Document Type: Original Article


1 Dental Student, Student's Research Committee, Babol University of Medical Sciences, Babol, Iran.

2 Cellular and Molecular Biology Research Center, Health Research Institute, Babol University of Medical Sciences, Babol, Iran.

3 Non-Communicable Pediatric Diseases Research Center, Health Research Institute, Babol University of Medical Sciences, Babol, Iran.

4 Clinical Biochemistry, Babol University of Medical Sciences, Babol, Iran.

5 Oral Health Research Center, Dept. of Pediatric Dentistry, Faculty of Dentistry, Babol University of Medical Sciences, Babol, Iran.

6 Biostatistics & Epidemiology, Medicine Faculty, Babol University of Medical Sciences, Babol, Iran.


Statement of the Problem: Alteration in salivary composition and its effect on the oral cavity in diabetic child patients remains equivocal.
Purpose: This study was done to assess the relationship between salivary factors and gingival status in children with type-1 Diabetes Mellitus (DM).
Materials and Method: In this cross-sectional study,120 subjects aged 6-16 years (60 well-controlled and poorly-controlled diabetics and 60 healthy individuals) were examined to determine the gingival index (GI) and plaque index (PI). The unstimulated saliva samples were collected to measure the salivary triglyceride, Cholesterol, Albumin, α-Amylase, total protein levels by the laboratory kits. Total antioxidant capacity and the free radicals scavenger index were measured by the Ferric Reducing Ability Of Plasma (FRAP) and 1,1-Diphenyl-2-picryl-hydrazyl (DPPH) assays, respectively. Data were analyzed by parametric and non-parametric, Pearson correlation, and T-tests at a 5% error level.
Results: GI of diabetics was significantly higher than that of healthy individuals (1.51± 0.71 and 0.9±0.81, respectively, p < 0.001). No significant difference was found between the PI of diabetics compared to healthy volunteers (1.59±0.69, 1.63±0.74, respectively). The levels of salivary Triglyceride and Cholesterol, Albumin and Total proteins in healthy subjects were significantly higher than those of people with DM (p < 0.001). A significantly more salivary α-Amylase activity was found in diabetics compared to non-diabetics (p < 0.001). No significant differences were found between diabetic and non-diabetic subjects in terms of DPPH (95.5, 95.9%, respectively) and FRAP (9.77±0.13, 9.78±0.12 (µmol/ mL), respectively).
Conclusion: More gingival inflammation and salivary α-Amylase activity and lower level of salivary lipids, Albumin, and total proteins were found in diabetic patients, but there was no association between the level of lipids, proteins, and the total antioxidant capacity of saliva with periodontal health indicators in patients with DM and healthy individuals.


[1]  Rubin RR, Peyrot M. Quality of life and diabetes. Diabetes Metab Res Rev. 1999; 15: 205-218.

[2]  Wändell PE. Quality of life of patients with diabetes mellitus an overview of research in primary health care in the Nordic countries. Scandinavian Journal of Primary Health Care. 2005; 23: 68-74.

[3]  Association AD. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2014; 37 (Supplement 1): S81-S90.

[4]  Saeedi P, Petersohn I, Salpea P, Malanda B, Karuranga S, Unwin N, et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: Results from the International Diabetes Federation Diabetes Atlas. Diabetes Research and Clinical Practice. 2019; 157: 107843.

[5]  Saini R, Saini S, Sugandha R. Periodontal disease: The sixth complication of diabetes. Journal of Family and Community Medicine. 2011; 18: 31.

[6]  Löe H. Periodontal disease: the sixth complication of diabetes mellitus. Diabetes Care. 1993; 16: 329-334.

[7]  Cianciola L, Park B, Bruck E, Mosovich L, Genco R. Prevalence of periodontal disease in insulin-dependent diabetes mellitus (juvenile diabetes). The Journal of the American Dental Association. 1982; 104: 653-660.

[8]  Jenkins WM, Papapanou PN. Epidemiology of periodontal disease in children and adolescents. Periodontology 2000. 2001; 26: 16-32.

[9]  Lalla E, Cheng B, Lal S, Tucker S, Greenberg E, Goland R, et al. Periodontal changes in children and adolescents with diabetes: a case-control study. Diabetes Care. 2006; 29: 295-299.

[10]          Yeh CK, Christodoulides NJ, Floriano PN, Miller CS, Ebersole JL, Weigum SE, et al. Current development of saliva/oral fluid-based diagnostics. Texas Dental Journal. 2010; 127: 651.

[11]          Ebersole JL, Nagarajan R, Akers D, Miller CS. Targeted salivary biomarkers for discrimination of periodontal health and disease (s). Frontiers in Cellular and Infection Microbiology. 2015; 5: 62.

[12]          Syndergaard B, Al‐Sabbagh M, Kryscio RJ, Xi J, Ding X, Ebersole JL, et al. Salivary biomarkers associated with gingivitis and response to therapy. Journal of Periodontology. 2014; 85: e295-e303.

[13]          Wu YC, Ning L, Tu YK, Huang CP, Huang NT, Chen YF, et al. Salivary biomarker combination prediction model for the diagnosis of periodontitis in a Taiwanese population. Journal of the Formosan Medical Association. 2018; 117: 841-848.

[14]          Casanova L, Hughes F, Preshaw P. Diabetes and periodontal disease. BDJ Team. 2015; 1: 15007.

[15]          Lasisi T, Fasanmade A. Salivary flow and composition in diabetic and non-diabetic subjects. 2012.

[16]          Meurman JH, Rantonen P, Pajukoski H, Sulkava R. Salivary albumin and other constituents and their relation to oral and general health in the elderly. Oral Surg Oral Med Oral Patho Oral Radio Endo. 2002; 94: 432-438.

[17]          Navalkar A, Bhoweer A. Alterations in whole saliva constituents in patients with diabetes mellitus and periodontal disease. Journal of Indian Academy of Oral Medicine and Radiology. 2011; 23: 498.

[18]          Baik JE, Hong SW, Choi S, Jeon JH, Park OJ, Cho K, et al. Alpha‐amylase is a human salivary protein with affinity to lipopolysaccharide of Aggregatibacter actinomycetemcomitans. Molecular Oral Microbiology. 2013; 28: 142-153.

[19]          Ochiai A, Harada K, Hashimoto K, Shibata K, Ishiyama Y, Mitsui T, et al. α‐Amylase is a potential growth inhibitor of P orphyromonas gingivalis, a periodontal pathogenic bacterium. Journal of Periodontal Research. 2014; 49: 62-68.

[20]          Fábián TK, Hermann P, Beck A, Fejérdy P, Fábián G. Salivary defense proteins: their network and role in innate and acquired oral immunity. International Journal of Molecular Sciences. 2012; 13: 4295-4320.

[21]          Giannobile WV, Beikler T, Kinney JS, Ramseier CA, Morelli T, Wong DT. Saliva as a diagnostic tool for periodontal disease: current state and future directions. Periodontology 2000. 2009; 50: 52.

[22]          Kuczmarski RJ, Ogden CL, Guo SS, Grummer-Strawn LM, Flegal KM, Mei Z, et al. 2000 CDC Growth Charts for the United States: methods and development. Vital Health Stat 11. 2002; 246: 1-190. PMID: 12043359.

[23]          Ismail AF, McGrath CP, Yiu CK. Oral health status of children with type 1 diabetes: a comparative study. Journal of Pediatric Endocrinology and Metabolism. 2017; 30: 1155-1159.

[24]          Babu KG, Subramaniam P, Kaje K. Assessment of dental caries and gingival status among a group of type 1 diabetes mellitus and healthy children of South India–a comparative study. Journal of Pediatric Endocrinology and Metabolism. 2018; 31: 1305-1310.

[25]          Rewers MJ, Pillay K, De*Beaufort C, Craig ME, Hanas R, Acerini CL, et al. Assessment and monitoring of glycemic control in children and adolescents with diabetes. Pediatric diabetes. 2014; 15: 102-114.

[26]          Owlia F, Akhavan Karbassi M, Ahadian H. Comparison of salivary pH in diabetic patients referring to Diabetes Center of Shahid Sadoughi University of Medical Sciences with non-diabetic controls. SSU Journals. 2012; 20: 82-89.

[27]          Singh S, Ramesh V, Oza N, Balamurali PD, Prashad KV, Balakrishnan P. Evaluation of serum and salivary lipid profile: A correlative study. Journal of Oral and Maxillofacial Pathology, JOMFP. 2014; 18: 4.

[28]          Jafari A, Pouramir M, Shirzad A, Motallebnejad M, Bijani A, Moudi S, et al. Evaluation of salivary alpha amylase as a biomarker for dental anxiety. Iran J Psychiatry Behav Sci. 2018; 12: e9350.

[29]          Arash VA, Mahjoub S, Haj*Ahmadi M, Padganeh T. Amounts of salivary total protein before and after orthodontic tooth movement. Journal of Babol University of Medical Sciences (JBUMS). 2008; 10: 43.

[30]          Lubran MM. The measurement of total serum proteins by the Biuret method. Annals of Clinical & Laboratory Science. 1978; 8: 106-110.

[31]          Apak Ra, Özyürek M, Güçlü K, Çapanoğlu E. Antioxidant activity/capacity measurement. 1. Classification, physicochemical principles, mechanisms, and electron transfer (ET)-based assays. Journal of Agricultural and Food Chemistry. 2016; 64: 997-1027.

[32]          Alam MN, Bristi NJ, Rafiquzzaman M. Review on in v-ivo and in vitro methods evaluation of antioxidant activity. Saudi Pharmaceutical Journal. 2013; 21: 143-152.

[33]          Löe H. The gingival index, the plaque index and the retention index systems. The Journal of Periodontology. 1967; 38: 610-616.

[34]          Alves C, Menezes R, Brandão M. Salivary flow and dental caries in Brazilian youth with type 1 diabetes m-ellitus. Indian Journal Dental Research. 2012; 23: 758.

[35]          Machado D, Coelho A, Paula A, Caramelo F, Carrilho F, Barros L, et al. Prevalence of dental caries in patients with type 1 diabetes mellitus treated with multiple insulin injections and that of individuals without diabetes. Acta Médica Portuguesa. 2017; 30: 402-408.

[36]          Daković D, Mileusnić I, Hajduković Z, Čakić S, Hadži-Mihajlović M. Gingivitis and periodontitis in children and adolescents suffering from type 1 diabetes mellitus. Vojnosanitetski Pregled. 2015; 72: 265-273.

[37]          Sanz M, Ceriello A, Buysschaert M, Chapple I, Demmer RT, Graziani F, et al. Scientific evidence on the links between periodontal diseases and diabetes: consensus report and guidelines of the joint workshop on periodontal diseases and diabetes by the international diabetes federation and the European Federation of Periodontology. Diabetes Research and Clinical Practice. 2018; 137: 231-241.

[38]          Buczko P, Zalewska A, Szarmach I. Saliva and oxidative stress in oral cavity and in some systemic disorders. J Physiol Pharmacol. 2015; 66: 1-7.

[39]          Sadeghi R, Taleghani F, Mohammadi S, Zohri Z. The effect of diabetes mellitus type I on periodontal and dental status. Journal of Clinical and Diagnostic Research, JCDR. 2017; 11: ZC14.

[40]          Subramaniam P, Sharma A, Kaje K. Association of salivary triglycerides and cholesterol with dental caries in children with type 1 diabetes mellitus. Special Care in Dentistry. 2015; 35: 120-122.

[41]          Lakshmi PD, Sridevi E, Sankar AS, Kumar MM, Sridhar M, Sujatha B. Diagnostic perspective of saliva in insulin dependent diabetes mellitus children: an in vivo study. Contemporary Clinical Dentistry. 2015; 6: 443.

[42]          Panchbhai AS, Degwekar SS, Bhowte RR. Estimation of salivary glucose, salivary amylase, salivary total protein and salivary flow rate in diabetics in India. Journal of Oral Science. 2010; 52: 359-368.

[43]          Basir L, Aminzade M, Javid AZ, Khanehmasiedi M, Rezaeifar K. Oral health and characteristics of saliva in diabetic and healthy children. Australasian Medical Journal (Online). 2017; 10: 884-889.

[44]          Astaneie F, Afshari M, Mojtahedi A, Mostafalou S, Zamani MJ, Larijani B, et al. Total antioxidant capacity and levels of epidermal growth factor and nitric oxide in blood and saliva of insulin-dependent diabetic patients. Archives of Medical Research. 2005; 36: 376-81.

[45]          Gümüş P, Buduneli N, Çetinkalp Ş, Hawkins SI, Renaud D, Kinane DF, et al. Salivary antioxidants in patients with type 1 or 2 diabetes and inflammatory periodontal disease: a case‐control study. Journal of Periodontology. 2009; 80: 1440-1446.

[46]          Rai K, Hegde A, Kamath A, Shetty S. Dental caries and salivary alterations in Type I Diabetes. Journal of Clinical Pediatric Dentistry. 2011; 36: 181-184.

[47]          Aral CA, Nalbantoğlu Ö, Nur BG, Altunsoy M, Aral K. Metabolic control and periodontal treatment decreases elevated oxidative stress in the early phases of type 1 diabetes onset. Archives of Oral Bbiology. 2017; 82: 115-120.

[48]          Reznick AZ, Shehadeh N, Shafir Y, Nagler RM. Free radicals related effects and antioxidants in saliva and serum of adolescents with Type 1 diabetes mellitus. Archives of Oral Bbiology. 2006; 51: 640-648.