Journal of Islamabad Medical & Dental College (JIMDC); 1211(1):10-13 10 Original Article Correlation between Salivary Glucose Level and Gingivitis in Patients with Diabetes Sadia Iqbal*, Saad Asad**, Farhat Kazmi***, Fareeha Bokhari**** * Assistant Professor, Department of Oral Pathology, Lahore Medical & Dental College, Lahore. **Correspondence: Assistant Prof Department of Orthodontics, Head of Oral Biology & Tooth Morphology, The University College of Dentistry, The University of Lahore. *** Assistant Professor & Head of Oral Pathology, University College of Dentistry, The University of Lahore. ****Assistant Professor, Department of Orthodontics, The University College of Dentistry, The University of Lahore. Abstract: Introduction: Type 1 Diabetes has been linked with an increased risk of gingivitis and periodontal disease. Patients with periodontal disease and/or diabetes show differences in the profile of constituents in whole saliva. This profile reflects the nature and amplitude of the host response to a periodontal microbial challenge and /or response to diabetes mellitus. Objectives: Tto compare gingival health between control group and patients with type I Diabetes and to assess whether there is any association between gingivitis/periodontitis and salivary glucose level. Patients & Methods: Study was conducted on 90 subjects; 30 control and 60 diabetics. Gingival and periodontal status was assessed for both the groups clinically. Then un-stimulated whole saliva samples from diabetics and control group were collected stored and frozen at -200 C. Saliva samples were then thawed, centrifuged and its supernatant portion was analyzed by Dimension Clinical Chemistry System for Salivary glucose levels. SPSS 17.0 was used for statistical analysis. Results: Results showed that gingivitis was statistically significantly higher among the type I diabetic patients when compared with the control group p < 0.05. Conclusion: It was concluded that gingival health was compromised in diabetic children. It was also concluded that salivary glucose levels were higher in the patients with type I as compared to control group Key Words: salivary glucose level, type I Diabetes, gingivitis, periodontitis Introduction Diabetes mellitus (DM) is a common disease and has been linked with an increased risk of oral diseases.1 Changed oral environment in diabetes causes increase in colonization of pathogenic bacteria which leads to destruction of hard and soft tissues of mouth. Oral lesions associated to diabetes thus include gingivitis and periodontal disease, xerostomia and salivary gland dysfunction, increased susceptibility to bacterial, viral and fungal infections, dental caries, and periapical abscesses, loss of teeth, taste impairment, lichen planus and burning mouth syndrome.2 These findings are associated with excessive loss of fluids due to polyuria, altered response to infection, altered connective tissue metabolism, micro vascular changes and impaired saliva.3 Gingivitis has been rated as sixth most common complication of diabetes mellitus. It is the most common oral complication associated with diabetes. Firatli et al found that clinical attachment loss is more common in diabetic children and adolescents than in controls.4 Bridges RB et al in their study concluded that diabetic men have poorer periodontal status than non-diabetic men 5. Young diabetic patients have been reported to have significantly higher gingival inflammation scores than controls 6-8. Diabetic patients aged 40-49 have more periodontal pockets ≥6 mm and more extensive alveolar bone loss than non- diabetic patients in the same age-group 9. There is more attachment loss among subjects with type I diabetes with poor metabolic balance and/or multiple complications, and probed pocket depth ≥4 mm often re-occurs faster after periodontal therapy.10 Few studies however, have reported gingival inflammation & periodontal destruction to be equal in diabetic patients and controls. 11 The inconsistency in the results of these studies may be due to the differences in metabolic control, duration of diabetes and age of subjects between different study populations.12 There are several possible mechanisms involved in diabetes that mediate the increased risk for periodontal diseases. A prolonged hyperglycemic condition leads to no enzymatic formation of advanced glycation end products (AGEs), which affects the structure of many cells and tissue proteins, including collagen, predisposing the person to macro- and micro vascular complications. There are reports of decreased collagen synthesis and increased collagen degradation, i.e. increased collagenase activity 13. The host response to local infection is inefficient in diabetic patients. Disorders in neutrophil function together with AGE-related activation of inflammatory cells change the profile of cytokines and tissue growth factors. Consequently, the inflammation response and tissue homeostasis are altered.14-16 Two-way relationship between periodontal disease and diabetes Journal of Islamabad Medical & Dental College (JIMDC); 1211(1):10-13 11 mellitus has been postulated by Davies et al. 17 Thus, periodontitis, as a chronic infection, may impair metabolic control and increase the need for insulin and hence have an influence on the systemic level. On the whole, knowledge is currently insufficient regarding the ability of periodontal therapy to improve the metabolic control of diabetes.18 Diagnosis and monitoring of DM is based on serum glucose concentration or glycosylated hemoglobin concentration however in the recent past because of chances of cross infection, assessment of other body fluids as diagnostic tool has also increased.19 Saliva has gained importance as a diagnostic tool because it is readily available; collection requires non-invasive approach, no chances of cross infection and above all being the representative of various changes occurring in the body.20 If diabetic patients could be screened by saliva with same level of accuracy as is assessed with blood or urine then it would be advantageous for not only dental patients but also for all diabetic patients.21,22 Moreover researchers have gained interest in establishing the relationship between gingival health and salivary sugar levels: whether with increase in salivary sugar level the gingival health deteriorates or not? Present study has been aimed at comparing gingival health between control groups and type 1 diabetic patient and to assess whether there is any association between gingivitis / periodontitis and salivary glucose level in the subjects under study. Patients & Methods The study was conducted on 90 children (3-14 years), out of whom 60 were diabetics (Fasting Blood Sugar Level >120mg/dl) 23-25, who were registered in the endocrinology department of Shaikh Zayed Medical Complex, Lahore and 30 were normal non-diabetics (fasting blood sugar level between 70-120mg/dl), who were under treatment in dental/orthodontic department of Faculty of Dentistry, The University of Lahore. Un-cooperative patients, patients with any active systemic disease and patients with missing teeth were excluded from the study. Consent was taken from the patients/parents and also control group. Un-stimulated whole saliva from diabetic and control group was collected in sterilized plastic jars through spitting method and stored in freezer at -200C and then brought to the laboratory in an ice chilled box. Saliva samples were thawed, centrifuged and its supernatant portion was used for analysis which was carried out by using auto analyzer (Dimension Clinical Chemistry System). The glucose method used on the Dimension® clinical chemistry system is an in vitro diagnostic test. The Glucose method is an adaptation of the hexokinase-glucose-6-phosphate dehydrogenase method. For cases and controls percentage of subjects with reference to their gingival status was computed based on full mouth examination. Table 1: Salivary Glucose Levels among study groups Study Groups Salivary Glucose Level Mean ± SD Control (n=30) Fasting Blood Sugar Level between 70-120mg/dl 7.33 ± 1.36 Patients (n=60) Fasting Blood Sugar Level >120mg/dl 15.26 ± 2.52 Table 2: Comparison of gingival status among study group Oral hygiene status Controls (n=30) N (%) Cases (n=60) N (%) p value Healthy 16 (53.3%) 13 (21.7%) p < 0.05 Gingivitis with or without Calculus 14 (46.7%) 47 (78.3%) p < 0.05 Table 3: Correlation of salivary glucose level with gingival status among study Group Gingivitis status Good (Healthy) Gingivitis/calculus Salivary glucose 14.02 + 1.73 (mg/dl) 17.6 + 1.23 (mg/dl) SPSS 17.0 was used for statistical evaluation. Descriptive Statistics were calculated for each variable for each subject. Chi-square test was applied to show the association of diabetes with the oral hygiene condition and p value was calculated. P value of < 0.05 was taken as statistically significant. Student’s t-test was applied to show the difference between salivary glucose level for normal & diabetics was assessed and co-relation with gingivitis incidence was established. Results Glucose concentration (mg/dl) in saliva in patients with diabetes mellitus was compared with healthy population. As shown in table 1 the mean salivary glucose level in diabetic cases was 15.26 ± 2.52 ranging from 10.5 to 20.0 mg/dl and that of control was 7.33 ± 1.36 ranging from 3.0 to 9.0 mg/dl. Comparison of gingival status among study groups showed that glucose concentration in saliva of diabetic patients was significantly higher as compared to healthy population (t =16.11, p = 0.001 < 0.05). It was also observed that there was a significant difference between case and control subjects in regard to gingival status. (table 2) Table 3 shows that mean salivary glucose level among cases having good oral hygienic condition (healthy) was 14.02 + 1.73, while mean salivary glucose level among cases having poor oral health (Gingivitis/ calculus) was 17.6 + 1.23. It was also observed that salivary glucose was significantly Journal of Islamabad Medical & Dental College (JIMDC); 1211(1):10-13 12 higher in cases having poor hygiene status than having good oral health (p = 0.021 <0.05). Discussion Present study revealed that glucose levels in the un- stimulated whole saliva of type 1 diabetic group were higher than in healthy subjects. The mean salivary glucose level in diabetic patients was 15.26 ± 2.52 and that of control was 7.33 ± 1.36mg/dl., so glucose concentration in saliva of diabetic patients was significantly higher as compared to healthy population (p = 0.001 < 0.05). These results are in agreement with reports of other researchers who found the same increased correlated levels of glucose in the saliva.26 In one of the studies, mean and standard deviation of glucose level in diabetic children was found to be 2.05±1.63 where as in non-diabetic children was 1.03±1.03, indicating that salivary glucose level was higher in diabetics.5 Kjellman et al and Thorstensson et al 27,28 reported significantly higher values of glucose in whole saliva in diabetics than in healthy controls. In contrast, other studies of diabetics and healthy individuals indicate that no such relationship exists.29 DM and periodontitis are common multigenic and multifactorial chronic diseases. Both of the morbidities negatively affect periodontal health and systemic health, thus affecting the quality of life. An abundance of recent evidence has consolidated a bidirectional correlation between diabetes and periodontitis. While diabetes is an independent risk factor for periodontitis, periodontitis as a chronic inflammation has a negative impact on the metabolic control of diabetes. In particular, periodontitis ranks sixth among all complications of diabetes. The present study shows that there was a significant difference between case and control subjects in regard to healthy gums, gingivitis and calculus. There is a significant level (p < 0.05) of marginal gingivitis observed amongst diabetic children (78.3%). However, the percentage of calculus in diabetic children is comparable to that of healthy children and is not of much significant difference (p > 0.5). These results were supported by a previous study in which gingival health (bleeding on probing) and oral hygiene (plaque percent) were assessed in 2 groups of children and adolescents with insulin-dependent diabetes mellitus.30 In another study, diabetic children with poor metabolic control showed a clear tendency towards higher gingival index scores than non- diabetics. 31 In present study calculus among normal control and that of diabetic show no association. This is in contrast to the study which indicates that children with type 1 DM are more prone to calculus accumulation which seemed to be a predisposing factor in development of gingivitis in these individuals. 32 Thus an increase in gingivitis in association with hyperglycemia suggests that hyperglycemia-associated biological alterations, which lower host resistance towards plaque, have apparently taken place. 33-35 Conclusion It was concluded that salivary glucose levels were higher in the patients with type I diabetes as compared to control group and gingival health is compromised in diabetic children. Though not all cases of gingivitis proceed into a destructive periodontal disease, prevention of plaque- induced gingival inflammation should be emphasized, particularly in children and adolescents with poorly controlled diabetes. References 1. Ira B et al. The Relationship between Oral Health and Diabetes Mellitus. JADA 2008; 139 (5): 19S-24S 2. Awuti G et al. Epidemiological Survey on the Prevalence of Periodontitis and Diabetes Mellitus in Uyghur Adults from Rural Hotan Area in Xinjiang. Exp Diabetes Res. 2012; Published online 2011. 3. Iqbal S et al. Dental Caries & Diabetes Mellitus. Pak Oral & Dent J. 2011; 31(1): 60 -63 4. Firatli E. The relationship between clinical periodontal status and insulin-dependent diabetes mellitus, results after 5 years. J Periodontal 1997; 68: 136–40. 5. Bridges RB, Anderson JW, Saxe SR, Gregory K , Bridges SR. Periodontal status of diabetic and non-diabetic men: effects of smoking, glycemic control, and socioeconomic factors. J Periodontal 1996; 67: 1185– 92. 6. Novaes Jr AB, Pereira ALA, de Moraes N , Novaes AB. Manifestations of insulin-dependent diabetes mellitus in the periodontium of young Brazilian patients. J Periodontol 1991; 62: 116–22. 7. Sandholm L, Swanljung O, Rytömaa I, Kaprio EA , Mäenpää J. Periodontal status of Finnish adolescents with insulin- dependent diabetes mellitus. J Clin Periodontol 1989;16: 617–20. 8. Faulconbridge AR, Bradshaw WCL, Jenkins PA, Baum JD. The dental status of a group of diabetic children. Br Dent J.1981; 151: 253–5. 9. Thorstensson H, Hugoson A. Periodontal disease experience in adult long-duration insulin-dependent diabetics. J Clin. Periodontal 1993; 20: 352– 8. 10. Tervonen T, Karjalainen K. Periodontal disease related to diabetic status. A pilot study of the response to periodontal therapy in type 1 diabetes. J Clin Periodontol 1997;24: 505–10 11. Goteiner D, Vogel R, Deasy M, Goteiner C Periodontal and caries experience in children with insulin-dependent diabetes mellitus. J Am Dent Assoc 1986; 113: 277–9. 12. Bacic M, Plancak D , Granic M. CPITN assessment of periodontal disease in diabetic patients. J Periodontol 1988; 59: 816–22. 13. Reiser KMN. On enzymatic glycation of collagen in aging and diabetes. Proc Soc Exp BiolMed 1991; 196: 17–29. 14. Vlassara H. Recent progress in advanced glycation end products and diabetic complications. Diabetes 1997; 46: 19–25. 15. Sánchez GA, Miozza V, Delgado A, Busch L. Determination of salivary levels of mucin and amylase in chronic Journal of Islamabad Medical & Dental College (JIMDC); 1211(1):10-13 13 periodontitis patients J Periodontal Res. 2011 Apr;46(2):221-7. 16. Koss MA, Castro CE, Salúm KM, López ME. Changes in saliva protein composition in patients with periodontal disease. Acta Odontol Latinoam. 2009; 22(2):105-12. 17. Davies RC, Jaedicke KM, Barksby HE, Jitprasertwong P, Al- Shahwani RM, Taylor JJ, Preshaw PM. Do patients with aggressive periodontitis have evidence of diabetes? A pilot study. J Periodontal Res. 2011; 17 18. Taylor GW. Periodontal treatment and its effects on glycemic control. Oral Surg Oral Med Oral Pathos Oral Radiol Endod 1999; 87: 311–6. 19. Herenia P Lawrence. Salivary Markers of Systemic Disease: Non invasive Diagnosis and Monitoring of General Health. J Can Dent Assoc 2002; 68:170-74. 20. Ahmadi Motamayel, F. Davoodi, P. Dalband, M. Hendi, S.S. Saliva as a Mirror of the Body Health .DJH 2010; 1(2): 1- 15 21. Dale AG. Salivary Glands. In: Ten Cate A.R, editor. Oral Histology, development, structure and function. 7th ed. Mosby; 2010.p. 315-316 22. Lopez M E et al. A. Salivary characteristics of diabetic children: Brazilian Dental Journal. June 2003:14:1. 23. Jawad M, Shahid SM, Qader SA, Azhar A. Dental Caries in diabetes mellitus.Vernillo A T. Dental consideration for the treatment of patients with diabetes mellitus: Role of salivary flow rate & minerals. J Diabetes Complications 2010;25(3):183- 86. 24. Vasconcelos AC et al. Comparative study of the concentration of salivary and blood glucose in type 2 diabetic patients. J Oral Sci. 2010;52(2):293- 8 25. Jurysta C, et al. Salivary glucose concentration and excretion in normal and diabetic subjects. J Biomed Biotechnol. 2009;:430426. 26. Rodbard D. Clinical interpretation of indices of quality of glycemic control and glycemic variability. Postgrad Med. 2011 Jul;123(4):107-18 27. Darwazeh AMG et al. Mixed salivary glucose levels and candidal carriage in patients with diabetes mellitus. J Oral Pathol Med 1991; 20: 280– 83. 28. Camp Bell MJA. Glucose in the saliva of the non diabetic and the diabetic patient .Archive of Oral Biology 1965; 10:197-205. 29. Kjellman O. The presence of glucose in gingival exudates and resting saliva of subjects with insulin-treated diabetes mellitus. Swede Dent J 1970; 63: 11–19. 30. horstensson H et al. Some salivary factors in insulin- dependent diabetics. Acta Odontol Scand 1989; 47: 175– 83. 31. Karjalainen KM, Knuuttila ML, kaar ML. Salivary factors in children and adolescents with insulin dependent diabetes mellitus. Pied .Dent 1996; 18:306-11. 32. Gislen G, Nilsson KO, Matsson L .Gingival inflammation in diabetic children related to degree of metabolic control. Acta Odontol Scand.1980; 38(4):241-6. 33. SiudikieneJ, Maciulskiene V, Dobrovolskiene R, Nedzeiskiene I .Oral hygiene in children with type 1 DM. Stomatologia 2005; 7(1); 24-7. 34. Patino MN, Loyola RJP, et al. Effect of metabolic control in type diabetes patients and its association with periodontal disease .Rev Invest Clin.2002 May-Jun; 54(3):218-25. 35. Marchisio O, Esposito MR, Genovesi A. Salivary pH level and bacterial plaque evaluation in orthodontic patients treated with Recaldent products. Int J Dent Hyg. 2010 Aug;8(3):232-36.