMA-IR (r = 0.52, p = 0.0005), in HIV patients.

Conclusions

Our results showed a clear correlation between plasma LPS and markers of insulin resistance, suggesting a relationship between LPS levels and metabolic alterations, particularly affecting lipids and insulin resistance in HIV patients.
Literature
1.
go back to reference Lewden C, Bouteloup V, De Wit S, Sabin C, Mocroft A, Wasmuth JC, van Sighem A, Kirk O, Obel N, Panos G, 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;41:433–45.CrossRefPubMed Lewden C, Bouteloup V, De Wit S, Sabin C, Mocroft A, Wasmuth JC, van Sighem A, Kirk O, Obel N, Panos G, 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;41:433–45.CrossRefPubMed
2.
go back to reference Guaraldi G, Orlando G, Zona S, Menozzi M, Carli F, Garlassi E, Berti A, Rossi E, Roverato A, Palella F. Premature age-related comorbidities among HIV-infected persons compared with the general population. Clin Infect Dis. 2011;53:1120–6.CrossRefPubMed Guaraldi G, Orlando G, Zona S, Menozzi M, Carli F, Garlassi E, Berti A, Rossi E, Roverato A, Palella F. Premature age-related comorbidities among HIV-infected persons compared with the general population. Clin Infect Dis. 2011;53:1120–6.CrossRefPubMed
3.
go back to reference Tiozzo E, Konefal J, Adwan S, Martinez LA, Villabona J, Lopez J, Cutrono S, Mehdi SM, Rodriguez A, Woolger JM, Lewis JE. A cross-sectional assessment of metabolic syndrome in HIV-infected people of low socio-economic status receiving antiretroviral therapy. Diabetol Metab Syndr. 2015;7:15.CrossRefPubMedPubMedCentral Tiozzo E, Konefal J, Adwan S, Martinez LA, Villabona J, Lopez J, Cutrono S, Mehdi SM, Rodriguez A, Woolger JM, Lewis JE. A cross-sectional assessment of metabolic syndrome in HIV-infected people of low socio-economic status receiving antiretroviral therapy. Diabetol Metab Syndr. 2015;7:15.CrossRefPubMedPubMedCentral
4.
go back to reference Beraldo RA, Santos APD, Guimarães MP, Vassimon HS, Paula FJA, Machado DRL, Foss-Freitas MC, Navarro AM. Body fat redistribution and changes in lipid and glucose metabolism in people living with HIV/AIDS. Rev Bras Epidemiol. 2017;20:526–36.CrossRefPubMed Beraldo RA, Santos APD, Guimarães MP, Vassimon HS, Paula FJA, Machado DRL, Foss-Freitas MC, Navarro AM. Body fat redistribution and changes in lipid and glucose metabolism in people living with HIV/AIDS. Rev Bras Epidemiol. 2017;20:526–36.CrossRefPubMed
5.
go back to reference Calmy A, Hirschel B, Cooper DA, Carr A. Clinical update: adverse effects of antiretroviral therapy. Lancet. 2007;370:12–4.CrossRefPubMed Calmy A, Hirschel B, Cooper DA, Carr A. Clinical update: adverse effects of antiretroviral therapy. Lancet. 2007;370:12–4.CrossRefPubMed
6.
go back to reference Calza L, Manfredi R, Chiodo F. Insulin resistance and diabetes mellitus in HIV-infected patients receiving antiretroviral therapy. Metab Syndr Relat Disord. 2004;2:241–50.CrossRefPubMed Calza L, Manfredi R, Chiodo F. Insulin resistance and diabetes mellitus in HIV-infected patients receiving antiretroviral therapy. Metab Syndr Relat Disord. 2004;2:241–50.CrossRefPubMed
7.
go back to reference Mbunkah HA, Meriki HD, Kukwah AT, Nfor O, Nkuo-Akenji T. Prevalence of metabolic syndrome in human immunodeficiency virus-infected patients from the South-West region of Cameroon, using the adult treatment panel III criteria. Diabetol Metab Syndr. 2014;6:92.CrossRefPubMedPubMedCentral Mbunkah HA, Meriki HD, Kukwah AT, Nfor O, Nkuo-Akenji T. Prevalence of metabolic syndrome in human immunodeficiency virus-infected patients from the South-West region of Cameroon, using the adult treatment panel III criteria. Diabetol Metab Syndr. 2014;6:92.CrossRefPubMedPubMedCentral
8.
go back to reference Visnegarwala F, Chen L, Raghavan S, Tedaldi E. Prevalence of diabetes mellitus and dyslipidemia among antiretroviral naive patients co-infected with hepatitis C virus (HCV) and HIV-1 compared to patients without co-infection. J Infect. 2005;50:331–7.CrossRefPubMed Visnegarwala F, Chen L, Raghavan S, Tedaldi E. Prevalence of diabetes mellitus and dyslipidemia among antiretroviral naive patients co-infected with hepatitis C virus (HCV) and HIV-1 compared to patients without co-infection. J Infect. 2005;50:331–7.CrossRefPubMed
9.
go back to reference Capeau J, Bouteloup V, Katlama C, Bastard JP, Guiyedi V, Salmon-Ceron D, Protopopescu C, Leport C, Raffi F, Chene G. Ten-year diabetes incidence in 1046 HIV-infected patients started on a combination antiretroviral treatment. Aids. 2012;26:303–14.CrossRefPubMed Capeau J, Bouteloup V, Katlama C, Bastard JP, Guiyedi V, Salmon-Ceron D, Protopopescu C, Leport C, Raffi F, Chene G. Ten-year diabetes incidence in 1046 HIV-infected patients started on a combination antiretroviral treatment. Aids. 2012;26:303–14.CrossRefPubMed
10.
go back to reference Guillen MA, Mejia FA, Villena J, Turin CG, Carcamo CP, Ticse R. Insulin resistance by homeostasis model assessment in HIV-infected patients on highly active antiretroviral therapy: cross-sectional study. Diabetol Metab Syndr. 2015;7:49.CrossRefPubMedPubMedCentral Guillen MA, Mejia FA, Villena J, Turin CG, Carcamo CP, Ticse R. Insulin resistance by homeostasis model assessment in HIV-infected patients on highly active antiretroviral therapy: cross-sectional study. Diabetol Metab Syndr. 2015;7:49.CrossRefPubMedPubMedCentral
11.
go back to reference Arama V, Tiliscan C, Streinu-Cercel A, Ion D, Mihailescu R, Munteanu D, Hristea A, Arama SS. Insulin resistance and adipokines serum levels in a caucasian cohort of HIV-positive patients undergoing antiretroviral therapy: a cross sectional study. BMC Endocr Disord. 2013;13:4.CrossRefPubMedPubMedCentral Arama V, Tiliscan C, Streinu-Cercel A, Ion D, Mihailescu R, Munteanu D, Hristea A, Arama SS. Insulin resistance and adipokines serum levels in a caucasian cohort of HIV-positive patients undergoing antiretroviral therapy: a cross sectional study. BMC Endocr Disord. 2013;13:4.CrossRefPubMedPubMedCentral
12.
go back to reference Boufassa F, Goujard C, Viard JP, Carlier R, Lefebvre B, Yeni P, Bouchaud O, Capeau J, Meyer L, Vigouroux C. Immune deficiency could be an early risk factor for altered insulin sensitivity in antiretroviral-naive HIV-1-infected patients: the ANRS COPANA cohort. Antivir Ther. 2012;17:91–100.CrossRefPubMedPubMedCentral Boufassa F, Goujard C, Viard JP, Carlier R, Lefebvre B, Yeni P, Bouchaud O, Capeau J, Meyer L, Vigouroux C. Immune deficiency could be an early risk factor for altered insulin sensitivity in antiretroviral-naive HIV-1-infected patients: the ANRS COPANA cohort. Antivir Ther. 2012;17:91–100.CrossRefPubMedPubMedCentral
13.
go back to reference 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;88:627–36.CrossRefPubMed 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;88:627–36.CrossRefPubMed
14.
go back to reference Estrada V, Martinez-Larrad MT, Gonzalez-Sanchez JL, de Villar NG, Zabena C, Fernandez C, Serrano-Rios M. Lipodystrophy and metabolic syndrome in HIV-infected patients treated with antiretroviral therapy. Metabolism. 2006;55:940–5.CrossRefPubMed Estrada V, Martinez-Larrad MT, Gonzalez-Sanchez JL, de Villar NG, Zabena C, Fernandez C, Serrano-Rios M. Lipodystrophy and metabolic syndrome in HIV-infected patients treated with antiretroviral therapy. Metabolism. 2006;55:940–5.CrossRefPubMed
15.
go back to reference Sweeney LL, Brennan AM, Mantzoros CS. The role of adipokines in relation to HIV lipodystrophy. Aids. 2007;21:895–904.CrossRefPubMed Sweeney LL, Brennan AM, Mantzoros CS. The role of adipokines in relation to HIV lipodystrophy. Aids. 2007;21:895–904.CrossRefPubMed
16.
go back to reference Leow MK, Addy CL, Mantzoros CS. Clinical review 159: human immunodeficiency virus/highly active antiretroviral therapy-associated metabolic syndrome: clinical presentation, pathophysiology, and therapeutic strategies. J Clin Endocrinol Metab. 2003;88:1961–76.CrossRefPubMed Leow MK, Addy CL, Mantzoros CS. Clinical review 159: human immunodeficiency virus/highly active antiretroviral therapy-associated metabolic syndrome: clinical presentation, pathophysiology, and therapeutic strategies. J Clin Endocrinol Metab. 2003;88:1961–76.CrossRefPubMed
17.
go back to reference Fiorenza CG, Chou SH, Mantzoros CS. Lipodystrophy: pathophysiology and advances in treatment. Nat Rev Endocrinol. 2011;7:137–50.CrossRefPubMed Fiorenza CG, Chou SH, Mantzoros CS. Lipodystrophy: pathophysiology and advances in treatment. Nat Rev Endocrinol. 2011;7:137–50.CrossRefPubMed
18.
go back to reference Freitas P, Carvalho D, Santos AC, Mesquita J, Matos MJ, Madureira AJ, Martinez E, Sarmento A, Medina JL. Lipodystrophy defined by Fat Mass Ratio in HIV-infected patients is associated with a high prevalence of glucose disturbances and insulin resistance. BMC Infect Dis. 2012;12:180.CrossRefPubMedPubMedCentral Freitas P, Carvalho D, Santos AC, Mesquita J, Matos MJ, Madureira AJ, Martinez E, Sarmento A, Medina JL. Lipodystrophy defined by Fat Mass Ratio in HIV-infected patients is associated with a high prevalence of glucose disturbances and insulin resistance. BMC Infect Dis. 2012;12:180.CrossRefPubMedPubMedCentral
19.
go back to reference Shlay JC, Visnegarwala F, Bartsch G, Wang J, Peng G, El-Sadr WM, Gibert C, Kotler D, Grunfeld C, Raghavan S. Body composition and metabolic changes in antiretroviral-naive patients randomized to didanosine and stavudine vs. abacavir and lamivudine. J Acquir Immune Defic Syndr. 2005;38:147–55.CrossRefPubMed Shlay JC, Visnegarwala F, Bartsch G, Wang J, Peng G, El-Sadr WM, Gibert C, Kotler D, Grunfeld C, Raghavan S. Body composition and metabolic changes in antiretroviral-naive patients randomized to didanosine and stavudine vs. abacavir and lamivudine. J Acquir Immune Defic Syndr. 2005;38:147–55.CrossRefPubMed
20.
go back to reference Magkos F, Mantzoros CS. Body fat redistribution and metabolic abnormalities in HIV-infected patients on highly active antiretroviral therapy: novel insights into pathophysiology and emerging opportunities for treatment. Metabolism. 2011;60:749–53.CrossRefPubMed Magkos F, Mantzoros CS. Body fat redistribution and metabolic abnormalities in HIV-infected patients on highly active antiretroviral therapy: novel insights into pathophysiology and emerging opportunities for treatment. Metabolism. 2011;60:749–53.CrossRefPubMed
22.
go back to reference Trujillo ME, Scherer PE. Adipose tissue-derived factors: impact on health and disease. Endocr Rev. 2006;27:762–78.CrossRefPubMed Trujillo ME, Scherer PE. Adipose tissue-derived factors: impact on health and disease. Endocr Rev. 2006;27:762–78.CrossRefPubMed
23.
go back to reference Gregor MF, Hotamisligil GS. Inflammatory mechanisms in obesity. Annu Rev Immunol. 2011;29:415–45.CrossRefPubMed Gregor MF, Hotamisligil GS. Inflammatory mechanisms in obesity. Annu Rev Immunol. 2011;29:415–45.CrossRefPubMed
26.
go back to reference Velloso LA, Folli F, Saad MJ. TLR4 at the crossroads of nutrients, gut microbiota, and metabolic inflammation. Endocr Rev. 2015;36:245–71.CrossRefPubMed Velloso LA, Folli F, Saad MJ. TLR4 at the crossroads of nutrients, gut microbiota, and metabolic inflammation. Endocr Rev. 2015;36:245–71.CrossRefPubMed
27.
28.
go back to reference Dardeno TA, Chou SH, Moon HS, Chamberland JP, Fiorenza CG, Mantzoros CS. Leptin in human physiology and therapeutics. Front Neuroendocrinol. 2010;31:377–93.CrossRefPubMedPubMedCentral Dardeno TA, Chou SH, Moon HS, Chamberland JP, Fiorenza CG, Mantzoros CS. Leptin in human physiology and therapeutics. Front Neuroendocrinol. 2010;31:377–93.CrossRefPubMedPubMedCentral
29.
go back to reference Ferrer M, Ruiz A, Lanza F, Haange SB, Oberbach A, Till H, Bargiela R, Campoy C, Segura MT, Richter M, et al. Microbiota from the distal guts of lean and obese adolescents exhibit partial functional redundancy besides clear differences in community structure. Environ Microbiol. 2013;15:211–26.CrossRefPubMed Ferrer M, Ruiz A, Lanza F, Haange SB, Oberbach A, Till H, Bargiela R, Campoy C, Segura MT, Richter M, et al. Microbiota from the distal guts of lean and obese adolescents exhibit partial functional redundancy besides clear differences in community structure. Environ Microbiol. 2013;15:211–26.CrossRefPubMed
30.
go back to reference Caricilli AM, Saad MJ. Gut microbiota composition and its effects on obesity and insulin resistance. Curr Opin Clin Nutr Metab Care. 2014;17:312–8.CrossRefPubMed Caricilli AM, Saad MJ. Gut microbiota composition and its effects on obesity and insulin resistance. Curr Opin Clin Nutr Metab Care. 2014;17:312–8.CrossRefPubMed
31.
go back to reference Carvalho BM, Saad MJ. Influence of gut microbiota on subclinical inflammation and insulin resistance. Mediat Inflamm. 2013;2013:986734.CrossRef Carvalho BM, Saad MJ. Influence of gut microbiota on subclinical inflammation and insulin resistance. Mediat Inflamm. 2013;2013:986734.CrossRef
32.
go back to reference Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007;56:1761–72.CrossRefPubMed Cani PD, Amar J, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007;56:1761–72.CrossRefPubMed
33.
go back to reference Manco M, Putignani L, Bottazzo GF. Gut microbiota, lipopolysaccharides, and innate immunity in the pathogenesis of obesity and cardiovascular risk. Endocr Rev. 2010;31:817–44.CrossRefPubMed Manco M, Putignani L, Bottazzo GF. Gut microbiota, lipopolysaccharides, and innate immunity in the pathogenesis of obesity and cardiovascular risk. Endocr Rev. 2010;31:817–44.CrossRefPubMed
34.
go back to reference Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S, Kazzaz Z, Bornstein E, Lambotte O, Altmann D, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med. 2006;12:1365–71.CrossRefPubMed Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S, Kazzaz Z, Bornstein E, Lambotte O, Altmann D, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med. 2006;12:1365–71.CrossRefPubMed
35.
go back to reference Bukh AR, Melchjorsen J, Offersen R, Jensen JM, Toft L, Stovring H, Ostergaard L, Tolstrup M, Sogaard OS. Endotoxemia is associated with altered innate and adaptive immune responses in untreated HIV-1 infected individuals. PLoS ONE. 2011;6:e21275.CrossRefPubMedPubMedCentral Bukh AR, Melchjorsen J, Offersen R, Jensen JM, Toft L, Stovring H, Ostergaard L, Tolstrup M, Sogaard OS. Endotoxemia is associated with altered innate and adaptive immune responses in untreated HIV-1 infected individuals. PLoS ONE. 2011;6:e21275.CrossRefPubMedPubMedCentral
36.
go back to reference Carvalho BM, Oliveira AG, Ueno M, Araújo TG, Guadagnini D, Carvalho-Filho MA, Geloneze B, Lima MM, Pareja JC, Carvalheira JB, Saad MJ. Modulation of double-stranded RNA-activated protein kinase in insulin sensitive tissues of obese humans. Obesity. 2013;21:2452–7.CrossRefPubMed Carvalho BM, Oliveira AG, Ueno M, Araújo TG, Guadagnini D, Carvalho-Filho MA, Geloneze B, Lima MM, Pareja JC, Carvalheira JB, Saad MJ. Modulation of double-stranded RNA-activated protein kinase in insulin sensitive tissues of obese humans. Obesity. 2013;21:2452–7.CrossRefPubMed
37.
go back to reference Haugaard SB, Andersen O, Hansen BR, Andersen UB, Volund A, Iversen J, Nielsen JO, Madsbad S. In nondiabetic, human immunodeficiency virus-infected patients with lipodystrophy, hepatic insulin extraction and posthepatic insulin clearance rate are decreased in proportion to insulin resistance. Metabolism. 2005;54:171–9.CrossRefPubMed Haugaard SB, Andersen O, Hansen BR, Andersen UB, Volund A, Iversen J, Nielsen JO, Madsbad S. In nondiabetic, human immunodeficiency virus-infected patients with lipodystrophy, hepatic insulin extraction and posthepatic insulin clearance rate are decreased in proportion to insulin resistance. Metabolism. 2005;54:171–9.CrossRefPubMed
38.
go back to reference Chu JW, Abbasi F, Beatty GW, Khalili M, Koch J, Rosen A, Schmidt JM, Stansell JD, Reaven GM. Methods for quantifying insulin resistance in human immunodeficiency virus-positive patients. Metabolism. 2003;52:858–61.CrossRefPubMed Chu JW, Abbasi F, Beatty GW, Khalili M, Koch J, Rosen A, Schmidt JM, Stansell JD, Reaven GM. Methods for quantifying insulin resistance in human immunodeficiency virus-positive patients. Metabolism. 2003;52:858–61.CrossRefPubMed
39.
go back to reference McLaughlin T, Abbasi F, Cheal K, Chu J, Lamendola C, Reaven G. Use of metabolic markers to identify overweight individuals who are insulin resistant. Ann Intern Med. 2003;139:802–9.CrossRefPubMed McLaughlin T, Abbasi F, Cheal K, Chu J, Lamendola C, Reaven G. Use of metabolic markers to identify overweight individuals who are insulin resistant. Ann Intern Med. 2003;139:802–9.CrossRefPubMed
40.
go back to reference McLaughlin T, Reaven G, Abbasi F, Lamendola C, Saad M, Waters D, Simon J, Krauss RM. Is there a simple way to identify insulin-resistant individuals at increased risk of cardiovascular disease? Am J Cardiol. 2005;96:399–404.CrossRefPubMed McLaughlin T, Reaven G, Abbasi F, Lamendola C, Saad M, Waters D, Simon J, Krauss RM. Is there a simple way to identify insulin-resistant individuals at increased risk of cardiovascular disease? Am J Cardiol. 2005;96:399–404.CrossRefPubMed
41.
42.
go back to reference Mosoian A, Zhang L, Hong F, Cunyat F, Rahman A, Bhalla R, Panchal A, Saiman Y, Fiel MI, Florman S, et al. Frontline Science: HIV infection of Kupffer cells results in an amplified proinflammatory response to LPS. J Leukoc Biol. 2017;101:1083–90.CrossRefPubMed Mosoian A, Zhang L, Hong F, Cunyat F, Rahman A, Bhalla R, Panchal A, Saiman Y, Fiel MI, Florman S, et al. Frontline Science: HIV infection of Kupffer cells results in an amplified proinflammatory response to LPS. J Leukoc Biol. 2017;101:1083–90.CrossRefPubMed
43.
go back to reference Naidu S, Ponnampalvanar S, Kamaruzzaman SB, Kamarulzaman A. Prevalence of metabolic syndrome among people living with HIV in developing countries: a systematic review. AIDS Patient Care STDS. 2017;31:1–13.CrossRefPubMed Naidu S, Ponnampalvanar S, Kamaruzzaman SB, Kamarulzaman A. Prevalence of metabolic syndrome among people living with HIV in developing countries: a systematic review. AIDS Patient Care STDS. 2017;31:1–13.CrossRefPubMed
45.
go back to reference Sun L, Yu Z, Ye X, Zou S, Li H, Yu D, Wu H, Chen Y, Dore J, Clement K, et al. A marker of endotoxemia is associated with obesity and related metabolic disorders in apparently healthy Chinese. Diabetes Care. 2010;33:1925–32.CrossRefPubMedPubMedCentral Sun L, Yu Z, Ye X, Zou S, Li H, Yu D, Wu H, Chen Y, Dore J, Clement K, et al. A marker of endotoxemia is associated with obesity and related metabolic disorders in apparently healthy Chinese. Diabetes Care. 2010;33:1925–32.CrossRefPubMedPubMedCentral
46.
go back to reference Schaffler A, Scholmerich J. Innate immunity and adipose tissue biology. Trends Immunol. 2010;31:228–35.CrossRefPubMed Schaffler A, Scholmerich J. Innate immunity and adipose tissue biology. Trends Immunol. 2010;31:228–35.CrossRefPubMed
47.
go back to reference Cani PDAJ, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, Waget A, Delmee E, Cousin B, Sulpice T, Chamontin B, Ferrieres J, Tanti JF, Gibson GR, Casteilla L, Delzenne NM, Alessi MC, Burcelin R. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007;56:1761–72.CrossRefPubMed Cani PDAJ, Iglesias MA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, Waget A, Delmee E, Cousin B, Sulpice T, Chamontin B, Ferrieres J, Tanti JF, Gibson GR, Casteilla L, Delzenne NM, Alessi MC, Burcelin R. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007;56:1761–72.CrossRefPubMed
48.
go back to reference Creely SJ, McTernan PG, Kusminski CM, Fisher FM, Da Silva NF, Khanolkar M, Evans M, Harte AL, Kumar S. Lipopolysaccharide activates an innate immune system response in human adipose tissue in obesity and type 2 diabetes. Am J Physiol Endocrinol Metab. 2007;292:E740–7.CrossRefPubMed Creely SJ, McTernan PG, Kusminski CM, Fisher FM, Da Silva NF, Khanolkar M, Evans M, Harte AL, Kumar S. Lipopolysaccharide activates an innate immune system response in human adipose tissue in obesity and type 2 diabetes. Am J Physiol Endocrinol Metab. 2007;292:E740–7.CrossRefPubMed
49.
go back to reference Kelesidis T, Kendall MA, Yang OO, Hodis HN, Currier JS. Biomarkers of microbial translocation and macrophage activation: association with progression of subclinical atherosclerosis in HIV-1 infection. J Infect Dis. 2012;206:1558–67.CrossRefPubMedPubMedCentral Kelesidis T, Kendall MA, Yang OO, Hodis HN, Currier JS. Biomarkers of microbial translocation and macrophage activation: association with progression of subclinical atherosclerosis in HIV-1 infection. J Infect Dis. 2012;206:1558–67.CrossRefPubMedPubMedCentral
50.
go back to reference Blodget E, Shen C, Aldrovandi G, Rollie A, Gupta SK, Stein JH, Dube MP. Relationship between microbial translocation and endothelial function in HIV infected patients. PLoS ONE. 2012;7:e42624.CrossRefPubMedPubMedCentral Blodget E, Shen C, Aldrovandi G, Rollie A, Gupta SK, Stein JH, Dube MP. Relationship between microbial translocation and endothelial function in HIV infected patients. PLoS ONE. 2012;7:e42624.CrossRefPubMedPubMedCentral
51.
go back to reference Mora S, Otvos JD, Rifai N, Rosenson RS, Buring JE, Ridker PM. Lipoprotein particle profiles by nuclear magnetic resonance compared with standard lipids and apolipoproteins in predicting incident cardiovascular disease in women. Circulation. 2009;119:931–9.CrossRefPubMedPubMedCentral Mora S, Otvos JD, Rifai N, Rosenson RS, Buring JE, Ridker PM. Lipoprotein particle profiles by nuclear magnetic resonance compared with standard lipids and apolipoproteins in predicting incident cardiovascular disease in women. Circulation. 2009;119:931–9.CrossRefPubMedPubMedCentral
52.
go back to reference Ford MA, McConnell JP, Lavi S, Rihal CS, Prasad A, Sandhu GS, Hartman SJ, Lerman LO, Lerman A. Coronary artery endothelial dysfunction is positively correlated with low density lipoprotein and inversely correlated with high density lipoprotein subclass particles measured by nuclear magnetic resonance spectroscopy. Atherosclerosis. 2009;207:111–5.CrossRefPubMedPubMedCentral Ford MA, McConnell JP, Lavi S, Rihal CS, Prasad A, Sandhu GS, Hartman SJ, Lerman LO, Lerman A. Coronary artery endothelial dysfunction is positively correlated with low density lipoprotein and inversely correlated with high density lipoprotein subclass particles measured by nuclear magnetic resonance spectroscopy. Atherosclerosis. 2009;207:111–5.CrossRefPubMedPubMedCentral
53.
go back to reference Duprez DA, Kuller LH, Tracy R, Otvos J, Cooper DA, Hoy J, Neuhaus J, Paton NI, Friis-Moller N, Lampe F, et al. Lipoprotein particle subclasses, cardiovascular disease and HIV infection. Atherosclerosis. 2009;207:524–9.CrossRefPubMedPubMedCentral Duprez DA, Kuller LH, Tracy R, Otvos J, Cooper DA, Hoy J, Neuhaus J, Paton NI, Friis-Moller N, Lampe F, et al. Lipoprotein particle subclasses, cardiovascular disease and HIV infection. Atherosclerosis. 2009;207:524–9.CrossRefPubMedPubMedCentral
Metadata
Title
Plasma levels of lipopolysaccharide correlate with insulin resistance in HIV patients
Authors
Marcelo Nardi Pedro
Daniela Oliveira Magro
Elizabete Urbano Pinaço Pinto da Silva
Dioze Guadagnini
Andrey Santos
Rogerio de Jesus Pedro
Mario José Abdalla Saad
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Diabetology & Metabolic Syndrome / Issue 1/2018
Electronic ISSN: 1758-5996
DOI
https://doi.org/10.1186/s13098-018-0308-7

Other articles of this Issue 1/2018

Diabetology & Metabolic Syndrome 1/2018 Go to the issue