Cited by 1,961Adipokines, Inflammation, and Metabolic DiseasesAdvanced Glycation End Products researchDiabetes Management and Research

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Inflammatory Cytokine Concentrations Are Acutely Increased by Hyperglycemia in Humans: Role of Oxidative Stress

Esposito, Katherine, Nappo, Francesco, Marfella, Raffaele, Giugliano, Giovanni, Giugliano, Francesco, Ciotola, Myriam, Quagliaro, Lisa, Ceriello, Antonio, Giugliano, Dario·2002·Circulation

DOI 10.1161/01.cir.0000034509.14906.ae

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Abstract

Background— Circulating levels of interleukin-6 (IL-6) and tumor necrosis factor-α (TNF-α) are elevated in diabetic patients. We assessed the role of glucose in the regulation of circulating levels of IL-6, TNF-α, and interleukin-18 (IL-18) in subjects with normal or impaired glucose tolerance (IGT), as well as the effect of the antioxidant glutathione. Methods and Results— Plasma glucose levels were acutely raised in 20 control and 15 IGT subjects and maintained at 15 mmol/L for 5 hours while endogenous insulin secretion was blocked with octreotide. In control subjects, plasma IL-6, TNF-α, and IL-18 levels rose ( P <0.01) within 2 hours of the clamp and returned to basal values at 3 hours. In another study, the same subjects received 3 consecutive pulses of intravenous glucose (0.33 g/kg) separated by a 2-hour interval. Plasma cytokine levels obtained at 3, 4, and 5 hours were higher ( P <0.05) than the corresponding values obtained during the clamp. The IGT subjects had fasting plasma IL-6 and TNF-α levels higher ( P <0.05) than those of control subjects. The increase in plasma cytokine levels during the clamping lasted longer (4 hours versus 2 hours, P <0.01) in the IGT subjects than in the control subjects, and the cytokine peaks of IGT subjects after the first glucose pulse were higher ( P <0.05) than those of control subjects. On another occasion, 10 control and 8 IGT subjects received the same glucose pulses as above during an infusion of glutathione; plasma cytokine levels did not show any significant change from baseline after the 3 glucose pulses. Conclusions— Hyperglycemia acutely increases circulating cytokine concentrations by an oxidative mechanism, and this effect is more pronounced in subjects with IGT. This suggests a causal role for hyperglycemia in the immune activation of diabetes.

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Background
Stress Induced Hyperglycemia in the Context of Acute Coronary Syndrome: Definitions, Interventions, and Underlying Mechanisms
Li, M., Chen, G., Feng, Y., & He, X. (2021) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2021.676892 · Cited by 40
Postmortem diagnosis of unsuspected diabetes mellitus
Palmière, C., Bardy, D., Mangin, P. J., & Werner, D. (2013) · Forensic Science International · doi:10.1016/j.forsciint.2013.01.004 · Cited by 42
“These markers included CRP, high sensitivity CRP (hs-CRP), IL-6, IL10, interleukin-2 (IL-2), interleukin-4 (IL-4), interleukin-8 (IL-8), interleukin-1a (IL-1a), interleukin-1b (IL-1b) and tumor necrosis factor alpha (TNF-a) [98–113].”
Background
Effect of prior hyperglycemia on IL-6 responses to exercise in children with type 1 diabetes
Galassetti, P. R., Iwanaga, K., Pontello, A. M., Zaldivar, F. P., Flores, R. L., & Larson, J. K. (2005) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00445.2005 · Cited by 38
Antioxidative and anti-inflammatory effects of repaglinide in plasma of diabetic animals
Gumieniczek, A., Hopkała, H., Roliński, J., & Bojarska-Junak, A. A. (2005) · Pharmacological Research · doi:10.1016/j.phrs.2005.02.019 · Cited by 39
Effect of Diabetes on Tendon Structure and Function: Not Limited to Collagen Crosslinking
Vaidya, R., Lake, S. P., & Zellers, J. A. (2022) · Journal of Diabetes Science and Technology · doi:10.1177/19322968221100842 · Cited by 38
Association between Sugar-Sweetened Beverage Consumption and the Risk of the Metabolic Syndrome: A Systematic Review and Meta-Analysis
Muñoz-Cabrejas, A., Guallar‐Castillón, P., Laclaustra, M., Sandoval‐Insausti, H., & Moreno‐Franco, B. (2023) · Nutrients · doi:10.3390/nu15020430 · Cited by 46
“Moreover, the high glycemic load after SSB consumption promotes pro-inflammatory cytokines released in response to hyperglycemia [44].”
Background
High glucose-induced endothelial STING activation inhibits diabetic wound healing through impairment of angiogenesis
Luo, L., An, Y., Geng, K., Wan, S., Zhang, F., Tan, X., Jiang, Z., & Xu, Y. (2023) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2023.05.081 · Cited by 39
Arguments for and against the Role of Glucose Variability in the Development of Diabetes Complications
Kilpatrick, E. S. (2009) · Journal of Diabetes Science and Technology · doi:10.1177/193229680900300405 · Cited by 38
The Emory University Perioperative Algorithm for the Management of Hyperglycemia and Diabetes in Non-cardiac Surgery Patients
Duggan, E. W., Klopman, M. A., Berry, A. J., & Umpierrez, G. E. (2016) · Current Diabetes Reports · doi:10.1007/s11892-016-0720-z · Cited by 39
Bergenin Reduces Experimental Painful Diabetic Neuropathy by Restoring Redox and Immune Homeostasis in the Nervous System
Villarreal, C. F., Santos, D. S., Lauria, P. S. S., Gama, K. B., Santo, R. F. D. E., Juíz, P. J. L., Alves, C. Q., David, J. M., & Soares, M. B. P. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21144850 · Cited by 40
“Along with its antioxidant properties, glutathione prevents cytokine increase caused by hyperglycemia [48], which might be an additional protective mechanism, considering the wellestablished role of cytokines in maintaining painful DN.”
Background
Fructosamine is a valuable marker for glycemic control and predicting adverse outcomes following total hip arthroplasty: a prospective multi-institutional investigation
Shohat, N., Goswami, K., Breckenridge, L., Held, M. B., Malkani, A. L., Shah, R. P., Schwarzkopf, R. M., & Parvizi, J. (2021) · Scientific Reports · doi:10.1038/s41598-021-81803-6 · Cited by 38
Lipocalin-2 in Diabetic Complications of the Nervous System: Physiology, Pathology, and Beyond
Bhusal, A., Lee, W., & Suk, K. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.638112 · Cited by 37
Post-Challenge Hyperglycemia in Older Adults Is Associated with Increased Cardiovascular Risk Profile
Crandall, J. P., Shamoon, H., Cohen, H. W., Reid, M., Gajavelli, S., Trandafirescu, G. G., Tabatabaie, V., & Barzilai, N. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-1829 · Cited by 38
“Transient, acute hyperglycemia (such as occurs after an oral glucose load) has been shown to induce inflammation and oxidative stress in both diabetic and nondiabetic subjects (13, 14), but such data are not available in FIG.”
Background
Cardiac Contractile Dysfunction and Apoptosis in Streptozotocin-Induced Diabetic Rats Are Ameliorated by Garlic Oil Supplementation
Ou, H., Tzang, B., Chang, M.-H., Liu, C., Liu, H. W., Lii, C., Bau, D., Chao, P., & Kuo, W. (2010) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf101606s · Cited by 38
Potential of Cranberry Powder for Management of Hyperglycemia Using In Vitro Models
Pinto, M. D. S., Ghaedian, R., Shinde, R., & Shetty, K. (2010) · Journal of Medicinal Food · doi:10.1089/jmf.2009.0225 · Cited by 37
Changes in Circulating Postprandial Proinflammatory Cytokine Concentrations in Diet-Controlled Type 2 Diabetes and the Effect of Ingested Fat
Manning, P. J., Sutherland, W. H. F., Hendry, G., de Jong, S. A., McGrath, M., & Williams, S. (2004) · Diabetes Care · doi:10.2337/diacare.27.10.2509 · Cited by 38
“The proinflammatory cytokines interleukin (IL)-6 and tumor necrosis factor (TNF)- are thought to impair insulin signaling (1,2), and abnormally high levels of them are associated with insulin resistance (3,4) and type 2 diabetes (3,5).”
Fasting Glucose Levels in Predicting 1-Year All-Cause Mortality in Patients Who Do Not Have Diabetes and Are on Maintenance Hemodialysis
Lin‐Tan, D., Lin, J., Wang, L., Wang, L., Huang, L.-M., Liu, L., Huang, J., & Huang, Y. (2007) · Journal of the American Society of Nephrology · doi:10.1681/asn.2006121409 · Cited by 38
TNFα Dynamics During the Oral Glucose Tolerance Test Vary According to the Level of Insulin Resistance in Pregnant Women
Guillemette, L., Lacroix, M., Battista, M., Doyon, M., Moreau, J., Ménard, J., Ardilouze, J., Perron, P., & Hivert, M. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-4016 · Cited by 38
Circulating IL-18 concentration is associated with insulin sensitivity and glucose tolerance through increased fat-free mass
Bosch, M., López‐Bermejo, A., Vendrell, J. J., Musri, M. M., Ricart, W., & Fernández‐Real, J. M. (2005) · Diabetologia · doi:10.1007/s00125-005-1859-3 · Cited by 38
“Acute hyperglycaemia also led to increased plasma IL-18 in healthy volunteers [22].”
Background
Postprandial hyperglycaemia and vascular damage - the benefits of acarbose
Båvenholm, P., & Efendić, S. (2006) · Diabetes and Vascular Disease Research · doi:10.3132/dvdr.2006.017 · Cited by 41
“found that indicators of subclinical inflammation, such as the cytokines interleukin-6 (IL-6) and tumour necrosis factor-α (TNF-α), were increased to a greater degree by intravenous pulses of glucose than by a sustained period of hyperglycaemia in individuals with NGT (n=20) and IGT (n=15).(25) Octreotide was used to…”
Method
Betulinic acid accelerates diabetic wound healing by modulating hyperglycemia-induced oxidative stress, inflammation and glucose intolerance
Xie, W., Hu, W., Huang, Z., Li, M., Zhang, H., Huang, X., & Yao, P. (2022) · Burns & Trauma · doi:10.1093/burnst/tkac007 · Cited by 39
“Diabetes significantly delays wound healing, leading to several defects in the regulation of the normal healing process via consistent oxidative stress [5–7], inflammation [8] and impaired reepithelialization [9,10].”
Glycemic Control Regimens in the Prevention of Surgical Site Infections: A Meta-Analysis of Randomized Clinical Trials
Lai, J., Li, Q., He, Y., Zou, S., Bai, X., & Rastogi, S. (2022) · Frontiers in Surgery · doi:10.3389/fsurg.2022.855409 · Cited by 37
Short-chain fatty acids as a link between diet and cardiometabolic risk: a narrative review
Birkeland, E., Gharagozlian, S., Valeur, J., & Aas, A. (2023) · Lipids in Health and Disease · doi:10.1186/s12944-023-01803-5 · Cited by 48
The Role of Inflammatory Mediators in the Pathogenesis of Obesity
Bakinowska, E., Krompiewski, M., Boboryko, D., Kiełbowski, K., & Pawlik, A. (2024) · Nutrients · doi:10.3390/nu16172822 · Cited by 42
“IL-18 levels are elevated in patients with obesity [135,136].”
Background
Decreased production of inflammatory cytokines by circulating monocytes and dendritic cells in type 2 diabetic men with atherosclerotic complications
Hernández, J. J. C., Almeida, M. D. G., Burgo, R. M., Hernández, P., Miralles, J. M., & Órfão, A. (2006) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2005.09.006 · Cited by 37
Severe Hyperglycemia Immediately After Allogeneic Hematopoietic Stem-Cell Transplantation is Predictive of Acute Graft-Versus-Host Disease
Gebremedhin, E. H., Behrendt, C. E., Nakamura, R., Parker, P. M., & Salehian, B. (2012) · Inflammation · doi:10.1007/s10753-012-9533-7 · Cited by 37
“Thus, we had access to data on MSG but not on cytokines such as IL6, IL-18, and TNF-α, which have been shown to rise after induction of hyperglycemia [16].”
Design, synthesis and biological evaluation of novel peptide MC2 analogues from Momordica charantia as potential anti-diabetic agents
Yang, B., Li, X., Zhang, C., Yan, S., Wei, W., Wang, X., Deng, X., Qian, H., Lin, H., & Huang, W. (2015) · Organic & Biomolecular Chemistry · doi:10.1039/c5ob00333d · Cited by 37
Cardioprotective Effects of Glucose and Insulin Administration While Maintaining Normoglycemia (GIN Therapy) in Patients Undergoing Coronary Artery Bypass Grafting
Carvalho, G., Pelletier, P., Albacker, T. B., Lachapelle, K. J., Joanisse, D. R., Hatzakorzian, R., Lattermann, R., Sato, H., Marette, A., & Schricker, T. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-1934 · Cited by 37
“Acute hyperglycemia adversely affects cardioprotective signal transduction pathways (13), isproinflammatory (14),andcausesvasoconstriction, platelet aggregation, and thrombosis (15).”
Background
Insulin Decreases Inflammatory Signal Transcription Factor Expression in Primary Human Liver Cells after LPS Challenge
Jeschke, M. G., Klein, D., Thasler, W. E., Bolder, U., Schlitt, H. J., Jauch, K., & Weiß, T. S. (2008) · Molecular Medicine · doi:10.2119/2007-00062.jeschke · Cited by 38
Influence of Postprandial Hyperglycemic Conditions on Arterial Stiffness in Patients With Type 2 Diabetes
Gordin, D., Saraheimo, M., Tuomikangas, J., Soro‐Paavonen, A., Forsblom, C. M., Paavonen, K., Steckel-Hamann, B., Vandenhende, F., Nicolaou, L., Pavo, I. J., et al. (2016) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2015-3635 · Cited by 38
Neuroendocrine System Regulatory Mechanisms: Acute Coronary Syndrome and Stress Hyperglycaemia
de la Hoz, R. A. P., Swieszkowski, S. P., Cintora, F. M., Aladio, M., Papini, C., Matsudo, M., & Scazziota, A. (2018) · European Cardiology Review · doi:10.15420/ecr.2017:19:3 · Cited by 37
Chronic cadmium exposure induced hepatic cellular stress and inflammation in aged female mice
Zhang, J., Wāng, Y., Fu, L., Wang, B., Ji, Y., Wang, H., & Xu, D. (2018) · Journal of Applied Toxicology · doi:10.1002/jat.3742 · Cited by 37
“An epidemiology study showed that hyperglycemia acutely increased circulating cytokine concentrations (interleukin‐6 and tumor necrosis factor alpha [TNF‐α]) by an oxidative mechanism, indicating the role of oxidative stress during the inflammatory responses (Esposito et al., 2002).”
Background
Adverse Outcomes after Major Surgeries in Patients with Diabetes: A Multicenter Matched Study
Lin, C., Chang, C., Lee, Y., Liu, C., Yeh, C., Chang, Y., Chuang, M., Chang, T., Chen, T.-L., & Liao, C. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm8010100 · Cited by 38
“The elevation of blood glucose levels might alter immune function including polymorphonuclear phagocytosis and neutrophil chemotaxis [24–26], cytokines [27,28], nitric oxide-mediated microvascular relaxation [29], and immunoglobin [30,31].”
Background
Arctium lappa contributes to the management of type 2 diabetes mellitus by regulating glucose homeostasis and improving oxidative stress: A critical review of in vitro and in vivo animal‐based studies
Annunziata, G., Barrea, L., Ciampaglia, R., Cicala, C., Arnone, A., Savastano, S., Nabavi, S. M., Tenore, G. C., & Novellino, E. (2019) · Phytotherapy Research · doi:10.1002/ptr.6416 · Cited by 39
“There is evidence that in diabetic subjects the hyperglycaemia is the main cause of oxidative stress (Esposito et al., 2002; Ganjifrockwala, Joseph & George, 2017).”
Background
Dairy Foods and Dairy Fats: New Perspectives on Pathways Implicated in Cardiometabolic Health
Hirahatake, K. M., Bruno, R. S., Bolling, B. W., Blesso, C. N., Alexander, L. M., & Adams, S. H. (2019) · Advances in Nutrition · doi:10.1093/advances/nmz105 · Cited by 37
Neopterin predicts the risk for fatal ischemic heart disease in type 2 diabetes mellitus
Vengen, I. T., Dale, A. C., Wiseth, R., Midthjell, K., & Videm, V. (2009) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2009.04.003 · Cited by 37
Plasma high sensitivity C-reactive protein and its relationship with cytokine levels in children with newly diagnosed type 1 diabetes and ketoacidosis
Karavanaki, K., Kakleas, K., Georga, S., Bartzeliotou, Α., Mavropoulos, G., Tsouvalas, M., Vogiatzi, A., Papassotiriou, I., & Karayianni, C. (2012) · Clinical Biochemistry · doi:10.1016/j.clinbiochem.2012.05.003 · Cited by 37
“Increased IL-6 production has been observed in patients with sepsis [10], non-infectious SIRS [11] and also during chronic inflammation and endothelial damage, such as in atherosclerosis [12].”
Background
Peripheral Immune Dysfunction: A Problem of Central Importance after Spinal Cord Injury
Jeffries, M. A., & Tom, V. J. (2021) · Biology · doi:10.3390/biology10090928 · Cited by 38
“Interestingly, type 2 diabetes is considered to be immune-driven yet also contributes to immunosuppression via diabetes-mediated hyperglycemia [104,105].”
Background
Biomarkers of Inflammation and Immune Function and Risk of Colorectal Cancer
García-Anguita, A., Κακούρου, Α., & Tsilidis, K. K. (2015) · Current Colorectal Cancer Reports · doi:10.1007/s11888-015-0282-5 · Cited by 36
Kolaviron Improved Resistance to Oxidative Stress and Inflammation in the Blood (Erythrocyte, Serum, and Plasma) of Streptozotocin-Induced Diabetic Rats
Ayepola, O. R., Brooks, N. L., & Oguntibeju, O. O. (2014) · The Scientific World JOURNAL · doi:10.1155/2014/921080 · Cited by 37
“Hyperglycaemia can result in elevated levels of circulating inflammatory mediators [48].”
Altered CD161bright CD8+ Mucosal Associated Invariant T (MAIT)-Like Cell Dynamics and Increased Differentiation States among Juvenile Type 1 Diabetics
Harms, R. Z., Lorenzo-Arteaga, K. M., Corley, K. P., Cabrera, M. S., & Sarvetnick, N. (2015) · PLoS ONE · doi:10.1371/journal.pone.0117335 · Cited by 38
“It is known that elevated glucose levels have been associated with the release of IL-18 among healthy individuals and those with impaired glucose tolerance [55].”
Background
Postprandial hyperglycemia and endothelial function in type 2 diabetes: focus on mitiglinide
Kitasato, L., Tojo, T., Hatakeyama, Y., Kameda, R., Hashikata, T., & Yamaoka‐Tojo, M. (2012) · Cardiovascular Diabetology · doi:10.1186/1475-2840-11-79 · Cited by 36
“Postprandial acceleration of oxidative stress and inflammation has been observed in patients with type 2 diabetes [49,55-58].”
Background
Soluble TNF Receptors and Kidney Dysfunction in the Elderly
Carlsson, A. C., Larsson, T. E., Helmersson‐Karlqvist, J., Larsson, A. O., Lind, L., & Ärnlöv, J. (2014) · Journal of the American Society of Nephrology · doi:10.1681/asn.2013080860 · Cited by 36

Authors: Esposito, K., Nappo, F., Marfella, R., Giugliano, G., Giugliano, F., Ciotola, M., Quagliaro, L., Ceriello, A., & Giugliano, D.
Affiliations: University of Udine (IT)
ORCID: Esposito, Katherine
Marfella, Raffaele
Ceriello, Antonio
Giugliano, Dario
Venue: Circulation
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2002-10-15
Volume: 106
Issue: 16
Pages: 2067-2072
ISSN: 0009-7322 (ISSN-L)
1524-4539
DOI: 10.1161/01.cir.0000034509.14906.ae
OpenAlex: W2123560318
Cited by: 1,961
References: 36
Citations by year: 2026: 57 · 2025: 69 · 2024: 88 · 2023: 95 · 2022: 106 · 2021: 91 · 2020: 102 · 2019: 83 · 2018: 86 · 2017: 70 · 2016: 87 · 2015: 112 · 2014: 99 · 2013: 102 · 2012: 101
FWCI: 38.18
Type: journal article
Language: en
Open access: closed
Locations: Circulation (publishedVersion)
PubMed (publishedVersion)
Institutional Research Information System (University of Udine) (submittedVersion)
Archivio Istituzionale della Ricerca - Università degli Studi della Campania "Luigi Vanvitelli" (submittedVersion)
Topics: Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Advanced Glycation End Products research
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Management and Research
Keywords: hyperglycemia, inflammatory cytokines, interleukin-6, TNF-α, IL-18, impaired glucose tolerance, glutathione, oxidative stress, glucose clamp
MeSH terms: Adult, Antioxidants, Blood Glucose, Diabetes Mellitus, Type 2, Female, Glucose Tolerance Test, Glutathione, Humans, Inflammation, Kinetics, Male, Tumor Necrosis Factor-alpha, Interleukin-6, Cytokines, Glucose Intolerance, Oxidative Stress, Interleukin-18

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Inflammatory Cytokine Concentrations Are Acutely Increased by Hyperglycemia in Humans: Role of Oxidative Stress

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