Assessment of Salivary Hemoglobin as Noninvasive Biomarker of Chronic Periodontitis in Type II Diabetics
Bettahalli S Avinash, Kenkere M Srinath, Basavagowda Madhu, Shivamurthy Ravindra, Appattira U Chinnappa
Keywords :
Diabetes mellitus, Periodontitis, Salivary hemoglobin, Tooth loss
Citation Information :
Avinash BS, Srinath KM, Madhu B, Ravindra S, Chinnappa AU. Assessment of Salivary Hemoglobin as Noninvasive Biomarker of Chronic Periodontitis in Type II Diabetics. World J Dent 2020; 11 (3):189-195.
Aim: The present study aimed at determining the association between salivary hemoglobin (SH) and chronic periodontitis in type II diabetic subjects and check whether SH can function as a noninvasive biomarker to assess the level of chronic periodontitis. Materials and methods: This cross-sectional comparative study included 40 subjects aged between 40 and 65 years with at least 20 teeth remaining. The diabetic status was confirmed with HbA1c levels and categorized into group I: healthy controls with HbA1c < 5.6% and no periodontitis with bleeding on probing (BOP) at ≤10% of sites, <3% of sites with probing pocket depth (PPD) ≥4 mm, and no sites with clinical attachment level (CAL) ≥ 2 mm and group II: type II diabetes mellitus (T2DM) cases with HbA1c > 5.7% and periodontitis with BOP at >10% of sites, with CAL ≥ 2 mm and with >5% of sites with PPD ≥ 4 mm. Unstimulated fasting whole saliva was collected from each participant and the salivary hemoglobin level analyzed using a colorimetric assay kit. Both groups were compared using the t-test and multiple linear regression model analysis. Relationship between different variables were compared using the Karl Pearson's correlation coefficient. Statistical significance was set at 5% level (p < 0.05). Results: A significant difference was observed between the salivary hemoglobin level (t −3.7710, p < 0.001), PPD (t −13.9023, p < 0.001), and CAL (t −9.3759, p < 0.001) between healthy controls and type II diabetics with T2DM subjects exhibiting much higher value compared to healthy controls. Conclusion: In conclusion, data from this study demonstrated that type II diabetic adults have high prevalence of chronic periodontitis and exhibit elevated salivary hemoglobin indicating a valuable noninvasive screening method for detecting periodontitis.
Chavarry 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.
Dhir S, Kumar V. Are cardiovascular risk parameters and glycemic levels associated with periodontitis in type II diabetes subjects? A clinical study. Indian Heart J 2018;70(3):430–432. DOI: 10.1016/j.ihj.2017.10.002.
Lu HK, Yang PC. Cross-sectional analysis of different variables of subjects with non-insulin dependent diabetes and their periodontal status. Int J Periodontics Restorative Dent 2004;24(1):71–79.
Nand KY, Oommen AM, Chacko RK, et al. Chronic periodontitis among diabetics and nondiabetics aged 35-65 years, in a rural block in Vellore, Tamil Nadu: a cross-sectional study. J Indian Soc Periodontol 2017;21(4):309–314. DOI: 10.4103/jisp.jisp_217_17.
Apoorva SM, Sridhar N, Suchetha A. Prevalence and severity of periodontal disease in type II diabetes mellitus (non-insulin-dependent diabetes mellitus) subjects in Bengaluru city: an epidemiological study. J Indian Soc Periodontol 2013;17(1):25–29. DOI: 10.4103/0972-124X.107470.
Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract 2010;87(1):4–14. DOI: 10.1016/j.diabres.2009.10.007.
Bascones-Martínez A, González-Febles J, Sanz-Esporrín J. Diabetes and periodontal disease. Review of the literature. Am J Dent 2014;27(2):63–67.
Tonetti MS, Jepsen S, Jin L, et al. Impact of the global burden of periodontal diseases on health, nutrition, and wellbeing of mankind: a call for global action. J Clin Periodontol 2017;44(5):456–462. DOI: 10.1111/jcpe.12732.
American Academy of Periodontology (AAP). Position Paper. Epidemiology of periodontal diseases. J Periodontol 2005;76(8): 1406–1419. DOI: 10.1902/jop.2005.76.8.1406.
Eldarrat AH. Awareness and attitude of diabetic patients about their increased risk for oral diseases. Oral Health Prev Dent 2011;9(3): 235–241.
Albert DA, Ward A, Allweiss P, et al. Diabetes and oral disease: implications for health professionals. Ann NY Acad Sci 2012;1255:1–15. DOI: 10.1111/j.1749-6632.2011.06460.x.
Ryan RJ. The accuracy of clinical parameters in detecting periodontal disease activity. J Am Dent Assoc 1985;111(5):753–760. DOI: 10.14219/jada.archive.1985.0195.
Okada A, Nomura Y, Sogabe K, et al. Comparison of salivary hemoglobin measurements for periodontitis screening. J Oral Sci 2017;59(1):63–69. DOI: 10.2334/josnusd.16-0204.
Ebersole JL, Nagarajan R, Akers D, et al. Targeted salivary biomarkers for discrimination of periodontal health and disease(s). Front Cell Infect Microbiol 2015;5:62. DOI: 10.3389/fcimb.2015.00062.
Gursoy UK, Könönen E, Pradhan-Palikhe P, et al. Salivary MMP-8, TIMP1, and ICTP as markers of advanced periodontitis. J Clin Periodontol 2010;37(6):487–493. DOI: 10.1111/j.1600-051X.2010.01563.x.
AlMoharib HS, AlMubarak A, AlRowis R, et al. Oral fluid based biomarkers in periodontal disease: part1. Saliva. J Int Oral Health 2014;6(4):95–103.
Miller CS, King Jr CP, Langub MC, et al. Salivary biomarkers of existing periodontal disease: a cross sectional study. J Am Dent Assoc 2006;137(3):322–329. DOI: 10.14219/jada.archive.2006.0181.
Wagener FA, Eggert A, Boerman OC, et al. Heme is a potent inducer of inflammation in mice and is counteracted by heme oxygenase. Blood 2001;98(6):1802–1811. DOI: 10.1182/blood.V98.6.1802.
Liu LY, McGregor N, Wong BK, et al. The association between clinical periodontal parameters and free haem concentration within the gingival crevicular fluid: a pilot study. J Periodontal Res 2016;51(1): 86–94. DOI: 10.1111/jre.12286.
Nomura Y, Okada A, Tamaki Y, et al. Salivary levels of hemoglobin for screening periodontal disease: a systematic review. Int J Dent 2018;2018:2541204. DOI: 10.1155/2018/2541204.
Nomura Y, Okada A, Kakuta E, et al. A new screening method for periodontitis: an alternative to the community periodontal index. BMC Oral Health 2016;16(1):64. DOI: 10.1186/s12903-016-0216-x.
Yamada H, Okada A, Murata T, et al. Prevalence of blood contamination in adult saliva and quantitative measurement of salivary hemoglobin level by using an anti-human hemoglobin monoclonal. Asian Pac J Dent 2016;16:9–13.
Nam SH, Jung HI, Kang SM, et al. Validity of screening methods for periodontitis using salivary hemoglobin level and self-report questionnaires in people with disabilities. J Periodontol 2015;86(4):536–545. DOI: 10.1902/jop.2015.140457.
Maeng YJ, Kim BR, Jung HI, et al. Diagnostic accuracy of a combination of salivary hemoglobin levels, self-report questionnaires, and age in periodontitis screening. J Periodontal Implant Sci 2016;46(1):10–21. DOI: 10.5051/jpis.2016.46.1.10.
Summary of revisions: standards of medical in diabetes-2019. Diabetes Care 2019;42(Suppl 1):S4–S6. DOI: 10.2337/dc19-Srev01.
Srivastava N, Nayak PA, Rana S. Point of care: a novel approach to periodontal diagnosis – a review. J Clin Diagn Res 2017;11(8): ZE01–ZE06. DOI: 10.7860/JCDR/2017/26626.10411.
Syndergaard B, Al-Sabbagh M, Kryscio RJ, et al. Salivary biomarkers associated with gingivitis and response to therapy. J Periodontol 2014;85(8):e295–e303. DOI: 10.1902/jop.2014. 130696.
Navazesh M. Methods for collecting saliva. Ann NY Acad Sci 1993;694(1):72–77. DOI: 10.1111/j.1749-6632.1993.tb18343.x.
Mealey BL, Oates TW, American Academy of Periodontology. Diabetes mellitus and periodontal diseases. J Periodontol 2006;77(8): 1289–1303. DOI: 10.1902/jop.2006.050459.
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.
Wolff RE, Wolff LF, Michalowicz BS. A pilot study of glycosylated hemoglobin levels in periodontitis cases and healthy controls. J Periodontol 2009;80(7):1057–1061. DOI: 10.1902/jop.2009. 080664.
Rajan P, Nera M, Pavalura AK, et al. Comparison of glycosylated hemoglobin (HbA1C) levels in patients with chronic periodontitis and healthy controls. Dent Res J (Isfahan) 2013;10(3):389–393.
Shaddox LM, Walker CB. Treating chronic periodontitis: current status, challenges, and future directions. Clin Cosmet Investig Dent 2010;2:79–91. DOI: 10.2147/CCIDE.S7712.
Eke PI, Page RC, Wei L, et al. Update of the case definitions for population-based surveillance of periodontitis. J Periodontol 2012;83(12):1449–1454. DOI: 10.1902/jop.2012.110664.
Choi JS, Kim HE, Donnelly LR. Relationship between salivary haemoglobin and number of remaining teeth in older Koreans. Gerodontology 2018;35(1):25–32. DOI: 10.1111/ger.12312.
Polak D, Shapira L. An update of the evidence for pathogenic mechanisms that may link periodontitis and diabetes. J Clin Periodontol 2018;45(2):150–166. DOI: 10.1111/jcpe.12803.
Madden TE, Herriges B, Boyd LD, et al. Alterations in HbA1c following minimal or enhanced non-surgical, non-antibiotic treatment of gingivitis or mild periodontitis in type II diabetic patients: a pilot trial. J Contemp Dent Pract 2008;9(5):9–16. DOI: 10.5005/jcdp- 9-5-9.
Bodet C, Chandad F, Grenier D. Hemoglobin and LPS act in synergy to amplify the inflammatory response. J Dent Res 2007;86(9):878–882. DOI: 10.1177/154405910708600914.
Sexton WM, Lin Y, Kryscio RJ, et al. Salivary biomarkers of periodontal disease in response to treatment. J Clin Periodontol 2011;38(5): 434–441. DOI: 10.1111/j.1600-051X.2011.01706.x.
Ji S, Choi Y. Point-of-care diagnosis of periodontitis using saliva: technically feasible but still a challenge. Front Cell Infect Microbiol 2015;5:65. DOI: 10.3389/fcimb.2015.00065.
Rantonen P. Salivary flow and composition in healthy and diseased adults. Helsinki: Panu Rantonen; 2003.
FenolI-Palomares C, Munoz-Montagud JV, Sanchiz V, et al. Unstimulated salivary flow rate, pH and buffer capacity of saliva in healthy volunteers. Rev Esp Enferm Dig 2004;96(11):773–783. DOI: 10.4321/S1130-01082004001100005.