Evaluation of Advanced Glycation End Products and Malondialdehyde in Type II Diabetes Patients with and without Periodontitis: A Cross-sectional Study
Bharathi A Kumar, Nina Shenoy, Kolluru S Chandra, Dipanjan Das
Keywords :
Chronic periodontitis, Glycemic control, Oxidative stress, Type II diabetes mellitus
Citation Information :
Kumar BA, Shenoy N, Chandra KS, Das D. Evaluation of Advanced Glycation End Products and Malondialdehyde in Type II Diabetes Patients with and without Periodontitis: A Cross-sectional Study. World J Dent 2024; 15 (8):721-727.
Aim: The present study aimed to compare the serum levels of advanced glycation end products (AGEs), malondialdehyde (MDA), and glycated hemoglobin (HbA1c) in type II diabetes patients (T2DM) with and without periodontitis.
Materials and methods: This cross-sectional study included 68 patients diagnosed with T2DM divided into two groups, with 34 chronic periodontitis [type II diabetes mellitus with periodontitis (T2DM-P)] and 34 periodontally healthy [type II diabetes mellitus without periodontitis (T2DM-H)], and their periodontal status was assessed. A commercially available ELISA kit was used to estimate serum AGEs levels. Serum MDA levels were determined using TCA–TBA–HCl reagents. Statistical significance was set at p < 0.05. Continuous data were compared between the groups using an unpaired t-test, and categorical data were analyzed using the Chi-squared test. The correlation between variables in both groups was assessed using Pearson's correlation.
Results: Periodontal clinical parameters [full mouth plaque score (FMPS), full mouth bleeding score (FMBS), probing depth (PD), clinical attachment level (CAL)] were significantly higher in the T2DM-P group when compared to the T2DM-H group. T2DM-P patients exhibited a significantly higher level of serum AGEs (p = 0.000) and HbA1c (p = 0.029) when compared to T2DM-H patients. No significant difference was found between the two study groups in terms of serum MDA. In the T2DM-P group, a statistically significant low positive correlation was exhibited by serum AGEs with FMPS (r = 0.440, p = 0.009) and FMBS (r = 0.457, p = 0.007) and HbA1c with CAL (r = 0.346, p = 0.045). HbA1c exhibited a low positive correlation with FMPS (r = 0.495, p = 0.003) and FMBS (r = 0.457, p = 0.007), which was statistically significant in the T2DM-H group. A negligible correlation was found between the other variables.
Conclusion: The study concluded that T2DM-P patients exhibited elevated levels of serum AGEs and HbA1c compared to T2DM-H, suggesting a possible relationship between periodontitis and exacerbated chronic inflammation in T2DM.
Clinical significance: This study underscores the bidirectional influence of chronic periodontitis and diabetes mellitus (DM), as evidenced by changes in inflammatory markers and glycemic control. Hence, optimal periodontal health could play a critical role in maintaining glycemic control among DM patients.
Slots J. Periodontitis: facts, fallacies and the future. Periodontol 2000 2017;75(1):7–23. DOI: 10.1111/prd.12221
Papapanou PN, Sanz M, Buduneli N, et al. Periodontitis: consensus report of workgroup 2 of the 2017 World Workshop on the classification of periodontal and peri-implant diseases and conditions. J Periodontol 2018;89(Suppl 1):S173–S182. DOI: 10.1002/JPER.17-0721
Genco RJ, Sanz M. Clinical and public health implications of periodontal and systemic diseases: an overview. Periodontol 2000 2020;83(1):7–13. DOI: 10.1111/prd.12344
Löe H. Periodontal disease. The complication of diabetes mellitussixth. Diabetes Care 1993;16(1):329–334. DOI: 10.2337/diacare.16.1.329
Barutta F, Bellini S, Durazzo M, et al. Novel insight into the mechanisms of the bidirectional relationship between diabetes and periodontitis. Biomedicines 2022;10(1):178. DOI: 10.3390/biomedicines10010178
Ganesan SM, Joshi V, Fellows M, et al. A tale of two risks: smoking, diabetes, and the subgingival microbiome. ISME J 2017;11(9):2075–2089. DOI: 10.1038/ismej.2017.73
Tonetti MS, Greenwell H, Kornman KS. Staging and grading of periodontitis: framework and proposal of a new classification and case definition. J Periodontol 2018;89(Suppl 1):S159–S172. DOI: 10.1002/JPER.18-0006
Taylor GW. Bidirectional interrelationships between diabetes and periodontal diseases: an epidemiologic perspective. Ann Periodontol 2001;6(1):99–112. DOI: 10.1902/annals.2001.6.1.99
Monea A, Mezei T, Popsor S, et al. Oxidative stress: a link between diabetes mellitus and periodontal disease. Int J Endocrinol 2014;2014:917631. DOI: 10.1155/2014/917631
Sharifi-Rad M, Anil Kumar NV, Zucca P, et al. Lifestyle, oxidative stress, and antioxidants: back and forth in the pathophysiology of chronic diseases. Front Physiol 2020;11:694. DOI: 10.3389/fphys.2020.00694
Mirnic J, Djuric M, Veljovic T, et al. Evaluation of lipid peroxidation in the saliva of diabetes mellitus type 2 patients with periodontal disease. Biomedicines 2022;10(12):3147. DOI: 10.3390/biomedicines10123147
Plemmenos G, Piperi C. Pathogenic molecular mechanisms in periodontitis and peri-implantitis: role of advanced glycation end products. Life (Basel) 2022;12(2):218. DOI: 10.3390/life12020218
Chen Y, Ji Y, Jin X, et al. Mitochondrial abnormalities are involved in periodontal ligament fibroblast apoptosis induced by oxidative stress. Biochem Biophys Res Commun 2019;509(2):483–490. DOI: 10.1016/j.bbrc.2018.12.143
Su LJ, Zhang JH, Gomez H, et al. Reactive oxygen species-induced lipid peroxidation in apoptosis, autophagy, and ferroptosis. Oxid Med Cell Longev 2019;2019:5080843. DOI: 10.1155/2019/5080843
de M Bandeira de S, da S Guedes G, da Fonseca LJS, et al. Characterization of blood oxidative stress in type 2 diabetes mellitus patients: increase in lipid peroxidation and SOD activity. Oxid Med Cell Longev 2012;2012:819310. DOI: 10.1155/2012/819310
Salgueiro ACF, Leal CQ, Bianchini MC, et al. The influence of Bauhinia forficata Link subsp. pruinosa tea on lipid peroxidation and non-protein SH groups in human erythrocytes exposed to high glucose concentrations. J Ethnopharmacol 2013;148(1):81–87. DOI: 10.1016/j.jep.2013.03.070
Del Rio D, Stewart AJ, Pellegrini N. A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr Metab Cardiovasc Dis 2005;15(4):316–328. DOI: 10.1016/j.numecd.2005.05.003
Tsikas D. Assessment of lipid peroxidation by measuring malondialdehyde (MDA) and relatives in biological samples: analytical and biological challenges. Anal Biochem 2017;524:13–30. DOI: 10.1016/j.ab.2016.10.021
Polak D, Shapira L. An update on the evidence for pathogenic mechanisms that may link periodontitis and diabetes. J Clin Periodontol 2018;45(2):150–166. DOI: 10.1111/jcpe.12803
Sherwani SI, Khan HA, Ekhzaimy A, et al. Significance of HbA1c test in diagnosis and prognosis of diabetic patients. Biomark Insights 2016;11:95–104. DOI: 10.4137/BMI.S38440
Banjar A, Alyafi R, AlGhamdi A, et al. The relationship between glycated hemoglobin level and the stage of periodontitis in individuals without diabetes. PLoS One 2023;18(1):e0279755. DOI: 10.1371/journal.pone.0279755
Takeda M, Ojima M, Yoshioka H, et al. Relationship of serum advanced glycation end products with deterioration of periodontitis in type 2 diabetes patients. J Periodontol 2006;77(1):15–20. DOI: 10.1902/jop.2006.77.1.15
American Diabetes Association. Standards of Medical Care in Diabetes-2022 abridged for primary care providers. Clin Diabetes 2022;40(1):10–38. DOI: 10.2337/cd22-as01
Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol 1999;4:1–6. DOI: 10.1902/annals.1999.4.1.1
O'Leary TJ, Drake RB, Naylor JE. The plaque control record. J Periodontol 1972;43(1):38. DOI: 10.1902/jop.1972.43.1.38
Ainamo J, Bay I. Problems and proposals for recording gingivitis and plaque. Int Dent J 1975;25(4):229–235. PMID: 1058834.
Newman MG, Takei H, Klokkevold PR, Carranza FA (Eds). Carranza's Clinical Periodontology, 13th edition. São Paulo: Elsevier; 2018.
Zhao M, Xie Y, Gao W, et al. Diabetes mellitus promotes susceptibility to periodontitis—novel insight into the molecular mechanisms. Front Endocrinol(Lausanne) 2023;14:1192625. DOI: 10.3389/fendo.2023.1192625
Hussein LK, Mohammed AN. Assessment of serum advanced glycation end-product level and its effect on periodontal health status in type 2 diabetic patients with chronic periodontitis. Indian J Forensic Med Toxicol 2020;14(1):2839–2845. DOI: 10.37506/v14/i1/2020/ijfmt/192968
Chávarry NGM, Vettore MV, Sansone C, et al. The relationship between diabetes mellitus and destructive periodontal disease: a meta-analysis. Oral Health Prev Dent 2009;7(2):107–127. DOI: 10.3290/j.ohpd.a15518
Son A, Pera C, Ueda P, et al. Clinical effects of supragingival plaque control on uncontrolled type 2 diabetes mellitus subjects with chronic periodontitis. Braz J Oral Sci 2012;11(1):47–52. DOI: 10.20396/bjos.v11i1.8641556
Grossi SG, Genco RJ. Periodontal disease and diabetes mellitus: a two-way relationship. Ann Periodontol 1998;3(1):51–61. DOI: 10.1902/annals.1998.3.1.51
Patil VS, Patil VP, Gokhale N, et al. Chronic periodontitis in type 2 diabetes mellitus: oxidative stress as a common factor in periodontal tissue injury. J Clin Diagn Res 2016;10(4):BC12. DOI: 10.7860/JCDR/2016/17350.7542
Yamagishi SI, Maeda S, Matsui T, et al. Role of advanced glycation end products (AGEs) and oxidative stress in vascular complications in diabetes. Biochim Biophys Acta 2012;1820(5):663–671. DOI: 10.1016/j.bbagen.2011.03.014
Altıngöz SM, Kurgan Ş, Önder C, et al. Salivary and serum oxidative stress biomarkers and advanced glycation end products in periodontitis patients with or without diabetes: a cross-sectional study. J Periodontol 2021;92(9):1274–1285. DOI: 10.1002/JPER.20-0406
Trivedi S, Lal N, Mahdi AA, et al. Evaluation of antioxidant enzymes activity and malondialdehyde levels in patients with chronic periodontitis and diabetes mellitus. J Periodontol 2014;85(5):713–720. DOI: 10.1902/jop.2013.130066
Rahim A, Hassan S, Ullah N, et al. Association and comparison of periodontal and oral hygiene status with serum HbA1c levels: a cross-sectional study. BMC Oral Health 2023;23(1):442. DOI: 10.1186/s12903-023-03042-7
Graziani F, Gennai S, Solini A, et al. A systematic review and meta-analysis of epidemiologic observational evidence on the effect of periodontitis on diabetes. An update of the EFP-AAP review. J Clin Periodontol 2018;45(2):167–187. DOI: 10.1111/jcpe.12837
Borgnakke WS, Ylöstalo PV, Taylor GW, et al. Effect of periodontal disease on diabetes: systematic review of epidemiologic observational evidence. J Periodontol 2013;84:S135–S152. DOI: 10.1902/jop.2013.1340013
Latha N, Uppoor A, Nayak SU, et al. Effect of non-surgical therapy on salivary nitric oxide and lipid peroxidation levels in type II diabetic and non-diabetic patients with periodontal disease. Asian J Pharm Clin Res 2018;11(8):330–336. DOI: 10.22159/ajpcr.2018.v11i8.25554