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Table of Contents
ORIGINAL ARTICLE
Year : 2019  |  Volume : 9  |  Issue : 3  |  Page : 99-107

Effect of glycemic control on periodontal disease and caries experience in diabetic patients: A pilot study


1 Department of Preventive Dentistry, Lagos State University College of Medicine, Lagos, Nigeria
2 Department of Preventive Dentistry, College of Medicine, University of Lagos, Lagos, Nigeria
3 Department of Medicine, Lagos State University College of Medicine, Lagos, Nigeria

Date of Submission04-Sep-2018
Date of Acceptance12-Nov-2019
Date of Web Publication20-Dec-2019

Correspondence Address:
Afolabi Oyapero
Department of Preventive Dentistry, Lagos State University College of Medicine, Ikeja, Lagos
Nigeria
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jid.jid_67_18

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   Abstract 


Background: Diabetes mellitus is a diverse set of metabolic disorders initiated by either a lack of insulin, opposition to its action, or both. The aim of this study was to assess the association between glycemic control and the periodontal/caries status of controlled diabetic patients at Lagos State University Teaching Hospital, Ikeja. Materials and Methods: Forty-eight diabetic patients with good glycemic control demonstrated by three consecutive results in their medical records and who gave informed consent were enlisted and screened for periodontal disease and dental caries. Glycemic control was assessed using fasting blood sugar, 2-h postprandial, and glycated hemoglobin (Hb1Ac). Caries was assessed by decayed missing filled teeth (DMFT) while oral hygiene index, gingival index (GI), clinical attachment loss (CAL), and probing pocket depth (PPD) were used to assess periodontal health. The data collected were analyzed using SPSS version 18 and test of statistical significance was done using Chi-square test and ANOVA test. A P ≤ 0.05 was recorded as statistically significant. Results: The PPD and CAL of the participants were significantly associated with their glycemic levels. Those with increased glycemic values had greater attachment loss and pocket depth. Gingival inflammation and oral hygiene were however not significantly associated with glycemic control. Respondents above 65 years similarly had significantly higher numbers of missing teeth (P = 0.04) and greater mean DMFT values (P = 0.03). Similarly, respondents above 66 years of age, those who had no education, and females were observed to have worse oral hygiene, gingival inflammation, and periodontal destruction evidenced by CAL and PPD than other respondents, even though the association was not significant. Conclusion: Oral health manifestations of diabetes need to be emphasized like other systemic diabetic complications. The salient role of glycemic control in periodontal health should also be continuously emphasized among diabetics.

Keywords: Dental caries, diabetes mellitus, glycemic control, periodontal disease


How to cite this article:
Oyapero A, Adeniyi AA, Sofola O, Ogbera AO. Effect of glycemic control on periodontal disease and caries experience in diabetic patients: A pilot study. J Interdiscip Dentistry 2019;9:99-107

How to cite this URL:
Oyapero A, Adeniyi AA, Sofola O, Ogbera AO. Effect of glycemic control on periodontal disease and caries experience in diabetic patients: A pilot study. J Interdiscip Dentistry [serial online] 2019 [cited 2020 Apr 7];9:99-107. Available from: http://www.jidonline.com/text.asp?2019/9/3/99/273664




   Clinical Relevance to Interdisciplinary Dentistry Top


Good glycaemic control results in improved periodontal health and a possible reduction in caries experience in diabetic patients. Periodontal therapy and similarly has a positive effect on glycaemic control. Periodontologists, Dental Public health Specialists and Restorative Dentistry Specialists should work in close collaboration with Physicians for optimum health in diabetic patients.


   Introduction Top


Diabetes mellitus is a diverse set of metabolic disorders initiated by either a lack of insulin, opposition to its action, or both.[1] Patients have hyperglycemia due to the body's incapacity to sustain normal blood glucose values through the body's homeostatic mechanisms. Diabetes mellitus deleteriously affects the patient's physical (short- and long-term organ complications),[2] emotional/mental (fatigue, depressed mood, frustration, and anxiety),[3] and social functioning. It also has detrimental effects on quality of life outcomes.[4] Diabetes mellitus is a highly prevalent noncommunicable disease globally,[5] being the fifth prominent reason for mortality in most developed countries, while it approaches epidemic levels in many developing and newly industrialized countries.[5] The prevalence of diabetes mellitus differs substantially all over the world, from <1% in certain populations like the rural Melanesians of Papua New Guinea to above 50% among Pima Indians of Arizona in North America.[6] The prevalence ranges from 2.2% to 7.9% in different regions in Nigeria.[7],[8] The primary reason for its increasing global prevalence is the significant alterations in diet and lifestyle as well as demographic changes, with an increasing number of elderly residents.[9] Diabetes mellitus has been unequivocally established as a risk factor for oral diseases.[10]

Hyperglycemia has double deleterious effect on oral health. First, a rise in the levels of glucose in the saliva and gingival crevicular fluid enables the growth of pathogenic bacterial species. Second, it intensifies the development of advanced glycation end-products (AGEs) and increased exposure of oral tissues to aldose sugars, which induce nonenzymatic glycation and oxidation.[11] Collagen and connective tissue metabolism is thus altered, resulting in significant periodontal destruction.[12] Degenerative vascular changes associated with diabetes also inhibit nutrient transfer and leukocyte passage to gingival tissues, thus reducing oxygen exchange and metabolic waste.[13] Soft tissue anomalies linked with diabetes mellitus in the oral cavity are periodontal diseases, oral fungal as well as bacterial infections, and salivary dysfunction. Other oral mucosal lesions in diabetics are stomatitis, geographic tongue, oral lichen planus, fissured tongue, lichenoid reactions, and angular cheilitis.[14] Furthermore, delayed wound healing, dental caries, and tooth loss have been described in diabetic patients.[15]

Diabetes mellitus has been unequivocally established as a major risk factor for periodontitis,[16] which has been recognized as the sixth complication of diabetes.[17] The risk of periodontitis is increased by approximately threefold in diabetic individuals when compared with nondiabetic patients.[18] Developing evidence depicts the association as bi-directional diabetes mellitus is a risk factor for severe periodontal disease while severe periodontal disease increases the severity of diabetes mellitus and complicates metabolic control.[19] This association can be explained by two similar but distinctive pathologic pathways, a direct causal association in which the effects of diabetes modify periodontal disease expression or otherwise a shared pathologic defect in which the host is susceptible to either or both diseases.[10] The control of blood glucose is a fundamental feature of diabetes management to minimize associated complications. Adequate glycemic control will not only reduce glucose concentration in the serum, gingival crevicular fluid, and saliva but will also reduce AGE formation and limit inflammation.[20]

Some studies have observed the impact of diabetes on poorly controlled diabetics, but very few studies in our environment have aimed to determine the periodontal health and caries status of controlled diabetic patients. The aim of this study is to determine the association between levels of glycemic control and the periodontal status of controlled diabetic patients in Lagos State University Teaching Hospital (LASUTH).


   Materials and Methods Top


Study design

This was a descriptive study on the effect of glycemic control on periodontal disease and caries experience in diabetic patients at the LASUTH, Ikeja, Lagos, Nigeria.

Ethical aspects

Ethical approval

Ethical clearance for the study was obtained from Health Research and Ethics Committee of the LASUTH (LREC.10/06/277). The protocol was implemented in accordance with provisions of the Declaration of Helsinki.

Informed consent

All participants completed written informed consent. The informed consent form contained the following information: those who agreed to participate in the study were assured of their confidentiality and that there was no undesirable consequence for those that declined.

Study setting and location

This study was conducted at the Diabetic Clinic in the Department of Medicine and at the Preventive Dentistry clinic of LASUTH, Ikeja, Lagos, Nigeria. LASUTH is a tertiary health facility situated in the Capital of Lagos State. It is a multispecialist hospital with a bed complement of 741.

Sample selection

Consecutive patients on appointment at the LASUTH diabetic clinic during the study period were screened for probable inclusion in the study. Diabetic patients with good glycemic control demonstrated by three consecutive results in their medical records and who gave informed consent were enlisted and screened for periodontal disease and dental caries.

Sample size determination

The estimated sample size of 40 was computed using the prevalence of clinical attachment loss (CAL) from a reference study, which measured the oral health-related quality of life before and after dental hygiene treatment in patients with periodontal disease.[21] Provision for drop out or attrition rate = Additional 20% of calculated sample size = 8. Total sample size = 48.

Eligibility criteria

Inclusion criteria

  • Patients above 18 years and diagnosed as having had type 1 or 2 diabetes for at least 1 year before the study commenced
  • Those on stable antidiabetic therapy for at least 6 months preceding the study. Eligible subjects had their case histories reviewed in the diabetic clinic to assess past compliance with their medication and control of their blood sugar
  • Those who gave their written informed consent were included.


Diagnostic criteria for periodontitis

A diagnosis of chronic periodontitis was made in patients who had PPD ≥3.6 mm and CAL ≥3 mm in two or more sites.

The severity of periodontitis was categorized as:[22]

  • Moderate attachment loss (moderate pockets): PPD = 3.6–6 mm; ≥2 sites with CAL ≥3 mm but ≥6 mm
  • Severe attachment loss (deep pockets): PPD = 6 mm and above; ≥2 sites with CAL ≥6 mm.


  • The extent of chronic periodontitis was categorized as:[22]
  • Localized: ≤30% of sites with CAL ≥3 mm.
  • Generalized: >30% of sites with CAL ≥3 mm.


Exclusion criteria

  • Poorly controlled diabetic patients
  • Those with known diabetic complication that could lead to hospitalization and those that had a known risk of bacterial endocarditis or had one or more known infectious diseases (HIV and hepatitis)
  • Hypertensive patients on calcium channel blockers such as nifedipine, diltiazem, or amlodipine that could precipitate gingival hyperplasia and further worsen gingival inflammation
  • Those who would require several tooth extractions or had undergone periodontal treatment within 6 months before the study
  • Those with aggressive periodontitis
  • Severe oral inflammation unrelated to periodontal conditions
  • Iatrogenic fixed or removable prosthesis, leading to severe mucosal inflammation
  • Need for immediate tooth extraction.


Glycemic measurements

All the subjects had venous blood samples taken to determine their fasting blood glucose (FBG), postprandial blood glucose, and glycated hemoglobin (HbA1c). They had this investigation done in the morning on each visit at the BT Health and Diagnostics Unit, LASUTH and made the results available in the dental clinic on the appointment day. Single HbAlc values during the period categorized as: <7% (good), 7%–8.6% (moderate), and >8.7% (poor). The fasting blood sugar (FBS) results were categorized as hypoglycemia (0-65 mg/dl), acceptable sugar level (66-130 mg/dl) and poorly controlled sugar level (131 and above). The 2-h postprandial (2-h PPD) blood sugar was categorized as those within acceptable limits (<140 mg/dl) and poorly controlled subjects (>140 mg/dl).

Periodontal examination

Oral examination was performed by the principal investigator for all respondents using the gingival index (GI), oral hygiene index-simplified (OHI-S), community periodontal index of treatment needs (CPITN), clinical attachment level (CAL), and probing pocket depth (PPD). The caries status was also recorded with the DMFT index.

Probing pocket depth and clinical attachment level

PPD was recorded from the gingival margin to the total probing depth, while CAL was recorded from the cementoenamel junction to the total probing depth at six tooth surfaces (mesial, mesiobuccal, distobuccal, mesiolingual, distolingual, distal) using a Williams periodontal probe. All the teeth were examined, and only the third molars were excluded in the clinical assessment. Care was taken to ensure that measurements were made with the probe tip parallel to the tooth. The clinical measurement for each surface was registered, and the final scores were interpreted as follows:

Data analysis

The data were analyzed using Statistical package for the Social Sciences for Windows (version 18, Chicago, IL, USA) statistical software package. Since the data were normally distributed-determined by the Shapiro–Wilk test, descriptive statistics, including means, standard deviations, and percentages, were used to present the demographic variables and health-related behavior of the study participants. The Chi-square test was used to determine the level of association between categorical variables. The ANOVA test was used to compare means the level of association between numerical variables. A P ≤ 0.05 was recorded as statistically significant.


   Results Top


Forty-eight study participants who were qualified by the inclusion and exclusion criteria and who gave their informed consent at the Diabetic Clinic of LASUTH were enlisted in the study. The study was conducted at the Preventive Dentistry Clinic, LASUTH.

Sociodemographic and clinical characteristics of the study participants

The age of the study participants ranged between 26 and 76 years (mean 46 ± 11.64 years). Majority (66.7%) were aged between 46 and 65 years; were females (60.4%); and were married (79.2%) while 52.1% had tertiary education. Most of them (89.6%) had type 2 diabetes mellitus [Table 1].
Table 1: Sociodemographic and clinical characteristics of the study participants

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Periodontal and diabetic parameters of the study participants

The mean OHI-S score of the participants was 2.37 ± 1.10, while the mean GI score was 1.36 ± 0.75. Their mean CAL was 3.30 ± 1.17, while the mean PPD measurement was 3.00 ± 1.26. Of the 288 sextants examined in the 48 subjects, 111 (38.5%) had CPITN scores of 3 and 4, while 37.5% of the subjects had moderate or severe periodontitis. The mean FBS of the study subjects was 104.2 (±14.09) mg/dl, while the mean 2-h PPD sugar reading was 126.1 (±16.35) mg/dl. The HbA1c level was 5.33 (±0.22) [Table 2].
Table 2: Periodontal and diabetic parameters of the study participants

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Association between the diabetic parameters of the study participants and their periodontal status

[Table 3] illustrates the relationship between the periodontal status of the subjects and their glycemic parameters. The clinical attachment level and the PPD of the subjects were significantly associated with the baseline 2-h PPD and HbA1c levels because subjects who had higher glycemic parameters had worse attachment levels and pocket depth. The level of gingival inflammation and oral hygiene were however not significantly associated with glycemic control.
Table 3: Association between the diabetic parameters of the study participants and their periodontal status

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Association between sociodemographic data of respondents and their periodontal and caries status

[Table 4] shows that respondents above 65 years similarly had a significantly higher number of missing teeth (P = 0.04) and higher mean DMFT (P = 0.03). Participants who had no education also had a significant higher number of decayed teeth (P = 0.02) and a greater mean DMFT (P = 0.01).
Table 4: Association between sociodemographic data of respondents and their caries experience

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Similarly, respondents above 66 years of age, those who had no education, and females were observed to have worse oral hygiene, gingival inflammation, and periodontal destruction evidenced by CAL and PPD than other respondents, even though the association was not significant [Table 5].
Table 5: Association between sociodemographic data of respondents and their periodontal status

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Relationship between knowledge and practices of respondents and oral health status

There was no significant association between the oral health knowledge and practices of the study respondents and their oral health status. However, respondents who knew that diabetes mellitus could affect oral health, those who had previously received oral health education, and those who had good oral hygiene practices had better periodontal status and less caries experience than those who did not [Table 6].
Table 6: Relationship between knowledge and practices of respondents and oral health status

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   Discussion Top


Majority of participants in this study were female, married, with tertiary education, and middle-aged or aged. Type 2 diabetic was about 90% of the study sample, and this observation mimics the prevalence observed among diabetics globally.[1] Almost 50% of the study participants had moderate or severe gingivitis, while majority had fair or poor oral hygiene. About a third of the participants also had moderate CAL and PPD. The prevalence of moderate and severe periodontitis in our study cohort was 37.5%, and this was in agreement with a study among diabetic subjects which observed that periodontitis was common among diabetics with over 40% of the subjects having periodontitis.[23]

All the study participants had good glycemic control, and not surprisingly, the level of gingival inflammation and CAL among majority of them was fair to good/mild to moderate, respectively. This finding is important because there was no significant difference in the oral hygiene of the study participants which was fair/poor among most of them. A study conducted by Offenbacher et al.[24] demonstrated that diabetes mellitus amplifies the gingival inflammatory response to plaque biofilm and that adequate glycemic control might improve the gingival inflammatory response and reduce oxidative stress through a decrease in the production of AGEs and oxygen radicals. Adequate glycemic control also reduces glucose levels in the serum, gingival crevicular fluid as well as the saliva.[25] The control of blood glucose is thus a critical feature of diabetes management to curtail associated complications.

Participants in our study who had increased glycemic parameters had significantly worse attachment loss and pocket depth. Periodontitis, in contrast to gingivitis, is the result of apical movement of the junctional epithelium and root surface bacterial colonization; hence, glycemic control without periodontal therapy will have a negligible effect on attachment level.[26] There are several mechanisms that might underscore the high prevalence of periodontitis in diabetics. These include a higher vulnerability to infection due to reduced neutrophil function, the accumulation of AGEs which intensify oxidative stress in tissues, and the binding of AGEs to cell surface receptors which stimulates the increased production of inflammatory cytokines resulting in delayed wound healing. Chronic periodontitis is asymptomatic in its early stages, and patients may be ignorant about their clinical periodontal status[27] as assessed by dental professionals.[28] In advanced stages, however, chronic periodontitis has been noted to be associated with tooth mobility, decreased masticatory efficiency, drifting teeth, and gingival recession, which result in poor esthetics and reduced social acceptance. Tooth loss is the final sequelae of untreated periodontitis, and this presents with speech problems and further worsens the appearance of the patient if anterior teeth are involved.[29] Evidence shows that well-controlled diabetic patients have a similar periodontal status with the general population, and hence, glycemic control should be seen as a regimen for periodontal health.[30]

Respondents aged 66 years and above and those with no education had significantly higher DMFT scores than other participants possibly, indicating the cumulative effect of aging and also educational attainment on caries experience. The uneducated respondents were also significantly likely to have more decayed teeth, while the aged respondents had more missing/extracted teeth. Some studies have reported that individuals with higher educational qualification have better oral health outcomes.[31] Diabetic patients have been observed to have more carious and dental fillings than nondiabetic patients.[32] Twetman et al.[33] observed that diabetics with poor metabolic control developed three times more lesions than those with superior metabolic control. An ecological shift in the composition of oral microflora resulting in higher counts of mutans streptococci and lactobacilli;[34] an increase in the concentration of glucose in the saliva and the gingival crevicular fluid of the periodontal pocket; and impaired functions of saliva[35] have been implicated in this caries pattern. The effect of saliva on caries development is also affected by a lower unstimulated flow rate and poorer composition of saliva,[35] dehydration due to osmotic diuresis as well as polyuria, autonomic neuropathy, microvascular abnormalities, and endothelial dysfunction in the salivary glands, resulting in altered flow rate and composition. Other researchers such as Edblad et al.[36] however were unable to demonstrate any significant differences in caries experience of diabetics in relation to their metabolic control.

Gingival inflammation and periodontal destruction were also observed to be higher among aged and uneducated respondents even though this was not significant. This is not surprising since periodontal status declines with increasing age even in the general population. Early identification and control of periodontal disease in diabetic patients are thus desirable to reverse the decline in oral health status associated with this systemic condition.

There was no significant association between the oral health knowledge and practices of the study respondents and their oral health status. However, respondents who knew that diabetes mellitus could affect oral health, those who had previously received oral health education, and those with good oral hygiene practices had better periodontal status and less caries experience than those who did not. The level of knowledge of oral health among diabetic patients has been shown to be relatively low when compared to subjects without diabetes.[37] The Behavior Risk Factor Surveillance System findings demonstrated that adults with diabetes were less likely than nondiabetic controls to attend a dental clinic within the preceding year, after controlling for relevant confounders.[38] That study also showed diabetic patients were less likely to visit a dentist than they were to visit a physician for diabetes care, eye care, or foot care. The greatest barrier to dental clinic attendance among diabetic patients in Nigeria was lack of perceived need for dental care.[39]

Diabetic patients may be uninformed about their heightened risk for periodontal disease, and thus, oral health education and behavior change are fundamental in improving periodontal health. Oral health manifestations of diabetes need to be emphasized like other systemic diabetic complications. Regular home-based oral hygiene practices are indispensable for appropriate supragingival plaque elimination, and this is best achieved by tooth brushing. Effective plaque control also includes interproximal cleaning and periodic professionally administered plaque removal.[40] Brushing twice-daily using a toothpaste-containing fluoride should thus be combined with the removal of interdental plaque once every 24 h.[41] The salient role of glycemic control in periodontal health should also be continuously emphasized among diabetics.


   Conclusion Top


Diabetes mellitus is a major risk factor for the development of periodontal disease. The clinical attachment level and the PPD of the participants were significantly associated with their glycemic levels. The level of gingival inflammation and oral hygiene was however not significantly associated with glycemic control. Respondents above 65 years similarly had a significantly higher number of missing teeth and higher mean DMFT. Well-controlled diabetic patients in our study had a good periodontal status, and hence, glycemic control should be seen as a regimen for periodontal health.

Study limitation

This uncontrolled descriptive study was hospital based, and it may or may not represent the whole diabetic population of the country. Patients presenting in the hospital in Nigeria tend to have severe disease with a tendency to present as advanced cases. It could also be considered a limitation of the present study that the subjects were taken from only one clinical setting. The pilot study however provides a template for further exploratory clinical studies.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
   References Top

1.
Daneman D. Type 1 diabetes. Lancet 2006;367:847-58.  Back to cited text no. 1
    
2.
Nazimek-Siewniak B, Moczulski D, Grzeszczak W. Risk of macrovascular and microvascular complications in type 2 diabetes: Results of longitudinal study design. J Diabetes Complications 2002;16:271-6.  Back to cited text no. 2
    
3.
Sultan S, Luminet O, Hartemann A. Cognitive and anxiety symptoms in screening for clinical depression in diabetes: A systematic examination of diagnostic performances of the HADS and BDI-SF. J Affect Disord 2010;123:332-6.  Back to cited text no. 3
    
4.
Rubin RR, Peyrot M. Quality of life and diabetes. Diabetes Metab Res Rev 1999;15:205-18.  Back to cited text no. 4
    
5.
Amos AF, McCarty DJ, Zimmet P. The rising global burden of diabetes and its complications: Estimates and projections to the year 2010. Diabet Med 1997;14 Suppl 5:S1-85.  Back to cited text no. 5
    
6.
Zimmet P, Whitehouse S. The effect of age on glucose tolerance: Studies in the Polynesian population of Funafuti. Acta Diabetol Lat 1982;19:65-74.  Back to cited text no. 6
    
7.
Akinkugbe OO, Akinyanju OO. Final Report-National Survey on Non-Communicable Diseases in Nigeria: Lagos: Federal Ministry of Health; 1997. p. 65-8.  Back to cited text no. 7
    
8.
Nyenwe EA, Odia OJ, Ihekwaba AE, Ojule A, Babatunde S. Type 2 diabetes in adult Nigerians: A study of its prevalence and risk factors in Port Harcourt, Nigeria. Diabetes Res Clin Pract 2003;62:177-85.  Back to cited text no. 8
    
9.
King H, Rewers M. Global estimates for prevalence of diabetes mellitus and impaired glucose tolerance in adults. WHO ad hoc diabetes reporting group. Diabetes Care 1993;16:157-77.  Back to cited text no. 9
    
10.
Yalda B, Offenbacher S, Collins JG. Diabetes as a modifier of periodontal disease expression. Periodontol 2000 1994;6:37-49.  Back to cited text no. 10
    
11.
Rohlfing CL, Wiedmeyer HM, Little RR, England JD, Tennill A, Goldstein DE, et al. Defining the relationship between plasma glucose and HbA(1c): Analysis of glucose profiles and HbA(1c) in the diabetes control and complications trial. Diabetes Care 2002;25:275-8.  Back to cited text no. 11
    
12.
Ryan ME, Carnu O, Kamer A. The influence of diabetes on the periodontal tissues. J Am Dent Assoc 2003;134:34S-40.  Back to cited text no. 12
    
13.
Sandberg GE, Sundberg HE, Fjellstrom CA, Wikblad KF. Type 2 diabetes and oral health: A comparison between diabetic and non-diabetic subjects. Diabetes Res Clin Pract 2000;50:27-34.  Back to cited text no. 13
    
14.
Quirino MR, Birman EG, Paula CR. Oral manifestations of diabetes mellitus in controlled and uncontrolled patients. Braz Dent J 1995;6:131-6.  Back to cited text no. 14
    
15.
Lamster IB, Lalla E, Borgnakke WS, Taylor GW. The relationship between oral health and diabetes mellitus. J Am Dent Assoc 2008;139 Suppl: 19S-24.  Back to cited text no. 15
    
16.
Khader YS, Dauod AS, El-Qaderi SS, Alkafajei A, Batayha WQ. Periodontal status of diabetics compared with nondiabetics: A meta-analysis. J Diabetes Complications 2006;20:59-68.  Back to cited text no. 16
    
17.
Salvi GE, Lawrence HP, Offenbacher S, Beck JD. Influence of risk factors on the pathogenesis of periodontitis. Periodontol 2000 1997;14:173-201.  Back to cited text no. 17
    
18.
Mealey BL, Ocampo GL. Diabetes mellitus and periodontal disease. Periodontol 2000 2007;44:127-53.  Back to cited text no. 18
    
19.
Grossi SG, Genco RJ. Periodontal disease and diabetes mellitus: A two-way relationship. Ann Periodontol 1998;3:51-61.  Back to cited text no. 19
    
20.
da Cruz GA, de Toledo S, Sallum EA, Sallum AW, Ambrosano GM, de Cássia Orlandi Sardi J. Clinical and laboratory evaluations of non-surgical periodontal treatment in subjects with diabetes mellitus. J Periodontol 2008;79:1150-7.  Back to cited text no. 20
    
21.
Ohrn K, Jonsson B. Oral Health-Related Quality of life Among Patients with Periodontal Disease. Available from: http://dalea.du.se/research. [Last accessed on 2012 Feb 20].  Back to cited text no. 21
    
22.
Haffajee AD, Socransky SS. Attachment level changes in destructive periodontal diseases. J Clin Periodontol 1986;13:461-75.  Back to cited text no. 22
    
23.
Spangler L, Reid RJ, Inge R, Newton KM, Hujoel P, Chaudhari M, et al. Cross-sectional study of periodontal care and glycosylated hemoglobin in an insured population. Diabetes Care 2010;33:1753-8.  Back to cited text no. 23
    
24.
Offenbacher S, Barros SP, Singer RE, Moss K, Williams RC, Beck JD, et al. Periodontal disease at the biofilm-gingival interface. J Periodontol 2007;78:1911-25.  Back to cited text no. 24
    
25.
da Cruz GA, de Toledo S, Sallum EA, Sallum AW, Ambrosano GM, de Cássia Orlandi Sardi J, et al. Clinical and laboratory evaluations of non-surgical periodontal treatment in subjects with diabetes mellitus. J Periodontol 2008;79:1150-7.  Back to cited text no. 25
    
26.
Katagiri S, Nitta H, Nagasawa T, Izumi Y, Kanazawa M, Matsuo A, et al. Effect of glycemic control on periodontitis in type 2 diabetic patients with periodontal disease. J Diabetes Investig 2013;4:320-5.  Back to cited text no. 26
    
27.
Dietrich T, Stosch U, Dietrich D, Schamberger D, Bernimoulin JP, Joshipura K. The accuracy of individual self-reported items to determine periodontal disease history. Eur J Oral Sci 2005;113:135-40.  Back to cited text no. 27
    
28.
Tervonen T, Knuuttila M. Awareness of dental disorders and discrepancy between objective and subjective dental treatment needs. Community Dent Oral Epidemiol 1988;16:345-8.  Back to cited text no. 28
    
29.
D'Avila GB, Carvalho LH, Feres-Filho EJ, Feres M, Leão A. Oral health impacts on daily living related to four different treatment protocols for chronic periodontitis. J Periodontol 2005;76:1751-7.  Back to cited text no. 29
    
30.
Gonçalves D, Correa FO, Khalil NM, de Faria Oliveira OM, Orrico SR. The effect of non-surgical periodontal therapy on peroxidase activity in diabetic patients: A case-control pilot study. J Clin Periodontol 2008;35:799-806.  Back to cited text no. 30
    
31.
Tsakos G, Sheiham A, Iliffe S, Kharicha K, Harari D, Swift CG, et al. The impact of educational level on oral health-related quality of life in older people in London. Eur J Oral Sci 2009;117:286-92.  Back to cited text no. 31
    
32.
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;20:204-7.  Back to cited text no. 32
    
33.
Twetman S, Johansson I, Birkhed D, Nederfors T. Caries incidence in young type 1 diabetes mellitus patients in relation to metabolic control and caries-associated risk factors. Caries Res 2002;36:31-5.  Back to cited text no. 33
    
34.
Marsh PD. Microbial ecology of dental plaque and its significance in health and disease. Adv Dent Res 1994;8:263-71.  Back to cited text no. 34
    
35.
Bardow A, Hofer E, Nyvad B, ten Cate JM, Kirkeby S, Moe D, et al. Effect of saliva composition on experimental root caries. Caries Res 2005;39:71-7.  Back to cited text no. 35
    
36.
Edblad E, Lundin SA, Sjödin B, Aman J. Caries and salivary status in young adults with type 1 diabetes. Swed Dent J 2001;25:53-60.  Back to cited text no. 36
    
37.
Moore PA, Orchard T, Guggenheimer J, Weyant RJ. Diabetes and oral health promotion: A survey of disease prevention behaviors. J Am Dent Assoc 2000;131:1333-41.  Back to cited text no. 37
    
38.
Tomar SL, Lester A. Dental and other health care visits among U.S. Adults with diabetes. Diabetes Care 2000;23:1505-10.  Back to cited text no. 38
    
39.
Taiwo JO, Noah M. Pattern of dental clinic attendance of registered diabetic patients in Ibadan. J Med Biomed Res 2006;5:36-44.  Back to cited text no. 39
    
40.
Axelsson P, Nyström B, Lindhe J. The long-term effect of a plaque control program on tooth mortality, caries and periodontal disease in adults. Results after 30 years of maintenance. J Clin Periodontol 2004;31:749-57.  Back to cited text no. 40
    
41.
Claydon NC. Current concepts in toothbrushing and interdental cleaning. Periodontol 2000 2008;48:10-22.  Back to cited text no. 41
    



 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]



 

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