SALIVA IN CHILDREN WITH TYPE 1 DIABETES
ARTICLE ABSTRACT Background: Metabolic disturbances in diabetes mellitus can affect oral health. Altered levels of salivary lipids have been suggested as a risk for dental caries. There has been lack of research in this regard and in children with type 1 diabetes mellitus. Aim: To assess the salivary triglycerides and cholesterol levels in children with type 1 diabetes mellitus and correlate them with their dental caries status. Materials and methods: Thirty children aged 12–16 years with type 1 diabetes mellitus and 30 age- and gender-matched healthy children were included in the study. Unstimulated saliva was collected from each child and evaluated for salivary triglyceride and cholesterol levels. Dental caries status (DMFT) was recorded. Results: Salivary cholesterol and triglyceride levels were significantly higher in children with type 1 diabetes mellitus (p ≤ 0.05). In comparison to controls, mean DMFT score was higher in the diabetic children. Salivary triglycerides showed a significant correlation with dental caries status in the study group (p = 0.035). In normal children, salivary cholesterol levels showed a significant association with dental caries. (p = 0.008). Conclusion: Both salivary cholesterol and triglycerides levels were significantly higher in children with type 1 diabetes mellitus. Salivary triglycerides showed a significant association with dental caries in these children.
KEY WORDS: type 1 diabetes ellitus, salivary triglycerides, salivary m cholesterol, dental caries
Association of salivary triglycerides and cholesterol with dental caries in children with type 1 diabetes mellitus Priya Subramaniam, MDS;1* Akhliesh Sharma, MDS;2 Keerthan Kaje, BDS2 1
Principal, Professor and Head, Department of Pedodontics and Preventive Dentistry, The Oxford Dental College and Hospital, Bangalore, India; 2Department of Pedodontics and Preventive Dentistry, The Oxford Dental College and Hospital, Bangalore, India. *Corresponding author e-mail: [email protected] Spec Care Dentist XX(X): 1-3, 2014
Introd uct ion
Type 1 diabetes mellitus (DM1) is a metabolic dysfunction characterized by hyperglycemia resulting from definitive deficiency in insulin secretion caused by autoimmune illness and genetic factors. DM1 is one of the most common pediatric endocrine illnesses, which affects nearly 500,000 children below the age of 15 years. In India there are an estimated 97,700 children with DM1. In Karnataka, DM1 registry listed an incidence of 3.7/1,00,000 in boys and 4.0/1,00,000 in girls.1 The American Diabetes Association (ADA) reports that 75% of DM1 cases are diagnosed in persons under the age of 18 years. Children with diabetes differ from adults in many respects, including insulin sensitivity to sexual maturity, physical growth, and neurological vulnerability to hypoglycaemia.2 A major complication of DM1 is diabetic neuropathy.3 Oral manifestations include decreased salivary flow, difficulty in swallowing and speech, high susceptibility to oral infections, including candidiasis, dental caries, gingivitis, and mucositis.4–6 Most of the lipids in saliva are of glandular in origin and some of them are believed to diffuse directly from serum. Salivary cholesterol concentrations seem to reflect serum concentration to some extent in individuals with high cholesterol levels.7 Salivary lipids are associated with proteins, especially to glycoproteins and proline-rich proteins. Studies have proven the association of salivary peptides and protein compositions with that of dental caries.8,9 However, data is lack-
© 2014 Special Care Dentistry Association and Wiley Periodicals, Inc. DOI: 10.1111/scd.12097
scd12097.indd 1
ing on the association of salivary triglycerides and cholesterol with that of dental caries. Therefore, the aim of this study was to assess salivary triglycerides and cholesterol levels in children with DM1 and compare it with that of healthy children, and to correlate these salivary parameters with their dental caries status.
Ma t er ia l a nd m e t h o d s
The study group consisted of 30 children with DM1, aged 12–16 years, from Bangalore Diabetic Hospital, Bangalore, India. Only cooperative children having their complete medical records were included. Thirty healthy children matched for age and gender were selected from a public school in Bangalore to form the control group. Those children without any systemic condition or disease and who were not under any medication were included using systematic random allocation. In both groups, children having primary
Spec Care Dentist XX(X) 2014 1
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SALIVA IN CHILDREN WITH TYPE 1 DIABETES
dentition were excluded from the study. The nature of the study was described to authorities of both the diabetic centre and the school. Their written consent was taken to carry out the study. Ethical clearance to conduct the study was taken from the institution’s ethical review board. The study was explained to parents of both diabetic and healthy children. Prior written consent was obtained from parents of all the children. Each child was made to sit in coachman position and the pooled unstimulated saliva was collected in a sterile graduated cup over a period of 5 minutes. In order to minimize circadian rhythm effects and to have an interval of at least two hours following eating, tooth brushing or mouth rinsing, all saliva samples were collected between 10 and 11 am. The salivary samples were stored in ice at −4°C and transported immediately to the laboratory for biochemical analysis. Salivary total cholesterol and triglyceride levels were assessed by cholesterol oxidase (CHOD) and glycerol-3-phosphate oxidase (GPD) methods, respectively; with the use of commercially available kits (Ident-I Reagents and kits, Jeev diagnostics, Chennai, India).10,11 A single trained and calibrated examiner recorded dental caries status according to WHO criteria using a sterile mouth mirror and CPI probe.12 Student’s t test was used to find the significance of parameters between the two groups. Spearman correlation test was used to find the correlation between DMFT and the salivary parameters measured.
Res u lts
Salivary cholesterol and triglyceride levels were significantly higher in children with DM1 as compared to that of normal healthy controls (Table 1). The diabetic children had a higher mean DMFT score than that of the control group (Table 1). Salivary triglycerides had a significant correlation with DMFT score in diabetic children, whereas total cholesterol levels in saliva showed a significant association with dental caries in normal children (Table 2).
2 Spec Care Dentist XX(X) 2014
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Table 1. Salivary parameters and dental caries (DMFT) in diabetic children and healthy controls. Parameters
p Value
Study group (mean ± SD)
Control group (mean ± SD)
Triglycerides (mg/dl)
6.83 ± 1.77
5.69 ± 2.17
0.029*
Total cholesterol (mg/dl)
4.35 ± 0.93
2.38 ± 1.52
0.001**
DMFT
1.07 ± 2.43
0.50 ± 1.14
0.253
*p ≤ 0.05 is significant. **p ≤ 0.001 is highly significant.
Table 2. Correlation between DMFT and levels of triglycerides and total cholesterol in saliva. Pair
Study
Control
r Value
p Value
r Value
p Value
DMFT versus triglycerides (mg/dl)
0.387
0.035*
0.348
0.059
DMFT versus total cholesterol (mg/dl)
0.274
0.143
0.477
0.008*
*p ≤ 0.05 is significant.
D is cus s ion
Diabetes mellitus is a group of metabolic diseases characterized by hyperglycemia resulting from defects in insulin secretion, insulin action, or both.13 Dental caries is a disease with a multifactorial etiology. Among the several confounding factors for dental caries, increased levels of salivary lipids has also been suggested.14 A significant increase in cholesterol and triacylglyceride levels in parotid stimulated saliva has been observed in individuals with caries as compared to caries free individuals.14–16 Salivary lipids are mostly of glandular origin7 whereas cholesterol, a low molecular weight lipid, is thought to be derived from plasma and its clearance involves processes such as ultra filtration through gap junctions between cells and secretory units.17 Systemic diseases could alter these complex mechanisms and lead to tooth damage. In the present study, both salivary triglyceride and cholesterol levels were significantly higher among children with DM1, which is in accordance with earlier studies.10,18,19 There have been contradictory results regarding dental caries status in DM1 when compared with nondiabetics.4,20-24 Since diabetic patients are at an increased risk for dyslipidemia and have a higher lipid content in their saliva, it could
affect their dental caries experience. Increased salivary phospholipid content and lower salivary glycolipids have been associated with biofilm maturation.16 Salivary lipids plays a nucleating role in the early mineralization of dental plaque.7 Higher levels of salivary triglyceride and cholesterol lead to higher concentration of lipids in plaque which retards the diffusion of lactic acid from the plaque.14 This could be one of the reasons for the significant association observed between salivary triglyceride levels and dental caries of diabetic children in our study. The other reason could be due to the enhancement of glucosyl transferase enzyme activity by lipids which potentiates the cariogenicity of oral microorganisms. Also, the presence of lipids in saliva modifies the hydrophobic nature of bacterial surfaces and therefore, could help in their adsorption on to tooth surfaces.25 A cross sectional and questionnaire type of study that showed no difference in dental caries among children with DM1 attributed it to snacking of foods that are protective against dental caries.26 In this study, diabetic children did not differ significantly from the control group with regard to dental caries status as opposed to the usual scenario where diabetic children are expected to have much
Saliva in children with type 1 diabetes
15/11/14 3:53 PM
SALIVA IN CHILDREN WITH TYPE 1 DIABETES
more carious lesions. Regular health programs for diabetic individuals including oral health education and d ietary counselling were being provided at the diabetic centres. This could have resulted in increased awareness among parents and older children on the importance of glycemic control, diet, and oral hygiene.
C on clu s ion
Significantly higher levels of salivary triglycerides and cholesterol were seen in children with DM1. A significant association was found between salivary triglycerides and dental caries in permanent dentition of children with DM1. Further research is necessary on the association of other risk factors related to dental caries in children with DM1. A large number of biomolecules and compounds are present in saliva that could assist in the diagnosis and progression of metabolic diseases. These salivary biomarkers could predict risk of dental caries in children.
References 1. Kumar P, Krishna P, Reddy SC, Gurappa M, Aravind SR, Munichoodappa C. Incidence of type 1 diabetes mellitus and associated complications among children and young adults: results from Karnataka Diabetes Registry 1995–2008. J Indian Med Assoc 2008;106(11): 708–11. 2. American Diabetes Association-ADA. Standards of medical care in diabetes. Diabetes Care 2006;29(1):S4–42. 3. Trotta D, Verrotti A, Salladini C, Chiarelli F. Diabetic neuropathy in children and adolescents. Pediatr Diabetes. 2004;5(1):44–57. 4. Rai K, Hegde AM, Kamath A, Shetty S. Dental caries and salivary alterations in Type 1 Diabetes. J Clin Pediatr Dent 2011; 36(2):181–4. 5. Moreira AR, Passos IA, Sampaio FC, Soares MS, Oliveira RJ. Flow rate, pH and calcium
Subramaniam et al.
scd12097.indd 3
concentration of saliva of children and adolescents with type 1 diabetes mellitus. Br J Med Biol Res 2009;42(8):707–11. 6. http://www.intechopen.com/books/ type-1-diabetes-complications/impact-ofhyperglycemia-onxerostomia-and-salivarycomposition-and-flow-rate-of-adolescentswith-type-1-diabetes-mellitus. Accessed May 8, 2013. 7. Karjalainen S, Sewon L, Soderling E, et al. Salivary cholesterol of healthy adults in relation to serum cholesterol concentration and oral health. J Dent Res 1997;76(10):1637–43. 8. Bergandi L, Defabianis P, Re F, et al. Absence of soluble CD14 in saliva of young patients with dental caries. Eur J Oral Sci 2007; 115(2):93–6. 9. Hardt M, Thomas LR, Dixon SE, et al. Toward defining the human parotid gland salivary proteome and peptidome: identification and characterization using 2D SDS-PAGE, ultrafiltration, HPLC, and mass spectrometry. Biochem 2005;44:2885–99. 10. Gheena S, Chandrasekhar T, Ramani P. Salivary characteristics of diabetic children. Braz J Oral Sci 2011;10(2):93–7. 11. Fossati P, Prencipe L. Serum triglycerides determined colorimetrically with an enzyme that produces hydrogen peroxide. Clin Chem 1982;28(10):2077–80. 12. World Health Organization. Oral health surveys: basic methods, 4th ed. Geneva, Switzerland: WHO; 1997. 13. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2013;36(1):s67–s74. 14. Slomiany BL, Murty VL, Mandel ID, Zalesna G, Slomiany A. Physicochemical characteristics of mucus glycoproteins and lipids of the human oral mucosal mucus coat in relation to caries susceptibility. Arch Oral Biol 1989; 34(4):229–37. 15. Sugimoto M, Wong DT, Hirayama A, Soga T, Tomita M. Capillary electrophoresis mass spectrometry-based saliva metabolomics identified oral, breast and pancreatic cancer-specific profiles. Metabolomics 2010;6(1):78–95. 16. Slomiany BL, Murty VL, Slomiany A, Zielenski J, Mandel ID. Mucus glycoprotein
of human saliva: differences in the associated and covalently bound lipids with caries. Biochim Biophys Acta 1986;882(1): 18–28. 17. Pfaffe T, Cooper-White J, Beyerlein P, Kostner K, Punyadeera C. Diagnostic potential of saliva: current state and future applications. Clin Chem 2011;57(5):675–87. 18. Wiltshire EJ, Hirte C, Couper JJ. Dietary fats do not contribute to hyperlipidemia in children and adolescents with type 1 diabetes. Diabetes Care 2003;26(5):1356–61. 19. Ladeia AM, Adan L, Couto-Silva AC, Hiltner A, Guimarães AC. Lipid profile correlates with glycemic control in young patients with type 1 diabetes mellitus. Prev Cardiol 2006;9(2):82–8. 20. Tenovuo J, Alanen P, Larjava H, Viikari J, Lehtonen OP. Oral health of patients with insulin-dependent diabetes mellitus. Scand J Dent Res 1986;94(4):338–46. 21. Matsson L, Koch G. Caries frequency in children with controlled diabetes. Scand J Dent Res 1975;83(6):327–32. 22. Jones RB, McCallum RM, Kay EJ, Kirkin V, McDonald P. Oral health and oral health behaviour in a population of diabetic outpatient clinic attenders. Community Dent Oral Epidemiol 1992;20(4):204–7. 23. Tagelsir A, Cauwels R, van Aken S, Vanobbergen J, Martens LC. Dental caries and dental care level (restorative index) in children with diabetes mellitus type 1. Int J Paediatr Dent 2011;21(1):13–22. 24. Siudikiene J, Machiulskiene V, Nyvad B, Tenovuo J, Nedzelskiene I. Dental caries and salivary status in children with type 1 diabetes mellitus, related to the metabolic control of the disease. Eur J Oral Sci 2006;114(1): 8–14. 25. Beachey EH. Bacterial adherence: adhesinreceptor interactions mediating the attachment of bacteria to mucosal surface. J Infect Dis 1981;143(3):325–45. 26. Bassir L, Amani R, Masjedi MK, Ahangarpor F. Relationship between dietary patterns and dental health in type I diabetic children compared with healthy controls. Iran Red Cres Med J 2014;16(1):e9684.
Spec Care Dentist XX(X) 2014 3
15/11/14 3:53 PM
ARTICLE ABSTRACT Background: Metabolic disturbances in diabetes mellitus can affect oral health. Altered levels of salivary lipids have been suggested as a risk for dental caries. There has been lack of research in this regard and in children with type 1 diabetes mellitus. Aim: To assess the salivary triglycerides and cholesterol levels in children with type 1 diabetes mellitus and correlate them with their dental caries status. Materials and methods: Thirty children aged 12–16 years with type 1 diabetes mellitus and 30 age- and gender-matched healthy children were included in the study. Unstimulated saliva was collected from each child and evaluated for salivary triglyceride and cholesterol levels. Dental caries status (DMFT) was recorded. Results: Salivary cholesterol and triglyceride levels were significantly higher in children with type 1 diabetes mellitus (p ≤ 0.05). In comparison to controls, mean DMFT score was higher in the diabetic children. Salivary triglycerides showed a significant correlation with dental caries status in the study group (p = 0.035). In normal children, salivary cholesterol levels showed a significant association with dental caries. (p = 0.008). Conclusion: Both salivary cholesterol and triglycerides levels were significantly higher in children with type 1 diabetes mellitus. Salivary triglycerides showed a significant association with dental caries in these children.
KEY WORDS: type 1 diabetes ellitus, salivary triglycerides, salivary m cholesterol, dental caries
Association of salivary triglycerides and cholesterol with dental caries in children with type 1 diabetes mellitus Priya Subramaniam, MDS;1* Akhliesh Sharma, MDS;2 Keerthan Kaje, BDS2 1
Principal, Professor and Head, Department of Pedodontics and Preventive Dentistry, The Oxford Dental College and Hospital, Bangalore, India; 2Department of Pedodontics and Preventive Dentistry, The Oxford Dental College and Hospital, Bangalore, India. *Corresponding author e-mail: [email protected] Spec Care Dentist XX(X): 1-3, 2014
Introd uct ion
Type 1 diabetes mellitus (DM1) is a metabolic dysfunction characterized by hyperglycemia resulting from definitive deficiency in insulin secretion caused by autoimmune illness and genetic factors. DM1 is one of the most common pediatric endocrine illnesses, which affects nearly 500,000 children below the age of 15 years. In India there are an estimated 97,700 children with DM1. In Karnataka, DM1 registry listed an incidence of 3.7/1,00,000 in boys and 4.0/1,00,000 in girls.1 The American Diabetes Association (ADA) reports that 75% of DM1 cases are diagnosed in persons under the age of 18 years. Children with diabetes differ from adults in many respects, including insulin sensitivity to sexual maturity, physical growth, and neurological vulnerability to hypoglycaemia.2 A major complication of DM1 is diabetic neuropathy.3 Oral manifestations include decreased salivary flow, difficulty in swallowing and speech, high susceptibility to oral infections, including candidiasis, dental caries, gingivitis, and mucositis.4–6 Most of the lipids in saliva are of glandular in origin and some of them are believed to diffuse directly from serum. Salivary cholesterol concentrations seem to reflect serum concentration to some extent in individuals with high cholesterol levels.7 Salivary lipids are associated with proteins, especially to glycoproteins and proline-rich proteins. Studies have proven the association of salivary peptides and protein compositions with that of dental caries.8,9 However, data is lack-
© 2014 Special Care Dentistry Association and Wiley Periodicals, Inc. DOI: 10.1111/scd.12097
scd12097.indd 1
ing on the association of salivary triglycerides and cholesterol with that of dental caries. Therefore, the aim of this study was to assess salivary triglycerides and cholesterol levels in children with DM1 and compare it with that of healthy children, and to correlate these salivary parameters with their dental caries status.
Ma t er ia l a nd m e t h o d s
The study group consisted of 30 children with DM1, aged 12–16 years, from Bangalore Diabetic Hospital, Bangalore, India. Only cooperative children having their complete medical records were included. Thirty healthy children matched for age and gender were selected from a public school in Bangalore to form the control group. Those children without any systemic condition or disease and who were not under any medication were included using systematic random allocation. In both groups, children having primary
Spec Care Dentist XX(X) 2014 1
15/11/14 3:53 PM
SALIVA IN CHILDREN WITH TYPE 1 DIABETES
dentition were excluded from the study. The nature of the study was described to authorities of both the diabetic centre and the school. Their written consent was taken to carry out the study. Ethical clearance to conduct the study was taken from the institution’s ethical review board. The study was explained to parents of both diabetic and healthy children. Prior written consent was obtained from parents of all the children. Each child was made to sit in coachman position and the pooled unstimulated saliva was collected in a sterile graduated cup over a period of 5 minutes. In order to minimize circadian rhythm effects and to have an interval of at least two hours following eating, tooth brushing or mouth rinsing, all saliva samples were collected between 10 and 11 am. The salivary samples were stored in ice at −4°C and transported immediately to the laboratory for biochemical analysis. Salivary total cholesterol and triglyceride levels were assessed by cholesterol oxidase (CHOD) and glycerol-3-phosphate oxidase (GPD) methods, respectively; with the use of commercially available kits (Ident-I Reagents and kits, Jeev diagnostics, Chennai, India).10,11 A single trained and calibrated examiner recorded dental caries status according to WHO criteria using a sterile mouth mirror and CPI probe.12 Student’s t test was used to find the significance of parameters between the two groups. Spearman correlation test was used to find the correlation between DMFT and the salivary parameters measured.
Res u lts
Salivary cholesterol and triglyceride levels were significantly higher in children with DM1 as compared to that of normal healthy controls (Table 1). The diabetic children had a higher mean DMFT score than that of the control group (Table 1). Salivary triglycerides had a significant correlation with DMFT score in diabetic children, whereas total cholesterol levels in saliva showed a significant association with dental caries in normal children (Table 2).
2 Spec Care Dentist XX(X) 2014
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Table 1. Salivary parameters and dental caries (DMFT) in diabetic children and healthy controls. Parameters
p Value
Study group (mean ± SD)
Control group (mean ± SD)
Triglycerides (mg/dl)
6.83 ± 1.77
5.69 ± 2.17
0.029*
Total cholesterol (mg/dl)
4.35 ± 0.93
2.38 ± 1.52
0.001**
DMFT
1.07 ± 2.43
0.50 ± 1.14
0.253
*p ≤ 0.05 is significant. **p ≤ 0.001 is highly significant.
Table 2. Correlation between DMFT and levels of triglycerides and total cholesterol in saliva. Pair
Study
Control
r Value
p Value
r Value
p Value
DMFT versus triglycerides (mg/dl)
0.387
0.035*
0.348
0.059
DMFT versus total cholesterol (mg/dl)
0.274
0.143
0.477
0.008*
*p ≤ 0.05 is significant.
D is cus s ion
Diabetes mellitus is a group of metabolic diseases characterized by hyperglycemia resulting from defects in insulin secretion, insulin action, or both.13 Dental caries is a disease with a multifactorial etiology. Among the several confounding factors for dental caries, increased levels of salivary lipids has also been suggested.14 A significant increase in cholesterol and triacylglyceride levels in parotid stimulated saliva has been observed in individuals with caries as compared to caries free individuals.14–16 Salivary lipids are mostly of glandular origin7 whereas cholesterol, a low molecular weight lipid, is thought to be derived from plasma and its clearance involves processes such as ultra filtration through gap junctions between cells and secretory units.17 Systemic diseases could alter these complex mechanisms and lead to tooth damage. In the present study, both salivary triglyceride and cholesterol levels were significantly higher among children with DM1, which is in accordance with earlier studies.10,18,19 There have been contradictory results regarding dental caries status in DM1 when compared with nondiabetics.4,20-24 Since diabetic patients are at an increased risk for dyslipidemia and have a higher lipid content in their saliva, it could
affect their dental caries experience. Increased salivary phospholipid content and lower salivary glycolipids have been associated with biofilm maturation.16 Salivary lipids plays a nucleating role in the early mineralization of dental plaque.7 Higher levels of salivary triglyceride and cholesterol lead to higher concentration of lipids in plaque which retards the diffusion of lactic acid from the plaque.14 This could be one of the reasons for the significant association observed between salivary triglyceride levels and dental caries of diabetic children in our study. The other reason could be due to the enhancement of glucosyl transferase enzyme activity by lipids which potentiates the cariogenicity of oral microorganisms. Also, the presence of lipids in saliva modifies the hydrophobic nature of bacterial surfaces and therefore, could help in their adsorption on to tooth surfaces.25 A cross sectional and questionnaire type of study that showed no difference in dental caries among children with DM1 attributed it to snacking of foods that are protective against dental caries.26 In this study, diabetic children did not differ significantly from the control group with regard to dental caries status as opposed to the usual scenario where diabetic children are expected to have much
Saliva in children with type 1 diabetes
15/11/14 3:53 PM
SALIVA IN CHILDREN WITH TYPE 1 DIABETES
more carious lesions. Regular health programs for diabetic individuals including oral health education and d ietary counselling were being provided at the diabetic centres. This could have resulted in increased awareness among parents and older children on the importance of glycemic control, diet, and oral hygiene.
C on clu s ion
Significantly higher levels of salivary triglycerides and cholesterol were seen in children with DM1. A significant association was found between salivary triglycerides and dental caries in permanent dentition of children with DM1. Further research is necessary on the association of other risk factors related to dental caries in children with DM1. A large number of biomolecules and compounds are present in saliva that could assist in the diagnosis and progression of metabolic diseases. These salivary biomarkers could predict risk of dental caries in children.
References 1. Kumar P, Krishna P, Reddy SC, Gurappa M, Aravind SR, Munichoodappa C. Incidence of type 1 diabetes mellitus and associated complications among children and young adults: results from Karnataka Diabetes Registry 1995–2008. J Indian Med Assoc 2008;106(11): 708–11. 2. American Diabetes Association-ADA. Standards of medical care in diabetes. Diabetes Care 2006;29(1):S4–42. 3. Trotta D, Verrotti A, Salladini C, Chiarelli F. Diabetic neuropathy in children and adolescents. Pediatr Diabetes. 2004;5(1):44–57. 4. Rai K, Hegde AM, Kamath A, Shetty S. Dental caries and salivary alterations in Type 1 Diabetes. J Clin Pediatr Dent 2011; 36(2):181–4. 5. Moreira AR, Passos IA, Sampaio FC, Soares MS, Oliveira RJ. Flow rate, pH and calcium
Subramaniam et al.
scd12097.indd 3
concentration of saliva of children and adolescents with type 1 diabetes mellitus. Br J Med Biol Res 2009;42(8):707–11. 6. http://www.intechopen.com/books/ type-1-diabetes-complications/impact-ofhyperglycemia-onxerostomia-and-salivarycomposition-and-flow-rate-of-adolescentswith-type-1-diabetes-mellitus. Accessed May 8, 2013. 7. Karjalainen S, Sewon L, Soderling E, et al. Salivary cholesterol of healthy adults in relation to serum cholesterol concentration and oral health. J Dent Res 1997;76(10):1637–43. 8. Bergandi L, Defabianis P, Re F, et al. Absence of soluble CD14 in saliva of young patients with dental caries. Eur J Oral Sci 2007; 115(2):93–6. 9. Hardt M, Thomas LR, Dixon SE, et al. Toward defining the human parotid gland salivary proteome and peptidome: identification and characterization using 2D SDS-PAGE, ultrafiltration, HPLC, and mass spectrometry. Biochem 2005;44:2885–99. 10. Gheena S, Chandrasekhar T, Ramani P. Salivary characteristics of diabetic children. Braz J Oral Sci 2011;10(2):93–7. 11. Fossati P, Prencipe L. Serum triglycerides determined colorimetrically with an enzyme that produces hydrogen peroxide. Clin Chem 1982;28(10):2077–80. 12. World Health Organization. Oral health surveys: basic methods, 4th ed. Geneva, Switzerland: WHO; 1997. 13. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2013;36(1):s67–s74. 14. Slomiany BL, Murty VL, Mandel ID, Zalesna G, Slomiany A. Physicochemical characteristics of mucus glycoproteins and lipids of the human oral mucosal mucus coat in relation to caries susceptibility. Arch Oral Biol 1989; 34(4):229–37. 15. Sugimoto M, Wong DT, Hirayama A, Soga T, Tomita M. Capillary electrophoresis mass spectrometry-based saliva metabolomics identified oral, breast and pancreatic cancer-specific profiles. Metabolomics 2010;6(1):78–95. 16. Slomiany BL, Murty VL, Slomiany A, Zielenski J, Mandel ID. Mucus glycoprotein
of human saliva: differences in the associated and covalently bound lipids with caries. Biochim Biophys Acta 1986;882(1): 18–28. 17. Pfaffe T, Cooper-White J, Beyerlein P, Kostner K, Punyadeera C. Diagnostic potential of saliva: current state and future applications. Clin Chem 2011;57(5):675–87. 18. Wiltshire EJ, Hirte C, Couper JJ. Dietary fats do not contribute to hyperlipidemia in children and adolescents with type 1 diabetes. Diabetes Care 2003;26(5):1356–61. 19. Ladeia AM, Adan L, Couto-Silva AC, Hiltner A, Guimarães AC. Lipid profile correlates with glycemic control in young patients with type 1 diabetes mellitus. Prev Cardiol 2006;9(2):82–8. 20. Tenovuo J, Alanen P, Larjava H, Viikari J, Lehtonen OP. Oral health of patients with insulin-dependent diabetes mellitus. Scand J Dent Res 1986;94(4):338–46. 21. Matsson L, Koch G. Caries frequency in children with controlled diabetes. Scand J Dent Res 1975;83(6):327–32. 22. Jones RB, McCallum RM, Kay EJ, Kirkin V, McDonald P. Oral health and oral health behaviour in a population of diabetic outpatient clinic attenders. Community Dent Oral Epidemiol 1992;20(4):204–7. 23. Tagelsir A, Cauwels R, van Aken S, Vanobbergen J, Martens LC. Dental caries and dental care level (restorative index) in children with diabetes mellitus type 1. Int J Paediatr Dent 2011;21(1):13–22. 24. Siudikiene J, Machiulskiene V, Nyvad B, Tenovuo J, Nedzelskiene I. Dental caries and salivary status in children with type 1 diabetes mellitus, related to the metabolic control of the disease. Eur J Oral Sci 2006;114(1): 8–14. 25. Beachey EH. Bacterial adherence: adhesinreceptor interactions mediating the attachment of bacteria to mucosal surface. J Infect Dis 1981;143(3):325–45. 26. Bassir L, Amani R, Masjedi MK, Ahangarpor F. Relationship between dietary patterns and dental health in type I diabetic children compared with healthy controls. Iran Red Cres Med J 2014;16(1):e9684.
Spec Care Dentist XX(X) 2014 3
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