Association between Glycated Hemoglobin with the Levels of Serum Proinflammatory Cytokines and Antioxidants in Patients with Type 2 Diabetes Mellitus in Universitas Sumatera Utara Hospital


  • Mutiara Indah Sari Departement of Biochemistry, Faculty of Medicine, Universitas Sumatera Utara, Jl. Dr Mansur No.5 Medan, Indonesia
  • Zaimah Z. Tala Departement of Clinical Nutrition, Faculty of Medicine, Universitas Sumatera Utara, Jl. Dr Mansur No.5 Medan, Indonesia
  • Dian Dwi Wahyuni Departement of Microbiology, Faculty of Medicine, Universitas Sumatera Utara, Jl. Dr Mansur No.5 Medan, Indonesia



Glycated Hemoglobin, Interleukin-6, Glutathione peroxidase, Glutathione, T2DM


BACKGROUND: Hyperglycemia condition in diabetes mellitus (DM) influences proinflammatory cytokine levels and disrupts antioxidant balances. Glycated Hemoglobin is used as a biomarker of glycemic control in DM.

AIM: This study aimed to analyse the association between glycated Hemoglobin with the levels of serum proinflammatory cytokines (interleukin (IL)-6) and antioxidants (glutathione peroxidase (GPx) and glutathione (GSH)) in type 2 diabetes mellitus (T2DM) patients in Universitas Sumatera Utara (USU) Hospital.

METHODS: A total of eighty-nine T2DM patients were recruited at USU Hospital. Glycated Hemoglobin levels were measured using routine laboratory tests at USU Hospital. The IL-6, GPx, and GSH levels were measured using enzyme-linked immunosorbent (ELISA) method. The statistical significance was determined using the Kruskal Wallis test, followed by Mann-Whitney test (p < 0.05).

RESULTS: The mean of glycated hemoglobin (%), IL-6 (pg/ml), GPx (ng/ml), and GSH (ng/ml) levels in T2DM patients were 8.96 ± 2.28, 59.27 ± 16.04, 32.13 ± 12.10, and 7.42 ± 3.50, respectively. Regarding the glycated Hemoglobin levels, 28.09% of patients had controlled diabetes, 24.72% of patients had poorly controlled diabetes, and 47.19% of patients had uncontrolled diabetes. The IL-6 levels of the three study groups based on glycated Hemoglobin levels were related significantly (p < 0.05), but there was no statistically significant difference observed between the GPx and GSH levels (p > 0.05).

CONCLUSION: The present study suggests that the glycated Hemoglobin was associated with the levels of serum IL-6 levels but not GPx and GSH levels in T2DM patients in USU Hospital.


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American Diabetes Association/ ADA. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2014; 37(SUPPL.1):81-90.

World Health Organization. Global Report on Diabetes, Geneva. 2016; 978:1-88.

International Diabetic Federation. IDF Diabetic Atlas. Chapter 3, Eighth edition. 2017; (19): 43-46.

Badan Penelitian dan Pengembangan Kesehatan Kementrian Kesehatan Republik Indonesia 2013. RISET KESEHATAN DASAR Jakarta, 2013: 87.

Matough FA, Budin SB, Hamid ZA, Alwahaibi N, Mohamed J. Athe Role of Oxidative Stress and Antioxidants in Diabetic Complications. SQU Med J. 2012; 12(February):5–18.

Tiwari BK, Pandey KB, Abidi AB, Rizvi SI. Markers of oxidative stress during diabetes mellitus. Journal of biomarkers. 2013; 2013.

Wang X, Bao W, Liu J, OuYang Y-Y, Wang D, Rong S, Xiao X, Shan Z-L, Zhang Y, Yao P, and Liu L-G. Inflammatory Markers and Risk of Type 2 Diabetes: A systematic review and meta-analysis. Diabetes Care. 2013; 36(1):166–75. PMid:23264288 PMCid:PMC3526249

Al-Shukaili A, Al-Ghafri S, Al-Marhoobi S, Al-Abri S, Al-Lawati J, Al-Maskari M. Analysis of inflammatory mediators in type 2 diabetes patients. Int J Endocrinol. 2013; 8–10.

Jelinek HF, Stranieri A, Yatsko A, Venkatraman S. Data analytics identify glycated Hemoglobin co-markers for type 2 diabetes mellitus diagnosis. Comput Biol Med. 2016; 75:90–7. PMid:27268735

Flier JS and Maratos-Flier E. 'Biology of Obesity' at Harrison's Principle of Internal Medicine, ed. Kasper DL, Fauci AS, Hauser SL, Longo DL, Jameson JL, Loscalzo J. 18th edn, McGraw-Hill Education, 2010:622-629.

Kharroubi AT, Darwish HM, Akkawi MA, Ashareef AA, Almasri ZA, Bader KA, Khammash UM. Total Antioxidant Status in Type 2 Diabetic Patients in Palestine. J Diabetes Res. 2015; 2015:461271. PMid:26090472 PMCid:PMC4458273

Aouacheri O, Saka S, Krim M, Messaadia A, Maidi I. The Investigation of the Oxidative Stress-Related Parameters in Type2 Diabetes Mellitus. Can J Diabetes. 2015; 39(1):44–9. PMid:25065473

Gawlik K, Naskalski JW, Fedak D, Pawlica-Gosiewska D, Grudzień U, Dumnicka P, Małecki MT, Solnica B. Markers of Antioxidant Defense in Patients with Type 2 Diabetes. Oxid Med Cell Longev. 2016; 2016:2352361. PMid:26640613 PMCid:PMC4657103

Lubos E, Loscalzo J, Handy DE. Glutathione Peroxidase-1 in Health and Disease: From Molecular Mechanisms to Therapeutic Opportunities. Antioxid Redox Signal. 2011;15(7):1957–97. PMid:21087145 PMCid:PMC3159114

Deponte M. Glutathione catalysis and the reaction mechanisms of glutathione-dependent enzymes. Biochim Biophys Acta. 2013; 1830(5):3217-66. PMid:23036594

Perkeni PB. Konsensus pengelolaan dan pencegahan diabetes melitus tipe 2 di Indonesia. Jakarta: PB Perkeni, 2015:78.

Aldasouqi SA, Gossain VV. Hemoglobin A1c: past, present and future. Annals of Saudi medicine. 2008; 28(6):411-9.

Qiao YC, Shen J, He L, Hong XZ, Tian F, Pan YH, Liang L, Zhang XX, Zhao HL. Changes of Regulatory T Cells and of Proinflammatory and Immunosuppressive Cytokines in Patients with Type 2 Diabetes Mellitus: A Systematic Review and Meta-Analysis. J Diabetes Res. 2016; 2016:3694957. PMid:27777959 PMCid:PMC5061980

Ankush RD, Kulkarni DG. Erythrocyte reduced glutathione level in type -2 diabetic patients with and without nephropathy. 2017; 13(3):253–60.

Sherwani SI, Khan HA, Ekhzaimy A, Masood A, Sakharkar MK. Significance of HbA1c test in diagnosis and prognosis of diabetic patients. Biomark Insights. 2016; 11:95–104. PMid:27398023 PMCid:PMC4933534

Cavero-Redondo I, Peleteiro B, Ãlvarez-Bueno C, Rodriguez-Artalejo F, Martínez-Vizcaíno V. Glycated Hemoglobin A1c as a risk factor of cardiovascular outcomes and all-cause mortality in diabetic and non-diabetic populations: A systematic review and meta-analysis. BMJ Open. 2017; 7(7):1–12.

Khatab M, Khader YS, Al-Khawaldeh A, Ajlouni K. Factors associated with poor glycemic control among patients with Type 2 diabetes. Journal of Diabetes and its Complications. 2010; 24(2).

Almalki NR, Almalki TM, Alswat K. Diabetics retinopathy knowledge and awareness assessment among the type 2 diabetics. Open access Macedonian journal of medical sciences. 2018; 6(3):574-7. PMid:29610623 PMCid:PMC5874388

Haghighatpanah M, Nejad ASM, Haghighatpanah M, Thunga G, Mallayasamy S. Factors that Correlate with Poor Glycemic Control in Type 2 Diabetes Mellitus Patients with Complications. Osong Public Heal Res Perspect. 2018; 9(4):167–74. PMid:30159222 PMCid:PMC6110332

Asmat U, Abad K, Ismail K. Diabetes mellitus and oxidative stress—A concise review. Saudi Pharm J. 2016; 24(5):547–53. PMid:27752226 PMCid:PMC5059829

Volpe CMO, Villar-Delfino PH, Dos Anjos PMF, Nogueira-Machado JA. Cellular death, reactive oxygen species (ROS) and diabetic complications review-Article. Cell Death Dis. 2018; 9(2). PMid:29371661 PMCid:PMC5833737

Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O. Oxidative stress and antioxidant defense. World Allergy Organ J. 2012; 5(1):9–19. PMid:23268465 PMCid:PMC3488923

Sari MI, Ilyas S, Widyawati T, Antika MA. Effect of lawsonia innermis (linn) leaves ethanolic extract on blood glucose and malondialdehyde level in alloxan-induced diabetic rats. IOP Conf Ser Earth Environ Sci. 2018; 130(1).

Sharma M, Arora M, Mustafa I, Kumar S, Mittal A, Soam SS, Shukla C. Correlation of Glycated Hemoglobin with Oxidative Stress and Erythrocyte Fragility in Type-2 Diabetes Mellitus. Journal of Contemporary Medical Research. 2017; 4(9):1909-11.

Tanaka T, Narazaki M, Kishimoto T. IL-6 in inflammation, immunity, and disease. Cold Spring Harbor perspectives in biology. 2014; 6(10):a016295. PMid:25190079 PMCid:PMC4176007

Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S. The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochim Biophys Acta - Mol Cell Res. 2011; 1813(5):878–88. PMid:21296109

Ates I. Type 2 diabetes mechanisms, role of cytokines and their variations in disease development. Fabad J Pharm Sci. 2018; 43(1):31–40.

Barakat L, Shora H, El-Deen I, El-Sayed E-S. Inflammatory Biomarkers of Cardiometabolic Risk in Obese Egyptian Type 2 Diabetics. Med Sci. 2017; 5(4):25.

Hisalkar P, Patne A, Fawade M, Karnik A. Evaluation of plasma superoxide dismutase and glutathione peroxidase in type 2 diabetic patients Biology and Medicine. Biol Med. 2012; 4(2):65–72

Lutchmansingh FK, Hsu JW, Bennett FI, Badaloo A V., Norma MA, Georgiana MGS, et al. Glutathione metabolism in type 2 diabetes and its relationship with microvascular complications and glycemia. PLoS One. 2018; 13(6):1–12. PMid:29879181 PMCid:PMC5991679

Wong FN, Chua KH, Tan JAMA, Wong CM, Kuppusamy UR. Glycaemic control in type 2 diabetic patients with chronic kidney disease: the impacts on enzymatic antioxidants and soluble RAGE. PeerJ. 2018; 6:e4421. PMid:29610703 PMCid:PMC5880175

Pieme CA, Tatangmo JA, Simo G, Biapa Nya PC, Ama Moor VJ, Moukette Moukette B, et al. Relationship between hyperglycemia, antioxidant capacity and some enzymatic and non-enzymatic antioxidants in African patients with type 2 diabetes. BMC Res Notes. 2017; 10(1):1–7. PMid:28356165 PMCid:PMC5372257

Kalkan IH, Suher M. The relationship between the level of glutathione, impairment of glucose metabolism and complications of diabetes mellitus. Pakistan J Med Sci. 2013; 29(4):938–42.

Salmon AB. Oxidative stress in the etiology of age-associated decline in glucose metabolism. Longev Heal. 2012; 1(1):7. PMid:24764512 PMCid:PMC3922939



How to Cite

Sari MI, Tala ZZ, Wahyuni DD. Association between Glycated Hemoglobin with the Levels of Serum Proinflammatory Cytokines and Antioxidants in Patients with Type 2 Diabetes Mellitus in Universitas Sumatera Utara Hospital. Open Access Maced J Med Sci [Internet]. 2019 Mar. 10 [cited 2024 Apr. 21];7(5):715-20. Available from:



A - Basic Science

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